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PICTORIAL ESSAY
MDCT Anatomic Assessment of Right Inferior Phrenic ArteryOrigin Related to Potential Supply to Hepatocellular Carcinomaand its Embolization
Antonio Basile Æ Dimitrios Tsetis Æ Arturo Montineri Æ Stefano Puleo ÆCesare Massa Saluzzo Æ Giuseppe Runza Æ Francesco Coppolino ÆGiovanni Carlo Ettorre Æ Maria Teresa Patti
Received: 14 May 2007 / Accepted: 2 July 2007 / Published online: 11 December 2007
� Springer Science+Business Media, LLC 2007
Abstract
Purpose To prospectively assess the anatomic variation
of the right inferior phrenic artery (RIPA) origin with
multidetector computed tomography (MDCT) scans in
relation to the technical and angiographic findings during
transcatheter arterial embolization of hepatocellular carci-
noma (HCC).
Methods Two hundred patients with hepatocellular
carcinomas were examined with 16-section CT during
the arterial phase. The anatomy of the inferior phrenic
arteries was recorded, with particular reference to their
origin. All patients with subcapsular HCC located at
segments VII and VIII underwent arteriography of the
RIPA with subsequent embolization if neoplastic supply
was detected.
Results The RIPA origin was detected in all cases (sen-
sitivity 100%), while the left inferior phrenic artery origin
was detected in 187 cases (sensitivity 93.5%). RIPAs
originated from the aorta (49%), celiac trunk (41%), right
renal artery (5.5%), left gastric artery (4%), and proper
hepatic artery (0.5%), with 13 types of combinations with
the left IPA. Twenty-nine patients showed subcapsular
HCCs in segments VII and VIII and all but one underwent
RIPA selective angiography, followed by embolization in 7
cases.
Conclusion MDCT assesses well the anatomy of RIPAs,
which is fundamental for planning subsequent cannulation
and embolization of extrahepatic RIPA supply to HCC.
Keywords Chemoembolization � Hepatocellular
carcinoma � Multidetector computed tomography �Right inferior phrenic artery
Introduction
The right inferior phrenic artery (RIPA) is considered the
most common extrahepatic collateral pathway supplying
hepatocellular carcinomas (HCCs) [1–3]. Transcatheter
chemoembolization (TACE) of the RIPA has been
reported to have its own therapeutic role as an adjunct to
TACE of the hepatic artery, and this can be done
A. Basile (&) � M. T. Patti
Department of Diagnostic and Interventional Radiology,
Ospedale Ferrarotto, via Citelli 14, 95124 Catania, Italy
e-mail: [email protected]
D. Tsetis
Department of Radiology,
University Hospital of Heraklion,
Medical School of Crete, Heraklion, Greece
A. Montineri
Department of Infectious Diseases,
Ospedale Ferrarotto, via Citelli 14,
95124 Catania, Italy
S. Puleo
Department of General Surgery,
Ospedale Vittorio Emanuele, via Plebiscito 125,
95124 Catania, Italy
C. Massa Saluzzo
Department of Radiology, Policlinico S. Matteo, Pavia, Italy
G. Runza � F. Coppolino
Department of Radiology,
University Hospital Paolo Giaccone,
Palermo, Italy
G. C. Ettorre
Department of Radiology,
University Hospital, Catania, Italy
123
Cardiovasc Intervent Radiol (2008) 31:349–358
DOI 10.1007/s00270-007-9236-x
without causing serious procedural complications. A few
minor complications may occur, such as shoulder pain, a
small amount of pleural effusion, abdominal rash, basal
atelectasia, and transient mild hemoptysis [1, 4, 5];
because the RIPA is one of the major arteries supplying
blood to the diaphragm, post-TACE diaphragmatic
weakness has also been reported [6].
Due to the variable anatomy of its origin, cannulation of
the RIPA can be challenging, and in this context preoperative
multidetector computed tomographic (MDCT) angiography
reconstruction and mapping of phrenic artery anatomy can
be helpful in planning percutaneous angiography and sub-
sequent embolization. The aim of this pictorial essay is to
give an overview of RIPA anatomy obtained by MDCT
imaging data for planning angiographic cannulation and
embolization of extrahepatic RIPA supply to HCC.
Materials and Methods
A total of 200 patients (112 men, 88 women; mean age
67 years, range 42–78 years) with diagnosed HCC were
imaged during the period January 2006 to March 2007.
Scanning was performed with a 16-section CT unit
(Brilliance, Philips, Eindhoven, The Netherlands) using a
standard technique. A low-dose precontrast scan of the
abdomen was obtained by using 5 mm collimation, 120
kV, and 140 mA.
Subsequently, intravenous injection of 120–150 ml of
nonionic iodinated contrast material containing 350 mg of
iodine per milliliter was performed through an 18–20G
cannula placed into an antecubital vein at a rate of 4–5 ml/
sec using a mechanical injector (Stellant, MEDRAD). The
bolus triggering (automated software with scan triggering;
Philips) with a calculated 7 sec scan delay after achieve-
ment of preset aortic attenuation of 150 HU was used for
initiating the arterial phase imaging. This was followed by
portal (60–80 sec delay) and late venous phase imaging
(180 sec delay), from the time of initiation of contrast
Table 1 The combined origins of the right inferior phrenic artery (RIPA) and left inferior phrenic artery (LIPA)
Anatomy Type No. of cases Rate (%)
RIPA and LIPA originate separately from the celiac trunk 1 40 20
RIPA and LIPA originate as a common trunk from the celiac trunk 2 32 16
RIPA and LIPA originate as a common trunk from the aorta at the left side of the celiac trunk 3 24 12
RIPA and LIP originate separately from the lateral sides of the aorta 4 23 11.5
RIPA and LIPA originate as a common trunk from the middle ventral aortic wall above
the origin of the celiac trunk
5 18 9
RIPA originates from the aorta; LIPA originates from the celiac trunk 6 16 8
RIPA from the right renal artery LIPA from the aorta 7 11 5.5
RIPA originates from the LGA; LIPA originates from the aorta 8 8 4
RIPA and LIPA originate separately from the middle ventral aortic wall above
the origin of the celiac trunk
9 6 3
RIPA originates from the celiac trunk; LIPA originates from the aorta 10 4 2
RIPA originates from the aorta; LIPA originates from the left renal artery (LRA) 11 2 1
RIPA originates from the aorta; LIPA originates from the splenic artery 12 2 1
RIPA originates from the proper hepatic artery; LIPA originates from the aorta 13 1 0.5
RIPA originates from the celiac trunk; LIPA origin poor visible a 6 3
RIPA originates from the aorta; LIPA origin poor visible a 7 3.5
a Cases in which the LIPA origin was poorly detected
Table 2 Origins of the right inferior phrenic artery (RIPA)
Origin of the RIPA No. of cases (rate, %)
Aorta 98 (49%)
Celiac trunk 82 (41%)
Left gastric artery 8 (4%)
Right renal artery 11 (5.5%)
Proper hepatic artery 1 (0.5%)
Table 3 Origins of the left inferior phrenic artery (LIPA)
Origin of the LIPA No. of cases (rate, %)
Aorta 95 (47.5%)
Celiac trunk 88 (44%)
Splenic artery 2 (1%)
Left renal artery 2 (1%)
Poorly detected 13 (6.5%)
350 A. Basile et al.: MDCT Anatomic Assessment of Right Inferior Phrenic Artery Origin (2008) 31:349–358
123
material injection. A detector configuration of 16 9 1.5
mm was selected for the arterial phase of scanning, which
was performed using a section thickness of 2 mm, incre-
ment 1 mm, and rotation time 0.5 sec. Portal and venous
phase scanning were then performed using a section
thickness of 3 mm, increment 3 mm. Two- and three-
dimensional reconstructions of IPAs were generated using
maximum intensity projection (MIP) and multiplanar ref-
ormation of the arterial phase images. The origin of the
phrenic arteries, either as common trunk or as separate
vessels, from the aorta, celiac trunk, hepatic artery, left
gastric artery, and right renal artery were recorded. All
patients with subcapsular HCCs located in segment VII or
VIII were scheduled for selective arteriography of the
celiac, superior mesenteric, and right phrenic arteries with
subsequent TACE if neoplastic blood supply was detected.
Fig. 1 A–D Sequential axial
MDCT scans demonstrate the
origin of the inferior phrenic
arteries (IPAs) from the aorta as
a common trunk at the left side
of the celiac artery, and the
trajectory of the RIPA (white
arrows) in a patient with a
segment VII HCC (black
arrow). E Three-dimensional
reconstruction
Fig. 2 Axial MDCT scan shows the IPA origins at both sides of the
aorta (arrows)
A. Basile et al.: MDCT Anatomic Assessment of Right Inferior Phrenic Artery Origin (2008) 31:349–358 351
123
Results
The results of the anatomic findings are classified on the
basis of the combined origins of both the RIPA and left
inferior phrenic artery (LIPA) (Table 1), and considering
only the origin of the RIPA (Table 2). We found a total of
13 combined variations of the IPAs (Table 1). As shown in
Tables 1, 2, and 3, the RIPA: (a) originated either from the
aorta (49%), with a common trunk at the left side of the
celiac trunk (type 3, 12%; Fig. 1), separately at both lateral
sides of the aorta (type 4, 11.5%; Fig. 2), as a common
trunk above the origin of the celiac artery (type 5, 9%;
Fig. 3), or separately from the anterior aortic wall above
the origin of celiac trunk (type 9, 3%; Fig. 4), with the
LIPA originating either from the splenic artery (type 12,
1%), from the celiac trunk (type 6, 8%; Fig. 5), or from the
left renal artery (type 11, 1%; Fig. 6), or without visuali-
zation of the LIPA origin (3.5%); (b) originated from the
celiac trunk (41%) with a common origin with the LIPA in
16% of cases (type 2; Fig. 7), and separately in 20% of
cases (type 1; Fig. 8), with the LIPA originating from the
aorta (type 10, 2%), or without visualization of the LIPA
origin (3%); (c) originated from the right renal artery
(5.5%), with the LIPA originating from the aorta (Fig. 9);
(d) originated from the left gastric artery (4%), with the
Fig. 3 MIP reconstruction in A coronal, B axial, and C sagittal
planes shows a common origin (arrow) of the IPAs above the celiac
trunk
Fig. 4 A Coronal and B axial plane MDCT scans show the separate
origin of the IPAs from the anterior aortic wall above the celiac trunk
352 A. Basile et al.: MDCT Anatomic Assessment of Right Inferior Phrenic Artery Origin (2008) 31:349–358
123
LIPA originating from the aorta (Fig. 10); or (e) originated
from the proper hepatic artery (0.5%; Fig. 11). Twenty-
nine patients had subphrenic HCCs located in segments VII
and VIII; all but one underwent selective angiography of
the hepatic artery and of the RIPA followed by emboliza-
tion. In all but one case the cannulation of the RIPA was
performed at the same session as angiography. In one case,
the angle of the RIPA originating from the celiac trunk
made the cannulation impossible, despite using the tech-
nique described by Miyayama and colleagues [7](Fig. 12).
In 16 of 29 cases, the RIPA originated from the celiac trunk
(Fig. 13), in 11 cases from the aorta (Fig. 14), and in 1 case
from the right renal artery (Fig. 15) and from the proper
hepatic artery (Fig. 16). MDCT scans were fundamental in
detecting the different RIPA origins, helping us in selec-
tively catheterizing the vessel and obviating the need for
Fig. 5 Axial MDCT scan shows the RIPA originating from the aorta
(white arrow) and the LIPA (black arrow) from the celiac trunk
Fig. 6 Coronal plane MIP reconstruction shows the LIPA originating
from the left renal artery (white arrow)
Fig. 7 Axial MDCT scans demonstrate the IPAs (white arrows)
originating as a common trunk from the celiac artery (black arrow)
A. Basile et al.: MDCT Anatomic Assessment of Right Inferior Phrenic Artery Origin (2008) 31:349–358 353
123
several injections of contrast and angiograms in different
projections. Seven of the 29 RIPAs catheterized supplied
the neoplasms and all of these were embolized using a
microcatheter and lipiodol. Five patients with RIPA neo-
plastic supply had been previously treated with TACE (n =
5) or with radiofrequency ablation (n = 2). In 2 cases the
neoplasm was solely supplied by the RIPA. In one of these
the RIPA directly supplied the segment VII tumor in a
patient with bifocal HCC who had not previously
Fig. 8 Axial MDCT scan shows the IPAs originating separately from
the celiac trunk (arrows)
Fig. 9 Coronal plane MIP reconstruction shows type 7 anatomy of
the IPAs, with the RIPA originating from the right renal artery (black
arrow) and the LIPA originating from the aorta (white arrow)
Fig. 10 Axial MIP reconstruction shows type 8 anatomy of the IPAs,
with the RIPA originating from the left gastric artery (black arrow)
and the LIPA originating from the aorta (white arrow)
Fig. 11 Axial plane MIP reconstruction shows the RIPA originating
from the proper hepatic artery
Fig. 12 Sagittal plane MIP reconstruction shows the acute celiac-
phrenic angle impossible to cannulate
354 A. Basile et al.: MDCT Anatomic Assessment of Right Inferior Phrenic Artery Origin (2008) 31:349–358
123
undergone percutaneous treatments (Fig. 13); in the other
case, the patient had already been treated with TACE and
radiofrequency ablation and showed a recurrence at 1 year
follow-up (Fig. 16). In 4 cases the neoplasms received
blood either from the hepatic arteries or from the RIPA
(Fig. 14). The diameter of the RIPAs supplying HCCs
ranged between 18 and 32 mm on MDCT imaging, and in 6
cases (85.7%) the RIPA was larger than the LIPA
(Table 4). All but one patient who underwent RIPA
embolization suffered shoulder pain; in 3 cases lipiodol
was detected in the ipsilateral lung vessels, fortunately with
no clinical consequences.
Fig. 13 A–N. A 56-year-old man. A Bifocal HCCs at segments I
(black arrow) and VII (white arrow). B–E Axial plane MDCT scans
show the trajectory of the RIPA (white arrows). F Sagittal, G coronal,
and H curved plane MIP reconstructions show the anatomy of the
RIPA. I Celiac angiography demonstrates the origin of the RIPA
(black arrow), the sole feeding vessel of J the segment VII neoplasm
(arrow). K Post-embolization angiogram shows the occlusion of the
RIPA branch supplying the HCC. L CT control after embolization
shows the neoplasm completely filled with lipiodol
A. Basile et al.: MDCT Anatomic Assessment of Right Inferior Phrenic Artery Origin (2008) 31:349–358 355
123
Discussion
Recently, CT angiography with helical multidetector row
technology and multiplanar reconstructions has become
the imaging technique of choice for a variety of vascular
districts, in conjunction with bolus tracking or automated
scan triggering. With this new technique, a comprehen-
sive evaluation of the inferior phrenic artery anatomy
can be performed with a relatively quick review of the
three-dimensional dataset alone, and it can be useful in
planning embolization sessions. In recent years particular
attention has been focused on the importance of the
development of various extrahepatic collateral vessels
supplying HCCs according either to tumor size and
location, or on previous treatment such as surgical liga-
tion of the hepatic artery or repeated embolizations [8,
9].
However, HCCs can frequently be supplied by extra-
hepatic collateral arteries even when the hepatic artery is
patent, and sometimes these can be the only supply [8,
9]. Extrahepatic collaterals to HCCs from the IPA,
internal mammary artery, omental artery, intercostal
artery, lumbar artery, adrenal artery, renal artery, left
gastric artery, cystic artery, and superior mesenteric
artery have been reported [1–3, 9, 10]. In two recent
series the RIPA was found to be the most common
extrahepatic collateral vessel that supplies HCC [1, 2].
Kim and colleagues [1] observed 2,104 extrahepatic
collateral vessels in 860 patients over 5.5 years; 1,026
RIPAs supplying tumors were observed at angiography
and 864 (84%) were embolized. Miyayama and col-
leagues [2] retrospectively evaluated extrahepatic
collateral pathways to HCCs on angiography in 386
procedures on 181 consecutive patients with an incidence
of 83% of a collateral source to HCCs from the RIPA.
Transient pleural effusion, reported in up to 33% of
RIPA embolization, basal atelectasia mainly due to
iodized oil accumulation in the lung, reported in up to
8% of these cases, and shoulder and neck pain during
embolization have been reported as common complica-
tions of RIPA embolization [1, 8].
A recent anatomic evaluation of the phrenic arteries has
been reported by Loukas and colleagues on cadavers [11].
The authors examined 300 adult human cadavers; in
addition, 30 livers containing HCC were examined, to
observe any arterial differences between normal and dis-
eased cadavers, with special emphasis on vessel origin and
dimensions. The results showed that the RIPA was always
associated with HCC and served as the major collateral
artery adjunct to the hepatic artery; its origin was from: (a)
the celiac trunk in 40% of the specimens; (b) the aorta in
38%; (c) the renal artery in 17%; (d) the left gastric artery
in 3%; and (e) the proper hepatic artery in 2% of the
specimens. The authors also found that HCC not previously
treated received branches from a RIPA, in addition to a
hepatic artery; from their findings in patients with
Fig. 14 A–D. A 63-year-old
man with solitary HCC. ACoronal plane MIP
reconstruction perfectly
matches B the celiac
angiographic finding, performed
after lipiodol embolization from
the hepatic artery. C The RIPA
supplying the HCC was
detected followed by
embolization. D Post-
embolization control shows the
occluded RIPA (black arrow)
356 A. Basile et al.: MDCT Anatomic Assessment of Right Inferior Phrenic Artery Origin (2008) 31:349–358
123
neoplasms, a RIPA with an internal diameter of more than
2.5 mm suggested a neoplastic supply.
The are only two reported CT studies focused on the
anatomy of the RIPA. In the first, published by Gokan et al.
in 2001 [12], the authors described the appearance of the
RIPA on single-slice CT in 16 patients with arteriograph-
ically proven HCCs supplied by the RIPAs. They showed
dilated RIPAs with an average diameter of 3.3 mm, sig-
nificantly larger than that of the LIPA (average 1.5 mm),
and concluded that asymmetric dilatation of the RIPA
could be considered an indicator of an extrahepatic col-
lateral of HCC in such patients. In the other article,
published by Hiwatashi and Yoshida in 2003 [13], the
authors assessed the origin of the RIPA in 216 patients
using arterial-phase contrast-enhanced multidetector row
helical CT, confirmed in 26 patients by angiography.
The data in our series partially match those in these other
studies; in fact the RIPAs supplying the neoplasm showed a
larger diameter than the LIPAs in 85.7% of cases, with a
diameter range of 2 to 3.2 mm. The cannulation of the RIPA
can be challenging because of its small size and origin, and
different techniques have been published to help operators
[6, 14]. As reported by Mirayama and colleagues [2], the
cannulation of the RIPA can be directly related to the level of
the expertise of the operators. The authors reported 285
TACE procedures through the phrenic arteries including
repeated sessions, with a technical failure in the first 10
attempts and with intimal injury occurring in 1 procedure
(0.3%). In the other 7 cases, TACE was retried, after a first
unsuccessful attempt, with a second or third attempt through
different arterial accesses including the left brachial artery,
or by using a catheter with a large side hole with the tech-
nique reported by the same authors in 2001 (7).
On the basis of our experience, selective arteriography
of the RIPA should be performed in all cases of subphrenic
HCC located at segments VII and VIII, and in these cases
preinterventional CT angiography with helical multide-
tector row technology and multiplanar reconstructions is
fundamental to planning the cannulation of the RIPA,
especially in cases of rare anatomy.
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Fig. 15 A MDCT scan in the coronal plane and B the selective
angiogram show the RIPA originating from the right renal artery in a
patient with a segment VIII HCC. C The selective angiogram did not
detect any neoplastic supply from the RIPA
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Fig. 16 A A 68-year-old woman with a solitary segment VIII HCC
already treated with chemoembolization plus radiofrequency ablation
showed a recurrence at the 12 month MDCT follow-up (black arrow).
B Coronal plane MIP reconstruction shows the origin of the RIPA
from the proper hepatic artery (black arrow). C Hepatic arteriography
did not detect any supply. D, E Selective angiogram of the RIPA
demonstrates the HCC supply (black arrows). F Post-embolization
angiogram shows the occluded RIPA
Table 4 Diameters of the right (RIPA) and left (LIPA) phrenic
arteries
Patient age
(years)/
Gender
Type of HCC RIPA diamete
r(mm)
LIPA diameter
(mm)
72/M Multifocal 2.2 1.8
63/M Solitary (segment VII) 3.2 2.5
56/M Two lesions
(segments I and VII)
2.7 1.8
55/M Multifocal 2.1 2
68/F Solitary (segment VIII) 2 2
52/M Multifocal 2.5 2
71/M Solitary (segment VIII) 3 2.2
358 A. Basile et al.: MDCT Anatomic Assessment of Right Inferior Phrenic Artery Origin (2008) 31:349–358
123