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Introduction
The median nerve (MN) is the terminal branch of the brachial plexus that receives sensory, motor and sympathetic fibers from the lower cervical and first thoracic spinal nerves [1]. The MN is responsible for pronation of forearm and flexion of wrist joint. It also innervates the thenar muscles and sends sensory branches to palmar surface of thumb, index and middle fingers [2]. The MN is formed by the union of the medial and lateral roots that arise from the medial and lateral cords, respectively [3]. The lateral root contains fibers of ventral rami of C5, C6, C7 spinal nerves and medial root has fibers of C8 and T1. These roots unite inferior to pectoralis minor to form main trunk of MN in anterior lateral relation to axillary artery [4]. The MN courses parallel to the brachial artery along the arm. It originates on the lateral aspect of the artery, traverses to the medial side at approximately the mid-arm level, and persists medially till it approaches the elbow. At that point, the MN gives rise to a branch innervating the pronator teres muscle, in addition to vascular branches to the brachial artery. Furthermore, an articular branch arises at the elbow joint [5].
The atypical formation of MN by 1 medial root and supernumerary lateral roots and other types of variations have been described previously (Table 1) [6-12]. In addition, the communication between MN and musculocutaneous nerve (MCN) is the most frequent of brachial plexus variations [13].
The anatomical variations of MN can be explained from an embryological point of view. The brachial plexus develops as a radicular cone of axons in upper limb bud. These axons form a primary plexus within the mesenchymal tissue of limb bud and then it divides into ventral and dorsal divisions. The MN and ulnar nerve are derived from the ventral divisions and MCN separates from MN later [14]. The outgrowth of peripheral nerve axons into the limb bud and formation of brachial plexus is complex and controlled by different chemical tracers, growth factors and their receptors. So, the alterations of such signaling molecules may contribute to different peripheral nerve formation patterns [15]. These differences are often asymptomatic and observed only during dissection, autopsy or surgery [16]. However, such variations are clinically important for surgical approaches and nerve block in axillary region. In the current work we considered the origin of MN in relation to other anatomical structures within axilla and described the communicating branches between MCN and MN.
Materials and Methods
The upper extremities of twenty-six human cadaveric specimens (n=26) were dissected based on Grant’s Dissector [17]. The upper limb was abducted to 45°. A longitudinal skin incision was made at mid-axillary line and then the superficial fascia was removed carefully. The pectoralis major muscle was incised and reflected laterally. A longitudinal incision was made at anterior wall of axillary sheath and its contents (axillary vessels and brachial plexus) were separated using blunt dissection. The terminal branches of brachial plexus (MCN, MN, medial, and lateral roots, medial and lateral cords and ulnar nerve) were identified. These nerves usually form an “M”-shaped plexus anterior to third part of axillary artery. The morphology and relations of MCN, MN, and ulnar nerve to adjacent structures were investigated. The variations (communicating branches) were recorded by digital photography and categorized into 3 types according to Venieratos and Anagnostopoulou [18]. 1) Type 1: the communicating branch is proximal to the coracobrachialis. 2) Type 2: the communication branch is distal to the coracobrachialis. 3) Type 3: the MCN doesn’t penetrate the coracobrachialis. Instead the MN gives off a muscular branch to the coracobrachialis (Fig. 1).
Results
The “M” distribution of musculocutaneous, median and ulnar nerves
The typical formation of the MN was observed in 19 (73.07%) upper limbs. In these specimens, the main branches of the lateral and medial cords were distributed normally inferior to the pectoralis minor and posterior to the pectoralis major muscles. The “M”-shaped configuration between the MCN, MN, and ulnar nerves was obvious. The MCN originated from the lateral cord and reached the coracobrachialis muscle (at the pierce point) and innervated the all muscles of anterior compartment of the arm (coracobrachialis, biceps brachii and brachialis). Thereafter, this nerve continued as the lateral cutaneous nerve of the forearm. The medial root of MN crossed the 3rd part of the axillary artery inferior to the pectoralis minor and it united with the lateral root from lateral cord. The axillary artery was embraced with roots of the MN and after some distance it was continued as the brachial artery. The axillary vein was located in the medial part of the axillary region and it was related to the ulnar nerve and medial cutaneous nerve of the forearm. In addition, some axillary lymph nodes were embedded in axillary adipose tissue (Fig. 2).
The median nerve originating from 2 lateral and 1 medial roots (type 1)
In six specimens, a supernumerary lateral root separated from the medial aspect of MCN and joined the medial root proximal to the pierce point of the coracobrachialis. The bilateral variation of type 2 was observed in case 13 only (Tables 2 and 3). In Case 1, we observed that the left MCN was completely formed posterior to the pectoralis minor muscle and pierced the coracobrachialis. The Y shaped connecting branch was also separated from MCN and its distal part divided into slender first and second lateral roots (LR1 and LR2) (Fig. 3A). The medial root didn’t cross the third part of axillary artery and it united with double lateral roots. Other branches of the medial cord, including the ulnar nerve and the medial cutaneous nerve of the forearm were originated inferior to the pectoralis minor muscle. On the right side, the main branches of the medial and lateral cords were normally distributed.
In case 3, the second lateral root separated from the MCN just proximal to the coracobrachialis. The medial root of the MN crossed the 3rd part of the axillary artery and received lateral roots (Fig. 3B). On the left side, the arrangement of main branches of the brachial plexus was normal and the MCN, MN, and ulnar nerves formed the M-shaped connection as described before. A similar variation was observed in case 4 and on the left side. The medial root of MN originated from the medial cord and crossed the axillary artery. The proximal and distal lateral roots of MN were also separated from the lateral cord and MCN, respectively. In this specimen, the Y shaped roots of MN completely surrounded the 3rd part of the axillary artery (Fig. 3C). We also discovered type 2 variation in the left axillary region of case 5 (Fig. 3D). However, there was no variation in the right axillary region of this case.
A communicating branch connecting the musculocutaneous and median nerves distal to coracobrachialis (type 2)
In Case 2, we discovered a communicating branch between the right MCN and MN distal to the coracobrachialis muscle (Fig. 4A). The MCN originated from the lateral cord, 5 cm distal to the coracoid process. About 6 cm distal to the pierce point of coracobrachialis, the muscular and communicating branches were separated from MCN. The communicating branch crossed the brachial artery from lateral to medial and joined the MN in the upper part of the arm. We didn’t find any variation in the left upper extremity but the medial and lateral roots were atypically long. The left MCN was separated from the lateral cord near the shoulder joint (4.5 cm distal to the coracoid process) and pierced the coracobrachialis after passing 1 cm. The MN and ulnar nerves also originated 11 and 7 cm distal to the coracoid process respectively (Fig. 4B).
Discussion
In the present study, we observed unilateral MN supernumerary lateral roots in 23.07% of specimens. The bilateral formation of MN by 2 lateral roots and 1 medial root was observed in a single case. In consistency, Budhiraja et al. [8] studied the MN formation and variations in the Indian population. They observed 3 roots forming the MN from 22.4% upper limbs. In 14.2% of specimens, the supernumerary lateral root was derived from the lateral cord. Whilst, in 8.16% of the upper extremities, the communicating branch separated from the MCN. In addition, the MN formation by 4 roots was noted in 3.57% of the upper extremities [8]. Similarly, Ghosh et al. [19] reported the MN formation by 3 lateral roots in 13 specimens (21.7%) from 60 upper limbs. In addition, they observed MN formation by 4 roots (1 medial and 3 lateral roots) in 3 specimens [19]. Clinically, MN and other branches of brachial plexus are vulnerable to surgical interventions or trauma. If the MN with the additional lateral root is damaged within the axilla, the pronation of forearm and flexion of the wrist joint are lost. The additional lateral root contains fibers of C5 and C6. So, any damage to these fibers may lead to weakness of arm flexion and anesthesia of the lateral half of the forearm [20].
Typically, the medial root of MN crosses the third part of axillary artery and unites with the lateral root to form MN anterior or lateral to the axillary artery. In contrast, the atypical lateral root of MN may cross the axillary artery obliquely and MN forms medially [21, 22]. However, the ischemia of the upper extremity induced by compression of the axillary artery has not been documented in such cases. The present study also revealed that the double lateral roots were in close relation to the third part of the axillary artery. These roots were associated with the anterior aspect of the axillary artery and joined the medial root to form MN.
We found a single specimen in which the MN and MCN had a connecting branch distal to the coracobrachialis muscle (type 2). The MCN is well protected by biceps brachii muscle but it’s prone to damage in shoulder dislocations, coracoid process grafting, arthroscopies and plastic surgeries [23]. If the distal communicating branch is present, any proximal lesion to MCN may impact the MN fibers [24]. In the current study we did not find variation type 3. In this case, the MCN does not innervate the coracobrachialis and instead the lateral cord sends a motor branch to this muscle [25]. The absence of MCN and innervation of coracobrachialis by MN is very rare [26]. Tatar et al. [27] described the innervation of coracobrachialis by a branch from the lateral cord. This branch originated from the lateral root and bifurcated into upper and lower filaments and entered the coracobrachialis [27].
In conclusion, the anatomical knowledge of MN origin and its variations is necessary for clinicians, especially for orthopedic surgeons and anesthesiologists. Understanding of these abnormalities may prevent sensory and motor injuries during surgical approaches in axillary region.
Study limitations
The main limitations of current work are the small sample size and an unknown history of pathologies. In fact, we had access to a limited number of fresh specimens and our study highlights a single center anatomical experience. Therefore, we recommend a meta-analysis of MN variations to acquire more reliable results.
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