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312 Future directions in radioembolization
Percentage tumor burden (%)
Dosage (GBq)
80
4
15.4.1.1 Pharmaceutical methods
Tumor angiogenesis results in the formation of
arterioles and capillaries that are structurally and
physiologically abnormal and support modication of T:N using both pharmaceutical and physical techniques. Tumor arterioles are abnormal
in that they do not have complete formation of
smooth muscle coat and lack autonomic innervation and, therefore, autoregulatory response
(Mattsson et al., 1977; Ashraf et al., 1996; Burke
et al., 2001; Tanaka et al., 2008). Tumor capillaries
are abnormal, owing to both incomplete formation
of the basement membrane and pericyte detachment (Nagy et al., 2009).
Intra-arterial infusion of the vasoconstrictor
angiotensin II has been used in several studies
(Sasaki et al., 1985; Goldberg et al., 1991a, 1991b;
Burke et al., 2001; Flower et al., 2001) as a means
to preferentially constrict arterioles feeding normal liver tissue, while arterioles supplying tumor
will remain largely unaected owing, again, to
the lack of innervation and incomplete smooth
muscle coat (Mattsson et al., 1977; Hafström et al.,
1980; Burke et al., 2001). A recent review by van
den Hoven etal. (2014b) summarized the results of
all published studies that quantied the degree of
change in T:N before and aer infusion of angiotensin II. In these publications spanning ndings
in 71 patients, an increase in T:N ranging from
180% to 310% following infusion of angiotensin II
has been reported. ese changes, which are substantial, can dramatically aect the distribution of
radioactive microspheres. Figure 15.1 shows the
absorbed dose to the tumor and to the uninvolved
liver as a function of T:N with the pre- and postangiotensin II (van den Hoven et al., 2014b) ranges,
highlighted to illustrate the potential benet.
Angiotensin II is not the only vasoconstrictor that has been evaluated as a tool to improve
liver-directed therapies. e eect of intra-arterial
infusion of antidiuretic hormone (ADH) has
been demonstrated in a porcine model (Durack
et al., 2012). Specically, the benets of ADH have
been quantied in terms of its ability to reduce
NTE by preferential constriction of gastroenteric
No angiotensin II, 2:1 T:N, 150 Gy tumor dose
3.5
3
2.5
2
1.5
Figure 15.1 The theoretical treatment dosage (GBq) of yttrium-90 (90Y) radioembolization neces-
sary to achieve an average tumor absorbed dose of 150 Gy. Baseline in the absence of intra-arterial
antiotensin II administration assumes a 2:1 tumor to normal uptake ratio (T:N) and a 1300 cc total liver
volume. The slope of the curve indicates the necessary increase in the ideal treatment dosage as a
function of percentage tumor inltration. With angiotensin II and its related lower and upper limit
of efcacy on T:N (van den Hoven et al., 2014b), the treatment dosage required to achieve 150 Gy is
decreased substantially at low tumor inltration. As percentage tumor inltration rises, the benet of
angiotensin II is reduced. (From van den Hoven, A.F. et al., PLoS ONE, 9, e86394, 2014b.)
0.5
1
0
0
Angiotensin II lower-limit effect, 150 Gy tumor dose
Angiotensin II upper- limit effect, 150 Gy tumor dose
70605040302010
15.4 Improving efcacy and safety / 15.4.1 Enhancement of T:N 313
collaterals. ADH was eective in reducing the
ratio of gastric to hepatic activity by a factor of two
(Durack et al., 2012). Similar analyses based on
infusion of catecholamines (Hafström et al., 1980;
Tanaka et al., 2008) have been performed on both
rats (Hafström et al., 1980) and humans (Tanaka
et al., 2008) with concomitant increases in T:N
from norepinephrine (Hafström et al., 1980) and
epinephrine (Tanaka et al., 2008). While vasoconstrictors can illicit a positive increase on T:N that
may contribute to the improved safety and ecacy
of radioembolization in some patients, their use
must be weighed against the potential contraindications related to their systemic eects. Median
increases in systolic blood pressure of more than
40 mm Hg (Sasaki et al., 1985; Goldberg et al.,
1991a) have been reported following hepatic arterial infusion of angiotensin II, and while transient,
this increase may be an important safety consideration in some patients.
15.4.1.2 Physical techniques
As described in Chapter 3, pretreatment occlusion
of the right gastric artery (RGA) and gastroduodenal arteries (GDA) is oen performed prior to
radioembolization to prevent extrahepatic NTE.
e use of specialty catheters, or antireux catheters, such as the Surere Infusion System (Surere
Medical Inc., Westminster, CO), may also protect
extrahepatic tissues from NTE by preventing retrograde ow (Arepally et al., 2013; Fischman et al.,
2014; van den Hoven et al., 2014a; Morshedi et al.,
2015) of microspheres into unprotected collaterals.
However, antireux catheters (Figure 15.2) have
recently been shown to alter the hepatic distribution of radioembolization and other liver-directed
therapies (Arepally et al., 2013; Pasciak et al., 2015;
van den Hoven et al., 2015). Arepally et al. (2013)
showed increases in distal arterial penetration
of tantalum microspheres following renal artery
embolization in a porcine model with the use of
an antireux microcatheter compared with a conventional end-hole catheter, sparking interest in
the use of these devices for a purpose other than
preventing reux.
While pharmaceutical techniques for increasing T:N take advantage of the lack of complete
smooth muscle coat and innervation in tumor
arterioles, physical techniques build upon the
related inability of tumor arterioles to autoregulate in the setting of changing arterial pressure.
Figure 15.2 The Surere Precision Infusion system. (Surere Medical, Denver, CO.)
314 Future directions in radioembolization
Rose et al. (2013) made in vivo downstream
hepatic-arterial blood pressure measurements
with the expandable tip (Figure 15.3) of an
antireux catheter open and with it closed. e
ndings of this study indicated that the open
tip of the antireux catheter reduced downstream systolic and diastolic arterial pressure by
nearly 50%. In theory, owing to the autoregulatory response of normal arteries and arterioles,
radioembolization performed using an antireux
microcatheter may trigger vasoconstriction of
the vessels perfusing uninvolved hepatic parenchyma. At the same time, the structurally abnormal angiogenesis-induced tumor arterioles are
not likely to constrict owing to absence of smooth
muscle, innervation, and autoregulatory properties (Mattsson et al., 1977; Burke et al., 2001). is
process could preferentially shunt microspheres
toward the tumor compartment, temporarily
increasing the T:N.
e eect of an antireux catheter on T:N in
radioembolization has been shown experimentally using
99m
Tc-MAA with a two-step same-day
infusion (Figure 15.4) based on a protocol tradi-
tionally used for routine renal and cardiac perfusion imaging (Pasciak et al., 2015). Statistically
signicant increases in tumor uptake, commensurate with decreases in uninvolved liver, support the premise that an antireux catheter can
increase T:N (Pasciak et al., 2015). Dierences in
hepatic distribution of
99m
Tc-MAA with an endhole catheter and an antireux catheter are shown
in Figure 15.4a and b, respectively. e distribution of 90Y resin microspheres following infusion
with the antireux catheter and imaged directly
using 90Y PET/CT is shown in Figure15.4d and
demonstrates excellent agreement to Figure 15.4b.
While it is convenient to cite downstream
pressure changes to explain the eect of an antireux catheter, it is likely that centering of the
tip as well as turbulence of ow also contributes
to the impact of these devices. For example, the
open semiocclusive tip (Figure 15.3) will result
in an increase in the turbulence of downstream
arterial ow. Increased turbulence of ow may
result in a more homogenous cross-sectional
distribution of microspheres in downstream
arteries, potentially improving homogeneity of
deposition (van den Hoven et al., 2015).
15.4.2 ALTERNATIVE METHODS
TO ENHANCE TUMOR
TARGETING
A more proactive approach to increasing T:N
involves the occlusion of arteries supplying
uninvolved areas of the liver in an eort to redirect hepatic-arterial blood ow, and thus 90Y
microspheres, to the tumor itself. Naturally,
(a)
Figure 15.3 Proper hepatic angiogram showing (a) an end-hole catheter and (b) an antireux catheter
with the tip expanded.
(b)
15.5 Toward improved posttreatment imaging / 15.5.1 New tracers and methods 315
(a)
(c) (d)
Figure 15.4 (a) Single-photon emission computed tomography (SPECT) following infusion
of technetium-99m-macroaggregated albumin
99m
(
Tc-MAA) using a conventional end-hole
catheter and (b) using an antireux catheter.
The catheter tip position was identical in each
case. (c) The distribution of
compared with contrast-enhanced computed
tomography (CT) in this patient with focal
hepatocellular carcinoma (HCC). (d) 90Y positron
emission tomography (PET)/CT following infusion
of resin 90Y microspheres with the antireux catheter. The distribution of 90Y was well predicted
99m
with
Tc-MAA, as shown in (b).
(b)
99m
Tc-MAA can be
such eorts would only be indicated with temporary methods of occlusion such as biodegradable starch microspheres or gelatin powder.
Degradable starch microspheres (DSM) have
been shown in a porcine model to have a short
biological half-life with complete re-perfusion
in the liver in 30 minutes (Pieper et al., 2015).
DSM may have utility in improving safety by
protecting normal liver tissue in situations where
subselection or repositioning of the microcatheter to avoid microsphere deposition in large
volumes of uninvolved liver is not a possibility
(Meyer et al., 2013).
15.5 TOWARD IMPROVED
POSTTREATMENT IMAGING
15.5.1 NEW TRACERS AND
METHODS
In the past, the diculty of directly imaging 90Y has
led to a variety of interesting experimental modications to 90Y microspheres. Aliva-Rodriguez was
able to successfully bind 86Y and 89Zr to the surface
of resin 90Y microspheres. Spheres were radiolabeled
and the binding stability for in vivo applications was
conrmed out to 24 hours at a physiological pH temperature (Avila-Rodriguez etal., 2007). is technique had the benet of direct quantitative imaging
of 86Y and 89Zr using PET/CT. Investigations into
dual isotope 90Y and
been performed (Poorbaygi et al., 2011), with eective imaging of the gamma emissions of
SPECT/CT.
166
Ho radioembolization, as already discussed, is perhaps the best in multimodality direct
imaging of radioactive microspheres.
Chapters 10 and 11 discussed in detail tech-
niques for quantication of 90Y bremsstrahlung
SPECT and 90Y PET/CT, which have been substantially rened over the past 5 years. Particularly in
the case of 90Y PET/CT, many modern PET/CT systems are able to accurately quantify 90Y right out of
the box using existing soware (Willowson et al.,
2015). In light of this information, the driving force
behind development of directly imageable microspheres using alternative tracers has decreased
substantially. is is not to say, however, that there
are no areas for improvement.
As quantitative imaging of 90Y radioembolization becomes more common, routine techniques
normally reserved for diagnostic studies can be
applied. One such example is respiratory gating,
which has been shown to aect both lesion size and
quantication in 2-deoxy-2-[uorine-18]uoro-glucose (18FDG) PET/CT (Suenaga et al., 2013).
is technique can be applied to postradioembolization quantitative imaging, including 90Y PET/
CT (Pasciak et al., 2014), and may be capable of
improving lesion detection and quantitative accuracy. Figure 15.5 visually illustrates the advantages
of amplitude-based respiratory gating in postradioembolization imaging.
177
Lu microspheres have also
177
Lu using
316 Future directions in radioembolization
(a) (b)
(c)
Figure 15.5 (a) Posttreatment 90Y PET/CT on a Siemens mCT Flow without respiratory gating and
(b)using amplitude-based gating (Siemens HD•Chest). Figure parts (a) and (b) were both reconstructed from the same acquisition data, making the decreased segment VIII lesion size easy to
appreciate when amplitude-based gating is used. Respiratory motion can effect image quality and
quantication in hepatic 90Y PET/CT just as it can in 2-deoxy-2-[uorine-18]uoro-d -glucose (18FDG)
PET/CT. (c) Pretreatment hepatic protocol magnetic resonance imaging (MRI) for comparison.
●
15.5.2 IMAGE ANALYSIS
ere are many ways to contour the tumor.
Contouring based on 90Y uptake on postradio-
e increasing use of quantitative postradioembolization imaging based on either alternative
radiotracers, 90Y PET/CT, or quantitative bremsstrahlung SPECT suggests the need for standardized techniques to interpret these images. While
there are numerous methods that can be used
to convert quantitative 90Y images into threedimensional representations of absorbed dose
as described in Chapter 12, there is a signicant
ambiguity in the simple process of using this information to determine the absorbed dose to a tumor.
Using this interpreted tumor absorbed-dose data
embolization imaging or contouring on pre-
treatment 18FDG PET/CT, contrast-enhanced
CT, or hepatic protocol MRI?
●
Published dose–response thresholds are based
on a particular method of dose characteriza-
tion that may or may not be reproducible or
even specied in the literature.
●
Finally, the quantitative imaging modality
usedfor postradioembolization imaging will
itself eect the dose measurement owing to
dierences in quantication accuracy and
contrast recovery (a function of tumor size).
to predict treatment ecacy is associated with
several pitfalls:
e future of radioembolization includes the
use of quantitative postradioembolization imag-
●
What “dose metric” to the tumor correlates
with published tumoricidal thresholds?
Average dose, maximum dose, something else?
ing to predict treatment ecacy by comparison to
tumoricidal thresholds. is is incredibly powerful
since it allows a physician to immediately consider
15.5 Toward improved posttreatment imaging / 15.5.2 Image analysis 317
(a) (b)
alternative or adjuvant therapy, allowing radioembolization to mesh synergistically with the spectrum of treatment options available to the patient.
Several examples in the literature have illustrated
the benets of quantitative postradioembolization
imaging as a tool to inuence patient care decisions
(Chang et al., 2013; Bourgeois et al., 2014; Pasciak
et al., 2014). ese techniques are also discussed in
Chapter 14.
As we progress as a eld we must become unied and consistent to avoid the aforementioned
pitfalls. To this end, the suggestions in Section
15.5.2.1 may serve as a starting point.
15.5.2.1 Tumor contouring on
postradioembolization
quantitative imaging
Posttreatment imaging of radioact ive microspheres
is not a diagnostic test for liver cancer and should
not be treated as such. Although contouring tumor
based on areas of high 90Y activity concentration
may sometimes correlate with active tumor, more
oen it will not. erefore, this practice may lead to
unreliable correlation with dose–response thresholds and poor prognostic accuracy of quantitative
postradioembolization imaging. Instead, the following guidelines should be applied.
Figure 15.6 An example of count-preserving
deformable registration using the MIM 6 (MIM
Software Inc., Cleveland, OH) software package. (a) Semiautomatic contouring of liver and
tumor is performedon hepatic protocol MRI.
(b) Deformable registration algorithm is used to
copy contours onto 90YPET/CT posttreatment
imaging. To preserve absorbed dose quantication, contours are deformed to match the previously dened registration.
diagnostic scan is referenced. ose involved
in this task must understand that microsphere
deposition is a mechanical process and, again,
postradioembolization imaging is not diagnostic
evaluation of tumor location or activity.
15.5.2.2 Dose metrics of interest
1. Tumor contours on quantitative posttreatment
imaging should be dened based on pretreat-
ment diagnostic scans. Pretreatment diagnostic
imaging may include 18FDG PET/CT, three-
phase hepatic CT, hepatic protocol MRI, and,
for example, specialty procedures such as
111
In
octreotide SPECT for neuroendocrine tumors.
Based on the patient’s history, the appropriate
standard of care diagnostic imaging procedure
should be selected by the care provider and
used to dene tumor contours.
2. Tumor contours on pretreatment imaging
should be translated onto postradioembolization quantitative imaging using countpreserving deformable image-registration
soware. An example of this process is shown in
Figure 15.6.
Certainly, the soware in (2) above may not
always be available. A qualied radiologist or
nuclear medicine physician can still reliably draw
contours manually so long as the pretreatment
e most common dose metric reported in the literature is the average absorbed dose to the tumor
(D
). In many respects, D
avg
is awed despite its
avg
wide use for convenience. e failure of radioactive microspheres to penetrate into small areas of
tumor will articially reduce the D
measure-
avg
ments, even if the majority of the tumor may
respond to the therapy. On the other hand, D
avg
may be articially inated if a small portion of the
tumor receives a large dose, even if the majority of
it is le untreated.
Alternatively, some authors have used stan-
dards from external beam radiation therapy such
as D70 and V
for tumor analysis (Kao et al.,
100
2013). D70 is the minimum absorbed dose delivered to 70% of the tumor volume, while V
100
is
the percentage of tumor volume exceeding 100
Gy. D70 is not skewed by either of the aforementioned scenarios and is a more reproducible metric for dosimetry based on postradioembolization
quantitative imaging. While not reported by
some nuclear image analysis soware packages,
318 Future directions in radioembolization
D70 can always be computed from dose–volume
histogram data exported from a tumor contour.
15.5.2.3 Standardization
Even if count-preserving deformable image registration soware is used to measure a robust dose
metric such as D70, dose–response data used for
comparison must also have been measured in a similar reproducible way. Standardization as a eld is
essential to utilizing dose–response data to inuence
the clinical decision-making process for a patient.
In this regard, radioembolization is decades behind
external beam radiation therapy. Published guidelines from the Society of Nuclear Medicine, Society
of Interventional Radiology, American Association
of Physics in Medicine, or the American Society of
erapeutic Radiation Oncology would be helpful
in moving the eld of radioembolization forward in
the establishment of dose–response thresholds.
15.6 TOWARD EXTRAHE PATIC
TUMOR
RADIOEMBOLIZATION
Several attempts at using radioembolization for
extrahepatic tumor control and other endpoints
have been investigated. One that has received
some attention is renal artery radioembolization
for renal cell carcinoma (RCC). While renal arter y
embolization with bland microspheres prior to
surgical resection is a widely used tool that aids
in the control of blood loss during surgery, renal
artery radioembolization as a treatment modality is much more controversial. Over 20 years
ago, selective renal artery radioembolization
(RARE) using 90Y microspheres was performed
in a porcine model, with the capacity to deliver in
excess of 100 Gy to the kidney with greater than
95% dose retention and sparing of extrarenal tissues (Zimmermann et al., 1995). However, its use
in humans has never progressed beyond a few
case reports. One such example of a large (14.7 ×
11.1 cm) focal RCC mass was embolized with 90Y
glass microspheres delivering an average tumor
dose of 80 Gy (Hamoui et al., 2013). At 8 weeks
following RARE, CT imaging revealed patchy
tumor hypodensity consistent with necrosis. e
patient lived 23 months following RARE and
expired from extrarenal metastases; however, the
primary renal tumor remained well controlled
and stable (Hamoui et al., 2013). Several smallscale clinical trials are underway to continue the
investigation into the utility of RARE for RCC.
Radioembolization of lung metastases via the
bronchial artery has also been performed in a small
patient series by Ricke et al. (2013). Two patients,
one with colorectal cancer and the another with
RCC lung metastasis who had failed chemotherapy
and were not surgica l candidates, were treated usi ng
radioembolization via the bronchial artery (Ricke
et al., 2013). A conservative treatment plan was
assumed based on a T:N of 1:1 owing to the diering arterial anatomy in the lung and liver. 200 MBq
of 90Y resin microspheres was infused into both
patients through a branch of the bronchial artery
perfusing multiple lung segments. e authors
performed both posttreatment bremsstrahlung
SPECT and 90Y PET/CT and found, surprisingly,
that pulmonary deposition of microspheres was
limited only to active tumor (Ricke et al., 2013). In
fact, the T:N for bronchial artery radioembolization seems far higher than typical T:N for hepatic
radioembolization. is nding is critical in that
it supports future investigations into the utility of
radioembolization for lung metastases.
A nononcologic extrahepatic use of radioembolization has also recently been explored. Pasciak et
al. (2016) infused 90Y radioembolization into the
gastric fundus in a porcine model to evaluate the
potential of radioembolization in the management
of obesity. Although the animal cohort was small,
decreased weight gain was noted. e mechanism of action was thought to be both a decrease
in ghrelin producing cells in the gastric mucosa
and a decrease in stomach size and volume. While
this is an interesting application of radioembolization, additional animal studies are needed before a
human trial is considered.
15.7 CONCLUSIONS
Many of the ideas provided in this chapter on the
future of radioembolization stand upon research
done in the past. In some cases, interesting and novel
trials related to improving radioembolization were
performed years ago, before radioembolization was
References 319
widely used. However, the failure to widely adopt
these methods may simply be due to the fact that
radioembolization has shown strong clinical ecacy and safety as-is. is has made drastic changes
in the procedure or treatment dicult to justify.
at said, an improved understanding of radioembolization dose–response may be within reach due
to the availability of new imaging techniques such as
90
Y PET/CT. ese data could have a broad impact
on both treatment planning, patient selection, and
patient follow-up. However, this information cannot
eectively be elucidated by individual researchers;
instead, an international eort should be organized
in order to obtain useful and reproducible results,
ideally through professional societies.
As more is understood about the biological
effects of radioembolization, it will in turn will
further the multidisciplinary nature of radioembolization, expanding the role of medical
physicists, radiation oncologists, and nuclear
medicine radiologists in this treatment modality. Because of the unique nature of this therapy,
we believe this can only result in the improved
patient outcomes.
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