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Advanced staging
CHAPTER 7
Interventional radiology in the management
of hepatopancreatobiliary malignancy and
surgical complications
Steven Y. Huang and Michael J. Wallace
Department of Interventional Radiology, Division of Diagnostic Imaging, University of Texas MD Anderson Cancer Center, Houston, USA
EDITOR COMMENT
The best friend of the HPB surgeon is the intervention al radiologist. Advanced laparoscopic HPB surgery can be done safely only in an
environment where skillful interventional radiology exists. Therefore excellent communication between HPB surgeon and interventional
radiologist is critical for accurate diagnostic and challenging therapeutic interventions. This chapter reviews the important role that
interventional radiology plays in the management of HPB patients from diagnosis to management of surgical complications. In addition,
options for unresectable patients (i.e. chemoembolization, radioembolization, and thermal ablation) are presented.
Keywords: biopsy, drainage, interventional radiology, locoregional therapy, palliation
7.1 Diagnosis
Percutaneous biopsy is one of the most commonly performed procedures in radiology departments [1]. Traditionally, the role of image-guided biopsy was to
differentiate benign from malignant disease, to stage
known malignancy, and to culture an organism in the
case of infection. The recent explosion of molecular
techniques (i.e. immunohistochemistry staining, polymerase chain reaction, fluorescence in situ hybridization,
and gene sequencing) has expanded these baseline indications to include molecular profiling and genomic analysis of oncological specimens to guide treatment.
Percutaneous techniques are particularly well suited for
the liver, while lesions originating from the biliary system
and pancreas should be evaluated on a case-by-case basis.
The liver is the most common solid organ biopsied in
the abdomen and pelvis. The liver tolerates needle transgression well, with percutaneous techniques yielding an
accuracy of approximately 96% for focal liver lesions [2].
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.
Major complications are rare and include hemorrhage,
abscess, and needle track seeding. The risk of hemorrhage
can be minimized by choosing a biopsy path which transgresses at least 1 cm of normal liver parenchyma. Plugging
the biopsy track with gelatin particles and coils has been
described to decrease the risk of hemorrhage following
biopsy [3,4].
Percutaneous biopsy of the pancreas and biliary system
has largely been supplanted by endoscopic techniques
utilizing brush cytology, forceps biopsy, and endoscopic
ultrasound-guided fine needle aspiration (EUS-guided
FNA). When endoscopy has failed or is contraindicated,
needle biopsy of the pancreas can be used to effectively
delineate focal pancreatitis, malignancy, and metastasis.
Sensitivity of computed tomography (CT)-guided pancreatic biopsy for pancreatic neoplasm ranges from 45%
to 90% [5,6] (Figure 7.1). A concern with pancreatic
biopsies is the potential for peritoneal tumor s eeding [7]. This concern, however, is diffi cult to substantiate, given that many of these patients are inoperable
100
Interventional radiology for hepatopancreatobiliary diseases 101
Figure 7.1 Axial CT image during CT-guided biopsy of a pancreatic tail mass (arrows). Biopsy needle passes anterior
to the spleen (arrowhead).
and suffer from limited survival, making tissue confirmation and long-term imaging follow-up difficult.
Needle biopsy of the biliary system can be accomplished when the obstructing lesion, such as cholangiocarcinoma, is visible with US, CT, or is located
adjacent to an endoscopically placed stent. For biliary
strictures, brush biopsy can be performed, though
diagnostic yield is limited. In a study of 65 patients
over a five-year period, Rabinovitz et al. found that
biliary brushing from a percutaneous approach was
useful to exclude malignancy, especially after multiple
attempts with a probability of 6% of having bile duct
carcinoma following three sequential negative cytological brushings [8].
In addition to percutaneous tissue acquisition, interventional radiologists are occasionally asked to evaluate
patients with persistent hypoglycemia due to endogenous
insulin production. When insulinoma, often associated
with multiple endocrine neoplasia type 1, or nesidioblastosis, a form of acquired hyperinsulinism, are potential
diagnoses, preoperative localization is crucial to guide
surgical resection. In spite of recent advances in imaging,
localizing pancreatic lesions <2 cm in diameter and differentiating them from other lesions is challenging.
Therefore, calcium arterial stimulation with hepatic
venous sampling (ASVS) was developed by Doppman
et al. in 1989 to localize insulin-secreting tumor cells
to regions of the pancreas based on arterial supply [9]
(Figure 7.2). The physiological rationale of the test is that
a high concentration of extracellular calcium triggers
release of insulin from insulinoma cells, while there is
no increase in insulin secretion from normal pancreatic
β-cells. ASVS has the highest accuracy for localization of
insulinomas (84–88%), in comparison with magnetic
resonance imaging (43%), arteriography (36%), CT
(17%), and transabdominal US (17%) [10,11]. ASVS is
especially important in the era of laparoscopic surgery,
where accurate localization of lesions may help surgeons
determine which procedures are amenable to laparoscopy versus laparotomy.
102 Chapter 7
Figure 7.2 Pancreatic blood supply.
7.2 Interventional radiology
management of postoperative
complications
7.2.1 Catheter drainage of postoperative
fluid collections
Following laparoscopic liver resection, intra-abdominal
abscess, intra-abdominal fluid collection not otherwise
specified, and liver abscess are relatively infrequent occurrences with a combined frequency of approximately
0.5% [12]. Percutaneous drainage can be safely performed
with CT, US, or a combination of US with fluoroscopy. In a
prospective multicenter trial of 96 patients with 137 intraabdominal abscesses, percutaneous catheter drainage was
effective as a single treatment in 70% of patients and
increased to 82% with a second attempt [13]. In subgroup
analysis, the success varied by the organ of origin: appendix, 95% (18/19); liver or biliary tract, 85% (17/20); colon
and rectum, 78% (21/27); pancreas, 58% (7/12); other,
100% (18/18) (analysis of variance; P = 0.04). Importantly, negative predictors of successful outcome included
the presence of yeast (odds ratio [OR]= 0.63; 95% confidence interval [95% CI] 0.51–0.78; P < 0.001) and pancreatic origin (OR = 0.78; 95% CI 0.63–0.96; P = 0.002).
The mainstays of the treatment of pyogenic liver
abscesses are catheter-directed drainage and antibiotics [14]. However, in the setting of hepatobiliary-pancreatic malignancy, percutaneous drainage is successful in
only 66% of cases [15]. Independent predictors of failure
include presence of yeast, biliary communication, and
multiloculation [15,16]. Lai et al. found that patients who
fail management with percutaneous drainage have a
significantly higher mortality than patients successfully
treated (60% versus 17%, P = 0.007) [16].
Subphrenic abscesses are typically encountered in the
postoperative patient following surgery involving the
Interventional radiology for hepatopancreatobiliary diseases 103
liver, pancreas, stomach or spleen. The pleura is attached
to the eighth rib anteriorly, 10th rib laterally, and 12th rib
posteriorly.Ideally, the drainage approach of a subphrenic
abscess follows an extrapleural approach to avoid
contamination of the pleural space by infected abdominal
contents.This angled approachcan be obtained most easily
with ultrasonography, allowing direct, real-timevisualization using an off-axis approach [17] (Figure 7.3).
Figure 7.3 A 48-year-old man with pancreatic tail cancer at postoperative day 5 from distal pancreatectomy and splenectomy
presents with fever and left upper upper quadrant pain. (a) Thick-slab coronal reformatted CT image of the upper abdomen
demonstrates a fluid collection (arrows). (b) Given the location of the collection immediately underneath the diaphragm, there is the
potential risk of causing an ipsilateral empyema with placement of a drainage catheter through the pleural space. Volume-rendered
CT image demonstrates the steep trajectory of the drainage catheter (arrow) entering the abdomen below the 12th rib to avoid the
pleural space. (c) Thick-slab coronal reformatted CT image of the upper abdomen 10 days following drainage catheter placement
(black arrow) demonstrates near-complete interval resolution of the subphrenic fluid collection. The patient’s fever and left upper
quadrant quickly subsided after catheter placement. Source: Reproduced with permission of Sanjay Gupta MD.
104 Chapter 7
However, shadowing from adjacent bones and air-filled
loops of bowel may obscure visualization. CT is limited to
the axial plane, but the ability to angle the gantry up to 30°
allows some limited flexibility in needle placement. An
alternative to angling the gantry is the triangulation
method [18]. While every attempt to avoid the pleural
space should be made, most patients with a subphrenic
abscess will be successfully drained following either
extrapleural or transpleural catheter drainage. In a study
of 62 patients with subphrenic abscesses treated percutaneously, catheter-directed drainage was successful
in 85% of cases [17]. Six (10%) patients in this study
were drained through an intercostal approach, with one
patient developing an empyema. Concern about transgression of the pleural space to drain an infected subphrenic collection may be mitigated by the fact that the
pleural space adjacent to an inflammatory reaction arising
from the adjacent abscess can be obliterated. In a small
study of 28 drainageprocedures for left subphrenic abscess
following splenectomy, 20 drainages were transpleural
and eight were extrapleural [19]; no patient developed
empyema. At the authors’ institution, every attempt is
made to follow an extrapleural approach. When a transpleural route is used, the authors prefer to place an ipsilateral pleural drainage catheter.
Following pancreatic surgery, fluid collections from anastomotic leaks of gastrointestinal, biliary or pancreatic origin
develop in 29–34% of patients [20–24]. The presence of a
fluid collection does not warrant immediate intervention, as
many postoperative pancreatic leaks are simple and resolve
spontaneously [25]. In the setting of inadequate drainage by
surgical drains, signs of suprainfection (e.g. rim enhancement, air) or patient decompensation (e.g. pain, leukocytosis, fever, tachycardia), interventional radiologists may be
asked to place a drainage catheter (Figure 7.4). Depending
on fluid viscosity, catheters as large as 30 Fr may be needed,
with inadequate catheter size representing a known independent predictor of drainage failure [20]. Cronin et al.
examined catheter-directed management of peripancreatic
fluid collections in a single-center retrospective review of
51 patients who underwent 57 image-guided procedures
following distal pancreatectomy [20]. The primary clinical
success rate, defined as resolution of the peripancreatic
collection with percutaneous drainage only, was 60%.
Owing to the complex nature of peripancreatic collections
and the relatively high rate of pancreatic fistulas following
surgery, 20 of 57 cases (35%) required secondary catheter
manipulation, ERCP or stenting to resolve the collection and
seal the leak. The success of catheter-directed drainage
increased to 95% following secondary intervention, obviating the need for re-exploration.
The importance of identifying a pancreatic fistula cannot be overstated as fistulas are difficult to treat and may
lead to recurrent collections if the catheter is prematurely
removed. Fluid location following pancreatic surgery is
important as location adjacent to the pancreas has been
Figure 7.4 A 62-year-old man with pancreatic head adenocarcinoma, who is nine days post pancreaticoduodenectomy, presents with
fever and elevated white blood cell count. (a) Axial image from a CT scan with contrast demonstrates a rim-enhancing collection in the
surgical resection bed (arrowheads). (b) Axial image from a CT scan following CT-guided placement of a 12 Fr drainage catheter; 30 mL of
purulent fluid was aspirated. Follow-up CT scan (not shown) performed two weeks later demonstrated resolution of the collection.
Interventional radiology for hepatopancreatobiliary diseases 105
shown to correlate with pancreatic duct leaks [24,26]. In
the study by Cronin et al., the authors noted that amylase
was present in 88% of the collections drained (mean
11 557 IU/L, range 33–68 915 IU/L); however, the number of patients with a pancreatic fistula, as defined by the
International Study Group [27] as output on or after
postoperative day 3 with amylase content >3 times serum
amylase, was unclear. The high reintervention rate of
patients in their study (35%) suggests that many of the
collections represented pancreatic fistulas. Cabay et al.
reported on 20 patients with external pancreatic fistulas
treated by percutaneous drainage [28]. Treatment was
successful in 16 of 20 patients with high-output fistula
(>200 mL/day), but only two of four patients with lowoutput fistula. Thus, while pancreatic fistulas are difficult
entities to treat, conservative management with percutaneous catheter-directed drainage appears to be a
reasonable alternative following medical management.
7.2.2 Biliary duct injury with and
without biloma
Iatrogenic injury to the biliary system is relatively rare,
occurring most often following laparoscopic cholecystectomy with an incidence of 0.6% [29–31]. Optimal management is provided by a multidisciplinary team
incorporating hepatobiliary surgeons, endoscopists, and
interventional radiologists. Initial management of bile
duct injury is focused on draining any collections, biliary
diversion, and completely characterizing the injury.
Image-guided catheter drainage of collections with communicationto the biliary tree is morelikely to be successful
than collections with a communication to the pancreatic
duct. In a retrospective review of 57 patients, the success
rates of catheter drainage for abdominal collections containing biliary and pancreatic ductal communication were
93% (39/42) and 67% (10/15), respectively (P = 0.01) [32].
Delayed drainage of bilomas is associated with abscess
formation, cholangitis, and sepsis [33].
When biliary injury is suspected, endoscopic or percutaneous biliary drainage is often requested. The goal
of biliary drainage is to eliminate the transpapillary
pressure gradient to prevent extravasation at the site of
the leak. Endoscopic therapy is larg ely successful with
postcholecystectomy biliary leak, preventing any additional surgery. When there is complete ductal ligation,
injury to an intrahepatic duct or ligation of an aberrant
right hepatic bile duct, percutaneous transhepatic
cholangiography with biliary drain placement is often
needed for diagnosis and decompression [34– 38]
(Figure 7.5). Percutaneous drainage of nondilated biliary
systems is technically challenging, with a success rate of
65–75% [39]. Some patients may require more than one
session to place a drainage catheter, and in some cases, the
area of extravasation may not be crossed.
Biliary drainage will not be effective when the injury
does not communicate with the common bile duct and
small bowel. In these cases, some authors advocate the
use of repeated ethanol injection to sclerose the biliary
epithelium [40,41]. Others have described the use of glue
(n-butyl-cyanoacrylate) to obliterate the isolated duct(s)
and seal the fistula [42–44]. Though the data on utilizing
glue arise from small retrospective case series, the early
clinical success warrants further attention.
7.2.3 Arterial injury
Intra-abdominal bleeding following laparoscopic liver
resection is a relatively rare occurrence with a frequency
of 10 out of 2804 (0.4%) patients [12]. Postpancreatectomy hemorrhage occurs in less than 10% of patients but
accounts for 11–38% of mortality [45]; it is also correlated
with bile leaks, pancreatic fistula, abscess, and sepsis [46–48]. Hemorrhagic scenarios include gastroduodenal artery stump leak, common and proper
hepatic artery erosion, celiac axis erosion, splenic artery
erosion, inferior pancreaticoduodenal artery aneurysm,
and arc of Buehler aneurysm and pseudoaneurysm [49].
Depending on the location, embolization can be performed with coils, absorbable gelatin powder, n-butylcyanoacrylate, thrombin or flow-diverting stent grafts.
Arterial embolization of postpancreatectomy hemorrhage
is successful in 77–88% of cases (Figure 7.6) [50,51].
7.2.4 Portal venous hypertension
7.2.4.1 Prehepatic portal hypertension from portal
vein obstruction
Prehepatic portal hypertension can result from hypercoagulable states (portal vein thrombosis), alterations in
the portal vein wall from adjacent inflammation or surgery, and in association with malignancy (e.g. hepatocellular carcinoma [HCC], pancreatic cancer, bile duct
cancer) [52,53]. Based on results from small retrospective
studies, transhepatic portography with stent placement
appears to be an effective procedure to relieve portal
hypertension in patients with prehepatic portal vein
106 Chapter 7
Figure 7.5 A 62-year-old man with pancreatic cancer status post pancreaticoduodenectomy. Postoperative course was complicated
by an intrahepatic biloma. (a) Coronal reformation from a CT scan obtained two months following pancreaticoduodenectomy
demonstrates a low-density intrahepatic fluid collection (arrow). (b) Intrahepatic fluid collection (arrow) was aspirated through a
22 gauge Chiba needle yielding bile with ultrasound guidance. A 12 Fr drain was subsequently placed. (c) One month following
drainage, contrast injection through the intrahepatic biloma drainage catheter (thick arrow) demonstrated multiple segment VIII
biliary radicles (thin arrows). A segment of the biliary tree was conspicuously absent (arrowhead) and likely represented the region of
injury. (d) The biloma drainage catheter was successfully converted into an internal/external biliary drain, which crossed the
segment of biliary injury. Six weeks later, the previously injured intrahepatic duct is normal (arrowheads) and communicates with
the remainder of the biliary tree. The intrahepatic biloma was also resolved (not shown).
obstruction (Figure 7.7) [53,54]. In a study of 14 patients, 7.2.4.2 Portal hypertension and malignancy
Novellas et al. found that symptoms of portal venous The transjugular intrahepatic portosystemic shunt
hypertension were relieved in 10 patients (71%) follow- (TIPS) is a mainstay in the treatment of complications
ing stent placement [54], with occlusion rates ranging of portal hypertension. It hasbeenproventhatearly
from 21% to 40% [53,54]. The reason for occlusion use of TIPS could control acute variceal hemorrhage
appears to be a combination of tumor in-growth and with significant reductions in treatment failure and
thrombosis [55]. mortality [56]. We reported our pre liminary e xperie nce
Interventional radiology for hepatopancreatobiliary diseases 107
Figure 7.6 A 68-year-old man two days post pancreaticoduodenectomy for ampullary adenocarcinoma presents with an acute drop
in hematocrit. (a) Superior mesenteric arteriography demonstrates a replaced right hepatic artery. There is a large subcapsular
hepatic hematoma, as evidenced by the space between the diaphragm and enhancing liver margin (double arrow). (b) Left hepatic
arteriogram demonstrates frank extravasation of contrast from a branch of a segment IVb hepatic artery. (c) The injured hepatic
segment IVb branch was successfully coil embolized (arrow) and the patient’s hemodynamic status immediately improved.
Source: Reproduced with permission of Sanjay Gupta MD.
with TIPS in oncology patients and f ound that TIPS
could be performed safely without increasing procedure-related complications [57]. We encountered no
overt tumor seeding, despite shunt formation through
tumor in nin e patients. In our series, all TIPS were
created with bar e metal stents. With the use of polytetrafluoroethylene-covered stent grafts designed specifically f or TIPS proce dures [58], the theoretical risk of
tumor seeding from TIPS which traverse tumor is likely
reduced further.
108 Chapter 7
Figure 7.7 A 52-year-old woman with pancreatic cancer presents with ascites requiring serial large-volume paracentesis. Cytology
from the fluid failed to demonstrate malignant cells. (a) Coronal reformation from a CT scan demonstrates a mass in the pancreatic
head (arrowheads) and narrowing of the portal vein (arrow). (b) Transhepatic portography through a 5 Fr Kumpe catheter (Cook
Medical Inc., Bloomington, IN) advanced to the portal vein stenosis demonstrates high-grade, short-segment narrowing of the
superior mesenteric vein (arrow) and inferior mesenteric vein (arrowhead). There is an incidental biliary stent. (c) Venogram
following placement of an 8 mm balloon-expandable stent (arrow) across the segment of SMV stenosis demonstrates brisk flow into
the portal vein. The patient’s ascites subsequently resolved.
7.3 Image-guided locoregional
therapy of hepatobiliarypancreatic malignancy
external beam radiation, ablation, and transarterial embolization. Only 10–20% of patients with HCC and metastatic
colorectal carcinoma (CRC) are amenable to surgical resec-
tion [59,60]. Ablative and transarterial techniqueshave been
Therapy for liver cancer includes surgical resection, hepatic
transplantation (in cases of HCC), systemic chemotherapy,
developed as minimally invasive options to treat patients
who would otherwise be unsuitable for liver surgery.
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