MDCT Anatomic Assessment of Right Inferior Phrenic Artery Origin Related to Potential Supply to...

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


University Hospital Paolo Giaccone,

Palermo, Italy

G. C. Ettorre


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


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)


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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


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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


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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)


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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.

References

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supply to hepatocellular carcinoma: Angiographic demonstration

and transcatheter arterial chemoembolization. Cardiovasc Inter-

vent Radiol 29:39–48

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


123

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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


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