Kaohsiung Journal of Medical Sciences (2011) 27, 121e124

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CASE REPORT

A rare case of multiple neuromuscular variationsin the axilla and arm腋窩與上臂多發神經肌肉變異的特殊個案

Pei Wang a, Yu-Lin Hsien b, Wan-Yi Ho b, Chun-Chih Liu b, Tin-Hsin Hsiao b,*王霈 a, 謝侑霖 b, 何宛怡 b, 劉俊馳 b, 蕭廷鑫 b,*

a School of Medicine, College of Medicine, Fu Jen Catholic University, Taipei, TaiwanbDepartment of Anatomy, Faculty of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung,Taiwan

Received 2 March 2010; accepted 18 June 2010Available online 8 February 2011

KEYWORDSAxillary arch muscle;Biceps brachii;Median nerve;Musculocutaneousnerve;Neuromuscular variation

關鍵詞腋弓肌;肱二頭肌;正中神經;肌皮神經;神經肌肉變異

* Corresponding author. DepartmeMedicine, College of Medicine, Kaohs100, Shih-Chuan 1st Road, Kaohsiung 8

E-mail address: d89446004@ntu.ed

1607-551X/$36 Copyright ª 2011, Elsedoi:10.1016/j.kjms.2010.06.004

Abstract During the dissection of a 73-year-old embalmed male cadaver, we noted unusualvariations in the flexor compartment of the upper limbdbilateral axillary arch muscles,a three-headed biceps brachii muscle with two supernumerary belliesdand variations in theorigin of the musculocutaneous and median nerves from the brachial plexus. The morpholog-ical and clinical significance of this unique coexistence of multiple neuromuscular variationsare discussed.

摘摘要要 在常規的大體解剖學實習課程中，我們由一位73歲男性大體老師上肢的屈肌部分同時發現

多個變異，包括有兩側的腋弓肌、右側具第三肌頭及兩個額外的肌腹的肱二頭肌、以及肌皮神經

和正中神經起源於臂神經叢的變異。我們將針對此獨特的神經肌肉變異在形態上及臨床上的重要

性進一步地探討。

Copyright ª 2011, Elsevier Taiwan LLC. All rights reserved.

nt of Anatomy, Faculty ofiung Medical University, No.0708, Taiwan.u.tw (T.-H. Hsiao).

vier Taiwan LLC. All rights reserv

Introduction

Anatomical variations in the upper limb are frequent, butthe coexistence of multiple combined neuromuscular vari-ations is rare. One of these variations is the coexistence ofthe axillary arch muscle (AAM) and the multiple-headed

ed.

122 P. Wang et al.

biceps brachii muscle (BBM) in the axilla and arm [1]. Inaddition, variations in the origin, course, and distribution ofthe musculocutaneous (MCN) and median nerves (MN) havebeen mentioned previously [2]. A case of neuromuscularvariation revealed the existence of common trunk of theMCN and the lateral root of the MN as well as accessoryheads of the coracobrachialis and BBM [3]. We presenta unique case of coexistence of AAM and three-headed BBMwith piercing of the coracobrachialis by the lateral cord ofthe brachial plexus.

Case presentation

A 73-year-old male cadaver of Chinese origin was dissectedduring the Gross Anatomy Dissection Course at KaohsiungMedical University, Kaohsiung, Taiwan. The cause of deathwas respiratory failure because of severe head injury.There was no gross pathology or history of surgical proce-dures involving the axilla, the anterior thoracic wall, or theupper limb. The cadaver was found to have bilateral AAMs(Fig. 1A and 1B). The muscle originated from the medialborder of the latissimus dorsi muscles. On the right side,the muscle terminated as a tendon continuing with thefascia on the coracobrachialis and short head of BBM. Onthe left side, the muscle ended on the coracoid process ofthe scapula, along with the tendon of the short head ofBBM. The AAMs crossed anterior to the brachial plexusesand axillary vessels on both sides. The cadaver also hada three-headed BBM with two small accessory bellies in theright arm (Fig. 1A). The two superior flat accessory belliesoriginated from the deep surface of the short head of BBM.They inserted into the anterior surface of the distal part ofthe coracobrachialis. Moreover, the third head originatedfrom the anteromedial surface of the humerus between theinsertion of the coracobrachialis and the origin of thebrachialis. This accessory head lay posteromedial to theBBM, medial to the brachialis, and lateral to the brachialvessels and MN. Its distal end bifurcated into two slips. Thelateral slip merged into the deep portion of the proximalpart of the common biceps tendon. The medial slip termi-nated as an aponeurotic band to join with the ordinarybicipital aponeurosis. The weight of this accessory headwas 27.5 g. The ordinary two-headed BBM (116.5 g inweight) provided roughly 80% of the total muscle mass(144 g in weight), whereas the remaining 20% of the totalmass was contributed by the third head. As expected, thenerve supply to this accessory head was from an excessbranch of the MCN, and the vascular supply was from twobranches of the brachial artery. Careful dissection toidentify the course of the MCN showed a variant pattern inthe brachial plexus. In both axillae, the lateral and medialcords of brachial plexuses were lateral to the second partof the axillary arteries, whereas the posterior cord wasposterior to the artery (Fig. 1A and 1B). In the right, thelateral cord was formed more distal than usual. It piercedthe coracobrachialis directly and then divided into twoterminal branches. The lateral one was the MCN, coursingsuperficial to the brachialis and giving branches to thethree heads of the BBM and the brachialis, and thencontinued laterally to the tendon of the BBM as the lateralantebrachial cutaneous nerve. The medial branchnerve crossed medially along the boundary between the

coracobrachialis and the third head of BBM and then joinedto give the MN. We took this branch as the variant lateralroot of the MN. In addition, deep to the distal end of thelateral root of the MN, a branch communicated the variantlateral root of the MN with the lateral antebrachial cuta-neous nerve by passing obliquely in the plane between thethird head of the BBM and the brachialis. A comparativeschematic diagram for distribution of nerves on the rightaxilla and arm in normal case and in the present variantcase is given in Fig. 1C.

Discussion

The AAM is the most common variation of the axilla witha reported frequency of 7e8% [4]. In general, the AAM hasbeen described as “complete” and “incomplete” dependingon its insertion. A complete AAM inserts mainly onto thepectoralis major tendon, whereas an incomplete oneinserts onto associated structures around the axilla, forexample, in muscles, such as the coracobrachialis, BBM,and the coracoid process [5]. In addition, a group of“clinical” AAM has recently been defined according to thepossible compression role of a variant muscular structurefor the nerves and vessels in the axilla [6]. The axillary veinmight be entrapped and might cause obstructive venouscompression because of AAM [7]. In the present case, thebilateral incomplete AAMs crossed in front of the neuro-muscular bundle in axillae, and the veins might becompressed in certain movements of the upper limb, suchas abduction and elevation of the arm or the placing of thehand behind the head.

The three- (or one supernumerary head), four-, and five-headed BBM are found in frequencies of 14.4%, 2.5%, and0.5%, respectively [8]. If the supernumerary heads arerelatively large, they may contribute additional strength tothe BBM [9]. In the present case, the supernumerary headprovided approximately half the weight of the long or shorthead; this may enhance the force of flexion and supinationof the forearm and may cause abnormal bone displacementafter a humeral fracture [10]. The distal end of theaccessory head formed an aponeurotic band and joined thebicipital aponeurosis to pass over the brachial artery andthe MN. When the BBM contracts, this slip would be pulledand would strengthen the aponeurosis as a ceiling toprotect the underlying brachial artery and MN, or thisextended slip might restrict the tunnel for vessels andnerves to pass [11].

Variations of brachial plexus and its terminal brancheswere common, including those that occur in the formationof cords, in the origin and combination of branches, and inthe relationship with the axillary artery [12]. Comparedwith the patterns of communications between MCN andMN, the communicating branch in this case from the MCNto the MN distal to the point of entry of the coraco-brachialis is partially similar to Pattern II in the classifi-cation scheme of Choi et al. [13] and pattern A2c noted byMaeda et al. [2]. The additional branch arising from thevariant lateral root of the MN back to unite with theterminal branch of the MCN in this case was not observedin previous studies. Probably, the fibers of the MCN took upa variant course for short-distance bypassing through thelateral root of the MN.

Figure 1. Photograph from anterior aspect of the dissected right axilla, arm, and cubital fossa (A) and left axilla (B). The PMjmuscle and the LHB and SHB were cut and reflected laterally. The MN [2 in (A) and (B), and MN in (C)] was pulled medially by theforceps. The axillary arch muscles (asterisk); the THB; the long and short superior supernumerary bellies of the biceps brachii(black arrows and arrowheads, respectively); variant lateral root of the median nerve (white arrows); and communicating branch(white arrowheads) arising from the median nerve and descending to unite with the LACN are shown. (C) A schematic view showsthe communication between the LC and the MN at right side. Note that the lateral and medial cords of the brachial plexus arelateral to the axillary artery in variant axilla. 1Z lateral cord of the brachial plexus; 2Zmedian nerve; 3Z ulnar nerve; 4Z leftmusculocutaneous nerve; AAZ axillary artery; BZ brachialis; BAZ bicipital aponeurosis; CBZ coracobrachialis; CommZ com-municating branch from MN to LACN; LACNZ lateral antebrachial cutaneous nerve; LCZ lateral cord; LHBZ long head of thebiceps brachii; LRZ lateral root of the median nerve; LSZ lateral slip; LSBZ long supernumerary belly of the biceps brachii;MCZmedial cord of the brachial plexus; MCNZmusculocutaneous nerve; MNZmedian nerve; MRZmedial root of the mediannerve; MSZmedial slip; PMiZ pectoralis minor muscle; PMjZ pectoralis major muscle; SHBZ short head of the biceps brachii;SSBZ short supernumerary belly of the biceps brachii; THBZ third head of the biceps brachii; UNZ ulnar nerve. Scale barZ 3 cm.

Multiple variations of the upper limb 123

The coexistence of these variations may be the result ofan abnormal embryological formation of the limb musclesand the peripheral nerves [14]. Multiple muscular varia-tions, including an AAM and a third head of BBM on an upperlimb, have been reported [1]. Neuromuscular variations inthe axilla and arm, though relatively rare, were also found.Interestingly, variations between the MCN and MN wereusually found along with the excessive heads of the BBM [2].

The four-headed BBM and triceps brachii muscles werereported with communication between the MCN and MN[10]. This communicating pattern was similar to the nerveconnection that we recognized as the lateral root of MNfrom the extended lateral cord in the present case. Anextended common trunk of the MCN and the lateral root ofthe MN and the distal fusion of two roots of the MN coex-isting with accessory heads of the BBM and coracobrachialis

124 P. Wang et al.

have also been reported [3]. Sometimes, in addition toa three-headed BBM, two MCNs originated from the lateralcord of the brachial plexus and the MN [15]. We suggestedthat the variations in the running path of the lateral cord ofbrachial plexus branching into MCN and MN might be thecoexistence of supernumerary heads of the BBM in cases ofneuromuscular variations.

Acknowledgments

The authors would like to thank Dr Lap-Ki Chan (Depart-ment of Anatomy, Li Ka Shing Faculty of Medicine, Univer-sity of Hong Kong, China) for his critical reading andcorrection of this article. The kind help of Mr Yuan-ChienLin during preparation of material in the dissecting room isgratefully acknowledged.

References

[1] Nayak SR, Krishnamurthy A, Ramanathan LA, Prabhu LV,Kumar CG, Tom DK, et al. Multiple muscular anomalies ofupper extremity: a cadaveric study. Rom J Morphol Embryo2008;49:411e5.

[2] Maeda S, Kawai K, Koizumi M, Ide J, Tokiyoshi A, Mizuta H,et al. Morphological study of the communication between themusculocutaneous and median nerves. Anat Sci Int 2009;84:34e40.

[3] Jakubowicz M, Ratajczak W. Variation in morphology of thebiceps brachii and coracobrachialis muscles associated withabnormal course of blood vessels and nerves. Folia Morphol2000;58:255e8.

[4] Loukas M, Noordeh N, Tubbs RS, Jordan R. Variation of theaxillary arch muscle with multiple insertions. Singapore Med J2009;50:e88e90.

[5] Besana-Ciani I, Greenall MJ. Langer’s axillary arch: anatomy,embryological features and surgical implications. Surg 2005;3:325e7.

[6] Jelev L, Georgiev GP, Surchev L. Axillary arch in human:common morphology and variety. Definition of “clinical”axillary arch and its classification. Ann Anat 2007;189:473e81.

[7] Georgiev GP, Jelev L, Surchev L. Axillary arch in Bulgarianpopulation: clinical significance of the arches. Clin Anat 2007;20:286e91.

[8] Nakatani T, Tanaka S, Mizukami S. Bilateral four-headedbiceps brachii muscles: the median nerve and brachial arterypassing through a tunnel formed by a muscle slip from theaccessory head. Clin Anat 1998;11:209e12.

[9] Swieter MG, Carmichael SW. Bilateral three-headed bicepsbrachii muscles. Anat Anz 1980;148:346e9.

[10] Nayak SR, Krishnamurthy A, Kumar M, Prabhu LV, Saralaya V,Thomas MM. Four-headed biceps and triceps brachii muscles,with neurovascular variation. Anat Sci Int 2008;83:107e11.

[11] Paraskevas G, Natsis K, Ioannidis O, Papaziogas B, Kitsoulis P,Spanidou S. Accessory muscles in the lower part of the ante-rior compartment of the arm that may entrap neurovascularelements. Clin Anat 2008;21:246e51.

[12] Pandey SK, Shukla VK. Anatomical variations of the cords ofbrachial plexus and the median nerve. Clin Anat 2007;20:150e6.

[13] Choi D, Rodrıguez-Niedenfuhr M, Vazquez T, Parkin I,Sanudo JR. Patterns of connections between the muscu-locutaneous and median nerves in the axilla and arm. ClinAnat 2002;15:11e7.

[14] Goyal N, Harjeet, Gupta M. Bilateral variant contributions inthe formation of median nerve. Surg Radiol Anat 2005;27:562e5.

[15] Abu-Hijleh MF. Three-headed biceps brachii muscle associatedwith duplicated musculocutaneous nerve. Clin Anat 2005;18:376e9.