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Multiple arterial variation of the human upper limb

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A N A T O M I C V A R I A T I O N S

B. Durgun Æ A.H. Yu¨cel Æ E.D. Kizilkanat Æ F. Dere

Multiple arterial variation of the human upper limb

Received: 6 September 2001 / Accepted: 2 December 2001 / Published online: 8 June 2002 Ó Springer-Verlag 2002

Abstract A case report of multiple variations involving

the arteries of the upper limb in a single cadaver is

presented. In addition to the proximal origin of the

ar-teries unusual arterial patterns on both the right and left

sides were present. On the right side, the subscapular

artery gave rise to a large posterior circumflex humeral

artery in addition to the thoracodorsal and circumflex

scapular arteries. On the left side, the radial and ulnar

arteries arose from the brachial artery at the level of

arm, with their origins being opposite to the usual

ar-rangement. There was an arciform anastomosis between

the radial and ulnar arteries, with the radial recurrent

artery arising from the concavity of the arch. The course

of both the radial and ulnar arteries was normal at the

wrist and hand, except for the absence of the first palmar

metacarpal artery and an early bifurcation of the second

palmar metacarpal artery. The French version of this

article is available in the form of electronic

supplemen-tary material and can be obtained by using the Springer

LINK

server

located

at

http://dx.doi.org/10.1007/

s00276-002-0011.

Variations arte´rielles multiples du membre supe´rieur

Re´sume´ Nous rapportons un cas de variations multiples

inte´ressant les arte`res du membre supe´rieur rencontre´es

sur le meˆme cadavre. En plus de l’origine proximale des

arte`res, on trouvait une disposition inhabituelle des

coˆte´s droit et gauche. A droite, l’arte`re subscapulaire

abandonnait

une

volumineuse

arte`re

circonflexe

hume´rale poste´rieure en plus de l’arte`re thoraco-dorsale

et de l’arte`re circonflexe de la scapula. Du coˆte´ gauche,

les arte`res radiale et ulnaire naissaient de l’arte`re

brac-hiale au niveau du bras et leurs origines e´taient dispose´es

inversement a` la disposition habituelle. Les arte`res

rad-iale et ulnaire e´taient relie´es par une anastomose

arci-forme.

L’arte`re

re´currente

radiale

naissait

de

la

concavite´ de cette arche. Les arte`res radiale et ulnaire

avaient un trajet normal au poignet et a` la main, a`

l’exception de l’absence de la premie`re arte`re

me´ta-carpienne palmaire et de la bifurcation pre´coce de la

deuxie`me arte`re me´tacarpienne palmaire.

Keywords Axillary artery Æ Brachial artery Æ

Arterial variation Æ Embryology

Introduction

The arterial pattern of the human upper limb shown in

textbooks is rarely encountered [16], withmajor and

minor variations being well documented. While

Tied-eman [13] was the first to describe these variations

sys-tematically, Quain’s series [11] was the first to provide

sufficient data for statistical evaluation. Some reports

have classified these variants and subdivided them into

groups [1, 4, 6, 8, 14], while others deal only with

indi-vidual examples of unusual patterns [2, 3, 7, 9, 10, 15].

These arterial variations can best be explained on the

basis of the embryological development of the vascular

networks in the upper limb.

The present case showed different arterial patterns on

the left and right sides. Its importance is explained from

anatomical, embryological and clinical viewpoints.

Case report

The dissection was conducted on both upper limbs and axilla of a 50-year-old-male cadaver as part of a teaching programme. The unusual branching of the principal arteries on the right side was different from those on the left. No scarring or surgical incisions Surg Radiol Anat (2002) 24: 125–128

DOI 10.1007/s00276-002-0011-z

The French version of this article is available in the form of electronic supplementary material and can be obtained by using the Springer LINK server located at http://dx.doi.org/10.1007/s00276-002-0011

B. Durgun (&) Æ A.H. Yu¨cel Æ E.D. Kizilkanat Æ F. Dere Department of Anatomy, Faculty of Medicine,

C¸ukurova University, 01330 Adana, Turkey E-mail: bdurgun@cu.edu.tr

Tel.: +90-322-3386530 Fax: +90-322-3386572

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were apparent in the skin. The nomenclature used in this report is the Terminologia Anatomica authorized by the FCAT in 1998 [12].

On the right side, the thoracoacromial and lateral thoracic aa. arose from the 1st part of the axillary a.; however these had been sacrificed by the students. The subscapular a. arose from the medial aspect of the 2nd part of the axillary a. Arising from the sub-scapular a. the posterior circumflex humeral a. then passed poste-riorly with the axillary n. through the lateral axillary space, after which its course and distribution followed the usual pattern (Fig. 1). The thoracodorsal a. arose from the subscapular a. as an anterior terminal branch, while some 4 cm distal to the origin of the subscapular a. the circumflex scapular a. arose as a posterior terminal branch. The latter curved around the lateral border of the scapula to supply the muscles on the dorsum of scapula and con-tributed to an extensive arterial anastomosis.

The subscapular n. passed behind the axillary and posterior circumflex humeral aa. The musculocutaneous n. passed between the axillary a. and coracobrachialis; the remaining branches of the brachial plexus were normal. The anterior circumflex humeral a. and a. profunda brachii arose from the lateral and inferior aspect of the 3rd part of the axillary a., respectively: both then followed their normal course.

On the left side, the subscapular a. arose from the 1st part of the axillary a.; however, its course and branching were usual (Fig. 2A). The profunda brachii, arising from the origin of the brachial a., had neither middle nor radial collateral branches. The most striking variation on the left side, however, was the high division of the brachial a., 3.5 cm distal to the inferior border of teres major (15.5 cm proximal to the intercondylar line), giving rise to the radial and ulnar aa. deep to biceps brachii (Fig. 2B). Two centimetres distal to its origin from the medial side of the brachial a. the radial a. crossed anteriorly and laterally to the ulnar a. and then followed the median n. down the lateral side of the arm. It gave muscular branches to biceps brachii at the crossing point and then passed down the arm between the medial border of the short head of biceps brachii and the median n. (Fig. 2A). The radial a. initially passed medial to the median n. and then anterior, leaving the nerve 2.5 cm proximal to the apex of the cubital fossa. In the forearm, it was situated between bra-chioradialis and pronator teres until 8 cm proximal to the wrist, where it became superficial, being covered only by skin, subcuta-neous tissue and deep fascia.

The ulnar a., the larger terminal branch of the brachial a., arose from the lateral side of the brachial a. and curved medially to lie on the medial side of the arm and forearm. As well as maintaining a close relationship with the ulnar n. and its usual branches, the ulnar a. gave rise to the superior and inferior ulnar collateral aa. 3 cm and 13 cm distal to its origin, respectively (Fig. 2B). The common interosseous a., a branchof the ulnar a., was approximately 1 cm in length, passing initially deep to pronator teres, then flexor digito-rum profundus, continuing distally on the anterior surface of the interosseous anterior a. The anterior interosseous a. gave off muscular branches as well as nutrient branches to radius and ulna. At the proximal border of pronator quadratus it pierced the int-erosseous membrane to gain access to the dorsum of the forearm and anastomosed with the posterior interosseous a.; however, it was most closely related to the anterior interosseous n.

Two centimetres above the lateral border of pronator teres an arciform anastomosis passing anterior to supinator was present as an oblique connection between the radial and ulnar aa.: it was 2.5 cm in length (Fig. 3). The recurrent radial a. arose from the concavity of the arch, while four rami arose from its convexity supplying supinator, and the long and short extensor carpi radialis mm. Both the radial and the ulnar aa. showed a normal position at the wrist and in the hand forming the superficial and deep palmar arches. There were, however, some exceptions: the radial a. passed under the flexor retinaculum, the 1st palmar metacarpal a. was absent, there was an early bifurcation of 2nd metacarpal a., and the connection between the 2nd dorsal metacarpal a. and the perfo-rating a. was via an anastomosis. No major variations in the muscles or brachial plexus were observed.

Discussion

The distribution and course of the arteries of human

upper limb are highly variable. The variations reported

to date can be classified into six groups to facilitate

discussion:

i) anomalous branching of the axillary a. [1, 7, 9, 17],

ii) variations in the point of origin of brachial branches

[3, 6, 8, 9, 14, 17],

iii) unusual course and distribution of brachial branches

[3, 8, 10],

iv) absence of the radial a. [10],

v) presence of an accessory brachial a. [8, 10, 15],

vi) variations in the arteries of hand [3, 4, 6].

In the present case the right subscapular a. that

normally arises from the 3rd part of the axillary a. arose

instead from the 2nd part. In addition to the

thoraco-dorsal and circumflex scapular aa., it also gave rise to

the posterior circumflex humeral a. The profunda

bra-chii also arose from the 3rd part of axillary a. Pestemalci

et al. [9] reported a common trunk of the subscapular

and posterior circumflex humeral aa. in 32% of their

Turkishcases.

In the present case the radial and ulnar aa. not only

arose high up, but also on the opposite side to usual. The

radial a. then crossed the ulnar to pass laterally in the

arm and forearm. This differs from the observations of

Danenow [2], in which the variation of the upper limb

vessels was at the level of forearm; however, it is similar

to the case described by Yu¨cel [17]. The radial and ulnar

aa. in the present case may not be regarded as either a

superficial brachial or a superficial ulnar a. because both

Fig. 1. Branches of the right axillary a. and their relationship with

the nerves. 1, pectoralis minor; 2, musculocutaneous n.; 3, thoracoacromial a. (sacrificed); 4, lateral thoracic a. (sacrificed); 5, axillary a.; 6, muscular branches of the axillary a.; 7, anterior circumflex humeral a.; 8, subscapular a.; 9, subscapular n.; 10, posterior circumflex humeral a.; 11, axillary n.; 12, vascular pedicle of vastus medialis; 13, thoracodorsal a.; 14, circumflex scapular a 126

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arteries were deep and did not bifurcate in the cubital

fossa.

The arterial supply of biceps brachii in the present

case was not classified in the study by Kanbayashi et al.

[5]. An oblique arciform vessel directly connecting the

radial and ulnar aa. as reported here has not been

pre-viously reported.

Absence of the left 1st metacarpal palmar a., early

bifurcation of the left 2nd metacarpal palmar a., and the

course of these branches along the metacarpals, together

with the presence of an anastomosis between the

per-forating and the 2nd dorsal metacarpal aa. in the present

case, differ from those reported previously. The 2nd

dorsal metacarpal a. is particularly important because of

its high incidence, as well as in providing a collateral

pathway from the dorsum to the palm of hand [4].

Variation of the axillary branches was limited to the

right side, while those of the brachial branches were on

the left side. Although these variable branches of the

axillary a. are well known as individual occurrences, the

multiple patterns described here have not previously

been reported in a single individual.

On the basis of the embryological development of

these arteries and the reported adult anomalies, the

de-velopment of this arterial pattern may be explained as

the follows:

Fig. 2. A Left axillary a. and the muscular branches of the left radial a. to biceps brachii. B Proximal origin of the radial and ulnar aa. from the left brachial a. 1, radial a.; 2, median n.; 3, ulnar a.; 4, superior collateral ulnar a.; 5, inferior collateral ulnar a.; 6, ulnar n. C Course of the left radial and ulnar aa. at the level of the forearm. 1, anastomosis between the radial and ulnar aa. in the cubital fossa; 2, radial recurrent a.; 3, muscular branches; 4, ulnar a.; 5, radial a.; 6, anterior interosseous a. D Arterial pattern of the left hand. 1, radial a.; 2, deep palmar arch; 3, 2nd metacarpal palmar a.; 4, perforating a.

Fig. 3. Diagram of the proposed embryological development of the arteries in the present case. u, ulnar a.; sr, superficial radial a.; a, axial a.; c, anastomotic connection; ia, anterior interosseous a.; dotted line, regression part

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i) The normal relationship between the arteries and the

nerves in the present case suggests that the axial a.

is normally derived from the 7th cervical

interseg-mental a.

ii) The proximal branching of the main arteries,

to-gether with the presence of unusual compound

ar-terial segments, suggests that the longitudinal

anastomoses occurring between intersegmental aa.

did not degenerate.

iii) The aberrant vessel connecting the radial and ulnar

aa. at the level of cubital fossa may occur as a result

of the regression of the primitive axial a. along the

arm, with the anastomoses between the primitive

axial, radial and ulnar aa. persisting.

iv) Not only regression of the primitive axial a. along

the arm, but also regression of the proximal part of

the superficial brachial-radial a., as reported by

Poteat [10] and Gonzales-Compta [3], may be the

cause of the high origin of the radial and ulnar aa.

from the brachial a. In the present case it appears

that the ulnar a. developed prior to the median a., as

postulated by Poteat. In addition, there may also be

an anastomotic connection between the primitive

ulnar and brachial-radial system in the present case.

Regression of the proximal part of the

brachial-ra-dial system and the distal part of the ulnar system,

together with a persistent anastomotic connection

between the radial and ulnar systems at the level of

arm, may be responsible for the main branches of

the brachial a. arising opposite to normal. This type

of arterial development is consistent withthe studies

of De Vriese, Mu¨ller and Senior as cited by

Mc-Cormack et al. [8] (Fig. 3). The presence of the

an-terior interosseous a. suggests that the primitive

axial a. at the level of forearm did not regress in the

present case.

v) The variations observed in the left hand may

rep-resent retention of the primitive pattern established

during prenatal growth.

The increasing use of invasive diagnostic and

inter-ventional procedures in cardiovascular diseases makes it

important that the type and frequency of vascular

variations

are

well

documented

and

understood.

Branches of the upper limb arteries have been used for

coronary bypass and flaps in reconstructive surgery. The

atypical distribution of the subscapular system, as in the

present case, may result in modified arches of rotation or

foreshortened pedicular lengths for latissimus dorsi and

serratus anterior, as well as for ortho- and parascapular

flaps. The anomalous origin and course of the radial a.

may result in some surprise and potential errors during

elevation of a radial forearm flap. Modifications of the

palmar arterial supply are also of practical importance

in hand reconstructive microsurgery. If the distal part of

the radial a. passes under the flexor retinaculum and

gives rise to a modified 1st palmar metacarpal a. this

may influence the reliability of vascularized skin islands,

which are usually harvested to reconstruct soft tissue

defects of the thumb or index finger.

References

1. Adachi B (1928) Das Arteriensystem der Japaner, vol I. Maruzen, Kyoto, pp 375–423

2. Danenow NA (1973) Rare variant of the vessels of the upper extremity (Englishabstract). ArkhAnat Histol Embriol 64:77– 78

3. Gonzales-Compta X (1991) Origin of the radial artery from the axillary and associated hand vascular anomalies. J Hand Surg [Am] 16:293–296

4. Ikeda A, Ugawa A, Kazihara Y, Hamada N (1988) Arterial patterns in the hand based on a three-dimensional analysis of 220 cadaver hands. J Hand Surg [Am] 13:501–509

5. Kanbayashi T, Takafuji T, Sato Y (1993) On the arterial supply in the human biceps brachii muscle. Folia Anat Jpn 69:289–310 6. Karlsson S, Niechajev IA (1982) Arterial anatomy of the upper

extremity. Acta Radiol Diagn 23:363–373

7. Maral T, C¸elik H, Hayran M, Kec¸ik A (1993) An anatomical variation of the thoracodorsal artery with comments on flaps based on the axillary artery. Eur J Plast Surg 16:231–233 8. McCormack LJ, Cauldwel MD, Anson BJ (1953) Brachial and

antebrachial arterial patterns: a study of 750 extremities. Surg Gynecol Obstet 96:43–45

9. Pestemalci T, Kahraman G, Yildiz Z, Yildirim M (1999) Common trunk variation of arteria subscapularis and arteria circumflexa humeri posterior with early origin. J Morphol 7:64-65

10. Poteat WL (1986) Report of a rare human variation: absence of the radial artery. Anat Rec 214:89–95

11. Quain R (1844) The anatomy of the arteries of the human body. Taylor & Walton, London, p 273

12. Terminologia anatomica. International anatomical terminology (1998) Thieme, Stuttgart

13. Tiedeman F (1831) Plates of arteries of human body. McLachlan & Stewart, Edinburgh

14. Uglietta JP, Kadir S (1989) Arteriographic study of variant arterial anatomy of the upper extremities. Cardiovasc Intervent Radiol 12:145–148

15. Weathersby HT (1956) Unusual variation of the arterial pattern of the human upper limb. Anat Rec 124:245–248

16. Williams PL, Bannister LH, Berry MM, et al (1995) Gray’s anatomy, 38th edn. Churchill-Livingstone, Edinburgh, pp 319– 320

17. Yu¨cel AH (1999) Unilateral variation of the arterial pattern of the human upper extremity with a muscle variation of the hand. Acta Med Okayama 53:61–65

Şekil

Fig. 2. A Left axillary a. and the muscular branches of the left radial a. to biceps brachii

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