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292 The use of postprocedural imaging in the medical management of patients
and cholecystitis are much more common than
those related to extrahepatic NTE (Singh and
Anil, 2013). In one large series, combined biliary complications occurred in approximately
10% of patients, requiring intervention in ~2%
(Atassi et al., 2008b). ese rates are generally
higher in patients with prior biliary intervention
or biliary-enteric anastomosis (Riaz, 2014). is
relatively high rate of biliary toxicity is explained
by the vascular supply of the biliary tree. Unlike
normal hepatic parenchyma, the biliary tree lacks
a dual blood supply (Northover and Terblanche,
1979). Instead, the supraduodenal common bile
duct and hepatic duct are supplied by either the
gastroduodenal artery (68%) or right hepatic
Figure 14.6 Fulminant hepatic failure is largely
a clinical diagnosis with nonspecic imaging
ndings. This patient underwent lobar radioembolization after left lobectomy for colorectal
carcinoma (CRC) metastasis. Eight weeks after
therapy, the patient was found to have fulminant
hepatic failure, manifested by patchy hypoenhancement. (Reproduced from Hamoui, N. and
Ryu, R., Semin. Intervent. Radiol., 28, 246–251,
2011. With permission.)
artery (32%) (Northover and Terblanche, 1979).
e intrahepatic biliary tree is supplied by its
accompanying lobar artery and its arterial vascular plexus (Northover and Terblanche, 1979).
is paucity of collateral vessels makes the biliary
tree particularly susceptible to ischemic injury.
Interestingly, peribiliary vascular hypertrophy
found in cirrhotic livers is thought to prevent
peribiliary microsphere deposition and reduce
rates of biliary injury (Yu et al., 2002).
REILD can lead to fulminant hepatic failure and
death (Hamoui and Ryu, 2011). e overall inci-
14.3.2.1 Biloma
dence of REILD from radioembolization ranges
from approximately 4% to 9%, although it can
reach 50% in patients receiving aggressive chemotherapy regimens (Sangro et al., 2008). REILD
is primarily diagnosed by its clinical features; it
has been accompanied by ill-dened heterogenous
hypoenhancement on short-term follow-up MRI
and CT (Hamoui and Ryu, 2011) (Figure 14.6).
Hepatic toxicity from90Y is discussed in more
detail in Chapter 8, including a comprehensive
discussion of the hepatic dose toxicity models.
e potential for biloma formation has been well
documented in patients undergoing chemoemboli-
zation for hepatic mal ignancy, occurring in approx-
imately 4% of all c ases (Minocha and Lewa ndowski,
2011). Biloma are most commonly caused by small
vessel ischemia resulting in bile duct disruption,
although radiation eects may also contribute.
Comparative rates of biloma in TACE and 90Y are
unclear as are incidence rates among the glass and
resin products. However, a large independent obser-
vational study reported rates approximating 1% for
radioembolization. On imaging, biloma typically
14.3.2 BILIARY EFFECTS
manifests as a well-dened intrahepatic collec-
tion approximating the biliary tree (Figure 14.7). A
While REILD is a serious concern that greatly
eects 90Y treatment planning and much technical emphasis is placed on avoiding complications from NTE, biliary toxicity provides some
of the most common adverse eects of radioembolization (Atassi et al., 2008b; Singh and Anil,
2013). With current techniques, it is now generally assumed that biliary complications including
radiation cholangitis, biloma, biliary stricture,
direct communication with the bile ducts may not
be seen by CT or MRI, but is usually demonstrated
by cholangiogr am (Figure 14.8). e presence of rim
enhancement is common and should be considered
suspicious for secondary infection only in the clini-
cal context of fever, right upper quadrant pain, and
leukocytosis (Singh and Anil, 2013). In this setting,
biloma may dicult to dierentiate from intrahe-
patic abscess.
14.3 Imaging of complications / 14.3.2 Biliary effects 293
(a) (b)
(a) (b)
Figure 14.7 (a) CT scan prior to radioembolization shows multiple hepatic metastatic lesions. (b) Two
months after therapy, the right hepatic lobe shows signicant volume loss and capsular retraction with several hypodense lesions typical of intrahepatic biloma. (Reproduced from Singh, P. and
Anil, G., Cancer Imag., 13, 645–657, 2013 under the terms of the Creative Commons Attribution 4.0
International License; http://creativecommons.org/licenses/by/4.0/.)
Figure 14.8 A 59-year-old male patient underwent radioembolization for melanoma metastasis
to liver. (a) Axial T1-weighted, fat-saturated MRI image 25 weeks after therapy shows nonenhancing lesions with thick rim enhancement in the right hepatic lobe and multiple left lobe metastasis.
(b) Administration contrast through a percutaneous drainage catheter demonstrates communication
with the biliary tree, conrming intrahepatic biloma. (Reproduced from Atassi et al., Radiographics,
28, 81–99, 2008a. With permission.)
14.3.2.2 Cholangitis and transient
hyperbilirubinemia
distinguished from worsening painless jaundice.
Grade III or higher bilirubin toxicity (total bili-
rubin >3.0 mg/dL) has been reported in as many
Radiation cholangitis is a clinical syndrome manifested by jaundice, fever, and right upper quadrant
pain. It is ra re aer radioemboliz ation, w ith unclear
incidence and no clearly dened characteristic
imaging ndings (Riaz, 2014). While radiation
cholangitis may be sterile, it is commonly treated
with antibiotics (Riaz, 2014). is should be
as one-third of patients aer therapy (Smits et al.,
2013). ese ndings are thought to more likely
represent eects of REILD than biliary toxicity
and may improve with conservative management
(Salem et al., 2013b). It should be emphasized that
isolated mild hyperbilirubinemia is commonly
asymptomatic and not associated with signicant
294 The use of postprocedural imaging in the medical management of patients
changes in synthetic liver function or impending hepatic decompensation (Salem et al., 2013b;
Smits et al., 2013).
14.3.2.3 Biliary stricture
Biliary stricture with upstream dilation oen
reects chronic sequela of bile duct injury on the
same spectrum biloma, potentially due to radiation
and/or ischemia, which most commonly eects
intrahepatic biliary radicals and is seen to a lesser
degree in cirrhotic livers. Many of these patients
will be asymptomatic, only requiring intervention
if clinical symptoms present as biliary obstruction
or secondary infection (Atassi et al., 2008a, 2008b;
Singh and Anil, 2013).
14.3.2.4 Radiation cholecystits
Radiation cholecystitis is a clinical syndrome
of cholecystits in patients recently undergoing
yttrium-90 radioembolization. Imaging ndings
of cholecystitis have been reported in approximately 2% of patients, manifested by gallbladder wall thickening and hyperenhancement
(Sag et al., 2014) (Figure 14.9). ese imaging
ndings accompany the clinical nding of right
upper quadrant pain, with or without fever and
leukocytosis. In clinical practice, rates of radia-
tion cholecystitis are highly variable, depending
on technical considerations such as prophylactic
embolization of the cystic artery and use of anti-
reux devices (Pasciak et al., 2015). Many inter-
ventional radiologists do not routinely embolize
the cystic artery to prevent NTE to the gallblad-
der when it is downstream to the infusion site.
is is due in large part to the possible risk of
ischemic cholecystits from prophylactic cystic
artery embolization, thought by many to out-
weigh the risk of gallbladder NTE (Hickey and
Lewandowski, 2011). In situations where the cys-
tic artery is likely to sump a signicant quantity
of 90Y activity from the tumor, or when signi-
cant deposition of MAA is seen on the pretreat-
ment simulation, prophylactic embolization can
be considered. Caution should be taken in embo-
lizing a dominant cystic artery that comprises all
or nearly all blood ow to the gallbladder, as this
is associated with increased risk of perforation
(Hickey and Lewandowski, 2011). Fortunately,
radiation cholecystitis is usually self-limited and
managed with conservative therapy. Rarely, gall-
bladder perforation and need for surgical cho-
lecystectomy have been reported, but both are
thought to occur in less than 1% of cases (Atassi
et al., 2008b).
(a) (b)
Figure 14.9 (a) Contrast-enhanced CT scan performed 3 days after radioembolization demonstrates
gallbladder wall thickening and pericholecystic uid suggestive of cholecystitis. The patient underwent
laparoscopic cholecystectomy 7 weeks later. (b) Microscopic analysis of the surgically removed gallbladder showed brosis, chronic inammation, and the presence of glass microspheres (arrow). (Reproduced
from Hickey, R. and Lewandowski, R., Semin. Intervent. Radiol., 28, 230–233, 2011. With permission.)
14.3 Imaging of complications / 14.3.4 Gastrointestinal nontarget embolization 295
14.3.3 HEPATIC ABSCESS
Any rim-enhancing intrahepatic uid collection
should be suspicious for abscess in a patient aer
radioembolization. e presence of internal gas
raises diagnostic probability; however, it should be
emphasized that loculated foci of gas may be present in the liver normally aer treatment. is is a
result of low-volume, intra-arterial gas injection
during 90Y infusion, when it can become trapped
between microspheres for several days before
resorbing (Singh and Anil, 2013). erefore, imaging ndings suggestive of abscess should be taken
in context of clinical presentation. Percutaneous
aspiration for culture may prove denitive in cases
of unclear imaging and clinical ndings (Singh
and Anil, 2013).
Hepatic abscess may occur aer radioembolization as a result of bacterial colonization
of necrotic tumor, necrotic nontarget hepatic
parenchyma, or biloma. Because ascending
infection through the biliary tree is the most
common route of infection, rates of hepatic
abscess are increased in patients with prior
sphincerotomy or biliary-enteric anastomosis.
In patients with an intact sphincter of Oddi,
abscess occurs in approximately 1%–2% of cases
(Brown et al., 2012). However, as many as 15%
of patients with prior biliary-enteric anastomosis, sphincerotomy, or indwelling biliary stent
experience an abscess, even when periprocedural
antibiotic were administered (Brown et al., 2012).
An aggressive antibiotic course combined with a
bowel prep regimen has been shown to reduce,
and potentially eliminate, this risk (Cholapranee
et al., 2014). Finally, radioembolization should be
deferred in patients with suspicion for bacteremia, as subsequent abscess formation has been
reported (Mascarenhas et al., 2011).
14.3.4 GASTROINTESTINAL
NONTARGET
EMBOLIZATION
Gastrointestinal (GI) tract ulceration from NTE
is one of the most feared complications of radioembolization due to its morbidity and the complex nature of surgical intervention in patients
containing residual radioactivity. Ulceration is
commonly caused by reux of microspheres into
the gastroduodenal (GDA) or right gastric arteries
(RGA), where they may deposit and cause hemorrhage, inammation, and/or ulceration (Veloso
et al., 2013; Baumann et al., 2015). Occasionally,
peripheral deposition of
result in clinically signicant dose deposition to
adjacent visceral structures (Singh and Anil, 2013).
Radiation-induced injury to mucosal stem cells
is thought to be the primary causative etiology,
with ischemia eects playing a lesser role. Because
mucosal stem cells are permanently depopulated
by radiation eects, radiation-induced GI tract
ulcers rarely resolve spontaneously. In order to
mitigate ulceration risks, prophylactic embolization of the GDA and RGA, antacid medicine, and/
or use of antireux devices may employed (Pasciak
et al., 2015). However, the practice of routine
GDA embolization has been called into question
in light of recent research and is performed based
on institution-specic preference (Haydar et al.,
2010). e exact toxicity thresholds to the small
bowel and stomach from 90Y are unclear, although
concurrent systemic chemotherapy likely sensitizes mucosal cells to radiation, increasing risk of
ulceration (Brown et al., 2012).
By imaging, radiation-induced GI tract ulcers
are indistinguishable from other forms of ulceration, and may manifest as focal mural thickening, regional inammatory changes, and/or signs
of perforation. Endoscopy is the gold standard for
diagnosis and should be considered in patients
with any level of suspicion for NTE to bowel (Singh
and Anil, 2013).
Acute pancreatitis is another rare sequela of
NTE observed in fewer than 1% of patients (Brown
et al., 2012; Riaz, 2014). Pancreatitis manifests
similarly when caused by radioembolization as
it does when caused by other etiologies, with elevated serum amylase/lipase and intense epigastric
pain. Imaging ndings of acute pancreatitis related
to 90Y are usually localized to the pancreatic head,
rather than diuse in nature (Singh and Anil,
2013). Postprocedural 90Y single-photon emission
computed tomography (SPECT/CT) or PET/CT
imaging may be helpful to conrm microsphere
deposition in the pancreas and exclude other
potential causative etiologies.
90
Y within the liver can
296 The use of postprocedural imaging in the medical management of patients
14.3.5 RADIATION PNEUMONITIS
AND OTHER SITES
OF NONTARGET
EMBOLIZATION
Radiation pneumonitis (RP) is the development
of pulmonary brosis and restrictive lung disease from exposure to sucient radiation dose.
It manifests in a similar fashion to organizing
pneumonia or chronic eosinophilic pneumonia
on CT, with patchy areas of ground-glass opacity, mild volume loss, and traction bronchiectasis
(Singh and Anil, 2013) (Figure 14.10). Making
the diagnosis RP is particularly important in
patients being considered for repeat radioembolization as the increased cumulative dose could
worsen pulmonary function (Wright et al., 2012).
Avoiding RP is a signicant emphasis in pretherapy treatment planning, and is the basis for
MAA administration and calculation of shunt
fraction. Dosimetric and radiobiologic considerations regarding RP are discussed in further
detail in Chapter 4. Although the avoidance of
RP is greatly emphasized in 90Y treatment planning, its incidence is exceedingly rare. It could
be argued that rigorous treatment planning helps
to avoid RP; however, it is rarely reported even
in cases in which the lungs receive the assumed
toxicity threshold of 50 Gy. In one cohort of 58
patients receiving a lung dose above 50 Gy no
cases of radiation pneumonitis were seen (Salem
et al., 2008). e rarity of RP makes it suboptimally studied with respect to risk factors and
optimal prevention strategies.
Nontarget embolization has been described
in other unusual locations such as colon and
kidney (Kao, 2014). ese represent rare sites of
NTE, with poorly understood clinical outcomes
as a result of their rarity. Of particular interest,
NTE to the abdominal wall from a falciform
artery has been reported. e falciform artery
is a small terminal arterial branch o the le
hepatic or proper hepatic arteries that extends to
the umbilicus and communicates with the epigastric arteries (Bhalani and Lewandowski, 2011)
(Figure 14.11). Failure to recognize and embolize
potential NTE to abdominal wall from a falciform artery can result in periumbilical abdominal pain, cutaneous burning sensation, or skin
necrosis (Bhalani and Lewandowski, 2011; Smith
et al., 2015). However, it has recently been shown
that topically applied ice to the abdominal wall
in the periprocedural period can induce sucient supercial vasoconstriction to eliminate
this risk.
14.4 POSTTREATMENT 90Y
IMAGING
Figure 14.10 Axial thoracic CT showed diffuse
ground glass opacity with traction bronchiectasis
in a patient following radioembolization. Given
this appearance and progressive nature, this was
determined to be a result of radiation pneumonitis. (Reproduced from Wright, C.L. et al., J. Vasc.
Interv. Radiol., 23, 2012. With permission.)
14.4.1 EVALUATING NONTARGET
EMBOLIZATION WITH
POSTTREATMENT
90
Y
IMAGING
Recall that there are no reliable angiographic
methods to ensure target delivery of microspheres and exclude nontarget embolization.
Both glass and resin microspheres are radiolucent
and thus not visualized on uoroscopy. Although
dilute iodinated contrast is commonly used to
ush the delivery catheter and conrm anterograde ow during infusion of resin microspheres,
this method provides limited evaluation for NTE.
It is also known that 90Y microspheres have the
potential to distribute in an unpredictable fashion compared with that of the preprocedural
Tc99m-MAA injection, owing to dierences in
particle size, catheter position, injection rate,
presence of stasis, and changes in tumor vascular
14.4 Posttreatment 90Y imaging / 14.4.2 Prognostication with 90Y PET/CT 297
(a) (b)
Figure 14.11 (a) Pretreatment angiography prior to radioembolization in a 57-year-old patient with
CRC metastases to liver. Selective angiogram of the segment 4 branch demonstrated the presence of
a falciform artery (arrows). However, its diminutive size prevented coil embolization. After treatment,
the patient experienced localized supraumbilical pain thought to be related to nontarget embolization of yttrium-90. (b) Left hepatic arteriogram prior to therapy in the same patient. (Reproduced
from Bhalani, S. and Lewandowski, R., Semin. Intervent. Radiol., 28, 234–239, 2011. With permission.)
dynamics (Lam, 2013c; Wondergem, 2013).
Consequently, methods of postprocedural imaging that allow for visualization of 90Y distribution
play an indispensible role in conrming technical
success and ensuring patient safety.
Identication of GI and other NTE on posttreatment imaging is covered in detail in Chapter 13, in
particular, the use of bremsstrahlung SPECT and
90
Y PET/CT to gauge technical success and detect
NTE, which is not straightforward due to signicant dierences between 90Y and conventional
diagnostic radionuclides.
14.4.2 PROGNOSTICATION WITH
90
Y PET/CT
Survival and response to radioembolization is
multifactorial, depending on nontreatmentrelated factors such as tumor burden, histologic
subtype, systemic radiosensitizers, and others
(Gunduz et al., 2014). When solely focusing on
tumor response, the amount of radiation delivered to the tumor (tumor absorbed dose) plays
a primary role. However, despite nearly two
decades of experience with radioembolization,
exact tumor toxicity threshold remains incompletely understood. Many factors contribute to
this uncertainty, including variable methods
of dose calculation, tumor heterogeneity, and
intrinsic dierences among the two 90Y microsphere products (Kao et al., 2013). Much of the
prior dose–response data for HCC and metastases derives from predictive dosimetry from
Tc99M-MAA SPECT/CT (Eaton et al., 2014;
Kokabi et al., 2014). ese studies have shown
tumor-response threshold ranging from 120 Gy
in HCC to 50 Gy in certain metastases (Dezarn
et al., 2011). While predictive dosimetry is feasible and commonly used, it is hindered by the
dierences between 90Y microspheres and MAA
discussed previously. erefore, dosimetry based
on Tc99M-MAA simulation provides only an
estimation of dose distribution that is likely to
have been delivered to a tumor (Kao et al., 2013).
Other dosimetry methods predicated on bremsstrahlung SPECT are further limited in their
accuracy.
e most exciting aspect of 90Y PET/CT is
the ability to obtain accurate tumor dosimetry, as previously discussed in Chapters 11
and 13. 90Y PET/CT has the capability to yield
298 The use of postprocedural imaging in the medical management of patients
)(
potentially important dose–response data and
prognostic information. According to phantom
studies, quantication of 90Y activity could be
performed with accuracy ranging from 0.4% to
10% depending on scan parameters, signicantly
better than SPECT/CT in comparative studies
(Lhommel et al., 2009; Elschot et al., 2013; Gates
et al., 2013). A recent international, multicenter
trial conrmed the consistent accuracy of 90Y
dosimetry using modern PET/CT imaging with
time-of-ight (ToF) on a number of scanners
with variable scan parameters (Willowson et al.,
2015). As quantitative dosimetry with PET/CT
has increased in scope, a more in-depth understanding of tumor response will likely come to
light. Such information, combined with 90Y PET/
CT dosimetry, will allow for prognostication of
(a
outcomes immediately following 90Y radioembolization. Figure 14.12 describes an example
of the utilization of PET/CT in the prognostication of a poor clinical response to therapy. Such
outcomes are not uncommon in radioembolization and can stem from relative hypovascularity
of tumor, poorly optimized treatment planning,
and numerous technical and patient-specic
challenges occurring during infusion. However,
early prognostication of these outcomes can
allow for consideration of alternative and adjuvant therapies several months earlier than was
previously possible. e potential benet of
using quantitative posttreatment 90Y imaging in
the clinical management of disease, particularly
in the context of terminal patients, cannot be
overstated.
b)
(c) (d)
Figure 14.12 A patient with multifocal CRC liver metastases is treated with 1300 MBq of 90Y resin
microspheres. (a) Lesion appears hypodense on pretreatment contrast-enhanced CT (CECT), with an
SUV
of 7.8 2 weeks prior to treatment as shown in (b). (c) Posttreatment quantitative 90Y positron
max
emission tomography/CT (PET/CT) reveals an average lesion dose of 64 Gy. (d) Follow-up PET/CT
at 8 weeks following treatment shows an SUV
the low absorbed dose delivered to the tumor.
of 8.0 with no apparent therapeutic effect owing to
max
References 299
14.5 TREATMENT MODIFICATION
WITH
90
Y PET/CT
14.5.1 INTERPROCEDURAL
TREATMENT MODIFICATION
Yttrium-90 PET/CT dosimetry data have also been
used in clinical practice to tailor treatments in various case reports. e rst example of this was published by Chang et al. (2013). In this case, a patient
with cholangiocarcinoma was treated with right
lobar infusion of resin microspheres for unresectable
recurrent disease aer Whipple and radiofrequency
ablation. Treatment planning was performed using
the standard body surface area approach. e patient
experienced minimal (<25%) response to radioembolization on follow-up FDG-PET/CT. Review of
the 90Y PET/CT performed immediately aer radioembolization yielded a tumor-absorbed dose of
70 Gy and tumor to normal uptake ratio (T/N) of
2.5:1. For a subsequent le lobar infusion, this low
calculated T/N was used to justify increased activity infusion that would approach toxicity thresholds
reported for HCC (Strigari et al., 2010). e le lobe
tumor received 110 Gy on postprocedural 90Y PET/
CT and achieved a complete response to therapy.
While this dosimetry method is somewhat time consuming, it is similar to partition model dosimetry
using Tc99m-MAA and represents a step toward the
renement of dosimetry calculation and treatment
personalization.
14.5.2 INTERPROCEDURAL
TREATMENT MODIFICATION
Another technique of treatment modication
using 90Y PET/CT was performed in a similar fashion, except both infusions targeted a single lesion
and the two infusions were performed on the same
day (Bourgeois et al., 2015). In this case, a patient
with HCC was treated with resin 90Y microspheres
via right lobar infusion using the body surface area
(BSA) dosimetry met hod. However, due to intraprocedural technical complications, only a fraction of
the 90Y was administered. e patient was promptly
transferred to have a 90Y PET/CT, which showed 52
Gy average tumor dose. A simple arithmetic conversion was used to calculate the needed activity to
reach 120 Gy tumor dose and the patient returned
for a second infusion on the same day. e net result
was a robust par tial treat ment response on follow-up
imaging. While the logistics of routinely using this
method make it prohibitive for routine use, it demonstrated that 90Y PET/CT may also have value in
allow ing salvage of a procedura l with simi lar technical complicati ons.
14.6 CONCLUSIONS
Imaging plays an important role in the planning, delivery, follow-up, and clinical management of patients undergoing radioembolization.
Familiarity with common complications and
associated imaging ndings may improve clinical
outcomes. Postprocedural imaging with bremsstrahlung SPECT and PET/CT can gauge early
treatment response and identify sites of nontarget
embolization. PET/CT is likely to play an important role in rening the safety and ecacy prole
of radioembolization.
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