Cas clinique

DOI of or1Discipline

Davila’’ Univ2Departme

and Pharmacy3Discipline

‘‘Carol DavilRoumanie.

4DepartmeHygiene and P

Trois variantes anatomiques tr�es rares del’art�ere h�epatique

Mugurel Constantin Rusu,1 Adelina Maria Jianu,2 Dorina Sztika,2 Dragos Cuzino,3

Carla Loreto,4 Bucarest et Timisoara, Roumanie; et Catane, Italie

De nombreuses variantes anatomiques de l’art�ere h�epatique, mais pas toutes, sont connues. Denouvelles ou extremement rares variantes anatomiques des art�eres h�epatiques peuvent cepen-dant etre rencontr�ees en pratique courante. Le premier cas rapport�e a �et�e document�e par lescanner et correspond �a une variante rare : une art�ere h�epatique propre r�etroporte anastomos�eeavec l’art�ere m�esent�erique sup�erieure par un arc de B€uhler. Le deuxi�eme cas pr�esente lesr�esultats d’une �etude de dissection, o�u une art�ere h�epatique moyenne (MHA) s’est av�er�ee naıtred’un tronc commun gastroh�epatique avec l’art�ere gastrique droite, du tronc de l’art�ere h�epatiquepropre ; cette MHA passait au-dessus de l’art�ere h�epatique gauche, la cachant. Par ailleurs,dans le cas 2, une art�ere h�epatique droite accessoire naissait de l’art�ere m�esent�eriquesup�erieure. Dans le troisi�eme cas rapport�e dans cet article, une boucle art�erielle associaitl’art�ere h�epatique commune et l’art�ere gastroduod�enale et envoyait une branche ascendante,diagnostiqu�ee comme MHA, et descendante, consid�er�e comme une art�ere gastroduod�enaledouble. Nous n’avons pas ne trouv�e de rapport pr�ec�edent de variantes comme celles des cas 2et 3, que nous consid�erons comme extremement rares. Cependant, les chirurgiens et lesradiologues doivent se rendre compte de telles possibilit�es morphologiques rares de l’art�ereh�epatique.

Hepatic artery variations are very important in sur-

gical and radiological procedures concerning the

liver.1 Therefore, rare or extremely rare anatomic

variants of the hepatic arteries still remain impor-

tant and should further be presented, even though

there are available studies performed on large lots.

For example, in a recent study performed using

spiral computed tomography (CT) and digital sub-

traction angiography, the celiac axis and common

hepatic artery (CHA) variations were documented

iginal article: 10.1016/j.avsg.2011.03.011.

of Anatomy, Faculty of Dental Medicine, ‘‘Carolersity of Medicine and Pharmacy, Bucarest, Roumanie.

nt of Anatomy, ‘‘Victor Babes’’ University of Medicine, Timisoara, Roumanie.

of Radiology and Medical Imaging, Faculty of Medicine,a’’ University of Medicine and Pharmacy, Bucarest,

nt of Anatomy, Diagnostic Pathology, Forensic Medicine,ublic Health, University of Catania, Catane, Italie.

in 5,002 patients.2 In more than 50% of cases,

arterial hepatic vascularization is not limited to a

single artery arising from the celiac trunk (CelT).3

Still new or extremely rare anatomical variations of

the hepatic arteries can be encountered in the cur-

rent practice.

The arch theory by Mac Kay and Tandler’s longi-

tudinal arterial anastomosis theory account for the

genesis of the arterial trunk anastomoses and the

main anatomic variations.3 According to these

Correspondance : Mugurel Constantin Rusu, Discipline of Anatomyand Embryology, Faculty of Dental Medicine, University of Medicineand Pharmacy, ‘‘Carol Davila’’ 8, Blvd. Eroilor Sanitari, RO-76241,Bucarest, Roumanie, E-mail: anatomon@gmail.com

Ann Vasc Surg 2011; 25: 1138.e1-1138.e7http://dx.doi.org/10.1016/j.acvfr.2012.12.003� Annals of Vascular Surgery Inc.�Edit�e par ELSEVIER MASSON SAS

1212.e1

Fig. 1. Computed tomographic anatomy of the arterial

variant reporteddretroportal hepatic artery and arc of

B€uhlerdon three-dimensional volume renderings (A, C)

and multiplanar reconstructions, oblique (B) and coronal

(D). 1, abdominal aorta ; 2, celiac trunk ; 3, splenic artery ;

4, left renal artery ; 5, left renal vein ; 6, superior mes-

enteric artery (SMA) ; 7, right renal artery ; 8, right renal

vein ; 9, inferior vena cava ; 10, proper hepatic artery

(PHA) ; 11, gastroduodenal artery (GDA) ; 12, portal

vein (PV), coursing between the retroportal hepatic

artery and the GDA ; 13, superior mesenteric vein ; 14,

splenic vein ; 15, left gastric artery, supplying a left

accessory hepatic branch (D, small white arrowheads)

apparently anastomosed within the hepatic parenchyma

with a left thin hepatic artery ; 16, retroduodenal arteries

that emerged from a plexus formed distal to the PV by

branches of the PHA and GDA ; 17, right hepatic artery.

Posterior to the distal end of the splenic vein and the

initial segment of the PV, the arc of B€uhler (B,

arrowhead ) joins the origins of the hepatic artery and

SMA.

1212.e2 Cas cliniques Annales de chirurgie vasculaire

theories, ventral longitudinal anastomoses occur in

development between segmental ventral branches

of the abdominal aorta. During the extensive

lengthening of the digestive tube, the absorption

and diversion will allow some branches to disappear

or further develop.3 The CelT and the superior

Vol. 25, No. 8, 2011 Cas cliniques 1212.e3

mesenteric artery (SMA) are joined together

through the pancreaticoduodenal arcades and the

arc of B€uhler. These anastomoses are divided during

pancreatic resections but are well represented in the

case of CelT stenosis.3 The anastomosis (arc, arcade)

of B€uhler between the CelT and the SMA, first

described in 1904, is a rare finding and is explained

by failure of regression of the ventral segmental

anastomoses between the 10th and 13th segmental

arteries during embryonic life.4 There are only a few

reports of the arc of B€uhler in current scientific

literature,4 and the collateral development of this

anastomosis relates to a different hemodynamic in

the upper visceral arteries.5

Fig. 2. The hepatic arterial variation in case report 1. 1,

PV ; 2, celiac trunk ; 3, SMA ; 4, splenic artery ; 5, left

gastric artery ; 6, PHA ; 7, GDA. The left main (arrow) and

accessory (double arrow) hepatic arteries are indicated.

The arc of B€uhler (arrowhead ) joins the SMA and the

PHA. *right hepatic artery.

CASE REPORT 1

A CT angiography performed on a 26-year-old male

patient revealed several rare anatomic variants that were

better detailed by use of both multiplanar reconstructions

and three-dimensional volume renderings instead of any

of these two alone (Fig. 1). The CelT was identified,

sending off the splenic artery and further dividing into the

proper hepatic artery (PHA) and the gastroduodenal

artery (GDA). The portal vein (PV) was found on three-

dimensional volume renderings coursing between the

PHA and the GDA. Therefore, a retroportal course of the

PHA was diagnosed, with that artery being continued on

the right posterior side of the PV toward the hepatic hilum.

From the PHA left, a large right hepatic artery (RHA) and a

thin left hepatic artery (LHA) entering the hepatic

parenchyma and anastomosing with a left accessory

hepatic branch emerged from the left gastric artery. On

multiplanar reconstructions, we identified retroportal and

retropancreatic anastomosis between the origins of the

PHA and the SMA, which was diagnosed as the arc of

B€uhler. These arterial variations are summarized in

Figure 2. Anastomoses of the PHA and the GDA were

identified distal to the PVdfrom that arterial network

were leaving retroduodenal arteries. Anastomoses of the

pancreaticoduodenal arteries, superior and inferior, were

also identified. An additional variation of the right renal

arteries was identified (Fig. 3), represented by a main or

hilar right renal artery (RRA) and a right inferior polar

artery, both with aortic origins. The hilar RRA left the side

of the aorta at an intermediate level between the origins of

the CelT and SMA, and had an initial course at the level of

the retroportal PHA, being separated from it by the infe-

rior caval vein.

Fig. 3. The variation of the right renal arteries in case

report 1. The abdominal aorta (1) sends off a main hilar

(2) and a lower polar (3) renal artery. (4) SMA ; com-

puted tomographic angiography, oblique multiplanar

reconstruction.

CASE REPORT 2

A second anatomical case study was performed in a

formalin-fixed adult cadaver, 59-year-old man. The CHA

was divided anterior to the left border of the PV into an

ascending branch, the PHA, and a descending one, the

GDA. Soon after its origin, the PHA split in two

trunksdone posterior (the PHA proper) and the other

anterior, anatomically uncommon. Because the latter sent

off the right gastric artery and a supernumerary hepatic

Fig. 4. Anterior view of the hepatic pedicle. 1, middle

hepatic artery (MHA) ; 2, left hepatic artery (LHA) ; 3,

PHA ; 4, gastrohepatic trunk ; 5, common hepatic artery

(CHA) ; 6, GDA ; 7, right gastric artery ; 8, right hepatic

artery (RHA) ; 9, PV ; 10, cystic artery ; 11, cystic duct ;

12, main bile duct.

1212.e4 Cas cliniques Annales de chirurgie vasculaire

artery, we termed it the ‘‘gastrohepatic trunk.’’ The PHA

continued anterior to the PV and was further divided into

a thick right branch (main RHA) and a thin left branch

(LHA), the former coursing anterior to the origin of the

proper hepatic duct where it sent off the cystic artery,

before entering the hepatic hilum. The supernumerary

hepatic artery that left the gastrohepatic trunk coursed

superposed on the anterior side of the LHA, completely

hiding it, and entered the hilum to continue within the

parenchyma of the medial segment of liver, with a left-to-

right course (Fig. 4). We evaluated that supernumerary

artery as being themiddle hepatic artery (MHA). A second

supernumerary hepatic artery was identified leaving the

SMA and was diagnosed as an accessory RHA ; it had a

retroportal and retrobiliar course toward the hepatic

hilum (Fig. 5).

Fig. 5. Schematic of case report 2. 1, gastrohepatic trunk ;

2, right gastric artery ; 3, MHA ; 4, GDA ; 5, PHA ; 6, LHA ;

7, main RHA ; 8, accessory RHA ; 9, cystic artery ; 10,

CHA ; 11, SMA.

CASE REPORT 3

The third variant reported in this article resulted after the

dissection of a human adult cadaver that was formalin-

fixed, aged 68 years, and male. In that case, the CHA

was identified properly dividing into the descending GDA

and the ascending PHA. PHA coursed on the left side of the

PV and was divided into the LHA and the RHA, the latter

coursing behind the common hepatic duct and sending off

the cystic artery. Additional arterial variation was further

identified : the two branches of the CHA seemed to

anastomose by an arterial loop, from which originated an

ascending and a descending branch : the ascending one

was identified as MHA and coursed anterior to the PV on

the right side of the PHA, and the descending one

appeared as a duplicate of the GDA, on the right side of it

(Figs. 6 and 7).

DISCUSSION

Absorption and shifting of the three embryonic

hepatic arterial roots may vary with persistence

Fig. 6. Multiple arteries in case report 3. 1, common hepatic duct ; 2, RHA ; 3, cystic artery ; 4, cystic duct ; 5, MHA ; 6,

main bile duct ; 7, duplicate GDA ; 8, LHA ; 9, PHA ; 10, PV ; 11, CHA ; 12, GDA ; 13, right gastric artery.

Vol. 25, No. 8, 2011 Cas cliniques 1212.e5

of embryonic hepatic arteries (left, middle, and

right) inducing variations of great interest for

hepatic and pancreatic surgery.3 In case report

1 : (1) the left primitive hepatic artery persisted

as a rudimentary vessel emerging from the left

gastric artery and anastomosed with the left

branch of the PHA, (2) the middle primitive

hepatic artery persisted as PHA, emerging directly

from the CelT and coursing posterior to the PV,

and (3) the right primitive hepatic artery that

emerged from the SMA was absorbed into the

PHA, except for its initial segment that persisted

as an arc of B€uhler.Song et al. (2010) found in 4,939 patients only six

cases (0.12%) of CHAs originating from the normal

CelT that had a retroportal course and therefore

were located in the portacaval space.2 Our case

shows that a retroportal PHA can be differentiated

from the RRA by identifying the inferior caval vein :

the PHA has a precaval course, whereas the RRA is

retrocaval.

There were reported cases of retroportal courses

of the RHA or CHA emerging from the SMA.2,5 In

such cases, the initial segment of the hepatic arteries

corresponds to the location of the arc of B€uhler,whereas the initial link of these hepatic arteries to

the CelT is lost.

Grabbe and B€ucheler (1980) discovered the arc of

B€uhler in 14 cases among 340 selective celiac and

superior mesenteric arteriographic studies (4.11%)

and evaluated that its existence permits conclusions

about further angiographic procedures and facilita-

tes the interpretation of visceral collaterals.6

McNulty et al. (2001) found the arc of B€uhler in

three of 300 cases (1%).4 It has also been described

that the arc of B€uhler may rarely give (1-2%)

branches for the pancreas, such as a transverse

pancreatic artery on the left and a Kirk arcade on the

right.3 Jeong et al. (2008) reported an asymptomatic

arc of B€uhler aneurysm successfully treated by

transcatheter coil embolization ; these authors

emphasized that aneurysms of that anastomosis are

Fig. 7. Schematic of the variant in case report 3. 1, PV ;

2, main bile duct ; 3, CHA ; 4, GDA ; 5, PHA ; 6, LHA ; 7,

RHA ; 8, cystic artery ; 9, MHA.

1212.e6 Cas cliniques Annales de chirurgie vasculaire

even more uncommon, and are associated with

stenosis or occlusion of the celiac axis.7

In conclusion, radiologistsmust be aware concep-

tually of the possibilities of arterial variation.

Moreover, the concomitant presence of more than

one variation, as in the case reported in this article,

is possible. Such situations are important to be

explored in detail, with two-dimensional and

three-dimensional CT tools because the provided

data may further help surgeons or interventional

radiologists during the approach of the suprameso-

colic and/or retroperitoneal spaces.

The MHA in either case report 2 or in case report

3 was not previously identified in studies dealing

with this artery.

To our knowledge, case report 2 is the first report

of a gastrohepatic trunk representing the common

origin of the right gastric artery and an extrahilar

MHAoriginating from the PHA.Moreover, we could

not find any mention for an MHA masquerading

as the LHA on the side of the PV, relation that may

be extremely important for both surgeons and

radiologists.

The complex arterial anatomy in case report 3,

with the arterial loop joining the primary branches

of the CHA and further sending an MHA and a

duplicate GDA, increases the arterial density on

the anterior side of the PV and thus the risk of surgi-

cal damage, if such variation is unexpected.

Two recent studies, one performed by dissec-

tions8 and the other performed on CTs,9 deal with

the MHA which, even though it is not identified as

such by the Nomina Anatomica (the only term

coined there is a.segmenti medialis),10 is extremely

important for surgeons. In living donor liver trans-

plantation, injuries to the MHA, which supplies

blood primarily to hepatic segment 4, may lead to a

reduction in the functional volume of the left

hepatic lobe and a decrease in the blood supply to

bile ducts of this lobe.9 The origin of the MHA is also

important for split liver transplantation.8

In the article by Jin et al. (2008), the PHA type of

MHA (MHA originating from the PHA)was encoun-

tered in three of 62 livers (4.8%) and left the bifur-

cation of the PHA, transforming it into a

trifurcation.8 Wang et al. found the MHA originat-

ing a further normally bifurcated PHA in two of 103

cases (1.94%).9 Wang et al. grouped as ‘‘type V’’

(6.8%) all the variants of MHA originating from a

non-LHA and non-RHA along the axis of the CHA ;

the respective authors state that patients with a type

V MHA should be assessed on a case-by-case basis.9

Neither of these two studies offers evidences for

such rare variants ofMHA from PHA ;moreover, the

arterial patterning is not topographically correlated

with the neighboring anatomical structures.

A detailed study of the hepatic arteries is manda-

tory for several pathological conditions affecting the

liver. For such studies, multidetector row CT angio-

graphy generates near isotropic voxels, producing

excellent image quality and detail. In particular,

presurgical planning for patients undergoing hepa-

tic surgery or selective chemotherapy infusion

requires a complete detailed assessment of hepatic

vessel anatomy.11

The first author was supported by the Sectoral Operational

Programme Human Resources Development, financed from the

European Social Fund, and by the Romanian Government

under the contract number POSDRU/89/1.5/S/64109.

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