Okajimas Folia Anat. Jpn., 80(1): 23–28, May, 2003

Rare Variation of the : Coexistence with the Superficial Brachial and Superficial Subscapular in the Absence of the Normal

By

Kazuya YOSHINAGA1,KodoKODAMA2, Katsuharu KAMETA3, Natsuko KARASAWA3, Naosuke KANENAKA3, Sayaka KOHNO3 and Tatsuo SUGANUMA4

1Department of Anatomy I, Miyazaki Medical College, Miyazaki 889-1692, Japan 2Department of Anatomy, Kumamoto University School of Medicine, Kumamoto 860-0811, Japan 3Undergraduate student and 4Department of Anatomy II, Miyazaki Medical College, Miyazaki 889-1692, Japan

– Received for Publication, March 17, 2003 –

Key Words: , Superficial brachial artery, Arterial variation, Gross anatomy, Human

Summary: A rare variation in the arterial pattern was found in the right arm of an 87-year-old male cadaver in a student dissection practice. In this case, the superficial brachial and superficial subscapular arteries coexisted in the absence of the normal brachial artery (A. brachialis profunda). After branching off a large-sized superficial , the axillary artery did not penetrate the brachial plexus and gave rise to a superficial brachial artery, which arose from the axillary artery at the point between the ansa pectoralis and ansa mediana, and descended ventral to the median nerve branching off the profunda brachii and superior and inferior ulnar collateral arteries. The superficial brachial artery fi- nally divided into the radial and ulnar arteries in the . The superficial subscapular artery passed inferior and dorsal to the medial cord of the brachial plexus, giving off the , and then branched off into the thoracodorsal, circumflex scapular and posterior circumflex humeral arteries. Thus the main nerves of the brachial plexus were sandwiched between the superficial brachial artery and the superficial subscapular artery system. The morphological and clinical significance of this variant are discussed.

Variations in the origin, branching and course During a student dissection of a cadaver, we of the main arteries of the human found the absence of the normal brachial artery are common and have long received the attention (A. brachialis profunda) and the coexistence of the of anatomists and surgeons (Adachi, 1928; Mc- superficial brachial artery with the superficial sub- Cormack et al., 1953; Williams et al., 1995; Kodama, scapular artery, resulting in the main nerves of the 2000). The axillary artery normally penetrates the brachial plexus being sandwiched between the two ventral stratum of the brachial plexus and then arteries. This variant is not only rare but also is continues as the brachial artery. Occasionally, the seemed to be significant for understanding the for- axillary artery does not penetrate the brachial mation of the arm arteries. The aim of the present plexus and gives rise to the superficial brachial ar- study is to describe the exact anatomic topography tery with a superficial course to the median nerve of this arterial variation and to discuss its morpho- (Mu¨ ller, 1903; Adachi, 1928; McCormack et al., logical and clinical significance. 1953; Kodama, 2000). It is also known that a branch derived from the axillary artery occasionally crosses over the medial cord of the brachial plexus and then Materials and Methods gives off the subscapular artery system (Chiba, 1986; Kodama et al., 1987; Aizawa et al., 1995), namely The arterial variation described below was found the superficial subscapular artery (Yamada, 1967). in the cadaver of an 87-year-old Japanese male in

Address correspondence to: Dr. Kazuya Yoshinaga, Department of Anatomy (I), Miyazaki Medical College, Kiyotake, Miyazaki 889-1692, Japan. E-mail: [email protected]

23 24 K. Yoshinaga et al.

the from the axillary artery, theaxillaryartery(9mmindiameter)branchedoff a large-sized subscapular artery (7 mm in diame- ter). The subscapular artery gave off the lateral thoracic arteries, which passed between the medial brachial cutaneous nerves (C8, T1) and crossed in- ferior and then posterior to the main nerves of the brachial plexus including the medial brachial cuta- neous, medial antebrachial cutaneous, ulnar, me- dian, and radial nerves (Fig. 2). It finally divided into the thoracodorsal, circumflex scapular, and posterior humeral circumflex arteries and the sub- scapular branch under the nerves. Thus the sub- scapular artery mentioned above corresponds to the superficial subscapular artery (Yamada, 1967). The axillary artery (8 mm in diameter) gave off the inferior pectoral artery near the branching point of the superficial subscapular artery and passed between C7 and C8 of the roots of the ansa pectoralis, which is composed of the medial and lateral pectoral nerves (Fig. 2). Without passing between the medial and lateral roots of the median nerve (ansa mediana), it descended and continued in the upper arm as the superficial brachial artery superficial to the median nerve, giving off the lat- eral mammary branch and the anterior humeral circumflex artery (Fig. 2). Distal to the teres major muscle, it branched off into the profunda brachii artery (2 mm in diameter) that gave off the middle and radial collateral arteries and terminated as the superior ulnar collateral artery (Fig. 2). After sending muscular branches to the biceps and bra- chialis, it branched off into the inferior ulnar col- lateral artery anterior to the medial epicondyle. The diameter of the superficial brachial artery was about 5 mm at the cubital fossa, where it divided Fig. 1. Photograph of anterior view of the right arm and axilla, showing the superficial brachial artery (SB) and the su- into the radial and ulnar arteries. The radial and perficial subscapular artery (arrow). Note that the radial ulnar arteries branched off into the radial and ulnar (R), median (M) and ulnar (U) nerves are sandwiched recurrent arteries, respectively, and exhibited their between the two arteries. Ax: axillary artery, MC: mus- normal courses and distributions in the forearm. culocutaneous nerve. The axillary and brachial and their tribu- taries corresponded to and coursed along the branches and ramifications of the axillary and the student dissection course at Miyazaki Medical brachial arteries described above. No muscle varia- College. No scars or surgical incisions were ob- tions were noted in the upper extremity of this served in the skin. The arterial patterns associated cadaver. with the nerves in the arm were carefully examined On the left side, no remarkable variations in the and the findings were recorded as measurements, arterial pattern of the arm and forearm were ob- line drawings and photographs. served.

Results Discussion

On the right arm, the course and branching The present study detailed the gross anatomical pattern of the subclavian artery were normal. As findings of a rare variant of the axillary artery, shown in Fig. 1, about 25 mm distal to the origin of which branches off a large superficial subscapular The Variant Arm Artery 25

Pectoralis C5 minor muscle C6 Pectoralis TA SS major muscle C7

C8

IP

Ax

ACH

MC AX Lm PCH

PB

Biceps R muscle Sb CS TD

SB Mbc LT

Latissimus dorsi muscle SUC U M IUC Mac

Fig. 2. Drawing of anterior view of the right arm and axilla, showing the superficial brachial artery (SB) and superficial subscapular artery (arrow). Note that the main nerves of the brachial plexus including the radial (R), median (M), ulnar (U), medial antebrachial cutaneous (Mac), or medial brachial cutaneous (Mbc) nerves, are sandwiched between the superficial brachial artery and superficial subscapular artery system. ACH: anterior circumflex humeral artery, AX: axillary nerve, Ax: axillary artery, CS: circumflex scapular artery, IP: inferior pectoral artery, IUC: inferior ulnar collateral artery, Lm: lateral mammary branch, LT: lateral thoracic artery, MC: musculocutaneous nerve, PB: profunda brachii artery, PCH: posterior circumflex hu- meral artery, Sb: subscapular branch, SS: supurascapular artery, SUC: superior ulnar collateral artery, TA: thoracoacromial artery, TD: .

artery and then gives rise to the superficial brachial scapular artery defined by Yamada (1967) and Ko- artery. Judging from its origin, course and relation dama (2000) or the S-type subscapular artery sys- to the brachial plexus, the subscapular artery in this tem by defined Aizawa et al. (1995). The superficial case corresponds to Type E of the superficial sub- subscapular artery is considered to be derived from 26 K. Yoshinaga et al. the lateral thoracic artery (Yamada, 1967; Chiba, 1986; Kodama et al., 1987; Aizawa et al., 1995). A Proposed model LC However, the superficial brachial artery in this case corresponds to the superior superficial brachial ar- Ax tery (BSS), which arises from the axillary artery at the point between the ansa pectoralis and ansa MC mediana, defined by Kodama (1987, 2000). Al- SB though several cases of the coexistence of the two superficial artery systems during anatomical dissec- SSs tions have been reported previously (Adachi, 1928; B LT Chiba, 1986; Kodama et al., 1987; Aizawa et al., 1995), a detailed investigation has not been per- formed. Recently, a similar finding was reported by M R U Nakatani et al. (1997). The chief difference between their findings and ours was the course and termi- B Normal case LC nation of the superficial subscapular artery, al- though Nakatani et al. (1997) did not mention the Ax point of origin of the superficial brachial artery. In the present case, the subscapular artery passed MC dorsal to the posterior cord of the brachial plexus and terminated as the posterior circumflex humeral artery, whereas in the other it passed between the ventral to the posterior cord and terminated as the B LT inferior ulnar collateral artery. In addition, muscles of the upper arm in this cadaver were mainly sup- plied by the superficial brachial artery, whereas in M R U the other it was mainly supplied by the superficial subscapular artery and its derivatives. C The present case LC Consistent with the previously reported cases of superficial brachial arteries (Adachi, 1928; Ko- Ax dama, 2000; Yoshinaga et al., 2003), the lateral mammary branch and muscular branches arose MC from the superior superficial brachial artery in SB the present case. Furthermore, we found that the inferior pectoral artery, which is the terminal SSs branch entering the lowest neurovascular hilum of LT the pectoralis major muscle (Kodama et al., 1987), ramified independently as the most proximal branch from the superior superficial brachial artery. M R U Kodama et al. (1987) suggest that the inferior pec- toral artery might be a derivative or trigger for morphogenesis of the superficial brachial artery. Fig. 3. Schematic representation of the arterial formation of the The arrangement of the arterial variations in the human upper arm. (A) A proposed model showing that axilla may be embryologically or morphologically the axillary artery (Ax) gives off three main branches, the explained by several hypotheses (Mu¨ ller, 1903; Ya- superficial brachial artery (SB), deep brachia artery (B), and superficial subscapular artery system (SSs). This dia- mada, 1967; Aizawa et al., 1995). Yamada (1967) gram is modified from Yamada (1967). (B) Normal case postulated that, before penetrating the brachial showing that the axillary artery (Ax) passes between the plexus, the axillary artery fundamentally branches medial (MC) and lateral (LC) cords of the brachial off the superficial brachial artery, the brachial ar- plexus, and continues as the deep brachia artery (B). (C ) tery (A. brachialis profunda), and the superficial The present case has both the superficial brachial artery (SB) and the superficial subscapular artery system (SSs). subscapular artery (Fig. 3A). Usually, the axillary LT: lateral thoracic artery, M: median nerve, R: passes through the ansa mediana and con- nerve, U: ulnar nerve. tinues as the brachial artery, while the superficial brachial and subscapular arteries regress (Fig. 3B). In contrast, development of both the superficial brachial and subscapular arteries, as well as regres- The Variant Arm Artery 27 sion of the brachial artery might result in the pres- ships between the arteries and the posterior cord of the ent arterial pattern (Fig. 3C). brachial plexus. Acta Anat Nippon 1995; 70:554–568. (in Although the incidence of this variant is very low Japanese with English Abstract) 3) Chiba S. Morphological study of the so-called Adachi’s and no clinical cases have been documented in the C-type brachial plexus. 3. Course of the axillary artery in available literature, it may be important for clini- relation to the brachial plexus. Acta Anat Nippon 1986; cians and surgeons to be aware of the presence of 61:9–28. (in Japanese with English Abstract) this arterial variation when surgical and diagnostic 4) Cohen SM. Accidental intra-arterial injection of drugs. procedures in axillary or upper arm region. It is Lancet 1948; 255:409–17. 5) Jurjus A, Sfeir R and Bezirdjian R. Unusual variation of possible that its superficial course would make it the arterial pattern of the human upper limb. Anat Rec more vulnerable to trauma and thus to serious 1986; 215:82–3. bleeding (Jurjus et al., 1986), and more subject to 6) Kodama K. Arteries of the upper limb. In: Sato T, Akita K, accidental intra-arterial injection (Cohen, 1948). It eds, Anatomic Variations in Japanese, University of Tokyo is also likely that compression of the main nerves of Press, Tokyo, 2000; 220–237 (in Japanese). 7) Kodama K, Yamada M, Kawai K, Okamoto K and Miz- the brachial plexus, including the ulnar, median and ukami S. The inferior pectoral artery, a new definition. radial nerves could cause paralysis of the forearm Okajimas Folia Anat Jpn 1987; 64:47–57. and hand, due to its location between large-sized 8) McCormack LJ, Cauldwell MD and Anson BJ. Brachial superficial brachial and subscapular arteries. and antebrachial arterial patterns. Surg Gynecol Obstet 1953; 96:43–54. 9) Mu¨ ller E. Beitra¨ge zur Morphologie des Gefa¨sssystems. I. Die Armarterien des Menschen. Anat Hefte 1903; 70: Bd Acknowledgements 22, 377–575. 10) Nakatani T, Tanaka S and Mizukami S. Case report: bilat- We thank Souyuki Ide and Yasunori Fujii for eral location of the axillary artery posterior to the medial their technical assistance. cord of the brachial plexus. J Anat 1996; 189:457–459. 11) Yamada M. Significance of the superficial subscapular artery, new designation. Nihon Iji-Shimpo 1967; 60:3–7. (in Japanese) References 12) Yoshinaga K, Tanii I and Kodama K. The superficial bra- chial artery crossing over the ulnar and median nerves from 1) Adachi B. Das Arteriensystem der Japaner. Bd I, Maruzen, posterior to anterior: embryological significance. Anat Sci Kyoto, 1928. Int 2003; in press. 2) Aizawa Y, Ohtsuka K and Kumaki K. Examination on the 13) Williams PL, Bannister LH, Berry MM, Collins P, Dyson courses of the arteries in the axillary region. I. The course M, Dussek JE and Ferguson MWJ. Gray’s Anatomy, 38th of the subscapular artery system, especially the relation- ed, New York, Churchill Livingstone, 1995.