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CHAPTER 19 

Magnetic resonance imaging of the liver, biliary


tract, and pancreas
Scott R. Gerst and Richard Kinh Gian Do

Magnetic resonance imaging (MRI) is a cross-sectional multi- tissues. Differences in T1 and T2 times intrinsic to various soft
planar imaging technique (Fig. 19.1). MRI uses magnetic fields tissues can be exploited to improve image contrast and diag-
and radiofrequency pulses to generate images with outstanding nostic accuracy. For example, free water, which has a long T1
tissue contrast and excellent spatial resolution. The principles relaxation, is low signal on standard T1-weighted imaging and
of nuclear magnetic resonance were first described in the 1940s markedly high signal on T2-weighted imaging. Thus so-called
by Bloch and colleagues (1946) and Purcell and colleagues heavily T2-weighted imaging sequences, such as those used in
(1946) as a method for in vitro chemical analysis. Several MR cholangiopancreatography, highlight high water content
decades later, Damadian (1971) and Lauterbur (1973) applied structures, such as bile and pancreatic ducts, while reducing
some of these basic principles to design MRI to allow in vivo the signals of other organs.
imaging. Today, MRI is used extensively as a medical imaging Diffusion-weighted MRI (DWI) is an alternative tissue con-
tool throughout the body to visualize and distinguish normal trast mechanism that produces images dependent on the local
and pathologic tissue. magnitude of water diffusion. DWI of the liver may be used to
help detect focal hepatic lesions, especially metastases, and may
PRINCIPLES OF MAGNETIC also be used to assess changes in the liver parenchyma, such as
RESONANCE IMAGING liver fibrosis. Tremendous interest in this sequence first arose
due to its increased sensitivity to early changes in the brain after
MRI harnesses the signal available from the magnetic moment a cerebrovascular accident compared with more traditional T1-
or spin present in certain nuclei, including hydrogen atoms. or T2-weighted imaging. Applications for DWI in body imaging,
When placed in a large static magnetic field, the nuclei align initially hampered by hardware and software limitations, were
themselves in a parallel or antiparallel direction to the field and addressed in the mid-2000s. With new advances in receiver coil
also rotate or spin at a precise frequency termed the Larmor design, improved gradient coils used to acquire images, and
frequency. This frequency depends on the specific type of nuclei motion correction through respiratory or navigator techniques,
imaged and the strength of the magnetic field. The most com- DWI has flourished as a functional imaging sequence in hepa-
monly imaged nucleus in clinical practice is hydrogen (H1) topancreatobiliary imaging (Taouli et al, 2010).
because of its great abundance in the human body, mostly in
the form of water. Other nuclei that may be imaged by MRI MAGNETIC RESONANCE IMAGING SAFETY
include phosphorus (P31), sodium (Na23), and carbon (C13).
When unperturbed in a static magnetic field, nuclei with MRI is safe for most patients. However, physicians and
magnetic spins are in equilibrium: An almost an equal number patients should be aware of some important considerations,
of nuclei are in an “up” (parallel) or “down” (antiparallel) such as MR contrast safety, and the risk of interactions
alignment. The slight difference between the two states creates between the patient (including their implants) with the strong
a net magnetic moment. A measurable signal is generated from static magnetic field of the scanner as well as the RF field
the magnetic moment after excitation by a radiofrequency (RF) used to generate images. The magnetic field interactions are
pulse at the resonance Larmor frequency. This signal is gener- potentially dangerous by causing the motion of ferromagnetic
ated as the excited nuclei in the body return to equilibrium, aneurysm clips or causing electronic malfunctioning of cardiac
releasing energy in the form of an electromagnetic field that is pacing devices and defibrillators. Many MRI facilities have
captured by a receiver coil. The strength of this emitted signal screening programs in place to address potentially contraindi-
determines the signal intensity (SI) of a tissue. The precise cated devices, under new MRI safety guidelines proposed by
tissue SI depends on several factors, including longitudinal the American College of Radiology (Expert Panel on MR
relaxation (T1), transverse relaxation (T2), proton density Safety, 2013). However, referring physicians should be aware
(essentially the number of nuclei present), and flow. Some of of their local imaging centers’ approach to MRI safety, such
these factors can be manipulated (e.g., through T1 and T2 as their ability to scan patients with MR-conditional or
weighing) to create images highlighting various soft tissue MR-unsafe pacemakers, for example.
properties. MRI has a role in patients with minimal or mild renal insuf-
All tissues have an intrinsic T1 value for relaxation along the ficiency. Iodinated contrast used in CT is associated with a risk
longitudinal magnetic axis, which varies between 200 and 800 of contrast-induced nephropathy; however, administration of
milliseconds. T2 time, or transverse relaxation, is a measure of intravenous gadolinium contrast agents in patients with severe
signal loss perpendicular to the long axis of the magnetic field renal insufficiency carries a risk of nephrogenic systemic fibrosis
and typically varies between 20 and 200 millisecconds for most (NSF). NSF is a serious and potentially fatal complication

358
Chapter 19  Magnetic resonance imaging of the liver, biliary tract, and pancreas 359

C
FIGURE 19.1.  Multiplanar T2-weighted images through the liver in a patient with multiple hepatic metastases. A, Axial image. B, Sagittal image.
C, Coronal image. A variety of techniques can be used to obtain these images. Note that fluid-containing structures, including small bowel (curved
arrow, A), gallbladder, biliary tree, and pancreatic duct (arrow, C), are bright.

related to free gadolinium deposition within soft tissues and an important role in imaging benign disorders, as well as com-
organs, with resulting scleroderma-like fibrosis. The exact prehensive evaluation of malignancies of the biliary system
causal mechanism of NSF remains unknown, but the risk of (Mandelia et al, 2013; Singh et al, 2014; Vaishali et al, 2004).
NSF increases in patients with a glomerular filtration rate Heavily T2-weighted images are used to provide an overview
(GFR) less than 30 mL/min, and particularly in patients with of biliary and pancreatic ductal anatomy, removing the signal
severe, end-stage disease (GFR < 15 mL/min). In addition, of surrounding structures. Excellent diagnostic-quality images
linear agents with lower thermodynamic stability carry a greater are obtainable, with high sensitivity and specificity for evalua-
risk than others. If available, more stable, lower-risk macrocy- tion of ductal dilatation, strictures, and intraductal abnormali-
clic agents can be used in patients with a GFR less than 30 mL/ ties (Hekimoglu et al, 2008; Palmucci et al, 2010a; Palmucci
min. Gadolinium contrast usage in patients with a GFR less et al, 2010b; Sandrasegaran et al, 2010). Cross-sectional
than 15 mL/min should only be performed if essential, after images and maximum intensity projection images (Fig. 19.2)
careful evaluation of risks versus benefits, and with consultation are produced with current MRCP techniques, and projection
with a nephrologist, if available. Since NSF was initially images are similar to direct contrast-enhanced cholangiograms
described, the rapid international investigation, dissemination obtained with either endoscopic retrograde cholangiopancrea-
of information, and swift adjustment to policy have led to a tography (ERCP) or percutaneous transhepatic cholangiogra-
precipitous drop of reported NSF cases. In multiple countries, phy (PTC; see Chapter 18). MRCP is noninvasive, eliminating
NSF has essentially disappeared since 2009 (Bennett et al, the potential morbidity associated with ERCP or PTC (Zhong
2012; Grobner, 2006; Idee et al, 2014). et al, 2004).
The basic principle of MRCP is to use T2-weighted imaging
MAGNETIC RESONANCE IMAGING to highlight stationary or slowly moving fluid, including bile, as
CHOLANGIOPANCREATOGRAPHY high in signal intensity; surrounding tissues, including retroperi-
toneal fat and the solid visceral organs, with shorter T2 values,
MR cholangiopancreatography (MRCP) is an imaging tech- are markedly reduced in signal. In addition to heavilyT2-weighted
nique used to evaluate the bile and pancreatic ducts and plays sequences, MRCP protocols also include routine intermediate
360 PART 2  DIAGNOSTIC TECHNIQUES

A B

C D
FIGURE 19.2.  Mixed main- and branch-duct intraductal papillary mucinous neoplasm (IPMN) of the pancreatic tail. A, Coronal T2 image. A lesion
with high T2 signal indicating cystic contents involves the pancreatic tail and shows multiple thin septations (arrow). B, Coronal three-dimensional
maximum intensity projection T2-weighted magnetic resonance cholangiopancreatography image. The multiseptated cystic pancreatic tail mass is
apparent (arrow). C, Axial T2 image. Multiple septations are apparent with dilated main pancreatic duct (star). Incidental note is made of a right renal
cyst with thin septations (open circle). D, Axial T1-weighted fat saturation image postintravenous gadolinium contrast. The numerous septations
enhance within the lesion (arrow). Some components appeared nodular, and the lesion was resected. Histopathology revealed an IPMN with a focus
of noninvasive mucinous cancer.

T2-weighted sequences and T1-weighted sequences to evaluate enhancement patterns between benign and malignant liver
surrounding structures. MR-specific techniques for obtaining lesions have been well reported and are discussed in individual
cholangiographic images include breath-hold, as well as respira- entities later.
tory and navigator gated techniques, which can generate images Several new hepatobiliary-specific contrast agents have been
in a patient during free breathing. developed to add additional functional information compared
with traditional ECF contrast agents. These hepatobiliary spe-
MAGNETIC RESONANCE IMAGING cific contrast agents are taken up to varying degrees by function-
CONTRAST AGENTS ing hepatocellular tissue and are excreted in bile as well as
through the kidneys. Hepatobiliary specific agents include
MRI contrast agents work primarily by altering the intrinsic T1 mangafodipir trisodium, gadobenate dimeglumine, and gadox-
relaxation times of various soft tissues where contrast accumu- etic acid (Gd-EOB-DTPA). Both gadobenate dimeglumine
lates. In the hepatobiliary system, MRI contrast agents can (MultiHance; Bracco Imaging, Cranbury Township, NJ) and
improve the detection of liver lesions and improve the charac- gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid
terization of focal liver abnormalities. MRI contrast agents for (Eovist/Primovist; Bayer Healthcare, Wayne, NJ) have been
hepatobiliary imaging are divided into two basic categories: approved in the United States. These contrast agents are all
extracellular fluid contrast (ECF) agents, and those with addi- administered intravenously, although the dose and pharmaco-
tional hepatobiliary excretion. In the past, the most commonly kinetics are different. These two agents are sometimes referred
used contrast agents were the ECF agents, such as gadopen- to as combination agents because of their dual capacity for
tetate dimeglumine (gadolinium diethylenetriaminepentaacetic imaging both in the dynamic phase (as done routinely with ECF
acid [Gd-DTPA]), which is distributed within the intravascular agents) and in the delayed, hepatocyte-specific phase. These
compartment initially and rapidly diffuses through the extra- agents provide comprehensive information about the hepatic
vascular space, similar to the action of iodinated contrast agents parenchyma, bile ducts, and liver vasculature (Burke et al,
in computed tomography (CT; see Chapter 18). Differences in 2013; Seale et al, 2009).
Chapter 19  Magnetic resonance imaging of the liver, biliary tract, and pancreas 361

NORMAL HEPATIC APPEARANCE ON or focal. The pattern of fatty liver is related to regional differ-
MAGNETIC RESONANCE IMAGING ences in perfusion. It may be difficult to distinguish focal fat
from focal hepatic lesions on CT because both appear low in
MRI is routinely used to evaluate diffuse and focal liver abnor- attenuation. Additionally, focal fatty sparing may appear similar
malities. With liver MRI, a combination of precontrast T1, T2, to an enhancing neoplasm on contrast-enhanced CT. Although
and DWI sequences are used. Normal hepatic parenchyma is geographic margins and location may aid in the diagnosis, this
brighter (hyperintense) than the spleen on T1-weighted images, is more readily distinguished on MRI due to different signal
whereas on T2-weighted images, the spleen is relatively brighter characteristics. T1-weighted in-phase and out-of-phase imaging
than the liver (Fig. 19.3). Although most hepatic lesions are allows differentiation of signals from fat and water when they
low in signal intensity on T1-weighted images, they have more are present in the same voxel, as it exploits minute differences
variable intensity on T2-weighted images, with cysts and hem- in resonance frequencies between fat and water protons (Fig.
angiomas having the highest T2 signal intensity in general. 19.4). Using fast gradient-echo techniques, fat and water
Precontrast and postcontrast T1-weighted imaging is also per- protons that share the same voxel will be imaged both “in phase”
formed to assess enhancement patterns of the liver parenchyma or 180 degrees “out of phase.” Tissues that have relatively equal
and liver lesions. If a hepatobiliary contrast agent is used, addi- quantities of fat and water will appear dark on the out-of-phase
tional delayed hepatobiliary phase images are acquired. sequence because the signals from fat and water are “opposed
in phase” and can cancel each other out (Boll et al, 2009;
DIFFUSE HEPATIC DISEASE Springer et al, 2010). Areas of fatty sparing will remain hyper-
intense relative to the surrounding fatty liver on out-of-phase
Fatty Liver imaging. On standard T1-weighted imaging, areas of focal fat
Fat may accumulate within hepatocytes for many reasons, can show increased signal. The appearance on T2-weighted
including alcohol intake, diabetes, medications, and obesity (see images depends on the type of sequence acquired and whether
Chapters 71 and 100). Hepatic steatosis may be diffuse, patchy, fat saturation is used. The ability of MRI to exploit those signal

A B

C
FIGURE 19.3.  Normal hepatic magnetic resonance image. A, T1-weighted spin-echo image. The liver is brighter (hyperintense) relative to the signal
of the spleen. There are normal flow voids that appear as dark areas in the visualized vessels (straight arrow, intrahepatic portion of the inferior vena
cava; curved arrow, aorta). B, T2-weighted fast spin-echo image. Because of reversal of the liver/spleen contrast, the normal spleen is brighter than
the liver. Note the flow voids within the vessels (straight arrow, intrahepatic portion of the inferior vena cava; curved arrow, aorta). C, Postcontrast
T1-weighted gradient-echo image. Normal enhancement in the liver and spleen is evident, and the parenchyma of both is about equal in this phase
of the injection. All the vessels are bright as a result of the T1 shortening effect of gadolinium (straight arrow, intrahepatic portion of the inferior vena
cava; curved arrow, aorta).
362 PART 2  DIAGNOSTIC TECHNIQUES

A B

C D

E
FIGURE 19.4.  Focal fat within the liver. A, Non–contrast-enhanced computed tomography image in a young adult with history of testicular cancer
shows heterogeneous regions of low attenuation in the right hepatic lobe (arrows). B, T1-weighted in-phase image at the same level now shows
signal abnormality in this region. C, T1-weighted out-of-phase image shows geographic areas (arrow) that have lost signal. On the out-of-phase
images, a black line “India ink effect” surrounds tissue interfaces. D, T1-weighted fat saturation precontrast image also shows mild signal loss in this
area (arrow). E, T1-weighted fat saturation postcontrast image. The area in question has normal vascularity coursing through it; no mass was
present—the typical appearance of fatty infiltration.
Chapter 19  Magnetic resonance imaging of the liver, biliary tract, and pancreas 363

differences, as well as to apply diffusion-weighted and postcon-


trast imaging, offers an advantage over CT when evaluating for Cysts
focal lesions on a background of hepatic steatosis. Cysts are common hepatic lesions that may be sporadic (see
Newer, breath-hold three-dimensional (3D) T1 techniques Chapters 75 and 90B) or associated with polycystic disease of
with interpolation allow fast single breath-hold acquisition with the kidney (Fig. 19.6). Small cysts (<1 cm) may be difficult to
added fat and water separation (Bashir et al, 2012). Enhance- characterize on CT because of volume averaging but are easily
ment characteristics also aid in the diagnosis, as focal fatty liver diagnosed by MRI. The MRI criteria for a simple cyst is a
enhancement should parallel surrounding normal hepatic nonenhancing lesion that is homogeneously low in signal inten-
parenchyma. This is important because other lesions, including sity on T1-weighted images and homogeneously very bright on
hepatocellular carcinoma (HCC) and adenoma, may contain T2-weighted images, similar to cerebrospinal fluid. Cysts main-
small quantities of fat within them (see Chapters 90A and 91). tain their markedly high signal on heavily T2-weighted images,
similar to fluid in the cerebrospinal fluid, bile ducts, and pan-
Iron Deposition Disease creatic duct.
Hepatic iron deposition may occur from primary genetic hemo-
chromatosis or from secondary nongenetic systemic overload Hemangioma
(see Chapter 76). Primary hemochromatosis is an autosomal Hepatic hemangiomas (see Chapter 90A) are benign tumors of
recessive genetic disorder characterized by abnormal intestinal the liver with an estimated incidence of 20% (Albiin, 2012).
iron absorption, with accumulation of iron in the nonreticulo- Most hemangiomas are thus commonly found incidentally on
endothelial organ system. This predominantly occurs in hepa- other imaging studies, such as CT or ultrasound. MRI is ideal
tocytes later in the disease when other viscera, including the for characterizing hemangiomas and is the preferred modality
pancreas and heart, are more likely to be involved. The liver for imaging. On T1-weighted images, hemangiomas are hypoin-
shows abnormally low signal intensity compared with spleen on tense compared with the surrounding hepatic parenchyma,
T1-weighted in-phase sequences. T1-weighted gradient-echo have smooth, well-marginated borders, and are frequently lob-
sequences are very sensitive for detecting the presence of iron ulated. Hemangiomas are markedly hyperintense compared
within the hepatic parenchyma due to the local field inhomo- with normal liver on T2-weighted images. Hemangiomas also
geneities caused by the presence of iron. Primary, or genetic, tend to retain a high signal on more heavily T2-weighted
hemochromatosis is important to diagnose because this entity sequences, almost to the same degree as cysts, and become
may be unnoticed until late in the disease process, and its long- more conspicuous compared with surrounding liver paren-
term sequelae include fibrosis, cirrhosis, and HCC. chyma. After the administration of contrast, the presence of
Nongenetic systemic iron overload from secondary causes peripheral nodular discontinuous enhancement, with either
can sometimes be distinguished from primary hemochromato- partial or complete filling in on successive postcontrast phases,
sis based on the pattern of organ involvement. Nongenetic has been shown to be highly accurate for the diagnosis of hem-
systemic iron overload is typically associated with multiple angioma (Fig. 19.7; Silva et al, 2009).
blood transfusions, myelodysplastic syndrome (MDS), or Dynamic contrast-enhanced MRI after administration of
abnormal iron absorption in patients with cirrhosis (Queiroz- intravenous gadolinium is useful for increasing the specificity
Andrade et al, 2009). In secondary iron overload, there is pre- of diagnosis of hepatic hemangioma and for differentiating this
dominant accumulation of iron in the reticuloendothelial lesion from others, including metastases and HCCs (Albiin,
system (RES), with splenic and bone marrow iron deposition 2012). Larger hemangiomas tend to follow these criteria more
early and hepatic deposition later. If the iron deposition is frequently, although giant hemangiomas also may have variable
limited to the RES only, it is termed hemosiderosis. If non-RES signal intensity and a central scar (Prasanna et al, 2010). Prob-
organ involvement is seen, it is termed secondary hemochroma- lems arise with smaller hemangiomas, however, which may
tosis. These distinguishing characteristics and the patient’s “flash fill” and appear as hypervascular, homogeneous lesions.
history often allow correct differentiation. MRI is excellent for These smaller lesions (usually <1 cm) may be distinguished by
identifying the abnormal signal intensity due to iron deposition, both their T2 signal characteristics and enhancement pattern
and gradient-echo imaging has been shown to reliably quantify paralleling enhancing vessels (Albiin, 2012). In addition, hem-
hepatic iron load (Fig. 19.5) (Mavrogeni et al, 2013; Queiroz- angiomas have higher apparent diffusion coefficient values
Andrade et al, 2009). Iron quantification may have indirect obtained from DWI than metastases (Miller et al, 2010).
added uses; for example, limited data suggest it may help Caution must be used when assessing enhancement using the
predict nonrelapse mortality prior to allogeneic stem cell trans- hepatobiliary contrast agent gadoxetate disodium, however, as
plant in patients with MDS and acute myeloid leukemia the overlapping extracellular phase and hepatobiliary excretion
(Wermke et al, 2012). of this contrast may confound the typical hemangioma enhance-
ment and lead to “pseudowashout” in late dynamic phase,
FOCAL HEPATIC LESIONS making characterization more difficult (Goshima et al, 2010).
For this reason, we prefer not to use gadoxetate as the contrast
The advantage of MRI over CT is in the improved characteriza- agent for initial liver lesion characterization and use a tradi-
tion of liver lesions by improved soft tissue contrast combined tional ECF agent instead.
with novel tissue contrast mechanism. We will discuss common Sclerosed hemangiomas represent a diagnostic challenge,
benign and malignant liver lesions and emphasize distinguish- often mimicking malignancies in the liver; limited data suggest
ing imaging characteristics. Familiarity with typical lesion T1 that increasing sclerosis shows corresponding decreased T2
and T2 signal, as well as enhancement characteristics, will aid signal and less avid enhancement, probably corresponding to
the clinician in developing an approach to assess the most com- areas of fibrosis. Adjacent capsular retraction and adjacent
monly encountered hepatic lesions. wedge-shaped transient perfusional changes, as well as size
364 PART 2  DIAGNOSTIC TECHNIQUES

A B

C D

E F

G
FIGURE 19.5.  Iron deposition. A, T1-weighted in-phase gradient-echo image (echo time [TE] 4.8) shows abnormal liver/spleen contrast. The liver
is homogeneously darker than the spleen from preferential deposition of iron within the hepatic parenchyma. This is a pediatric patient who had
undergone numerous transfusions while undergoing therapy for cancer. Note the difference from Figure 19.X. B, T1-weighted out-of-phase gradient-
echo image (TE 2.2) shows the liver/spleen contrast reverses, with the liver being brighter than spleen. This is opposite from Figure 19.X and shows
iron deposition disease within the liver. C, Axial T2-weighted fast spin-echo sequence shows marked low T2 signal within both liver and spleen. D-G,
Using T2-weighted multigradient-echo technique, there is progressive signal loss in the liver. This type of multiecho imaging allows estimation of iron
quantification using computer software.
Chapter 19  Magnetic resonance imaging of the liver, biliary tract, and pancreas 365

A B
FIGURE 19.6.  Hepatic cysts associated with polycystic kidney disease. A, Axial T2-weighted image at the level of the kidneys shows bilaterally
enlarged kidneys with multiple hyperintense cysts. Little normal renal parenchyma is present at this level, and multiple small hepatic cysts (arrow)
are seen. B, Coronal T2-weighted images through the kidneys show similar findings of enlarged kidneys containing multiple cysts (black arrows),
and small hepatic cysts are identified (white arrow).

decrease over time, may all offer clues to suggest the diagnosis, Hepatic Adenoma
but biopsy may be necessary for confirmation, depending on Hepatocellular adenomas (HCAs) (see Chapter 90A) also are
the clinical picture (Ridge et al, 2014). benign liver lesions, but unlike FNH, are associated with com-
plications, including abdominal pain, bleeding, and rarely,
Focal Nodular Hyperplasia malignant degeneration. HCAs are strongly associated with oral
Focal nodular hyperplasia (FNH; see Chapter 90A) is the contraceptive or steroid use and are more common in women
second most common benign tumor of the liver after heman- of childbearing age. Newer low-dose oral contraceptives have
gioma. Pathologically, FNH contains all the elements of normal a less strong association with HCAs. Although HCA may be
liver and may have a central fibrous scar, which shows delayed large at presentation, they are increasingly incidentally discov-
enhancement, and is surrounded by hepatocytes and small bile ered and often less than 4 cm in diameter (Grazioli et al, 2012).
ducts (see Chapter 89). FNH has been associated with oral Hemorrhage may be life threatening if it extends into the peri-
contraceptive use (Scalori, 2002) as well as chemotherapy in toneum. Although imaging characteristics vary, a combination
the pediatric age group (Do et al, 2011; Sudour et al, 2009). of features, including enhancement characteristics, intralesional
Most FNH are isointense to normal liver parenchyma on T1- lipid, and hypointensity on delayed hepatobiliary phase imaging,
and T2-weighted images, and a few are mildly T1 hypointense may help increase diagnostic confidence (Mohajer et al, 2012).
or minimally hyperintense on T2-weighted images (Fig. 19.8A Nonetheless, small adenomas without hemorrhage may be dif-
and B). When discussing relative T1 and T2 signal, a normal ficult to differentiate from FNH without a central scar and from
background liver parenchyma is assumed. In a liver with iron well-differentiated HCC.
deposition, which diffusely lowers the signal intensity of the Recently, distinct genetic subtypes of adenomas have been
liver parenchyma, T1 and T2 relative hyperintensity can be described and show differing behaviors, histopathology, and
expected. This may be seen, for example, in pediatric oncologic imaging features. These include inflammatory, hepatocyte
patients who have concomitant iron deposition (Do et al, nuclear factor-1α (HNF-1α–mutated), and β-catenin–mutated
2011). Frequently, FNH is visualized by displacement of the HCAs (see Chapter 89). Of note, some adenomas may be both
normal hepatic vasculature, and classic FNH shows strong β-catenin mutated and inflammatory. A group remains unclas-
arterial peak enhancement following administration of an intra- sified and encompasses other HCAs without any genetic abnor-
venous contrast agent, with lack of washout in portal venous or malities (Grazioli et al, 2013). Inflammatory HCA, the most
late dynamic phase imaging. common subtype (30% to 50% of HCAs) typically seen in
A common feature of FNH is the presence of a central scar. women with a history of oral contraceptive use, is generally
This distinguishing feature is hypointense on T1-weighted hypointense on T1 images, hyperintense on T2, and frequently
images and hyperintense on T2-weighted images with enhance- heterogeneous. They usually show moderate arterial enhance-
ment on delayed imaging beginning at approximately 3 minutes ment, persistent dynamic phase enhancement, and variable
by using ECF contrast agents (Fig. 19.8C) (Karam et al, uptake in delayed hepatobiliary phase (Grazioli et al, 2013).
2010). The presence of enhancement, similar to or higher- The enhancement pattern may reflect a mix of poorly function-
than-normal parenchyma, during the delayed hepatobiliary ing hepatocytes, arterioles without accompanying veins,
phase with a hepatocyte-specific contrast agent is expected for inflamed bile ducts, and dilated sinusoids. On MRI, small
the majority of FNHs. Of note, with the hepatobiliary agent amounts of intralesional lipid may be seen. A small percentage
gadoxetate disodium, a central scar, if present, does not usually of these HCA show contrast washout in late dynamic phases,
enhance relative to the hepatocytes present in this lesion. whereas others retain contrast similar to hemangiomas. Delayed
366 PART 2  DIAGNOSTIC TECHNIQUES

A B C

D E F
FIGURE 19.7.  Hepatic hemangioma undergoing sclerosis. A, Heavily T2-weighted image (echo time [TE] 150) shows a mass (m) that is hyperintense
to hepatic parenchyma with well-defined margins. B, Precontrast T1-weighted fat saturation image at the same level shows the mass to be low
signal compared with background parenchyma. C, T1-weighted postcontrast image in early portal venous phase shows peripheral nodular enhance-
ment within this mass (arrows). Portions of the lesion fail to show enhancement during this phase. D, Equilibrium phase T1-weighted image post-
contrast shows the lesion has partially filled in toward the central portion. This constellation of findings is typical for hepatic hemangioma. 
E-F, The same lesion 5 years later on T1-weighted postcontrast scans in portal venous and equilibrium phase imaging shows less avid enhancement
and has shown slight size decrease, consistent with developing sclerosis. Sclerosing hemangiomas may show size decrease with less avid enhance-
ment, associated capsular retraction, and lower T2 signal than nonsclerosed hemangiomas.

peripheral rim enhancement in hepatobiliary phase may also be malignant degeneration. They show moderate, often heteroge-
seen (Grazioli et al, 2013). neous arterial phase enhancement, which may persist but is
Hepatocyte nuclear factor-1α mutated HCAs (30% to 35% variable in late dynamic and delayed phases. Although T1
of HCAs) are almost exclusively seen in women and often show hypointensity and T2 hyperintensity are common, it is often
large amounts of intralesional lipid. They enhance less avidly heterogeneous. These lesions show diffuse glutamine synthetase
in arterial phase than inflammatory HCA and typically are expression from upregulation, although it may be heteroge-
homogeneously low in signal on delayed hepatobiliary phase. neous. This is in contradistinction to FNH, which shows map-
They may also remain low signal in portal venous or equilib- like glutamine synthetase expression distribution adjacent to
rium dynamic phases, but that may be due to the opposed- hepatic veins (Agarwal et al, 2014; Balabaud et al, 2013; Grazi-
phase property of postcontrast T1-weighted imaging (Grazioli oli et al, 2013).
et al, 2013). Unclassified HCA (10% of HCAs) have no specific genetic
β-Catenin–mutated HCAs (10% to 15% of HCAs) are asso- or histopathologic abnormalities. No specific imaging features
ciated with glycogen storage disease, androgen use, and have a have been identified for these lesions, although experience
male predilection; they also have a higher chance of undergoing remains limited due to their infrequent diagnosis.
Chapter 19  Magnetic resonance imaging of the liver, biliary tract, and pancreas 367

A B

C D
FIGURE 19.8.  Focal nodular hyperplasia (FNH). A, T2-weighted image shows a mass that is isointense to hepatic parenchyma (arrows). Centrally,
within this mass is a linear, hyperintense focus (arrowhead). B, A precontrast, T1-weighted gradient-echo image shows the mass (arrows) to be
mildly hypointense to liver. C, Arterial dominant phase T1-weighted gradient-echo sequence shows that the mass enhances intensely with respect
to hepatic parenchyma (arrows). The central focus, which was bright on the T2-weighted images, does not show enhancement on this phase of the
injection (arrowhead). D, Postcontrast equilibrium phase image shows the mass to be isointense to background hepatic parenchyma. The central
portion of scar shows delayed enhancement (arrowhead) characteristic of FNH.

Hepatic Abscess/Infection lesions, including hemangiomas or focal fat, may appear similar
CT is generally the modality of choice in recent postoperative to metastases when imaged with CT or ultrasound. In general,
patients in whom there is a clinical suspicion of a hepatic metastases are mildly hypointense on T1-weighted images and
abscess (see Chapter 72). Patients with more atypical symptoms are mildly hyperintense on T2-weighted images. Unless they are
may present a diagnostic dilemma. Although some patients necrotic, mucinous, or cystic, metastases are not as bright on
show symptoms suggesting abscesses, others do not, but T2-weighted images as hemangiomas or cysts and often become
patients suspicious for abscesses or bile leaks may be imaged less conspicuous with greater (longer echo time [TE]) T2
with MRI. Abscesses are usually hyperintense on T2-weighted weighting. A number of metastases are hypervascular and best
images with an irregular rim of intermediate signal intensity seen on arterial phase imaging, such as those arising from a
surrounding a hyperintense outer rim. Abscesses are generally primary neuroendocrine tumor, renal cell carcinoma, or intra-
hypointense on T1-weighted images, unless they have hemor- hepatic metastases from hepatocellular carcinoma. Most
rhage or proteinaceous debris within them. After administration metastases, however, are hypovascular and tend to have less
of contrast material, the rim enhances, whereas the central well-defined borders after contrast enhancement than other
portion does not. The imaging findings may overlap with malig- benign lesions (Fig. 19.9). During contrast administration,
nancies, including gallbladder cancer. Infected cystic hepatic metastases often show early peripheral marginal enhancement.
lesions also may occur, such as parasitic echinococcal infec- These peripheral rims may wash out and appear hypointense on
tions. Echinococcal cysts are typically multiloculated with inter- delayed images (Fig. 19.10). Larger metastases tend to have a
nal thin-walled daughter cysts, and typically show no internal thick irregular rim of enhancement representing viable tumor
enhancement. A peripheral low T1 and T2 signal rim, as well with areas of central necrosis. Multiple studies have demon-
as correlation with a history of possible exposure, may provide strated superior accuracy of hepatobiliary agent contrast-
added clues to the diagnosis (see Chapter 74) (Qian et al, enhanced MRI over contrast-enhanced CT (Lafaro et al, 2013).
2013). Both ECF and hepatobiliary agent contrast-enhanced MRI has
shown higher sensitivity and specificity than CT–positron-emis-
Hepatic Metastases sion tomography (PET) imaging as well, particularly for small
The liver is the most common site for the hematogenous spread (<1 cm) lesions, and hepatobiliary contrast-enhanced MRI
of malignant neoplasms (see Chapters 92 to 94). Other hepatic combined with PET imaging may offer added benefit (Donati
368 PART 2  DIAGNOSTIC TECHNIQUES

A B

C D
FIGURE 19.9.  Hepatic metastasis from colorectal carcinoma. A, T1-weighted image shows a low signal intensity metastasis (arrow) within segment
IVB of the liver. B, T2-weighted image shows the mass is mildly brighter than background hepatic parenchyma. C, Post–contrast-enhanced,
T1-weighted fat saturation image shows the lesion as centrally hypointense, in contrast to the normal surrounding hepatic parenchyma, with minimal
areas of marginal enhancement. D, Fused computed tomography/fluorodeoxyglucose–positron-emission tomography image confirms avid tracer
uptake within the lesion, consistent with active tumor. Note the differences in appearance from hemangioma (see Fig. 19.7).

et al, 2010; Maegerlein et al, 2015; Seo et al, 2011). Arterial of disease, progressing from benign to malignant, which occurs
phase imaging may also provide anatomic detail preoperatively; in response to hepatic parenchymal damage and scarring (Lee
however, CT angiography offers improved spatial resolution et al, 2012). The advantage of MRI in the evaluation of HCC
over MRI. is that areas of carcinoma show differences in signal intensity,
diffusion, blood pool, and functional hepatocyte enhancement
Hepatocellular Carcinoma and growth compared with regenerative or dysplastic nodules,
The diagnosis of HCC (see Chapter 91) on CT and ultrasound or background cirrhotic parenchyma. MRI also has an advan-
can be challenging. It is often associated with cirrhosis and tage over other modalities in assessing vascular invasion.
parenchymal heterogeneity (Fig. 19.11), increasing the diffi- Although HCC generally is hypointense on T1-weighted
culty in distinguishing focal hepatic lesions. Cirrhotic livers and hyperintense on T2-weighted images, and shows arterial
show both nodular hepatic contour and parenchymal multi- phase hyperenhancement with delayed dynamic phase washout,
nodular change. These nodules represent a spectrum, from signal intensity may be variable (Silva et al, 2009), particularly
regenerative or dysplastic nodules to HCC. These nodular for early HCC measuring less than 2 cm (Rhee et al, 2012).
lesions are generally thought to constitute a multistep spectrum On T2-weighted images, larger, more poorly differentiated
Chapter 19  Magnetic resonance imaging of the liver, biliary tract, and pancreas 369

A B

C D
FIGURE 19.10.  Hepatic metastasis from breast carcinoma. A, T2-weighted image shows a small lesion within the liver (straight arrow) that is mildly
hyperintense. Portal lymphadenopathy also is present (curved arrow). B, Pre-contrast-enhanced, T1-weighted gradient-echo image shows a well-
defined mass (arrow) that is hypointense to liver. C, T1-weighted gradient-echo image after the administration of contrast shows the peripheral portion
that enhanced irregularly during the arterial dominant phase (not shown) beginning to wash out, suggesting an early target appearance (arrow). D,
Delayed postcontrast gradient-echo image shows continued filling of the central portion of this lesion; the periphery has washed out (arrow).

A B
FIGURE 19.11.  Liver with cirrhotic configuration. A, T1-weighted spin-echo image at the level of the portal vein shows hypertrophy of the left lobe
and caudate with atrophy of the right lobe of the liver. B, T2-weighted image of the liver at the same level shows mildly heterogeneous signal in the
atrophied right lobe, making exclusion of an underlying mass difficult. Note also the focal hepatic scarring (arrow).
370 PART 2  DIAGNOSTIC TECHNIQUES

A B
FIGURE 19.12.  Large hepatocellular carcinoma showing the mosaic pattern. A, T1-weighted image shows a large heterogeneous mass (m) in the
liver. Note the hypertrophied left hepatic lobe and caudate. B, T2-weighted image also shows the mass (m) to be heterogeneous, with islands of
tissue that are hyperintense with respect to other portions of the same mass. This pattern is known as the mosaic pattern, and it can be seen in
hepatocellular carcinoma, especially when the lesion is large.

A B
FIGURE 19.13.  Hepatocellular carcinoma containing intracellular lipid. A, T1-weighted in-phase gradient-echo image shows a mass in the liver
that is darker than normal parenchyma, with a small internal area of brighter signal (arrow). B, T1-weighted out-of-phase gradient-echo image shows
the same area (arrow) has lost signal, which is consistent with an admixture of fat and water-containing tissue.

HCCs may be heterogeneous due to areas of necrosis (Fig. hyperenhance, they tend to be more homogeneous and isoin-
19.12). Areas of heterogeneity may indicate moderate to poorly tense to background liver parenchyma during the equilibrium
differentiated tumors (Witjes et al, 2012). HCC may show high phase, often show low T2 signal, and are variable on delayed
T1 signal (Fig. 19.13) (Basaran et al, 2005), and lesions with hepatobiliary phase imaging (Cruite et al, 2010). In HCC,
intracellular lipid show signal loss on out-of-phase T1-weighted hepatocyte contrast agents generally show hypointensity in
imaging. Intracellular lipid may be an important clue to small delayed hepatobiliary phase imaging compared with surround-
HCCs without typical enhancement patterns, as early HCC are ing liver in the vast majority of cases, with a small percentage
sometimes hypovascular in arterial phase (Rhee et al, 2012). showing variable internal uptake, which may reflect either the
Contrast washout in portal venous or later dynamic phase grade of tumor differentiation or specific enzyme production
MRI, as well as heterogeneous enhancement, has been associ- and tumor receptors. (Cruite et al, 2010) Rarely, well-
ated with moderate to poorly differentiated tumors; a higher differentiated HCC may show tracer concentration in delayed
percentage of well-differentiated tumors may not demonstrate hepatobiliary phase with areas of increased signal intensity.
washout (Okamoto et al, 2012; Tan et al, 2011; Witjes et al, Due to the complexity of imaging features and overlap, as
2012). In addition to washout, peritumoral capsules, which are well as multimodality availability, there have been organized
low in signal intensity on the arterial dominant phase and efforts to improve report standardization and communication
enhance later, are also associated with microvascular invasion, regarding imaging findings, as well as recommendations regard-
an important feature with clinical significance (Witjes et al, ing surveillance imaging and screening. The American Associa-
2012). These are distinguishing features in contrast to benign tion for the Study of Liver Diseases (AASLD) issued revised
or dysplastic nodules. Although dysplastic nodules may also recommendations in 2010, recommending HCC screening for
Chapter 19  Magnetic resonance imaging of the liver, biliary tract, and pancreas 371

patients at risk with ultrasound (US) every 6 months combined Although extracellular lipid is typical in HAMLs, they often
with serum α-fetoprotein (AFP). MRI imaging has an emphasis show brisk, avidly enhancing soft tissue components with
on arterial phase hyperenhancement and washout, with biopsy washout, which overlaps with other liver malignancies, such as
improving sensitivity for indeterminate lesions (Tan et al, hepatocellular carcinoma. HAML is generally considered a
2011). The Liver Imaging Reporting and Data System (LI- benign, solitary tumor comprising three elements: smooth
RADS), an initiative supported by the American College of muscle, thick-walled blood vessels, and mature adipose tissue
Radiology, as well as the Liver and Intestinal Organ Transplant (Cai et al, 2013), although they can also present without fat
Committee (OPTN) have also issued guidelines regarding (Butte et al, 2011). Limited data suggest a well demarcated,
HCC classification. LI-RADS was revised in 2014 to better lipid-containing tumor with a thin peripheral enhancing rim,
incorporate OPTN and AASLD guidelines regarding growth lack of peritumoral capsule, and an early draining vein that may
and lesion detection on screening ultrasound. Ancillary fea- offer clues to the diagnosis, particularly in patients without cir-
tures, including nodule-in-nodule or mosaic appearance, intra- rhosis or elevated serum AFP (Fig. 19.14) (Cai et al, 2013; Du
lesional fat, diffusion restriction, and perilesional or coronal et al, 2012). Surgical excision remains preferable, as there have
enhancement, for example, are also incorporated into the been reports of HAML hemorrhage and capsular rupture, as
LI-RADS imaging interpretation algorithm (http://nrdr.acr.org/ well as venous obstruction or Budd-Chiari syndrome from mass
lirads/). Although continued revisions are inevitable, consensus effect. Furthermore, pathologic analysis remains essential for
guidelines will encourage report standardization, improve com- diagnostic confirmation; immunohistochemical stains for
munication, and ultimately improve decision making. Agree- markers may offer increased accuracy (Du et al, 2012).
ment among readers using newer algorithms tends to be
moderate to substantial for expert readers but lower among Mesenchymal Tumors
novices, suggesting implementation of criteria may require a Rarely, tumors of mesenchymal origin, including hepatic angio-
learning curve (Davenport et al, 2014). sarcoma (HAS), leiomyosarcoma, and fibrous histiocytoma,
may be present within the liver (Anderson et al, 2009). The
Fibrolamellar Carcinoma MRI appearance of these tumors is nonspecific; they are gener-
Fibrolamellar HCC (FLHCC), a rare variant, occurs in young ally of low intensity on T1-weighted images and hyperintense
adults, and is distinct from conventional HCC on multiple on T2-weighted images, with heterogeneous enhancement.
levels, including molecular and clinical differences (see Chapter HAS typically shows hyperenhancement, often peripheral, but
91). The average age at presentation is 25 years, and the pres- sometimes central and irregular, with progressive fill-in on more
ence of nodal metastases is common (Ganeshan et al, 2014). delayed phases following blood pool. Although similar to cav-
FLHCC may have a central scar, and these scars tend to be ernous hemangiomas, HAS may also show centrifugal or
low in signal intensity on T1-weighted and T2-weighted images “reverse” enhancement patterns and show greater degrees of
due to fibrous changes. FNH also may have a central scar, variance and heterogeneity, with more disordered peripheral
although FNH scars generally show increased T2 signal; enhancement than nodular, discontinuous, clump-like enhance-
however, it is not always a reliable differentiating feature (Gane- ment typically seen in benign hemangiomas. HAS is typically
shan et al, 2014; Kim et al, 2009). FLHCC may show early multiple, of varying size, involving both hepatic lobes, and
heterogeneous enhancement with variable washout and may rapidly growing, as median survival has been reported as less
show partial hepatocyte agent concentration in delayed hepa- than 6 months (Huang et al, 2014; Pickhardt et al, 2015).
tocyte phase imaging (Meyers et al, 2011). Metastatic disease
is also common at presentation, both in the abdomen and chest, Epithelioid Hemangioendothelioma
with adenopathy being prominent (>2 cm) in a majority of Epithelioid hemangioendothelioma (EH) is a rare tumor of
cases (Do et al, 2014). adults that should be distinguished from infantile hemangioen-
dothelioma, which occurs in infants and children. The progno-
LESS COMMON HEPATIC TUMORS sis is better for EH than for other parenchymal tumors, such
as sarcoma, although extrahepatic metastases do occur. EH is
Lymphoma generally low in signal intensity on T1-weighted images and
Non-Hodgkin lymphoma accounts for most hepatic lympho- hyperintense on T2-weighted images but not as hyperintense
mas. MRI shows masses of varying size, which are generally as hemangiomas. They also may show a distinct target sign on
low in signal intensity on T1-weighted images and hyperintense T1- and T2-weighted images (Economopoulos et al, 2008).
on T2-weighted images (Coenegrachts et al, 2005; Rizzi et al, After Gd-DTPA administration, an irregular nodular and con-
2001), but not as great as with other benign hepatic lesions, centric enhancement may be seen. Capsular retraction also may
such as hemangiomas or cysts. This difference in signal inten- be seen with EH, helping to elucidate the diagnosis (Lin et al,
sity makes it relatively easy to determine the malignant nature 2010) (see Chapter 89).
of the lesion but not the specific tumor type. Lymphoma may
be relatively hypoenhancing in early dynamic phases, with Biliary Cystadenoma and Biliary Cystadenocarcinomas
isointensity in later phases (Coenegrachts et al, 2005). The Biliary cystadenomas and biliary cystadenocarcinomas are rare
imaging characteristics of lymphoma overlap with other malig- tumors of the liver that present as a predominantly cystic mass
nant hepatic lesions. containing enhancing septations (Fig. 19.15; see Chapters 89
and 90B). These lesions may be of low, intermediate, or
Angiomyolipoma increased signal on T1-weighted images, depending on the
Hepatic angiomyolipoma (HAML) is an uncommon tumor, protein or hemorrhagic content within the mass, and they are
more frequent in females, which currently presents a diagnostic usually hyperintense on T2-weighted sequences. Enhancing
challenge for imaging diagnosis (see Chapters 89 and 90). mural or internal irregular soft tissue nodularity, as well as
372 PART 2  DIAGNOSTIC TECHNIQUES

A B

C D
FIGURE 19.14.  Angiomyolipoma. A, T1-weighted in-phase image shows a high-signal right hepatic mass (arrow). B, T1-weighted out-of-phase
image shows low signal at its margin due to chemical shift artifact between the mass and surrounding liver, confirming the presence of bulk fat. 
C, Axial T2-weighted image with fat saturation shows the mass is dark. D, Axial T1-wieghted fat saturation image shows the mass is dark as well.

internal hemorrhage, has been shown in to be more often asso- high T2 signal thickening of the gallbladder wall, with early and
ciated with cystadenocarcinomas; however, differentiation may prolonged heterogeneous enhancement, often in patients with
not be possible (Arnaoutakis et al, 2015; Qian et al, 2013; multiple gallstones (Tan et al, 2013). Cholelithiasis is a predis-
Wang et al, 2012). Communication with the biliary ductal posing condition. Evidence of liver invasion and spread to
system on delayed hepatobiliary phase imaging with hepatocyte regional lymph nodes also may be identified with MRI, which
contrast agents has been reported, helping to differentiate these is optimal for evaluation of these lesions because of its out-
tumors from nonneoplastic simple hepatic cysts. (Billington standing tissue contrast, ability to image directly in multiple
et al, 2012; Marrone et al, 2011). Infectious cysts may also planes (Dai et al, 2009; Sikora et al, 2006), with DWI offering
communicate with the biliary tree, however, such as with added sensitivity and specificity for the primary tumor as well
complex cysts from echinococcal disease. as nodal or hepatic metastatic disease (Tan et al, 2013). Fluo-
rodeoxyglucose (FDG) PET imaging may also provide
BILIARY TUMORS improved sensitivity and specificity for nodal or distant meta-
static disease (Lee et al, 2010).
Gallbladder Carcinoma
MRI offers improved characterization of gallbladder cancer Bile Duct Cancer
compared with other modalities. However, its differentiation Bile duct tumors (see Chapters 50, 51, and 59) are well
from inflammatory conditions, which may occur concurrently, depicted on MRI and may be intrahepatic, hilar, or extrahe-
may be difficult (see Chapters 33 and 49). As opposed to the patic, with a mass-forming appearance or as periductal infil-
inflammatory associated wall thickening with maintained trating or papillary intraductal morphologies (Chung et al,
mucosal and submucosal layers, with differential enhancement, 2009). Tumors may show focal nodular thickening along
gallbladder cancer typically shows irregular intermediate to ductal walls or be discrete intrahepatic masses. Central hilar
Chapter 19  Magnetic resonance imaging of the liver, biliary tract, and pancreas 373

A B

C
FIGURE 19.15.  Biliary cystadenoma. A, Coronal T2-weighted image shows a lobulated mass (m) in close proximity to the left hepatic duct (arrow-
head). B, Projection image in the coronal oblique plane shows the well-defined hyperintense mass to be in continuity with a mildly dilated left-sided
biliary radicle (straight arrow). The normal right-sided biliary radicle (curved arrow) is easily seen with this technique. C, Postcontrast, T1-weighted
gradient-echo image shows no enhancement within this mass (m).

cholangiocarcinomas are the most common and are generally capsular retraction as well as vascular encasement, typically
associated with biliary ductal dilation. Bile duct tumors may without tumor thrombus (Chung et al, 2009). Smaller tumors
be seen as intermediate, mildly increased T2 signal (Fig. may show early, more uniform arterial enhancement, particu-
19.16), however, less so than the surrounding biliary dilata- larly when less than 4 cm in size (Kim et al, 2011). Intraductal
tion. The level of obstruction and continuity of the tumor with papillary neoplasm of the bile duct is an uncommon subtype of
the vasculature are well evaluated with MRI (Peporte et al, bile duct cancer with characteristics similar to pancreatic intra-
2013), although CT angiography with multiphasic imaging ductal mucinous neoplasms. The majority of tumors occur near
offers improved spatial resolution and similar accuracy to MRI the hilum or in extrahepatic ducts, and the clinical outcomes
to assess vascular involvement, and exceeds MRI accuracy are better than conventional bile duct cancers (Rocha et al,
when assessing for nodal and distant metastases (Aljiffry et al, 2012).
2009). Focused assessment of ductal, portal venous, and
hepatic arterial involvement is performed in staging and pre- BENIGN DISEASES OF THE BILIARY TRACT
operative imaging.
Peripheral, mass-forming intrahepatic cholangiocarcinomas Cholelithiasis and Choledocholithiasis
occur in approximately 10% of cases and generally have high Gallstones are well identified on T2-weighted images and on
T2 signals, lobulated heterogeneous masses with peripheral MRCP sequences (Fig. 19.18; see Chapters 32, 33, and 36).
enhancement, and gradual centripetal fill-in (Fig. 19.17) They usually appear as low signal intensity structures in a
(Hennedige et al, 2014, Kang et al, 2012) (see Chapter 50). fluid-filled gallbladder. Ultrasound is usually the modality of
Satellite lesions are common within the liver, and these lesions choice in the evaluation of uncomplicated cholelithiasis or cho-
tend to show low signal intensity on delayed hepatocyte imaging lecystitis due to its high sensitivity and lower cost, but choledo-
phase (Chung et al, 2009; Kim et al, 2011; Peporte et al, cholithiasis is more effectively imaged by MRI (Johnson et al,
2013). Intrahepatic cholangiocarcinomas may show adjacent 2010; Samaraee et al, 2009). Coronal T2-weighted imaging,
374 PART 2  DIAGNOSTIC TECHNIQUES

A B

C
FIGURE 19.16.  Hilar mass. A, Axial T2-weighted image shows dilatation of the left hepatic duct and a low to intermediate–intensity mass expand-
ing the right hepatic duct (arrow). B, T1-weighted late arterial phase postcontrast image shows early enhancement of the tumor (arrow). C, Portal
venous phase postcontrast T1-weighted imaging shows the mass (arrow) is hypoenhancing to liver. Biopsy of a more superior intrahepatic mass in
this patient with cirrhosis showed poorly differentiated hepatocellular carcinoma. Extension into the biliary ducts with ductal expansion and obstruc-
tion is an uncommon finding in hepatocellular carcinoma (HCC). Although HCC and cholangiocarcinoma may exist simultaneously as two distinct
tumors, a distinct subtype of mixed HCC-cholangiocarcinoma is increasingly recognized.

performed routinely with MRI, readily identifies common duct have been described (Lee et al, 2009; Todani et al, 1977): type
stones (Fig. 19.19). MRCP can also be obtained to evaluate I has been subdivided into A, B, and C, in addition to types II,
whether retained stones are present after cholecystectomy, III, IVa, IVb, and V. Recently, there have been advocates for
although clips may limit examinations in the perioperative time dropping the numeric classification system, instead using a
period. If no stones are present on MRCP, this may obviate the more descriptive, clinically meaningful nomenclature (Visser
need for ERCP. et al, 2004). MRI is well suited not only to diagnose these cysts,
but also to classify the type of cyst. Not only can 3D MR chol-
Choledochal Cysts angiograms depict the normal and abnormal anatomy, but
Choledochal cysts (see Chapter 46) represent dilatation of the direct coronal imaging and delayed scans post–hepatocyte-
extrahepatic bile ducts with possible associated intrahepatic specific gadolinium-based contrast agents can be obtained for
biliary duct dilatation. This entity is a relatively uncommon further evaluation (Gupta et al, 2010).
congenital anomaly that usually presents before 10 years of age.
The classic triad includes a palpable mass, abdominal pain, and Postoperative Biliary Complications
jaundice. Cysts may be associated with chronic inflammation Complications from surgical procedures include bile leaks,
and increase the risk for cholangiocarcinoma. Five types of cysts abscess formation, and biliary strictures (see Chapters 27 and
Chapter 19  Magnetic resonance imaging of the liver, biliary tract, and pancreas 375

A B C

D E F
FIGURE 19.17.  Mass forming intrahepatic cholangiocarcinoma. A, T1-weighted in-phase gradient-echo image shows a peripheral hypointense
mass (m) with capsular retraction. B, A T2-weighted fat saturation image shows increased signal intensity within the mass. C, Diffusion-weighted
image shows restricted diffusion within the mass, which is brighter than liver. D, T1-weighted fat saturation post–contrast-enhanced image in late
arterial phase shows peripheral enhancement. E, T1-weighted post–contrast-enhanced image in late portal venous phase shows only partial filling
of the mass. F, T1-weighted post–contrast-enhanced image in late portal venous phase at a separate level shows an additional satellite lesion (arrow),
smaller in size with marginal enhancement, typical of intrahepatic metastasis.

A B
FIGURE 19.18.  Choledocholithiasis. A, Coronal T2-weighted single-shot fast spin-echo image through the common duct in a patient after chole-
cystectomy shows multiple stones within the common bile duct. Note the distal stone impacted at the level of the ampulla (arrow). B, Axial T2-weighted
image with the same technique also shows a stone, surrounded by bile, in the distal common bile duct (arrow).
376 PART 2  DIAGNOSTIC TECHNIQUES

biliary phase scans by opacifying the biliary tree, which may


improve diagnostic confidence to evaluate for active biliary leak,
anatomic variants, and choledocholithiasis (Boraschi & Donati,
2014; Gupta et al, 2010).

PANCREAS
Solid Tumors of the Pancreas
Pancreatic solid tumors include both neoplastic and nonneo-
plastic origins (see Chapter 59). Although MRI characteristics
alone may help predict etiologies, there may be imaging-feature
overlap between entities. Imaging characteristics combined
with clinical presentation and demographic data often guide
therapy and predict the diagnosis. Neoplastic etiologies include
tumors arising in the pancreas, such as adenocarcinoma, solid
pseudopapillary tumor, neuroendocrine tumors, or pancreatic
lymphoma. Metastases, lymphomas, and other rare tumors
may involve the pancreas (Low et al, 2011). In addition to
enhancement characteristics, such as early arterial enhance-
ment in neuroendocrine tumors, precontrast signal character-
istics, such as hemorrhage with increased T1 signal in solid
A pseudopapillary tumors, may provide clues to the diagnosis.
Nonneoplastic etiologies include focal pancreatitis, accessory
spleen, focal fat, congenital anomalies, and other rare etiolo-
gies. Intrapancreatic splenic tissue shows signal intensity and
enhancement characteristics paralleling that of spleen on all
MRI sequences. Focal pancreatitis may mimic pancreatic ade-
nocarcinoma; however, restricted diffusion on DWI is typically
seen in adenocarcinoma (Fattahi et al, 2009; Kartalis et al,
2009), compared with focal pancreatitis. Focal pancreatitis may
also cause irregular narrowing of the main pancreatic duct, as
opposed to the abrupt cutoff and upstream dilatation with
associated parenchymal atrophy noted in adenocarcinoma
(Low et al, 2011; Siddiqi et al, 2007).

Pancreatic Cancer
Pancreatic adenocarcinoma (see Chapters 59 and 62) is well
B evaluated on MRI and MRCP. T2, diffusion-weighted, and
dynamic contrast-enhanced T1-weighted MRI sequences are
FIGURE 19.19.  Afferent loop syndrome. A, Coronal T2-weighted particularly helpful to characterize pancreatic cancer and stage
sequence in a patient after pancreaticoduodenectomy for pancreatic patients (Tamm et al, 2012). MRI is generally thought to be
carcinoma. The patient has a hepaticojejunostomy with a patent anas-
highly accurate in assessing for vascular invasion or encasement
tomosis (white arrow). The afferent loop is markedly dilated (black arrow)
compared with other loops of bowel. No mechanical obstruction was
(tumor surrounds >50% of the vessel circumference), local-
noted. B, Axial T2-weighted image through the level of the anastomosis regional tumor extension, and liver metastases (Tamm et al,
(arrow) shows the site to be patent without evidence of a stricture. The 2012), although recent data have suggested MRI may under-
afferent loop is dilated. estimate tumor size (Hall et al, 2013; Legrand et al, 2015).
Similar to other modalities, accuracy is limited for assessment
of lymph node metastases with MRI techniques. Pancreatic
30). Although using other imaging modalities in the immediate cancer subtypes may be predicted based on imaging features,
postoperative setting to assess for bile leaks and abscesses may patient demographics, and clinical presentation, particularly
be prudent, MRI is uniquely suited for the assessment of the neuroendocrine tumors; however, there is overlap in the imaging
postoperative biliary tract. Bile duct injuries after surgery can appearance and location of solid and cystic neoplasms. Prelimi-
be caused by a number of things, but these may all lead to the nary data suggest grade of tumor enhancement may correlate
same result—a stricture at the anastomotic site. MRCP is with tumor grade in adenocarcinomas (Lauenstein et al, 2010).
uniquely suited for addressing this problem. Surgical clips near
the anastomosis may create streak artifacts during CT scan- Cystic Lesions of the Pancreas
ning, but currently used clips are less problematic for MRI. Detection of pancreatic cystic lesions (see Chapter 60) has
MRI has multiplanar capabilities and superior tissue contrast, increased in recent years with increased imaging and improved
and MRCP sequences can minimize susceptibility to artifacts spatial resolution. They are increasingly found incidentally.
to allow improved visualization of the region of the anastomosis Benign lesions may also progress to malignant lesions over
and improved diagnostic confidence (see Fig. 19.19). More time. Diagnostic possibilities include benign lesions, such as
recently, hepatocyte contrast agents also allow delayed hepato- pseudocysts, serous cystadenomas, and true epithelial cysts; to
Chapter 19  Magnetic resonance imaging of the liver, biliary tract, and pancreas 377

benign lesions with potential for malignant degeneration, such to have a higher association with malignancy; their presence
as intraductal mucinous or parenchymal mucinous cystic neo- may warrant surgical excision (Kim et al, 2014). Evaluation
plasms; to malignant lesions, such as rare cystic or necrotic after contrast administration helps assess cyst wall irregularity
adenocarcinomas or cystic neuroendocrine tumors (Kucera or enhancement of soft tissue components. Molecular analysis
et al, 2012). Multiple imaging modalities may be used to iden- of cyst contents to assess for genetic mutations or gene silencing
tify and characterize pancreatic cystic lesions, including ultra- associated with IPMN may offer improved accuracy in diag-
sound, CT, and MRI. nostic workup (Freeny et al, 2014).

Intraductal Papillary Mucinous Neoplasms Autoimmune Pancreatitis


Cystic lesions arising from intraductal papillary mucinous neo- An increasing incidence of autoimmune pancreatitis is most
plasms (IPMNs) of either branch-duct, main-duct, or mixed likely due to increased awareness and thereby increased detec-
type have been increasingly discovered (Campbell et al, 2015), tion (Vlachou et al, 2011) (see Chapter 59). Imaging features
and the International Association of Pancreatology has pub- may suggest the diagnosis and are correlated with clinical
lished consensus guidelines for their management, which were features, including elevated serum immunoglobulin G4, rela-
last revised in 2012 (see Chapter 60). The International Asso- tively indolent clinical presentation, and response to corticoste-
ciation of Pancreatology stratifies patients based on “high risk” roid therapy. Autoimmune pancreatitis may be diffuse, focal,
or “worrisome” features, with guidelines regarding resection, or multifocal, and often shows heterogeneous T1 hypointensity,
endoscopic ultrasound, and imaging follow-up (Tanaka et al, slight T2 hyperintensity, and delayed enhancement due to asso-
2012). A recent revision includes main duct dilatation greater ciated fibrosis. Fibrosis may also show diffuse T2 hypointensity
than 5 mm (without obvious cause) as a worrisome feature, but (Vlachou et al, 2011). Diffuse main pancreatic ductal narrow-
also downgraded size greater than or equal to 3 cm from high ing or irregularity, and upstream common bile duct dilatation
risk to worrisome (Tanaka et al, 2012). Soft tissue contrast is or wall thickening, may be present. There may also be a peri-
improved with MRI imaging, which permits optimal depiction pancreatic halo, which appears hypointense on T1- and
of features deemed worrisome or high risk, such as septations, T2-weighted imaging postcontrast (Heyn et al, 2012). Focal
thick enhancing walls, nodularity, or soft tissue components. disease, particularly when involving the head with associated
The single-shot fast spin-echo T2-weighted sequence is par- upstream pancreatic and main bile duct dilatation, may mimic
ticularly useful, as cystic lesions are high in T2 signal and bright ductal adenocarcinoma. Extrapancreatic manifestations may
on these sequences, and communication with the main duct also be present within the spectrum of immunoglobulin G G4-
may be more evident (Acar et al, 2011; Campbell et al, 2015). related sclerosing disease, including bile duct, renal, and retro-
Although branch-duct IPMNs have a lower incidence of malig- peritoneal involvement (Kim et al, 2013).
nancy compared with main- or mixed-duct subtypes, recent
meta-analysis has shown mural nodules in branch-duct IPMNs References are available at expertconsult.com.
Chapter 19  Magnetic resonance imaging of the liver, biliary tract, and pancreas 377.e1

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699, 2010.
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CHAPTER 20 
Direct cholangiography: approaches, techniques, and
current role
Robert H. Siegelbaum and Robin B. Mendelsohn

DIRECT CHOLANGIOGRAPHY OVERVIEW the gallbladder. The first report of PTC was by Huard and
Do-Xuan-Hop in 1937, who performed cholangiography with
Direct cholangiography, the introduction of contrast medium the suboptimal contrast agent Lipiodol. The use of transhe-
into the biliary system, can be performed under fluoroscopic patic cholangiography as a diagnostic tool gained popularity
guidance percutaneously, endoscopically, or intraoperatively 15 years later, after Carter and Saypol’s (1952) discussion of
via surgically placed catheters. The nonoperative techniques are PTC with the use of a water-soluble contrast agent. In the
percutaneous transhepatic cholangiography (PTC) and endo- ensuing years, many investigators (Flemma & Shingleton,
scopic retrograde cholangiopancreatography (ERCP). Cur- 1966; Glenn et al, 1962; Mujahed & Evans, 1966; Seldinger,
rently, noninvasive magnetic resonance imaging (MRI) and 1966; Shaldon et al, 1962; Weicher, 1964) described a variety
contrast-enhanced computed tomography (CECT) have virtu- of different methodologic details, including the use of sheathed
ally eliminated the indications and need for direct cholangiog- or unsheathed needles of various sizes and different puncture
raphy (Bakhal et al, 2009; Miller et al, 2007; Stroszczynski & sites with varying directions of puncture. The procedure
Hünerbein, 2005) (see Chapters 18 and 19). Today, ERCP and remained associated with a significant risk of bile peritonitis,
PTC are typically performed only as part of a planned inter- especially in obstructed biliary systems, and less frequently,
ventional procedure, such as biliary drainage, stent placement, hemorrhage. The use of fine needle technique was developed
stone extraction, or stricture dilation (see Chapters 29 and 30). at Chiba University and was first presented by Ohto and
Imaging evaluation of the biliary tree with magnetic reso- Tsuchiya (1969), and later by Tsuchiya (1969). Numerous
nance cholangiopancreatography (MRCP) or CECT is nonin- additional reports have also described decreased complications
vasive, does not require sedation, and is generally regarded as with fine needle transhepatic access, and the fine needle tech-
safe. Imaging protocols with multiplanar reconstruction allow nique has been generally accepted as the standard (Benjamin
a large field of view that enables visualization of the entire et al, 1978; Ferrucci et al, 1976; Fraser et al, 1978; Gold &
biliary tree and pancreatic duct (Fig. 20.1). Reconstructed Price, 1980; Harbin et al, 1980; Hinde et al, 1977; Jain et al,
three-dimensional data sets can be displayed in an appearance 1977; Pereiras et al, 1977).
similar to a diagnostic cholangiogram, with the added benefit Transhepatic cholangiography has essentially been sup-
of being able to rotate the images to further delineate the planted by noninvasive imaging techniques for the evaluation
anatomy of the bile duct and pancreatic duct. In comparison, of the biliary tree. In 1985, Kadir reported that less than 5%
injection of contrast dye under fluoroscopic guidance is limited of patients referred for evaluation of biliary disease required
to visualization of structures in direct continuity with the opaci- concomitant drainage procedures. With continued advance-
fied, nonisolated segments of the biliary tree (Fig. 20.2). While ment of cross-sectional imaging techniques, in particular
performing direct cholangiography with PTC, simultaneous MRCP (see Chapter 19) (Park et al, 2004; Romagnuolo et al,
cross-sectional imaging may be required to ensure that the 2003; Simone et al, 2004; Vaishali et al, 2004; Zhong et al,
entire biliary tree has been opacified, even with multiple per- 2003), percutaneous fluoroscopic imaging of the biliary tree is
cutaneous puncture sites and injections. Cross-sectional typically only performed as part of a planned radiologic inter-
imaging of the liver can be performed in a fluoroscopy room ventional procedure.
with rotational angiography or by direct CT imaging if there is Imaging evaluation of the biliary tree with MRCP or CECT
an in-line CT scanner. In addition, MRCP and CECT typically is noninvasive, does not require sedation, and is generally
provide superior diagnostic accuracy when compared with PTC regarded as safe (see Chapters 18 and 19). With direct puncture
or ERCP, allowing visualization of the bile duct wall, structures and contrast injection in the biliary tree, only bile ducts in
contiguous to the biliary tree (such as cysts and neoplasms), continuity with the punctured duct are visualized. Multiple
and structures adjacent to the liver. percutaneous punctures may be required to visualize the entire
biliary tree in the presence of bile duct isolation (see Fig. 20.2).
Even with multiple transhepatic bile duct punctures, CT
PERCUTANEOUS TRANSHEPATIC imaging performed at the time of the procedure can be helpful
CHOLANGIOGRAPHY to ensure that the biliary tree has been completely assessed.
Alternatively, MRI and CECT can image the entire biliary
History system and can demonstrate the presence and severity of bile
The first report of fluoroscopic imaging of the biliary tree was duct isolation (see Fig. 20.1). Furthermore, by also visualizing
presented by Burckhardt and Müller in 1921, who performed the bile duct wall, liver, and surrounding structures, additional
cholecystocholangiography through percutaneous puncture of anatomic information is provided with MRI or CECT.

378
Chapter 20  Direct cholangiography: approaches, techniques, and current role 379

Coagulation parameters and platelet count should be


checked prior to the procedure and corrected if necessary.
Informed consent is obtained in accordance with institutional
policy, including a discussion of the risks and benefits of the
procedure. Patients generally receive conscious sedation con-
sisting of an anxiolytic, such as midazolam, and an opiate, such
as fentanyl. All patients should receive broad-spectrum intra-
venous antibiotic coverage (according to institutional prefer-
ence), which should be administered approximately 1 hour
before the procedure to ensure appropriate blood levels at the
time of procedure.

Procedure
Although not always present in modern fluoroscopy suites,
PTC is ideally performed on a tilting fluoroscopic table. As the
specific gravity of contrast material is greater than that of bile,
less contrast dye is typically required to fully delineate the
biliary tree when the table is tilted.
FIGURE 20.1.  Magnetic resonance cholangiopancreatography. Three- Right-Sided Puncture
dimensional maximum intensity projection image showing marked dilata-
tion of the intrahepatic and extrahepatic biliary tree, as well as the After the patient has been prepared and draped in a sterile
pancreatic duct, in a patient with a head of pancreas mass. fashion, a puncture site is selected in the right midaxillary line,
typically one or two interspaces below the costophrenic angle.
Puncture sites are generally kept below the ninth intercostal
space to avoid inadvertent entry into the pleural space. One
percent lidocaine is infused subcutaneously, and a small derma-
totomy is made with a No. 11 scalpel. A 21- or 22-gauge, 15- to
20-cm Chiba-style needle is advanced under fluoroscopic guid-
ance superior to the closest rib to the target puncture site, to
avoid laceration of an intercostal vessel. Real-time ultrasound
guidance can be helpful for the initial puncture in the presence
of bile duct dilatation (Covey & Brown, 2008). The puncture
site and direction are chosen based on evaluation of the patient’s
cross-sectional imaging studies (Fig. 20.3A and B).
Care should be taken to avoid puncture of the gallbladder
or extrahepatic bile duct. A small amount of water-soluble
contrast agent is injected while slowly withdrawing the needle
until a bile duct is identified. Injection of contrast agent into a
bile duct has the appearance of oil being dropped in water.
Inadvertent opacification of a vascular structure is recognized
by the rapid clearance of the contrast agent. If a bile duct is not
entered during withdrawal of the needle, the needle is reintro-
duced in a slightly different direction. It is generally recom-
mended not to withdraw the needle completely from the liver,
to minimize the number of punctures through the liver capsule.
When opacification of the biliary tree is challenging, particu-
larly in the case of a nondilated biliary tree, the same puncture
FIGURE 20.2.  Hilar cholangiocarcinoma involving first-order right and site may be used multiple times prior to selecting a new percu-
left hepatic ducts. Separate needle punctures were required to fill the taneous access site. If successful puncture of a bile duct is
right and left ducts. unlikely from that site after multiple attempts, a new site should
be chosen. In patients with biliary obstruction, gentle injection
of 10 mL of iodinated contrast is typically sufficient for bile
Preprocedural Preparation duct opacification. A larger volume of contrast material is typi-
Ideally, all patients should undergo cross-sectional imaging cally required in nonobstructed systems. When the bile ducts
(CECT or MRI) prior to PTC. This imaging is particularly are visualized, fluoroscopic images should be acquired and
important in patients who have undergone prior liver resection. stored in multiple projections to identify specific portions of the
MRI or CECT are the imaging modalities of choice due to their biliary tree and to completely delineate abnormal findings, if
diagnostic accuracy in depicting the level of obstruction, posi- present.
tion of the liver, portal vein patency, the relationship of the liver
and bile ducts to other structures, and presence of tumors or Left-Sided Puncture
lobar atrophy, all of which could greatly facilitate successful There is considerable variation in size and anatomic position
puncture. of the left lateral segments of the liver, and careful review of
380 PART 2  DIAGNOSTIC TECHNIQUES

LOGIQ
preprocedural cross-sectional imaging is recommended to
E9 select an optimal puncture site. Although left-sided punctures
can be performed through the right liver via an anterior axillary
line approach to the segment IV bile ducts, the generally pre-
21 ferred method is a subxiphoid approach to a bile duct in
segment II or segment III. As in punctures of right sided bile
ducts, percutaneous access to the biliary tree can be simplified
by using real-time ultrasound guidance in the presence of
dilated bile ducts (Covey & Brown, 2008).

–21 Success Rate and Accuracy


cm/s Percutaneous opacification of the biliary tree is successful in
95% to 100% of patients with biliary obstruction (Harbin et al,
A 1980; Jain et al, 1977; Mueller et al, 1981). A success rate of
60% to 95% is reported for nondilated biliary systems. The
LOGIQ likelihood of success in a nondilated system is increased by the
E9 number of needle passes performed (Jaques et al, 1980). No
current radiologic descriptions of obstructed bile ducts are
pathognomonic for differentiation of benign and malignant
disease (Hadjis et al, 1985; Wetter et al, 1991). Bile cytology
and review of cross-sectional imaging can be helpful in conjunc-
tion with fluoroscopic images in diagnosing the cause of the
obstruction.

Pitfalls in Interpretation
Lack of Opacification
Failure to inject adequate volume of contrast agent can result
in false interpretation of the level of obstruction. This pitfall
can occur in the setting of complete obstruction and can be
B
recognized by the presence of a hazy margin at the level of the
FIGURE 20.3.  Real-time ultrasound guidance can be helpful for the apparent (false) obstruction (Fig. 20.4) (Kittredge & Baer,
initial puncture in the presence of bile duct dilatation. A, Color Doppler 1975). In high bile duct obstruction, especially when associated
image of the left liver revealing a dilated segment III bile duct. B, Static with variant anatomy, isolated segments of the biliary tree can
grayscale ultrasound image taken during puncture of the dilated bile duct be visualized only by direct puncture. If the wrong bile duct is
with an echogenic 21-gauge needle.
selected, or if puncture of an additional bile duct is needed but

A B
FIGURE 20.4.  Ampullary carcinoma. A, With the patient supine, contrast pools proximally, giving a false impression of a high bile duct obstruction.
The spurious nature of the level is suggested by the hazy inferior margin to the contrast column. B, With the patient sitting semierect, the contrast
pools at the true point of obstruction, which is sharply defined.
Chapter 20  Direct cholangiography: approaches, techniques, and current role 381

not performed, the diagnosis of bile duct injuries and bile leaks that ERCP, MRCP, and endoscopic ultrasound have compa-
can be missed. rable sensitivity and specificity in the diagnosis of common bile
duct (CBD) stones. With newer diagnostic imaging technolo-
Ductal Dilatation gies, however, ERCP has evolved into a predominantly thera-
The absence of bile duct dilatation does not exclude the pres- peutic procedure. They stated that avoidance of unnecessary
ence of clinically significant biliary obstruction. Disorders such ERCPs is the best way to reduce the number of complications
as sclerosing cholangitis, acquired immunodeficiency syn- and that endoscopists performing ERCPs should have appro-
drome, and chemotherapy-induced biliary sclerosis can present priate training and expertise. In 2005, the American Society of
with bile duct fibrosis, impeding the ability of the bile ducts to Gastrointestinal Endoscopy published guidelines, stating that
become dilated. Conversely, bile duct dilatation does not based on expert opinion, ERCP is primarily a therapeutic pro-
always imply the presence of an obstructed biliary system. For cedure for the management of pancreaticobiliary disorders
example, dilatation that may be seen in patients with Caroli (Adler et al, 2005). Therefore ERCP is rarely performed
disease, or choledochal cysts, can have the radiographic appear- without a therapeutic component.
ance of bile duct dilation without the presence of obstruction.
Technique
Complications Most ERCPs are performed as outpatient procedures in a hos-
Serious complications of PTC are rare and occur in approxi- pital setting, although they can be performed in ambulatory
mately 3% of patients (Harbin et al, 1980). The most common centers as well. Given that ERCP is a complex procedure,
major complications are bile leak (1% to 2%), sepsis (2% to requiring special equipment and training, the risks and benefits
3%), and hemorrhage (0.2% to 0.4%). Other rare complica- of the procedure must be heavily considered prior to proceed-
tions include pneumothorax, biliothorax, injury to the colon ing. Patients should be alert, oriented, and able to give informed
related to the puncture, and abscess formation. Puncture below consent. In the rare cases where patients are unable to give
the ninth intercostal space will clearly decrease the incidence informed consent, the next of kin can provide consent. Patient
of pleural and lung complications. The risk of infectious com- age and clinical picture are important. Elderly patients can
plications such as sepsis and abscess formation can be mitigated safely undergo ERCP; they have the same risks of bleeding and
with proper antibiotic coverage. Care should be taken to not perforation as younger patients and actually have a lower risk
overdistend the biliary tree, as opacification and incomplete of pancreatitis (Badalov et al, 2009).
drainage of the biliary tree can be a source of cholangitis (Covey Once consent is obtained, the patient is brought into a room
& Brown, 2008), particularly in the presence of bile duct with a C-arm for availability of fluoroscopy during the proce-
isolation. dure. Intravenous sedation is given under monitored control.
In the past, drug combinations of narcotics, such as meperidine
and droperidol, and benzodiazepines, such as midazolam or
ENDOSCOPIC RETROGRADE diazepam, were used. More recently, this has been replaced by
CHOLANGIOPANCREATOGRAPHY propofol, a short-acting sedative and amnestic with a rapid
recovery profile. Studies have shown that propofol is more
History effective than sedation with midazolam, is safe, and is associ-
Endoscopic retrograde cholangiopancreatography (ERCP) (see ated with a faster postprocedure recovery (Fanti et al, 2004;
Chapter 29) was first described in 1968 (McCune et al, 1968) Wehrman et al, 1999). In some centers, general anesthesia may
and rapidly became accepted as an important diagnostic modal- be used if the endoscopic procedure is expected to be difficult,
ity for patients with hepatobiliary and pancreatic diseases the patient has significant comorbid medical conditions, or if
(Cotton, 1977; Cotton et al, 1972; Freeney, 1988; Oi et al, there are any signs of functional or mechanical intestinal
1970). Over the last 4 decades, multiple advances in technology obstruction. Oxygen is administered by nasal cannula to avoid
and training have enhanced and expanded the scope of ERCP. hypoxemia, which has been described in 40% of patients under-
The improvement of the side-viewing duodenoscope with an going ERCP (Woods et al, 1989). The patient’s electrocardio-
elevator helped facilitate cannulation of the papilla of Vater gram, blood pressure, oxygen saturation, and overall condition
(Kasugai et al, 1971; Ogoshi et al, 1970; Takagi et al, 1970). are continually monitored throughout the procedure by a dedi-
In addition, the development of therapeutic applications cated nurse. Antibiotics are not given routinely for diagnostic
through ERCP, including sphincterotomy (Classen et al, 1975; procedures. All endoscopic equipment used for this procedure,
Cotton et al, 1976; Kawai et al 1974) and stenting (Laurence including the endoscopes, is either chemically disinfected or gas
et al, 1980; Soehendra et al, 1980), has evolved ERCP from a sterilized.
diagnostic into a therapeutic procedure. ERCP is considered to The patient is placed in a semiprone position with special
be an advanced procedure, requiring skills more difficult to positioning of the arms, to help optimize access to the ampulla
learn than routine endoscopic procedures, and is offered as an of Vater. A side-viewing duodenoscope is used to afford excel-
additional year of training beyond the standard gastroenterol- lent visualization of the ampulla of Vater. In patients with a
ogy fellowship. Billroth II type gastrojejunostomy, a standard forward-viewing
upper endoscope or pediatric colonoscope may be needed to
Indications successfully approach the ampulla. An initial endoscopic evalu-
With the exception of a few scenarios, diagnostic ERCP has ation of the stomach and duodenum is performed before can-
largely been replaced by noninvasive imaging techniques. In nulation of the ampulla. The ampulla is usually located in the
2002, the National Institutes of Health sponsored a consensus second portion of the duodenum but, in rare instances, may be
conference on ERCP and issued a statement proposing the found more proximal or distal. It is usually easily identified,
indications for ERCP (Cohen et al, 2002). They concluded although, in some cases, it may be distorted due to malignancy
382 PART 2  DIAGNOSTIC TECHNIQUES

A B

C D
FIGURE 20.5.  Pancreatic duct stent placement. A, Wire placement into the pancreatic duct. B, Contrast injection to confirm position in pancreatic
duct. C, Placement of a 5-Fr × 5-cm pancreatic duct stent with a full external pigtail and a single internal flap. D, Endoscopic view of 5-Fr pancreatic
duct stent.

or edema from pancreatitis, hidden behind a fold, or within a motility can be controlled by bolus injections of 0.25 to 1 mg
diverticulum. The orifice of the CBD is usually located on the of intravenous glucagon. If the pancreatic duct is inadvertently
left upper corner of the ampulla. In most patients, the CBD cannulated, placement of a pancreatic duct stent may help can-
and main pancreatic duct share a common channel. In a minor- nulation by both blocking the pancreatic duct orifice as well as
ity of patients, the orifices are separate. The minor papilla is by providing more information to the endoscopist about the
located about 1 to 2 cm above the major papilla. The CBD is angle of the bile duct, especially in cases of distorted anatomy
selectively cannulated with either a cannula or sphincterotome. (Fig. 20.5) (Goldberg et al, 2005). Another technique involves
Studies have shown that access to the biliary tree is easier and placing a guidewire into the pancreatic duct, which adds more
faster with a sphincterotome compared with a cannula (Kara- information about the optimal angle to approach cannulation
manolis et al, 2005; Laasch et al, 2003; Rossos et al, 1993). (Fig. 20.6). The studies are limited, but this technique
More recently, some endoscopists have been using guidewire- does not appear to increase the risk of post-ERCP pancreatitis
assisted cannulation. It remains controversial whether insertion (Draganov et al, 2005; Saad, 2004). Other more invasive
of a guidewire, as opposed to the more conventional technique maneuvers, including precut sphincterotomy with or without
of contrast injection, should be the preferred technique to pancreatic duct stent placement, may also improve success rate
access the bile ducts. A guidewire does not produce the hydro- but is associated with an increased risk of complications, includ-
static pressure associated with contrast injection and decreases ing bleeding, perforation, and pancreatitis, even in experienced
the risk of trauma to the pancreatic duct, thereby theoretically hands (Harewood et al, 2002).
decreasing the risk of post-ERCP pancreatitis. The data, Duodenal diverticula are common and almost always are
however, are mixed. A recent meta-analysis looking at 12 ran- located near the papilla in the descending duodenum. Although
domized trials with 3450 patients concluded that wire-guided usually asymptomatic, diverticula have been shown to be asso-
technique had a higher cannulation success rate (84% vs. 77%) ciated with choledocholithiasis. Periampullary diverticula
and a lower risk of post-ERCP pancreatitis (3.5% vs. 6.7%) may make cannulation more difficult, but the data are mixed
(Tse et al, 2013). However, a prospective trial with 1249 (Rajnakova et al, 2003; Tham & Kelly, 2004).
patients showed no significant difference in post-ERCP pancre- In patients with surgically altered anatomy, ERCP may be
atitis in the guidewire group (5.2%) compared with the contrast quite challenging. In patients with a Billroth II gastrojejunos-
injection group (4.4%) (Mariani et al, 2012). tomy, success rates for bile duct cannulation are much lower
In the event of a difficult cannulation, there are techniques (Forbes et al, 1984). The papilla is found in the afferent limb,
to help facilitate access to the bile duct. Excess duodenal which may be difficult to traverse. In addition, the orientation
Chapter 20  Direct cholangiography: approaches, techniques, and current role 383

A B C
FIGURE 20.6.  Guidewire placement in pancreatic duct to facilitate bile duct cannulation. A, Wire placement into pancreatic duct. B, This provided
more information to the endoscopist about the angle of the bile duct, and the cannulatome was adjusted under fluoroscopic guidance. C, Contrast
injection confirmed position in common bile duct.

of the ampulla is upside down compared with standard ERCP.


In patients with Roux-en-Y gastrectomies, it is often difficult
even to reach the papilla, given the long Roux limb. If the
papilla is identified, cannulation may still be extremely difficult
due to the location and position of the ampulla (Byron et al,
2002). Recently, double-balloon enteroscopy has been reported
to be successful in enabling access to the afferent limb (Sato
et al, 2005). This is mostly only offered in tertiary care centers.
ERCP after bariatric surgery is extremely difficult, and most
consider it too complex to attempt.
Once the bile duct is selectively cannulated, a contrast agent
is injected under fluoroscopic control, with subsequent radio-
graphic images obtained of the duct anatomy. Choice of con-
trast agent differs among endoscopists. Many choose to use half
strength contrast when looking for stones. Material for patho-
logic and cytologic evaluation can be obtained from either the
biliary or pancreatic duct system with a variety of dedicated
endoscopic biopsy forceps and cytology brushes. Pathologic
and cytologic material may be obtained from the ampulla of
Vater, duodenum, and stomach for diagnostic purposes during
the procedure as well.

Pancreatography
Imaging the pancreatic duct can be an important adjunct to
cholangiography during ERCP. Strictures, stones, and other FIGURE 20.7.  Pancreas divisum. The cannula is in the major papillary
obstructing lesions can be identified. Most recommend guide- orifice, and contrast injection opacifies the proximal portion of the major
wire cannulation of the pancreatic duct over contrast injection pancreatic duct (Wirsung). Injection through the minor papillae allows
as this produces less hydrostatic pressure in the duct, possibly opacification of the duct of Santorini and the distal duct of Wirsung.
decreasing the risk of post-ERCP pancreatitis. In general, the
pancreatic duct is about 20 cm in length and variable in caliber.
With increasing age comes progressive atrophy and fibrosis of
the pancreas. The diameter of the main pancreatic duct also Cholangioscopy and Pancreatoscopy
increases with age, although one study found no difference in Cholangioscopy and pancreatoscopy involve using miniature
pancreatic duct length among patients younger than 40 years endoscopes through the channel of the duodenoscope, allowing
compared with older patients. Duct diameter throughout the direct visualization of the bile and pancreatic ducts, respec-
pancreas was significantly greater, however, in patients older tively. A new skill set is necessary to perform these procedures,
than 40 years (Anand et al, 1989). given that this technique uses two different endoscopes. Diag-
Anatomic variations, such as pancreas divisum (Fig. 20.7), nostic cholangioscopy may be used to evaluate indeterminate
also may be identified on a pancreatogram (see Chapter 2). This biliary strictures and filling defects. Similarly, diagnostic pan-
abnormality has been described in 7.5% of ERCP procedures creatoscopy may be used to evaluate pancreatic strictures and
and can be confirmed by cannulation of the main pancreatic intraductal papillary mucinous neoplasms. Studies have shown
duct through the orifice in the minor papilla (Bernard et al, that it is an accurate diagnostic tool for patients with pancreati-
1990). cobiliary disorders (Fukuda et al, 2005; Itoi et al, 2010; Yamao
384 PART 2  DIAGNOSTIC TECHNIQUES

et al, 2003). One prospective multicenter study of 87 patients et al, 1985), and a meta-analysis showed no significant differ-
reported that endoscopists were able to distinguish benign from ence in post-ERCP pancreatitis among different contrast media
malignant indeterminate biliary lesions 92.1% of the time with (George et al, 2004).
cholangioscopy with visualization alone (Osanai et al, 2013). Although it remains unclear whether these mechanisms
Complications of cholangiopancreatoscopy include bacteremia, work independently or in conjunction, recent data have helped
bleeding, and pancreatitis. One retrospective study reported to elucidate both patient- and procedure-related risk factors
that complications of cholangiopancreatoscopy are increased that are independently associated with post-ERCP pancreatitis.
compared with ERCP alone and are associated with a much These risk factors are additive (Freeman et al, 2001). Patient-
higher risk of cholangitis (Sethi et al, 2011). related factors include younger age, female sex, normal serum
bilirubin, recurrent pancreatitis, history of post-ERCP pancre-
Complications atitis, and sphincter of Oddi dysfunction. Procedure-related
Complications of ERCP include those associated with endo- factors include difficult cannulation, pancreatic duct injection,
scopic procedures in general as well as those specific to ERCP. precut sphincterotomy, pancreatic sphincterotomy, minor
Incidence rates of complications vary in the literature. A sys- papilla sphincterotomy, balloon sphincteroplasty, ampullec-
tematic survey of prospective studies reviewed 21 studies with tomy, and sphincter of Oddi manometry. One study showed
16,855 patients and reported a specific complication rate of that trainee participation was an independent risk factor (Cheng
6.9% and a mortality rate of 0.33% (Andriulli et al, 2007). The et al, 2006). Most studies, however, have not shown a correla-
experience of the endoscopist and case volume also has an tion between case volume and rates of pancreatitis (Freeman
impact on the complication rate. In a study conducted in et al, 2001; Loperfido et al, 1998; Testoni et al, 2010).
Austria, endoscopists performing more that 50 ERCP proce- Specific techniques and measures to decrease the risk of
dures per year were compared with those performing fewer than pancreatitis have been studied. The risk is reduced by minimiz-
50 per year. Those in the higher case-volume group had a ing the number of attempts of cannulation, avoiding pancreatic
significantly higher success rate (86.9% vs. 80.3%; P < .001) duct cannulation if not necessary, and by avoiding overdisten-
and a lower overall complication rate (10.2% vs. 13.6%; P = sion or “acinarization” of the pancreatic duct by minimizing
.007) (Kapral et al, 2008). the volume of contrast medium into the pancreatic duct.
Placement of a temporary pancreatic duct stent may also
Pancreatitis reduce the risk. One meta-analysis demonstrated that the use
The most common complication of ERCP is pancreatitis, with of pancreatic duct stents in high-risk patients decreased the rate
reported incidences ranging from 1% to 40%, but most fre- of post-ERCP pancreatitis by about two thirds (Singh et al,
quently reported around 3% to 5% (Andriulli et al, 2007; 2004). Their use is not routinely recommended but is reserved
Cheng et al, 2006; Christensen et al, 2004; Freeman et al for high-risk patients. Studies have shown a benefit of pancre-
2001; Loperfido et al, 1998) (see Chapter 54). The incidence atic duct stents in biliary sphincterotomy for sphincter of Oddi
of post-ERCP pancreatitis in children is quite low, about 2.5% dysfunction, precut sphincterotomy, balloon sphincteroplasty,
in one study (Iqbal et al, 2008). The consensus classification endoscopic ampullectomy, and difficult cannulation (Fazel
defined post-ERCP pancreatitis as the clinical picture of new et al, 2003; Freeman et al, 2004; Singh et al, 2004).
or worsened abdominal pain with amylase at least three times Many pharmacologic agents have been studied. A recent
normal at 24 hours after the procedure and requiring hospital- systematic review included 85 randomized clinical trials and 28
ization (Cotton et al, 1991). They further defined it as mild if meta-analyses evaluating pharmacologic prevention of post-
hospitalization is 2 to 3 days, moderate if hospitalization is 4 ERCP pancreatitis. They concluded that rectal nonsteroidal
to 10 days, and severe if hospitalization is more than 10 days, antiinflammatory drugs (NSAIDs) were beneficial, especially in
if there is a pseudocyst or hemorrhagic pancreatitis, or if an high-risk patients. Data on bolus-administered somatostatin,
intervention is required. Post-ERCP pancreatitis should be dis- sublingual nitroglycerin, and some protease inhibitors were
tinguished from transient asymptomatic hyperamylasemia, considered promising, but confirmatory studies are necessary
which occurs in 40% to 75% of cases and disappears within 1 (Kubiliun et al, 2015).
to 2 days (Classen & Demling, 1975; Okuno et al, 1985). Most NSAIDs inhibit prostaglandin synthesis, phospholipase A2
cases of post-ERCP pancreatitis are mild and usually resolve in activity, and neutrophil/endothelial cell attachment, which are
a few days with conservative measures of bowel rest and intra- all thought to play a major role in the pathogenesis of pancre-
venous fluids. The management is the same as for pancreatitis atitis, and thus may have a role in post-ERCP pancreatitis
from other causes. prevention. A meta-analysis that included 10 randomized con-
There have been multiple potential mechanisms proposed trolled trials with a total of 2269 patients concluded that
to explain the pathogenesis of post-ERCP pancreatitis. Mechan- NSAID use decreased the risk of post-ERCP pancreatitis (risk
ical injury to the pancreatic duct from manipulation of the ratio, 0.57; 95% confidence interval [CI], 0.38 to 0.86; P =
papilla, instrumentation of the pancreatic duct, or injection of .007) (Ding et al, 2012). However, these studies were extremely
the pancreatic duct likely plays a role (Johnson et al, 1997). heterogeneous in regard to type of NSAID as well as to route
Similarly, thermal injury from electrocautery leading to edema and timing of administration. A randomized, placebo-
and possible obstruction of the duct has been invoked (Ratani controlled, double-blind clinical trial of high-risk patients
et al, 1999). Hydrostatic pressure from contrast injection showed that patients who received rectal indomethacin imme-
leading to injury is also likely a component. The contrast itself diately after the procedure were less likely to develop post-
theoretically may cause a chemical or allergic injury. However, ERCP pancreatitis than the control group (9.2% vs. 16.9%;
the use of nonionic contrast medium of low osmolarity has P = .0005) and were less likely to develop moderate to severe
shown no advantage over the less expensive ionic contrast pancreatitis (4.4% vs. 8.8%; P = .03) (Elmunzer et al, 2012).
medium in preventing ERCP-related pancreatitis (Hannigan A meta-analysis that specifically looked at studies of rectal
Chapter 20  Direct cholangiography: approaches, techniques, and current role 385

indomethacin included four studies with 1470 patients showed (25%; P = .012) (Hao et al, 2009). In both studies, however,
that the rate of pancreatitis was significantly lower using indo- the consensus definition for pancreatitis was not used, which
methacin compared with placebo (odds ratio, 0.49; CI, 0.34 to may account for the high rates of pancreatitis in the control
.71; P = .0002) (Yaghoobi et al, 2013). A network meta-analysis groups. One recent randomized controlled trial of 300 patients
compared rectal indomethacin to pancreatic duct stenting and showed that the combination of rectal indomethacin and sub-
concluded that rectal indomethacin alone was superior to pan- lingual nitroglycerin was superior to rectal indomethacin alone
creatic duct stenting in post-ERCP prevention (odds ratio, at prevention of post-ERCP pancreatitis (6.7% vs. 15.3%; P =
0.48; 95% CI, 0.26 to 0.87) (Akbar et al, 2013). The European .016) (Sotoudehmanesh et al, 2014). More studies are needed
Society of Gastrointestinal Endoscopy guidelines recommend to further clarify the benefit of nitroglycerin in post-ERCP
routine prophylactic use of rectal NSAIDs immediately before pancreatitis.
or after ERCP in all patients without a contraindication Protease inhibitors, such as gabexate mesylate, nafamostat
(Dumonceau et al, 2014). mesylate, and ulinastatin, have been investigated, given that
Somatostatin and its analogue octreotide inhibit pancreatic activation of proteolytic enzymes likely contributes to the
secretions, decrease sphincter of Oddi pressure, modulate pathogenesis of pancreatitis. A meta-analysis of 18 studies with
cytokines, and lead to apoptosis of pancreatic acinar cells, and a total of 4966 patients showed a significant, yet small, risk
therefore may be protective against post-ERCP pancreatitis. reduction in post-ERCP pancreatitis with the protease inhibi-
They have been studied extensively with conflicting results. tors (Seta & Noguchi, 2011). They stated there was no solid
One meta-analysis included seven homogeneous high-quality evidence to support their use at this time. A recent pilot study
studies involving 3130 patients and concluded that somatosta- investigated whether aggressive periprocedural hydration
tin administered as a bolus was effective in prevention of post- reduced the risk of post-ERCP pancreatitis and found that
ERCP pancreatitis (Rudin et al, 2007). A more recent none of the patients in the aggressive hydration group devel-
meta-analysis looked at 17 studies with a total of 3818 patients oped pancreatitis compared with 17% of patients in the stan-
and found that somatostatin and high-dose octreotide pre- dard hydration group (Buxbaum et al, 2014). Larger studies
vented post-ERCP pancreatitis if given over 12 hours or in are needed to corroborate these findings. Many other agents
bolus form (Omata et al, 2010). Subsequent randomized trials have been investigated, including secretin, corticosteroids, allo-
have yielded mixed results. One double-blinded, placebo- purinol, and topical epinephrine, with conflicting results, and
controlled, randomized study involved 391 patients in three are not recommended at this time.
hospitals. Patients were randomized to receive 3 mg of soma-
tostatin in 500 mL normal saline infused for 12 hours, starting Infection
30 minutes before the ERCP or 500 mL normal saline infused A serious complication of ERCP is the development of post-
for 12 hours, starting 30 minutes before the ERCP. They procedure infectious complications, most commonly cholangi-
found a significantly lower risk of pancreatitis in the soma- tis and cholecystitis. In a systematic survey of 21 prospective
tostatin group (3.6% vs. 9.6% in the placebo group; P = .02) studies with 16,855 patients, the incidence of infectious com-
(Lee et al, 2008). Another study involved 133 patients who plications was 1.4% (Andriulli et al, 2007).
were randomized to a bolus of somatostatin infusion before Cholangitis most commonly occurs when there is failed or
ERCP, followed by continuous infusion for 12 hours, a bolus incomplete biliary drainage. The risk is increased in patients
of somatostatin before ERCP only, and placebo alone; no sig- with hilar obstruction and sclerosing cholangitis, given the
nificant differences were found among the three groups (Chan increased risk of incomplete drainage (Bangarulingam et al,
et al, 2008). A recent randomized trial of 510 patients ran- 2009; Rerknimitr et al, 2004). Other risk factors include jaun-
domized to an intravenous bolus of 250 µg of somatostatin dice, small endoscopy center, and delay in performing ERCP
prior to cannulation, followed by a 4-hour continuous infusion (Loperfido et al, 1998; Navaneethan et al, 2013). Treatment
of the drug at 250 µg/hr, or placebo with normal saline showed involves supportive care with antibiotics and decompression of
no significant difference in rates of post-ERCP pancreatitis the obstruction. Studies have shown that prophylactic antibiot-
(Concepcion et al, 2014). In addition, when pancreatitis has ics significantly reduce the frequency of procedure-related bac-
developed, the use of somatostatin does not improve its clini- teremia but have not shown a difference in rates of cholangitis
cal course (Phillip et al, 1985). Future research is necessary to (Sauter et al, 1990). Two meta-analyses failed to demonstrate
elucidate the role of somatostatin in prevention of post-ERCP a benefit of giving routine prophylactic antibiotics (Bai et al,
pancreatitis. 2009; Harris et al, 1999). Antibiotics added to the injected
Nitroglycerin acts as a smooth muscle relaxant and subse- radiographic contrast medium are also of no benefit (Jendrze-
quently may decrease sphincter of Oddi pressures, thereby jewski et al, 1980).
decreasing the risk of post-ERCP pancreatitis. Only three out It has also been found that endoscopic instruments used in
of seven randomized controlled studies showed that nitroglyc- ERCP can be the source of serious infections (Earnshaw et al,
erin was effective, but two of the three positive studies used 1985). Salmonella species are the most common organisms
sublingual nitroglycerin (Kubiliun et al, 2015). One compared transmitted by contaminated endoscopes (Axon, 1991), and for
2 mg sublingual nitroglycerin given 5 minutes prior to endos- this reason, it is imperative to ensure that the endoscopic equip-
copy with placebo in 186 patients and found a lower incidence ment used for ERCP is adequately disinfected or sterilized.
of pancreatitis in the nitroglycerin group (7/90 vs. 17/96; P <
.05) (Sudhindran et al, 2001). The second one enrolled 74 Bleeding
patients and randomly assigned them to 5 mg sublingual glyc- Bleeding is a rare complication of diagnostic ERCP and is
eryl trinitrate versus 100 mg vitamin C, 5 minutes prior to the most commonly seen with sphincterotomy. Risk factors for
ERCP. They found a significant difference in post-ERCP pan- postsphincterotomy bleeding include bleeding during the
creatitis in the study group (7.9%) compared with placebo procedure, concomitant thrombocytopenia or coagulopathy,
386 PART 2  DIAGNOSTIC TECHNIQUES

anticoagulation started within 3 days of the sphincterotomy, confluence (Figs. 20.10 and 20.11B). A right sectoral duct
and low case volume of the endoscopist (Freeman et al, 1996). crosses to the left to join the left hepatic duct in 28% of cases,
Rarely, there may be a Mallory-Weiss tear from scope trauma according to Healey and Schroy (1953); in 22%, this is the
or submucosal hemorrhage from manipulation of the papilla posterior sectoral duct (see Figs. 20.9B and 20.11B), and in
(Loperfido et al, 1998). There have been case reports of intra- 6%, this is the anterior duct (see Figs. 20.9C and 20.11D).
peritoneal hemorrhage from injury to abdominal vessels, liver, Occasionally, a right sectoral or segmental duct, posterior more
and spleen (Lo et al, 1994; Wu & Katon, 1993). often than anterior, courses inferiorly and enters the common
hepatic duct directly (Fig. 20.12). The confluence of the right
Perforation and left ducts takes the form of a trifurcation rather than a
The most common type of perforation associated with ERCP bifurcation in 12% of cases according to Couinaud (1957; see
is retroperitoneal perforation and is usually associated with Fig. 20.9A).
sphincterotomy, with an incidence ranging from 0.5% to 2.1% In the left lobe, the superior and inferior lateral segment
(Cotton et al, 1991). In their systematic survey of 21 prospec- ducts, segments II and III, unite in the line of, or to the right
tive studies with 16,855 patients, Loperfido and colleagues
(1998) reported 101 perforations (0.6%) and 10 deaths from
perforation (0.06%). Free bowel wall perforation is quite rare
and is usually associated with a structural abnormality such as TABLE 20.1  Segmental Nomenclature
a stricture or Billroth II gastrectomy (Wilkinson et al, 1994). I Caudate lobe
The management of the perforation depends on the size, II Left lateral superior segment
location, and clinical picture. Free bowel wall perforations III Left lateral inferior segment
usually require surgery. Use of endoscopic clips for the treat- IV Left medial segment or quadrate lobe
ment of duodenal perforations has also been reported V Right anterior inferior segment
(Katsinelos et al, 2005; Solomon et al, 2012). VI Right posterior inferior segment
VII Right posterior superior segment
DIRECT CHOLANGIOGRAPHY AND VIII Right anterior superior segment
PANCREATOGRAPHY BY PERCUTANEOUS
TRANSHEPATIC CHOLANGIOGRAPHY OR
ENDOSCOPIC RETROGRADE RPSD
CHOLANGIOPANCREATOGRAPHY RHD
LHD
The anatomy of the bile ducts is discussed in Chapter 2. LHD
Knowledge of the common variations of ductal branching is
essential for accurate interpretations of cholangiograms, and CHD
these are shown in Figures 20.8 and 20.9; segmental nomen-
RASD Sectoral
clature is summarized in Table 20.1. In the right lobe, the
duct
posterior segments lie more laterally than the anterior seg- A D
ments, so that the most lateral ducts on a cholangiogram are
usually segments VI inferiorly and VII superiorly. The posterior RPSD
sectoral duct is often recognizable by an arched course near the
RHD
II
RPSD LHD
III
VII VIII
II RASD
IV
I B E

VI
V IV III RHD
RPSD
II
RASD LHD

IV III
RHD
LHD

CHD
RASD
FIGURE 20.8.  Standard intrahepatic ductal anatomy. The seg-
ments are numbered according to Couinaud’s description (see Table C F
20.1). CHD, Common hepatic duct; LHD, left hepatic duct; RASD, right FIGURE 20.9.  Variations of perihilar ductal anatomy. CHD, Com-
anterior sectoral duct; RHD, right hepatic duct; RPSD, right posterior mon hepatic duct; LHD, left hepatic duct; RASD, right anterior sectoral
sectoral duct. duct; RHD, right hepatic duct; RPSD, right posterior sectoral duct.
Chapter 20  Direct cholangiography: approaches, techniques, and current role 387

The upper limits of normal for the diameter of the extrahe-


patic bile ducts as measured by ERCP vary between 9 and
14 mm (Niederau et al, 1984). Combined radiologic and
manometric studies (Poralla et al, 1985) have shown that even
in the absence of extrahepatic cholestasis, the diameter of the
bile ducts and the pressure difference therein increases with
advancing age. The diameter of the bile ducts as measured by
ultrasonography is less than those measurements obtained
during ERCP (Niederau et al, 1984). Anatomic abnormalities
of the hepatobiliary system include cystic dilations (Fig. 20.13)
of the bile duct or of the intrahepatic bile ducts (Caroli disease;
see Chapter 46). There is a wide variation in where the cystic
duct joins the common hepatic duct. A low junction with a
correspondingly long cystic duct (Fig. 20.14) may result in
difficulties if not recognized. This is especially true when a
cholecystojejunostomy is performed as a palliative biliary bypass
for carcinoma of the head of the pancreas, and the jaundice
either is not relieved or recurs rapidly in the postoperative
period.

Interpretations
FIGURE 20.10.  Hilar cholangiocarcinoma involving first-order right Because of its inherent weakness of only allowing visualization
hepatic duct, proximal common hepatic duct, and faintly opacified left of the bile duct lumen, the main problem with the use of direct
hepatic duct (arrowhead). Note the characteristic arched course of the cholangiography is its lack of specificity. There are few, if any,
right posterior sectoral duct (arrow). pathognomonic radiologic findings. Many disease entities, from
benign to malignant, overlap greatly in their cholangiographic
appearances. The combination of history, blood markers, asso-
ciated radiologic findings, and clinical scenario can often sig-
TABLE 20.2  Average Duct Diameters Measured Directly from
nificantly narrow the differential diagnosis. However, it must
50 Normal Percutaneous Transhepatic Cholangiography be stressed strongly that because the cholangiographic appear-
Examinations ance of many biliary diseases may be indistinguishable, biopsy
Duct Diameter (mm) is often required to rule out malignancy or to confirm suspected
Right hepatic = 4.7 diagnosis.
Left hepatic = 5.2
Bile Leaks
Common hepatic = 6.5
Bile leaks are seen as sites of free extravasation of contrast
Common bile = 7.6
agent at a site of bile duct injury. Injury may be secondary to
From Okuda K, et al: Frequency of intrahepatic arteriovenous fistula as a sequela to percutaneous trauma, but most commonly it is iatrogenic in nature. Associ-
needle puncture of the liver, Gastroenterology 74:1204–1207, 1978.
ated bilomas may be seen at the point of bile leak. Diagnosis
of bile leak can usually be made by noninvasive imaging
techniques such as ultrasound, CT or MRI, but because the
of, the umbilical fissure in 92% of cases. In the latter instance, intrahepatic bile ducts are usually not dilated, a bile leak may
the quadrate lobe, segment IV, may drain wholly or partially not be evident on imaging. Cholescintography with techne-
into the segment II duct. Rarely, segment II and III ducts join tium 99m–hepatic iminodiacetic acid (HIDA scan) may be
at or close to the confluence (see Figs. 20.9E and 20.11C), and useful for diagnosis when the other imaging modalities are
segment IV drains directly into the common hepatic duct in inconclusive. ERCP can diagnose bile duct leaks effectively
1% of cases (see Fig. 20.9F) (Healey & Schroy, 1953). but is usually reserved for cases when a therapeutic interven-
The caudate ducts are often difficult to identify. Usually two tion is anticipated.
or three ducts drain most commonly into the right posterior
sectoral duct, right hepatic duct, or left hepatic duct (Healey Filling Defects
& Schroy, 1953). The recognizable caudate ducts are usually a Air Bubbles, Blood Clots, Calculi, Primary and Secondary Bile
few centimeters long and drain downward or to the right. Duct Cancers, and Parasitic Diseases
The left hepatic duct (average length, 17 mm) is consider- Air bubbles, although confusing, most commonly declare
ably longer than the right hepatic duct (average length, 9 mm) themselves by their perfectly circular shape and their distribu-
and has a longer extrahepatic course. The normal diameters of tion to nondependent structures. Blood clots in the bile duct
the main bile ducts as measured at PTC are shown in Table are seen more frequently with PTC than with ERCP. Hemobi-
20.2. These figures are greater than the true duct dimensions lia can sometimes take more than 48 hours to resolve, and when
because of some distension produced by direct cholangiogra- it is more severe, it can be castlike and may mask other filling
phy, together with considerable magnification occurring on any defects (see Chapter 125).
fluoroscopic “spot film.” The magnification is of the order of Calculous disease (see Chapters 36 and 39) remains the
40% (Nichols & Burhenne, 1984) and affects all structures in most common filling defect in the biliary system. Distinguishing
the image, including calculi, tubes, and strictures. characteristics of gallstones and primary bile duct calculi
388 PART 2  DIAGNOSTIC TECHNIQUES

A B

C D
FIGURE 20.11.  Postcholecystectomy strictures graded according to Bismuth. A, Grade I (>2 cm from the confluence of the right and left hepatic
ducts; arrowheads): Calculi lie above and below the stricture (arrow). B, Grade II (<2 cm from the confluence): There has been a previous hepato-
jejunostomy; the right posterior sectoral duct (arrowhead) has an exaggerated arched course and enters the left hepatic duct as a normal variant.
C, Grade III (the confluence is involved by stricture, but the right and left hepatic ducts are not completely separated): Ducts of segment II (white
arrow) and segment III (black arrow) join the confluence independently as a normal variant. D, Grade IV (the right and left ducts are separated by
the stricture): The right anterior sectoral duct (A) is draining into the left hepatic duct (L), which is separated from the right posterior sectoral duct (P)
by the stricture (arrows).

include a faceted appearance and disposition to move to gravity- more unusual causes of cholangiographic filling defects (Riopel,
dependent positions. Calculi may be seen as discrete filling 1997).
defects (Figs. 20.15 and 20.16) or castlike structures filling Parasitic infections, such as hydatid disease (see Chapter 74)
entire ducts, as occurs in recurrent pyogenic cholangitis, cystic and infections with Ascaris lumbricoides or Clonorchis sinensis (see
diseases of the bile ducts, or even proximal to strictures of any Chapter 45), are diseases with worldwide distribution that can
etiology. Impacted calculi may be difficult to differentiate from also present cholangiographically as intraductal filling defects.
strictures or tumors. A proportion of hepatic hydatid cysts (5% to 10%) rupture into
Primary bile duct cancer (see Chapter 51), specifically papil- the bile ducts and may simulate choledocholithiasis. Calcified
lary cholangiocarcinomas, can also present as cholangiographic cysts are easy to recognize on radiographs, and daughter cysts
filling defects (Fig. 20.17). T-shaped filling defects may also be can cause biliary obstruction. When the calcified cyst is not
detected (Fig. 20.18 ) (Torok & Gores, 2001), and papillary obvious, biliary strictures with obstruction may be noted on
bile duct cancers may cause filling defects as a result of mucin cholangiogram. The biliary ducts can show considerable irregu-
production (Fig. 20.19). Other malignancies, including mela- larities in caliber and extensive displacement of the intrahepatic
noma and intraductal metastases, such as colon cancer, are also branches secondary to the mass effect of a large hydatid cyst
Chapter 20  Direct cholangiography: approaches, techniques, and current role 389

FIGURE 20.12.  Pancreatitis producing a typical, incomplete long stric-


ture of the common bile duct. The right posterior sectoral duct has a
low entrance into the common hepatic duct, an uncommon but impor-
tant normal variant. FIGURE 20.13.  Choledochal cyst.

FIGURE 20.14.  Long cystic duct. FIGURE 20.15.  Choledocholithiasis.


390 PART 2  DIAGNOSTIC TECHNIQUES

FIGURE 20.16.  Benign stricture of the right hepatic duct (arrow) with
multiple ductal calculi proximal to it. The hepatojejunostomy is partially
strictured.

FIGURE 20.17.  Papillary hilar cholangiocarcinoma (arrowheads). Only


the right ducts are opacified.

FIGURE 20.18.  “Golf tee” appearance of a papillary bile duct cancer FIGURE 20.19.  Nasobiliary cholangiogram opacifying left hepatic
(arrow) involving the common hepatic duct. ducts. Main left hepatic duct contains a small mucin-secreting papillary
cholangiocarcinoma (arrow). The mucin results in expansion of the
common bile duct below the tumor and appears as strandlike filling
defects. (Courtesy Dr. A. Speer.)
Chapter 20  Direct cholangiography: approaches, techniques, and current role 391

FIGURE 20.21.  Extracted liver flukes.

biliary sludge and stones, and intrahepatic duct strictures,


which are predominantly found in the branches of the left
hepatic duct (Yellin & Donovan, 1981). The eggs of C. sinensis
act as a nucleus for the development of the bile duct stones
(Lam et al, 1978). Naval and colleagues (1984) reported suc-
FIGURE 20.20.  Liver flukes in the distal bile duct presenting as “biliary cessful endoscopic biliary lavage to eliminate the eggs.
sludge.” Invasion of Fasciola hepatica into the biliary tract also may
cause serious lesions (see Chapter 45). In the chronic stage, F.
hepatica infection can resemble sclerosing cholangitis (Hauser
(Cottone et al, 1978; Dyrszka & Sanghavi, 1983; Ibrahim & & Bynum, 1984). The appearance on ERCP is that of dilated
Kawanishi, 1981). bile ducts with unexplained sludge in the distal bile duct (Figs.
Ascaris lumbricoides is a commonly seen helminth with a 20.20 and 20.21).
prevalence of 90% in some parts of Africa and Asia (see Chapter
45). If the worm passes through the sphincter of Oddi, it may CONCLUSION
cause acute pancreatitis or a cholestasis syndrome (Winters
et al, 1984). In the acute stage, the worm occasionally may be The role of direct cholangiography in the diagnosis of biliary
found and extracted from the ampulla, and it can be detected disease has for the most part been supplanted by less invasive
in the biliary tract by cholangiography. imaging modalities, such as MR cholangiography and CT with
Eating raw meat has been associated with Clonorchis sinensis contrast. The ability to visualize the entire biliary tree, the bile
infestation. The prevalence of this disease has been estimated duct wall, and other structures other than the bile duct lumen
to be 60% of the general population of Hong Kong, based on increases the diagnostic accuracy and clinical utility of these
stool ova examinations. This worm can penetrate through the noninvasive techniques, which have become the gold standard
papilla into the bile ducts. In an ERCP study of 31 consecutive for cholangiography. Direct cholangiography is generally
patients, the typical filamentous, wavy, or elliptic appearance reserved for clinical scenarios involving concomitantly planned
of the worm in the bile ducts was believed to be pathogno- therapeutic interventions.
monic. Other common cholangiographic findings include
widely dilated extrahepatic bile ducts, which are filled with References are available at expertconsult.com.
Chapter 20  Direct cholangiography: approaches, techniques, and current role 391.e1

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Gastroenterol 109(6):903–909, 2014. 1991.
Stroszczynski C, Hünerbein M: Malignant biliary obstruction: value of Wilkinson ML, et al: Intestinal perforation after ERCP in Billroth II
imaging findings, Abdom Imaging 30(3):314–323, 2005. partial gastrectomy, Gastrointest Endosc 40(3):389–390, 1994.
Sudhindran S, et al: Prospective randomized double-blind placebo- Winters C, et al: Endoscopic documentation of Ascaris-induced acute
controlled trial of glyceryl trinitrate in endoscopic retrograde pancreatitis, Gastrointest Endosc 30:83–84, 1984.
cholangiopancreatography-induced pancreatitis, Br J Surg 88(9): Woods SD, et al: Hypoxia and tachycardia during endoscopic retro-
1178–1182, 2001. grade cholangiopancreatography: detection by pulse oximetry, Gas-
Takagi K, et al: Retrograde pancreatography and cholangiography by trointest Endosc 35:523–525, 1989.
fiber-duodenoscope, Gastroenterology 59:445–452, 1970. Wu WC, Katon RM: Injury to the liver and spleen after diagnostic
Testoni PA, et al: Risk factors for post-ERCP pancreatitis in high- and ERCP, Gastrointest Endosc 39(6):824–827, 1993.
low-volume centers and among experts and non-expert operators, a Yaghoobi M, et al: Meta-analysis: rectal indomethacin for the preven-
prospective multicenter study, Am J Gastroenterol 105:1753–1761, tion of post-ERCP pancreatitis, Aliment Pharmacol Ther 38:995–
2010. 1001, 2013.
Tham TCK, Kelly M: Periampullary duodenal diverticula, bile duct Yamao K, et al: Efficacy of peroral pancreatoscopy in the diagnosis of
stones, and ERCP, Endoscopy 36:1050–1053, 2004. pancreatic diseases, Gastrointest Endosc 57(2):205–209, 2003.
Torok N, Gores GJ: Cholangiocarcinoma, Semin Gastrointest Dis Yellin AE, Donovan AJ: Biliary lithiasis and helminthiasis, Am J Surg
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Endoscopy 45(8):605–618, 2013.
CHAPTER 21 
Diagnostic angiography in hepatobiliary and
pancreatic disease: indications
Hooman Yarmohammadi

OVERVIEW ANGIOGRAPHY TECHNIQUE


Indications for catheter angiography have substantially During the past few years, the angiography suites have been
changed. This is mainly due to the development of noninvasive updated with state-of-the-art imaging technology. Cut-film
imaging modalities such as multidetector computed tomogra- angiography has been replaced with digital flat-panel detectors
phy (MDCT) (see Chapter 18) and magnetic resonance and biplane angiography units. Biplane angiography is capable
imaging (MRI) (see Chapter 19). These imaging techniques of producing high-quality images in 3D views. These advances
can accurately demonstrate the visceral arterial and venous in technology allow for less contrast and minimum radiation
structures and are not associated with the morbidities of cath- exposure to the patients and the interventionalists.
eter angiography. Depending on the procedure, catheter angiography may be
Catheter angiography was commonly used for evaluation of performed under conscious sedation or general anesthesia.
the hepatic arterial anatomy, preoperative planning before liver Most procedures are performed as an outpatient procedure;
resection, assessment of vascular invasion by pancreatic cancer however, some patients may require overnight stay predomi-
or cholangiocarcinoma and to ascertain the organ of origin of nantly for pain control. All patients are seen in the clinic before
an abdominal mass. However, CT angiography (see Chapter the diagnostic or interventional catheter angiography proce-
18) and magnetic resonance angiography (MRA) (see Chapter dure. During this clinic visit, indications for performing the
19) have completely replaced catheter angiography for these procedure are reviewed. Additionally, patients are assessed for
indications. Currently, the main indications for catheter angi- any history of heart disease, lung disease, or renal problems.
ography are for treatment and intervention purposes, including Prior history of angiography or other surgical interventions are
embolization of gastrointestinal bleeding (see Chapters 27, 124, also assessed. Thorough physical examination, which includes
and 125), hepatic artery embolization and chemoembolization detailed pulse examination and assessment of airways, lungs,
(see Chapter 96A), pretreatment mapping and arterial anatomy and heart, is performed. Finally, patients’ performance status is
assessment prior to radioembolization (see Chapter 96B), and evaluated. Most institutions either use Eastern Cooperation
chemoperfusion (see Chapters 99 and 102). Oncology Group performance status or the Karnofsky perfor-
Recent progress in imaging technology, including advances mance status. The procedure is explained to the patient in
in C-arm cone-beam technology, has enabled the visualization detail, and after reviewing the risks and benefits of the proce-
of three-dimensional (3D) vascular anatomy with a single dure, consent is obtained.
acquisition by using nonselective C-arm computed tomography The relevant laboratory parameters include serum creatinine
(CBCT). Such capability allows visualization of the vascular or estimated glomerular filtration rate, hematocrit level, platelet
tree associated with the target tumor from multiple projections count, and international normalized ratio (INR), and these
during an embolization procedure. In addition to these should be reviewed. Additionally, at our practice a baseline 12
advances, another technologic advance is the development of lead electrocardiogram is obtained.
hybrid imaging. Hybrid imaging, or fusion of images, couples In patients with significant morbidities, a cardiology or
two imaging modalities to create unique images that can provide geriatric consult may be requested before the procedure to
information that would not be available with either technique ensure safety of conscious sedation or general anesthesia.
alone. Catheter angiography can be coupled with a cross- If the patient has impairment of renal function, a number of
sectional imaging modality, usually MDCT and, occasionally, prophylactic measures have been recommended to diminish the
MRI. The images can be postprocessed and rendered in a 3D risk of contrast-induced renal failure. These measures include
format to provide an anatomic depiction that would not be intravenous hydration with a sodium bicarbonate solution as
available by either technique alone. well as the administration of N-acetyl cysteine. The effective-
In this chapter, we will discuss angiographic anatomy relevant ness of these prophylactic measures is controversial; however,
to hepatobiliary and pancreatic surgery and discuss the main they carry a minimal risk to the patient and have been adopted
current indications for performing catheter angiography relevant by the majority of practitioners.
to hepatobiliary and pancreas. Additionally, we will discuss The risk of bleeding from the puncture site is low, and
localization of occult neuroendocrine tumors of the pancreas. hematomas complicate 1% of femoral punctures and 3% of
Our discussion on splanchnic veins will include venographic upper extremity punctures. An abnormal bleeding profile related
anatomy, venous sampling, techniques of catheter-based venous to thrombocytopenia or prolongation of the INR increases
imaging, and venous imaging before surgical or percutaneous the risk of hemorrhage. The necessity to correct an underlying
venous interventions. coagulopathy is dependent upon the specific procedure to be

392
Chapter 21  Diagnostic angiography in hepatobiliary and pancreatic disease: indications 393

performed and the preference of the angiographer. Based on the


recommendations from the Society of Interventional Radiology
(SIR) consensus guideline, catheter angiography (arterial inter- RHA
vention with access size up to 7 Fr) is classified as a category II
CyA LHA
procedure with moderate risk of bleeding. SIR recommends
platelet count higher than 50,000 × 106 per liter and an INR of
LGA
1.5 or less (Patel et al, 2013). Patients are advised to stop eating
6 hours prior to the procedure. Intravenous hydration is recom- CHA
RGEA GDA
mended before, during, and after the arteriogram to diminish
adverse effects of contrast media on renal function. The patient RGA SA
should also be encouraged to drink plenty of fluids following CA
the procedure.
The right common femoral artery is the most common
puncture site. The left common femoral artery, axillary artery,
brachial artery, or radial artery may be used as alternatives
when clinically appropriate. In the past few years, the radial
artery puncture site is becoming more favorable, particularly
with interventional cardiology procedures. A transradial FIGURE 21.1  Conventional celiac artery anatomy. CA, Celiac axis;
approach with regard to bleeding complications allows immedi- CHA, common hepatic artery; CyA, cystic artery; GDA, gastroduodenal
ate postprocedure ambulation, which is usually appreciated by artery; LGA, left gastric artery; LHA, left hepatic artery; RGA, right gastric
the patients. Additionally, recent studies demonstrate similar artery; RGEA, right gastroepiploic artery; RHA, right hepatic artery; SA,
procedural and clinical outcomes compared with a transfemoral splenic artery.
approach (Kiemeneij et al, 1997). The desired puncture area is
cleansed, and the patient is draped in sterile fashion. In most
centers, arterial entry is performed under real-time ultrasound
guidance by using a 21 gauge micropuncture set. The use of
ultrasonography allows assessment of the quality of the common
femoral artery, depicts the position of the profunda femoris,
and detects the presence of aberrant veins extending ventral to II
the puncture site. Following entry into the vessel, the appropri-
ate catheter is inserted for catheterization of the desired vessel. VIII IV
III
After diagnostically adequate images are obtained, the catheter
V
is removed, and one of a variety of closure devices is deployed
VII LHA
to seal the arteriotomy. Patients are observed in a postproce- RHA
dural area until they have recovered from sedation, and most
VI PHA
can be discharged home 2 to 4 hours later.

HEPATOBILIARY AND PANCREATIC


ARTERIAL ANATOMY
Arterial Anatomy
Arterial anatomy has been discussed elsewhere (see Chapters
1 and 2) and will be only briefly reviewed here. The most fre-
quently encountered anatomy (Fig. 21.1) is the left gastric
FIGURE 21.2  Arterial anatomy of the liver. LHA, Left hepatic artery;
artery, splenic artery, and common hepatic artery (CHA), PHA, proper hepatic artery; RHA, right hepatic artery. Additional vessels
taking origin from the celiac axis. The CHA divides into the are labeled in accordance to the Couinaud segment they supply.
gastroduodenal artery (GDA) and proper hepatic artery, with
the latter dividing into the right and left hepatic arteries. The
right gastric artery most often originates from the base of the variant origins. When the entire vessel has a variant origin, it is
left hepatic artery, and the cystic artery most often originates termed replaced. If the entire trunk does not take a variant
from the right hepatic artery (RHA), but considerable varia- origin, the vessel is termed accessory. For example, if the right
tions in the origins of these arteries exist (Kobayashi et al, lobe is supplied by a RHA originating from the CHA, as well
2014). Moreover, accessory duodenal arteries, either represent- as a RHA taking origin from the SMA, the latter would be
ing a supraduodenal or a retroduodenal artery, are frequently termed an accessory RHA. If the entire right lobe was supplied
encountered; this is critical to recognize when embolization, by an artery taking origin from the SMA, it would be called a
chemoembolization, and radioembolization are planned. replaced RHA.
The normal arterial supply to the liver is shown in Fig. 21.2, In most patients, the arteries to Couinaud segments I, II,
which shows the commonly recognized variations of the left III, and IV are branches of the LHA, and arteries to segments
hepatic artery (LHA), taking origin from the left gastric artery, V, VI, VII, and VIII are branches of the RHA. The most variable
and the RHA, taking origin from the superior mesenteric artery segmental branch is to segment IV. Although most frequently
(SMA). It is important to recognize that either a part or the the artery to segment IV takes origin from the LHA, it may also
entirety of the right and left hepatic arteries may have these take origin from the RHA, assuming the misnomer of a “middle
394 PART 2  DIAGNOSTIC TECHNIQUES

hepatic” artery in older works. Separate origins of segment IVA, confluence, but it may also enter the SMV either at or just
usually from the LHA, and segment IVB from the RHA are caudal to the confluence. The coronary vein most often drains
frequently identified. Also, a branch from the segment IV artery into the cephalic aspect of the main portal vein just beyond the
is often seen extending outside of the liver, supplying the confluence of the SMV and splenic vein. The number and
falciform ligament. Recognition of this vessel is important when location of veins draining the pancreas is variable. Multiple
embolization, chemoembolization, or radioembolization are small, unnamed veins drain directly into the splenic vein. Typi-
conducted to avoid nontarget embolization. cally, the anterior-superior pancreaticoduodenal vein drains
The RHA conventionally divides into an anterior (ventral) directly into the portal vein, and the posterior-superior pancre-
and a posterior (dorsal) branch. The anterior branch usually is aticoduodenal vein drains into the SMV. The inferior pancre-
more vertically oriented and supplies segments V and VIII. The aticoduodenal veins drain into the SMV at the caudal margin
posterior branch is usually more horizontally oriented and of the pancreas, and the portal vein courses obliquely cephalad
supplies segments VI and VII. More than one projection is from near the midline toward the liver, where it divides to
usually required to ascertain with certainty which is the anterior supply the right and left lobes. This division, as well as the
branch and which the posterior branch. In the right anterior division into segmental branches, is variable and must be
oblique projection, the anterior branch moves medially and the delineated when clinically relevant for each individual patient.
posterior branch moves laterally when compared with the
posteroanterior projection. The entire segmental arterial supply ANGIOGRAPHY INDICATIONS
to the liver should be accounted for before hepatic arterial
therapy (see Chapters 96 and 99), major hepatic resection, As mentioned earlier in this chapter, historic indications
partial hepatectomy (see Chapter 103), or living-donor liver for performing diagnostic catheter angiography have been
transplantation (see Chapters 104 and 117). replaced by multidetector computed tomography angiography
The arterial supply to the pancreas is somewhat variable. (MDCTA), including visceral angiography to assess the resect-
The most consistent supply is to the pancreatic head, through ability of pancreatic and biliary tract tumors by demonstrating
an arcade formed by the inferior pancreaticoduodenal branch presence or absence of vascular invasion; angiography for
of the SMA to the anterior- and posterior-superior pancreati- diagnosis of a hepatic mass, such as differentiating a cavernous
coduodenal branches of the GDA (Fig. 21.3). The transverse hemangioma from a hepatocellular carcinoma; and preopera-
pancreatic artery runs along the middle portion of the long axis tive arterial mapping of the arterial anatomy of the liver prior
of the pancreas and may take origin from the arterial arcade in to major hepatic resection. MDCTA provides higher sensitivity
the head of the pancreas, directly from the GDA, or as a branch and diagnostic accuracy for these indications. On rare occa-
of the dorsal pancreatic artery, which variably originates from sions, there is a specific piece of critical anatomic information
the CHA or the splenic artery (Fig. 21.4). A number of small that cannot be ascertained with certainty by MDCTA, such as
branches from the splenic artery supply the pancreatic body the origin and course of the artery to segment IV prior to a
and tail, but the number and location of these arteries vary and living-donor partial hepatectomy. In this circumstance, catheter
must be identified in each individual patient when clinically angiography can be useful to answer the question.
relevant. On extremely rare occasions, large tumors are identified on
cross-sectional imaging, but the organ of origin cannot be
Venous Anatomy determined. The majority of these are large sarcomas of the
The splenic vein and superior mesenteric vein (SMV) join retroperitoneum, but excluding a pancreatic source may be
to form the main portal vein (see Chapter 2). The inferior difficult. A similar situation can occur with large right adrenal
mesenteric vein usually enters the splenic adjacent to the or renal tumors blending with the hepatic parenchyma. In these

GDA

RGA
PSPD
DP

ASPD
TP

FIGURE 21.3  Arterial anatomy of the pancreas. ASPD, Anterior-


superior pancreaticoduodenal artery; GDA, gastroduodenal artery;
PSPD, posterior-superior pancreaticoduodenal artery; RGA, right gastric FIGURE 21.4  Arterial anatomy of the pancreas. DP, Dorsal pancreatic
artery. artery; TP, transverse pancreatic artery.
Chapter 21  Diagnostic angiography in hepatobiliary and pancreatic disease: indications 395

highly selected cases, catheter angiography can be useful in 5. Diagnosis of vasculitis


delineating the organ of origin by demonstrating the primary 6. Diagnosis of other visceral vascular disease
arterial supply. 7. Localization of functional pancreatic neuroendocrine tumors
In recent years, the most common indication for arteri­
ography is planning an arterial-based intervention, such as Treatment of Bleeding/Hemorrhage
embolization, chemoembolization, radioembolization, or che- Bleeding from the liver, spleen or pancreas is most often sec-
moperfusion, to treat a primary or metastatic hepatic malig- ondary to iatrogenic or noniatrogenic trauma (see Chapters 122
nancy. These specific interventions will be discussed elsewhere to 125), but it may occur spontaneously in patients with mycotic
in this book (see Chapters 96 and 99). Accurate delineation of aneurysms or pancreatitis. Angiography is usually not used to
arterial anatomy is remarkably important in procedures such as ascertain whether arterial hemorrhage is present, but rather to
embolization, chemoembolization, and radioembolization. precisely localize and treat the bleeding vessel. Embolization of
Inadvertent administration of embolic particles, radiation par- arterial bleeding will be discussed elsewhere in this book, but
ticles, or chemotherapeutic agents into arteries supplying the salient features will be reviewed in this chapter.
stomach or duodenum can lead to significant adverse outcomes
(Riaz et al, 2009). Communications from intrahepatic branches Splenic Bleeding
to the lower esophagus, stomach, and diaphragm are of equal The most common cause of bleeding from the spleen is blunt
importance (Miyayama et al, 2009). trauma, and nonoperative management is currently the stan-
As explained earlier in this chapter, most modern angiogra- dard of practice. Splenic artery embolization has been estab-
phy suites are equipped with CBCT imaging technology. This lished as a method to increase the success rate of nonoperative
technology uses a fixed C-arm system equipped with a flat- management of traumatic splenic injuries (Schnuriger et al,
panel detector and requires 3D CT volumetric images (Tacher 2011). A comparative study between two cohorts consisting of
et al, 2015). CBCT has improved the feasibility, effectiveness, 625 patients during a 15 year period revealed an improved
and safety of many image-guided procedures by allowing the success rate of nonoperative management from 77% to 96%
interventionalist to identify extrahepatic perfusion from aber- with the advent of splenic embolization (Rajani et al, 2006).
rant hepatic arterial branches (Fig. 21.5). The indications for splenic arteriography and splenic arterial
Other current indications of performing catheter angiogra- embolization are based upon CT findings and include active
phy in the hepatobiliary and pancreatic system are as follows: contrast blush beyond or within the splenic parenchyma,
1. Treatment of bleeding/hemorrhage from liver, spleen, and pseudoaneurysm, an associated large hemoperitoneum, and a
pancreas high-grade splenic injury (Schnuriger et al, 2011). Moreover,
2. Diagnosis of arterial occlusive diseases the American Association for the Surgery of Trauma recom-
3. Diagnosis and treatment of arterial stenosis mends angiography for grade III, IV, and V splenic injuries
4. Treatment of visceral arterial aneurysms (Raikhlin et al, 2008).

A B
FIGURE 21.5  Extrahepatic perfusion detected with C-arm computed tomography (CCT). A, Selective cystic arteriogram shows the gallbladder and
several branches extending medially (arrow). B, CCT performed during contrast injection of the cystic artery confirms aberrant perfusion of the
duodenum (arrowheads). (Courtesy Daniel Sze, Stanford University.)
396 PART 2  DIAGNOSTIC TECHNIQUES

Two techniques are used to perform splenic embolization: Obviously, the contribution of the embolization to these com-
the first is occlusion of the proximal splenic artery with coils or plications may be difficult to distinguish from sequelae of the
Amplatzer plugs (AGA Medical, Plymouth, MN), and the underlying traumatic injury.
second is selective small intrasplenic arterial embolization with Iatrogenic injury to the hepatic artery is suspected when a
a gelatin sponge or coils. Collaterals through the short gastric biliary drainage tube puts out blood following placement, or
arteries and the gastroepiploic arcade usually maintain splenic melena secondary to hemobilia develops in the patient follow-
viability following occlusion of the proximal splenic artery. ing an intervention through the hepatic parenchyma. CT in
Intrasplenic embolization generally results in a variable degree these patients may or may not reveal an abnormality, and
of splenic infarction, depending upon the size of the artery patients should undergo hepatic arteriography when a clinical
occluded, as intrasplenic arteries have no significant collateral suspicion of a hepatic arterial injury exists. Patients with iatro-
routes. Both techniques have equivalent rates of major infarc- genic injuries usually have a single, discrete bleeding source that
tions and infections requiring splenectomy (Ekeh et al, 2013). can be addressed with superselective embolization techniques.
Distal splenic embolization is associated with higher rates of Complications related to the embolization procedure tend to
infarction; however, these infarctions are limited to the seg- be lower when compared with patients who have had blunt
ments just distal to the site of embolization with questionable trauma, as the traumatic injury to the liver is less extensive.
clinical relevance. In summary, the current literature is incon-
clusive regarding whether the proximal or distal embolization Pancreas Bleeding
should be used. Minor complications including fever, pleural Bleeding is more commonly encountered in patients with
effusion, and partial splenic infarction have been reported in as pancreatitis (see Chapter 56) or pancreatic surgery (see Chap-
many as 34% of patients. Major complications including ters 66 and 67). Posttrauma bleeding from the pancreas is not
splenic abscesses, splenic infarction, splenic atrophy, and post- common. Hemorrhage can occur in the retroperitoneum, or it
procedure bleeding have been observed in 14% of patients may extend from the retroperitoneum into the peritoneal cavity
(Ekeh et al, 2013). or into the gastrointestinal tract via communication with the
pancreatic duct (hemosuccus pancreaticus). Vascular complica-
Hepatic Bleeding tions are seen in 25% of patients suffering from pancreatitis and
Hemorrhage from the liver may be encountered from blunt or are usually arterial in origin. Proteolytic enzymes coupled with
penetrating trauma (see Chapter 122) but is most commonly intense inflammation can erode small arterial branches and
due to an iatrogenic injury related to a biopsy (see Chapter 22) create foci of extravasation or create small pseudoaneurysms.
or percutaneous transhepatic biliary drainage (PTBD) (see Although this complication is encountered in only 2% to 5%
Chapters 30 and 52). Arteriographic findings indicating a of cases, it may be life threatening. Pseudocysts may erode small
source of hemorrhage include extravasation, pseudoaneurysm arterial branches, leading to hemorrhage within the pseudocyst,
formation, and/or arteriovenous fistula (see Chapter 124). or it may erode into larger arterial branches and create a large
Superselective catheterization by using coaxial microcatheters pseudoaneurysm (Fig. 21.6). These pseudoaneurysms are most
to deposit coil-spring emboli both distal and proximal to the frequently identified in the splenic artery or its branches (60%
area of injury is the preferred technique for embolization when to 65%), followed by the GDA (20% to 25%), pancreaticoduo-
a discrete bleeding site can be identified. In contrast to the denal arteries (10% to 15%), hepatic artery (5% to 10%), and
spleen, a rich collateral network exists in the hepatic arterial left gastric artery (2% to 5%) (Aswani et al, 2015; Kirby et al,
bed, making proximal occlusion of the offending artery ineffec- 2008).
tive in many cases. For more diffuse injuries with multiple MDCT has been reported to have 90% sensitivity in detect-
bleeding sites secondary to blunt trauma, using particulate ing pseudoaneurysms in patients with acute pancreatitis;
embolization with a gelatin sponge may be a useful adjunct. however, tiny aneurysms in the intrapancreatic arteries may
As with blunt splenic injuries, nonoperative management not be visible (Hyare et al, 2006). When a patient has clinical
has become the preferred method of management of hemody- evidence of significant hemorrhage, or a CT scan reveals a
namically stable patients. The success rate of this management pseudoaneurysm, arteriography followed by embolization is
exceeds 90% (Christmas et al, 2005). Two main indications for indicated. When the bleeding site is identified angiographically,
hepatic angioembolization are primary hemostatic control in a it can be controlled with embolotherapy in as many as 88% of
hemodynamically stable patient that has radiographic evidence patients (Mansueto et al, 2007).
of active arterial hemorrhage and adjunctive hemostatic control Angiography and embolization are feasible and safe in treat-
following surgical exploration and packing of a hepatic paren- ment of hemorrhagic complications following pancreatic surgery
chymal injury with evidence of continued bleeding or hemody- (Casadei et al, 2014; Yekebas et al, 2007). Yekebas and col-
namic instability. Additionally, patients who are seen with leagues (2007) reported significant hemorrhage in 5.7% of 1669
hemodynamic instability who can be successfully resuscitated consecutive patients following partial or total pancreatectomy.
can be treated effectively with transcatheter embolization (Mis- In a more recent study, Casadei and colleagues (2014) reported
selbeck et al, 2009). The yield of arteriography in identifying significant hemorrhage in 9.8% of 182 patients following pan-
an arterial injury amenable to embolization is higher when the creatic resection for pancreatic and periampullary diseases.
CT scan suggests a vascular injury. Bleeding may manifest clinically as gastrointestinal hemorrhage,
Complications following embolization of a hepatic arterial retroperitoneal or intraperitoneal bleeding, or bleeding through
injury secondary to blunt trauma are relatively frequent percutaneous or surgically placed drains. When a pancreatico-
(Letoublon et al, 2011). In a retrospective study, Letoublon jejunal anastomosis has been created, disruption of the anasto-
and colleagues reported a 70% liver complication rate. These mosis may lead to false localization of the bleeding site.
complications include hepatic ischemia, infarction, hepatic Specifically, an extraluminal bleeding site may drain into the
failure, gallbladder ischemia, bile leak, and abscess formation. bowel through the dehisced anastomosis, or bleeding from the
Chapter 21  Diagnostic angiography in hepatobiliary and pancreatic disease: indications 397

A B

C
FIGURE 21.6  Pseudoaneurysm secondary to pancreatitis treated with coil embolization. A, Contrast-enhanced computed tomography reveals a
pseudoaneurysm in the pancreatic head (arrow). B, Selective gastroduodenal arteriogram reveals the pseudoaneurysm (arrow) taking origin from a
branch of the anterior-superior pancreaticoduodenal artery. C, The pseudoaneurysm is occluded with coils (arrowheads).

bowel at the anastomosis may extend outside the lumen to cause but may be suggested by CT. If the underlying etiology is
an intraperitoneal hematoma or hemorrhage through a drain. compression of the splenic vein, percutaneous transhepatic
Angiography can be extremely useful in the diagnosis and stenting of the splenic vein may be potentially useful.
treatment of these patients. In 25 of 43 patients undergoing
angiography to diagnose and treat postpancreatectomy hemor- Diagnosis of Arterial Occlusive Disease
rhage, a bleeding site was located and embolized with an 80% Many arterial disorders that involve the primary branches of
success rate in controlling the hemorrhage (Yekebas et al, the celiac trunk, as well as the SMA, can be assessed adequately
2007). The relatively low rate of positive angiograms may be with MDCT or MRA. However, delineation of pathology in
explained by the high incidence of venous bleeding encountered smaller branches, such as with vasculitis, or subtle pathologic
in the postpancreatectomy patient. Regional portal hyperten- changes may require the increased morphologic detail afforded
sion develops in many of these patients as a result of splenic or by catheter angiography.
superior mesenteric venous compression or occlusion second- Arterial occlusive disease as a result of atherosclerosis and
ary either to the underlying pathology or a surgical complica- compression of the celiac axis by a median arcuate ligament are
tion. Venous extravasation is rarely identified by arteriography common diseases that do not generally influence the conduct
398 PART 2  DIAGNOSTIC TECHNIQUES

of hepatobiliary or pancreatic surgery. The principle exception Treatment of Visceral Arterial Aneurysms
is in the performance of orthotopic liver transplantation (OLT), Visceral artery aneurysms are rare entities that involve the
when preservation of brisk hepatic arterial flow is essential. In celiac, splenic, superior mesenteric, or inferior mesenteric
that circumstance, the inflow must be corrected either by surgi- arteries and their branches (see Chapter 124). The prevalence
cal or endovascular interventions. Another potential area of of visceral artery aneurysm is 0.1% to 2% (Hemp & Sabri,
concern is pancreaticoduodenectomy, particularly in jaundiced 2015; Tulsyan et al, 2007). True aneurysms involve all three
patients. In this situation, sacrifice of the GDA is required, vessel walls and are usually atherosclerotic or developmental
which interrupts the retrograde arterial flow from the SMA to in origin and differ from those encountered in pancreatic
the liver and could result in hepatic ischemia and necrosis. inflammatory disease, which are typically pseudoaneurysms.
Likewise, fibromuscular dysplasia may rarely involve the SMA, Depending on the size and location of the aneurysm, mortal-
but associated clinical sequelae are extremely uncommon. The ity from rupture ranges from 25% to 100% (Cordova &
SMA may also be compromised in very rare circumstances by Sumpio, 2013).
a median arcuate ligament. The splenic artery is the most common affected artery,
followed by the hepatic artery. Splenic artery aneurysms in
Diagnosis and Treatment of Arterial Stenosis women of childbearing age are of particular concern because
Hepatic arterial anastomotic stenoses are observed in as many of their propensity to rupture during childbirth. Most splenic
as 11% to 12% of patients following OLT (see Chapters 116 aneurysms are saccular and located in the mid to distal segment
and 120) (Duffy et al, 2009; Kim et al, 2012). Although these of the artery (Nosher et al, 2006). The rate of rupture ranges
stenoses are usually detected by surveillance duplex ultrasound from 3% to 20% (Lagana et al, 2006). Endovascular treatment
and confirmed with MDCTA, catheter angiography is often of splenic artery aneurysms depends on the tortuosity and
performed to improve morphologic delineation and assess the location of the aneurysm. Stent placement is used for more
degree of stenosis in preparation for endovascular treatment proximal disease and distal disease in a tortuous vessel is usually
(Vaidya et al, 2007). Stenosis of the hepatic artery anastomosis treated with coil embolization (Hemp & Sabri, 2015).
usually leads to allograft dysfunction, and stenoses of the Traditionally, surgical resection or ligation of the visceral
hepatic artery may also be more diffuse (Fig. 21.7). Severe aneurysms was the gold standard of therapy; however, endovas-
stenosis may lead to hepatic artery thrombosis. The hepatic cular treatments have largely replaced open resection. Large
artery supplies the bile duct, and the bile duct has been ren- studies have reported technical success rates ranging from 89%
dered devoid of collateral arterial supply during donor hepatec- to 98% (Hemp & Sabri, 2015; Sachdev et al, 2006; Tulsyan
tomy. Arterial insufficiency typically leads to biliary strictures et al, 2007). Endovascular treatments are associated with
and to potentially diffuse biliary ductal infarction. Hepatic shorter hospital stay, when compared with surgical repair: 3.8
artery thrombosis may lead to irretrievable allograft damage versus 12 days, respectively.
and may necessitate retransplantation. When a hepatic arterial
stenosis is identified before advanced biliary injury, endovascu- Diagnosis of Vasculitis
lar therapy with either balloon angioplasty and/or stent place- Vasculitis
ment is warranted. Vasculitides that involve the hepatic arterial system may require
the spatial resolution provided by catheter angiography for
definitive diagnosis, because the characteristic microaneurysms
and areas of arterial narrowing may not be apparent by MDCT.
The most common vasculitis with hepatic involvement is
polyarteritis nodosa, which may not lead to symptoms despite
involvement of the visceral arteries, although pancreatitis,
cholecystitis, and hepatic dysfunction may be observed.
Arterial abnormalities in the liver have also been identified
in patients with systemic lupus erythematosus and Wegener
granulomatosis. In most patients, the underlying diagnosis is
apparent, and the angiographic findings do not represent a
diagnostic dilemma.

Diagnosis of Other Visceral Vascular Disease


Segmental Arterial Mediolysis
A rare vascular disorder, segmental arterial mediolysis, may also
require catheter angiography for definitive diagnosis. This dis-
order is characterized pathologically by noninflammatory
destruction of smooth muscle cytoplasm, leading to arterial
dissection and aneurysm formation. Multifocal lesions with
skip areas involving the superior mesenteric, hepatic, renal, and
middle colic arteries in patients in their fourth to sixth decades
are typical (Fig. 21.8). Clinically, these lesions are prone to both
occlusion by dissection as well as rupture, leading to cata-
FIGURE 21.7  Hepatic artery stenosis following orthotopic liver trans- strophic abdominal hemorrhage. Treatment with coil emboliza-
plantation. Celiac arteriogram shows mild diffuse narrowing of the tion within noncritical arterial beds has been reported (Davran
hepatic artery with two areas of critical stenosis (arrowheads). et al, 2010).
Chapter 21  Diagnostic angiography in hepatobiliary and pancreatic disease: indications 399

Hereditary Hemorrhagic Telangiectasia depicting the malformations shunting hepatic arterial blood
Hereditary hemorrhagic telangiectasia (HHT) also known as into the hepatic venous system (Fig. 21.9) (Memeo et al, 2008).
Osler-Weber-Rendu syndrome, is an autosomal dominant vascular Although this disorder has been treated with transcatheter
disease, characterized by telangiectasias of the skin and mucous techniques, embolotherapy has currently fallen out of vogue
membranes. HHT is also associated with arteriovenous malfor- because of the risk of precipitating hepatic failure. OLT is
mations in the pulmonary and hepatic circulation that may be curative if high-output cardiac failure develops in the patient.
life-threatening. Diagnosis is usually based on family history
and clinical criteria. Cross-sectional imaging, including ultra- Peliosis Hepatitis
sound, CT or MRI, plays a fundamental role in detecting vis- Peliosis is an abnormality of the reticuloendothelial system that
ceral involvement in HHT. The hepatic arterial malformations is most commonly encountered in the liver (peliosis hepatis)
that shunt blood into the hepatic venous system may be initially (see Chapter 89). Pathologically, it is characterized by blood-
noted on a cross-sectional imaging study, but the findings may filled cystic spaces that range in size from a few millimeters to
be nonspecific. Catheter angiography can be diagnostic by almost a centimeter. This abnormality has been associated with
human immunodeficiency virus infection as well as with the use
of certain drugs, including immunosuppressives, antimetabo-
lites, and oral contraceptives. Although usually benign, it has
been associated with spontaneous massive hemorrhage and
therefore may be encountered angiographically during the
investigation of hepatic bleeding (Choi et al, 2009). Angio-
graphically (Fig. 21.10), the lesions are easily visible as a dis-
organized collection of amorphous channels not dissimilar to
those observed in HHT or hemangioma; however, the lack of
shunting to the hepatic venous system distinguishes it from
HHT, and the absence of sharp definition with persistence into
the late venous phase distinguishes it from hemangioma.
Localization of Functional Pancreatic Neuroendocrine
Tumors (See Chapter 65)
Calcium stimulation arteriography was developed and described
in 1991 (Doppman et al, 1991). Although unnecessary when
imaging can confidently detect the offending pancreatic lesion,
it is an extremely useful adjunct when the location of the lesion
cannot be defined with confidence (Fig. 21.11). When 1 mL of
10% calcium gluconate is injected into an artery supplying the
FIGURE 21.8  Segmental arterial mediolysis (SAM). Abdominal aorto- pancreas, tumor cells degranulate and release insulin into the
gram reveals a dissection with a small aneurysm in the celiac artery portal venous circulation. Sequential blood samples obtained
(arrow) as well as undulating irregularity of the common hepatic artery from the hepatic vein will demonstrate a significant rise in the
(arrowhead) typical of SAM. concentration of insulin when the portion of the pancreas

A B
FIGURE 21.9  Hereditary hemorrhagic telangiectasia (HHT). A, Selective hepatic arteriogram shows disorganized and dilated intrahepatic vessels
typical of HHT. Coils are being placed preoperatively for impending liver transplantation. B, Slightly later in the sequence, early opacification of the
hepatic vein is visible (arrowheads).
400 PART 2  DIAGNOSTIC TECHNIQUES

containing the tumor is injected. By sequentially injecting the determining the approximate areas of pancreatic arterial supply.
arterial supplies to different regions of the pancreas, it is pos- In the article by Guettier and colleagues (2009), calcium stimu-
sible to ascertain the location of the tumor. The GDA supplies lation arteriography was the most sensitive technique for local-
the head of the pancreas, the SMA supplies the head and izing surgically proven insulinomas, with an accuracy of 84%,
uncinate process, and the splenic artery supplies the body a false-negative rate of 11%, and a false-positive rate of 4%.
and tail. The origin of small branches supplying the pancreas Percutaneous transhepatic sampling of the splenic, superior
from the splenic artery and CHA are important to note in mesenteric, and portal venous system can be performed to
diagnose occult neuroendocrine tumors of the pancreas. This
may be done in conjunction with calcium stimulation as
described earlier, or it may be performed without stimulation
because of the higher concentration of the hormone when
obtained directly or adjacent to the venous tributary.

Insulinomas
Greater than 90% of insulinomas are single, benign tumors for
which surgical resection is curative. These tumors are the most
common tumors originating from the islets of Langerhans (see
Chapter 65). The most effective method of diagnosing these
tumors is a combination of dual-phase thin-section CT scan and
RIGHT endoscopic ultrasonography (EUS) (Jackson, 2005). Advances
in imaging technology have improved the sensitivity of CT and
MRI to greater than 80% and 70%, respectively (Nikfarjam
et al, 2008). The sensitivity of EUS in detecting and localizing
insulinomas ranges from 82% to 94% (McLean, 2004).

Gastrinomas
Gastrin-secreting tumors are the cause of Zollinger-Ellison
syndrome and in approximately one-third of the cases occur in
association with multiple endocrine neoplasia (MEN) type 1.
Fifty percent of gastrinomas occur in the pancreas, with the
FIGURE 21.10  Peliosis hepatitis. Multiple small contrast collections duodenum being the most common extrapancreatic location.
can be seen within the hepatic parenchyma. This patient had spontane- Approximately 60% to 90% of gastrinomas are malignant.
ous hemorrhage that created displacement of the hepatic parenchyma When a sporadic gastrinoma is identified, surgical resection is
(arrowheads). indicated. The role of surgery in patients with MEN type 1 is

A B
FIGURE 21.11  Insulinoma. A, Selective gastroduodenal arteriogram shows no definite abnormality during the arterial phase. B, A subtle area of
hypervascularity is identified during the capillary phase, possibly representing an insulinoma (arrowheads). This was confirmed as the region of tumor
by calcium stimulation with venous sampling.
Chapter 21  Diagnostic angiography in hepatobiliary and pancreatic disease: indications 401

A B
FIGURE 21.12  Arterial portography in a patient with cavernous transformation of the main portal vein. A, Venous phase of superior mesenteric
arterial injection shows the superior mesenteric vein (arrow) and cavernous transformation of the main portal vein. B, Venous phase of splenic arterial
injection from the same patient shows the splenic vein (arrow).

more controversial because of multiplicity of tumors and lack trunks and their primary branches in the vast majority of
of an established survival benefit. patients. Cross-sectional imaging can accurately depict the
The diagnosis and location of a gastrinoma can be estab- relationship of a mass in the pancreas to both the splenic and
lished with a combination of somatostatin receptor scintigraphy superior mesenteric veins. It also has the advantage of simulta-
and EUS in approximately 90% of patients. When an occult neous opacification of all of the venous structures. However, in
gastrinoma is encountered, angiography has been used for certain clinical situations, it is desirable to visualize the venous
localization. The principles are identical to the localization of structures with a higher level of clarity. These situations include
insulinomas; however, secretin has been used in addition to planning of percutaneous venous intervention in situations
calcium gluconate as the stimulating agent. Sensitivities of where occlusions are suspected or occasionally to plan a surgi-
arterial stimulation venous sampling (ASVS) in the detection cal portosystemic shunt.
of gastrinomas have ranged from 70% to 100% (Cohen et al, The most common technique to visualize the splanchnic
1997; Turner et al, 2002). vein is transarterial portography, in which selective splenic and
Angiographically, gastrinomas are less hypervascular and superior mesenteric arteriograms are performed with delayed
more difficult to detect in comparison to insulinomas. Sensitiv- imaging into the venous phase, depicting the splenic and supe-
ity of angiography alone without ASVS is less than 50%. rior mesenteric veins, respectively (Fig. 21.12). When detailed
Moreover, the 50% extrapancreatic location makes detection visualization of the venous anatomy is required, a higher dose
more difficult, often requiring superselective catheterization to of contrast media can be used for the arterial injection, increas-
evaluate the duodenum. ing the clarity of venous opacification.
When an extremely detailed evaluation is required, a com-
Glucagonoma bination of transarterial portography during MDCT can be
Glucagonomas may occur sporadically or may be associated performed (Fig. 21.13). The increased contrast sensitivity of the
with MEN type 1. These tumors are usually larger than gastri- MDCT coupled with multiplanar and 3D reconstruction allows
nomas or insulinomas at presentation; therefore localization can visualization of the veins that cannot be achieved by any other
generally be achieved with cross-sectional imaging or EUS. single technique. This is particularly useful in the presence of
Equchi and colleagues (2012) reported eight patients with portal vein occlusion, when a complex venous reconstruction
pancreatic hypervascular tumor and elevated serum glucagon or bypass is being considered.
level that glucagonomas were successfully localized using ASVS. Direct venography of the splanchnic veins can be achieved
by three routes: transjugular, transhepatic, and transsplenic. In the
Venographic Technique transjugular approach, a catheter is placed into the jugular vein
MDCT, magnetic resonance venography, and ultrasound are and advanced into a hepatic vein. Free and wedged hepatic
usually sufficient for depiction of the major visceral venous pressures can be obtained through this catheter. Using these
402 PART 2  DIAGNOSTIC TECHNIQUES

undergoing a transjugular intrahepatic portosystemic shunt, but


it is also used to manage selected patients with portal and SMV
thrombosis (Liu et al, 2009).
The portal venous system may also be accessed by a percu-
taneous transhepatic approach (Semiz-Oysu et al, 2007). After
sterile preparation of the right upper quadrant, an intrahepatic
portal venous radicle is punctured under real-time ultrasono-
graphic guidance, permitting a vascular access sheath to be
placed by using a Seldinger technique. Standard guidewire and
catheter manipulations are then used through the sheath for
selectively catheterizing the splenic vein and the SMV or its
branches. Once the diagnostic images have been taken or
venous interventions have been performed, the catheter is
removed. The transhepatic tract is then occluded by a variety
of techniques, including insertion of Gelfoam pledgets, deploy-
ment of coils, or injection of fibrin glue. The transhepatic
venographic procedure is usually performed as part of a direct
pancreatic venous sampling, lobar portal venous embolization
to stimulate contralateral hypertrophy before major hepatic
resection, assessment and management of an anastomotic
portal venous stenosis following OLT, pharmacomechanical
lysis of a splanchnic vein thrombosis, or, rarely, to control
bleeding from a splanchnic vein.
Percutaneous injection of the splenic parenchyma can also
be used to delineate the anatomy of the splenic and portal veins
as well as the draining tributaries. This examination is somewhat
FIGURE 21.13  Multidetector computed tomography with three- antiquated and has been generally replaced by MDCT or
dimensional reconstruction following superior mesenteric arterial injec- magnetic resonance venography. In infants, cross-sectional
tion. The superior mesenteric vein and cavernous transformation are
imaging may be inconclusive, and transarterial portography is
easily visualized.
risky because of the diminutive size of the femoral arteries;
however, it remains an alternative in planning a portosystemic
shunt procedure.
two pressures, the corrected sinusoidal pressure can be calcu- Percutaneous catheterization of the splanchnic veins is also
lated and can be used to assess portal hypertension. A biopsy possible from a transsplenic approach using a technique identi-
of the hepatic parenchyma (transjugular liver biopsy) may be cal to that described for transhepatic catheterization (Tuite
performed when desirable. Injection of carbon dioxide through et al, 2007). This procedure is usually done in conjunction with
a catheter wedged in a hepatic vein or through a balloon cath- a percutaneous procedure to assess a portal vein stenosis or
eter will often yield an image of the portal vein. If direct por- occlusion following OLT, but it may also be used in conjunction
tography is warranted, one of several specially designed needles with the assessment and treatment of a splenorenal venous
can be inserted to puncture the portal vein through the inter- bypass, when access cannot be achieved from the systemic
vening hepatic parenchyma and through catheters advanced venous circulation.
into the portal, splenic, or superior mesenteric venous system.
This procedure is performed almost exclusively in patients References are available at expertconsult.com.
Chapter 21  Diagnostic angiography in hepatobiliary and pancreatic disease: indications 402.e1

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