INTRODUCTION
Muscles demarcating the axilla are used as critical landmarks of the region. An understanding of accessory muscles located in this region allows more accurate decision making during surgical procedures involving lymph nodes in the breast [10, 17, 21]. One of the well-known accessory thoracic muscles of this class is the axillary arch (AA). The AA, also referred to as Langer’s AA [24] or Achselbogen muscle [3], is a musculotendinous slip that crosses the axilla anteriorly [9]. Typically, the AA originates from the anterior boarder of the latissimus dorsi near the base of the axilla and inserts onto the deep tendon of the pectoralis major. In some cases it inserts onto the coracoid process of the scapula, or onto musculotendinous structures near the proximal humerus [9]. The AA is one of the more common variations of accessory thoracic muscles. In a recent meta-analysis report, the prevalence of the AA has been reported as 5.3% [23], though it varies among populations [4, 14]. Another frequently reported accessory thoracic muscle associated with the axilla is the pectoralis quartus. The pectoralis quartus is defined as a muscular slip typically originating in the thorax lateral to, or at the lateral border of, the pectoralis major, and inserting onto the deep pectoralis major tendon, or onto the aforementioned insertion sites of the AA [3, 4, 8].
Because of their common occurrence and implied clinical relevance, accessory thoracic muscles associated with the axilla warrant close attention. Although the AA itself is common, occurrence of bilateral AAs as well as additional thoracic accessory muscle variations accompanying the AA are less common [4, 23]. In the current study we report 4 cases of AA variations identified among 48 donors (4/48 = 8.3%) of an ethnically diverse whole-body donation population. In one case, bilateral AAs were accompanied with a left pectoralis quartus, and in another a left AA was accompanied with bilateral pairs of pectoral fascicles, originating from the surface of the ribs and inserting onto the deep surface of the pectoralis major. We summarise these cases and briefly discuss their proposed origins based on the theories described in literature.
CASE REPORT
All 4 cases of AA variations described below were identified in the gross anatomy laboratory for first-year medical students at the University of California, Davis, School of Medicine over a 2-year period (2020 and 2021).
Case 1
Bilateral AAs and a left pectoralis quartus were identified in an 80-year-old male donor diagnosed with cerebral atherosclerosis and vascular dementia. The left pectoralis quartus was first noted during the dissection of the thoracic region as a slender muscle slip embedded within the sub-cutaneous fat. This muscle slip attached distally to the superior border of the 6th rib superficial to the external oblique, and then ran along the inferolateral boarder of the pectoralis major, which covered the proximal half of the pectoralis quartus slip (Fig. 1A). In its entirety, the pectoralis quartus travelled laterally to the pectoralis minor and inserted onto the deep fascia of the pectoralis major and measured 12 cm long and 1.2 cm wide near its distal attachment. Based on the relative location to the pectoralis major and its distal and proximal attachments, we classified this accessory thoracic muscle as a pectoralis quartus [22]. Its insertion site at the pectoralis major was encased in a thick fascia to which the proximal end of another muscle slip, a left AA, joined (Fig. 1B). Further dissection of this fascia revealed that the pectoralis quartus and AA were linked via an aponeurosis (Fig. 1C). The source of innervation to the pectoralis quartus was found to be the medial pectoral nerve, which branched where it penetrated the pectoralis minor and extended to the pectoralis quartus (Fig. 1C). We did not find clear innervation to the AA as seen for the pectoralis quartus.
The origin of the left AA was found at the anteroinferior margin of the tendinous part of the latissimus dorsi. The striation of the AA was perpendicular to that of the latissimus dorsi, with a defining tendinous ridge located between the two (Fig. 1D). The left AA measured 8 cm long and 0.6 cm wide at its midpoint. In addition, this donor had a right AA. Like the left AA, the right AA originated from the anteroinferior margin of the tendinous part of the latissimus dorsi and inserted onto the fascia deep to the pectoralis major (Fig. 1E). Its dimension was 7 cm long and 0.6 cm wide at its midpoint. Both AAs traversed across the axilla anterior to the brachial plexus (Fig. 1B, E).
Case 2
A left AA and bilateral pairs of thoracic fascicles deep to the pectoralis major were identified in an 83-year-old male donor diagnosed with vascular dementia. The AA was 8 cm long and 0.5 cm wide at its midpoint. Like the AAs described in Case 1, this AA originated from the anterior margin of the tendinous part of the latissimus dorsi, and it inserted onto the deep fascia of the pectoralis major (Fig. 2A). In addition to the AA, pairs of pectoral fascicles were observed, on both the left and right sides, anterior to the pectoralis minor (Fig. 2B). These fascicles originated from the anterior surface of the ribs and eventually merged into the deep fascia of the pectoralis major. The fascicle pair on the right originated at the level of the 4th rib and ran closely parallel to each other, between which the medial pectoral nerve traversed from the pectoralis minor to the pectoralis major (Fig. 2C). Both fascicles measured 11.5 cm in length. The superior fascicle was 0.8 cm wide and the inferior fascicle was 0.6 cm wide. The fascicles on the left were more distant from each other, with the superior fascicle originating at the level of the 1st rib and the inferior fascicle at the level of the 3rd rib (Fig. 2D). The superior fascicle measured 6.5 cm in length and 1.0 cm in width, and the inferior fascicle was 11 cm in length and 0.7 cm in width.
Case 3
A right AA was identified in an 82-year-old female donor diagnosed with Alzheimer’s disease (Fig. 3A). The arch originated from the anteroinferior margin of the tendinous part of the latissimus dorsi. Unlike the left AA in Case 1, the muscle fibres of this AA ran in parallel and were continuous with those of the latissimus dorsi. The arch traversed across the axilla anterior to the brachial plexus and inserted onto the deep fascia of the pectoralis major.
Case 4
A right AA crossing anterior to the intercostobrachial nerve in addition to the proximal terminal branches of the brachial plexus was identified in a 71-year-old male donor diagnosed with gastroesophageal adenocarcinoma (Fig. 3B). The AA arose from the anteroinferior border of the latissimus dorsi tendon, perpendicular to its striation, and inserted onto the deep fascia of the pectoralis major near its lateral border.
DISCUSSION
Accessory thoracic muscles in humans have been reported in the literature for over 200 years [20]. The embryonic origins of the AA and pectoralis quartus have been discussed by multiple authors based on their source of innervation as well as their phylogenetic relationships with thoracic muscles found in non-human mammalian species [3, 8, 11, 14, 26, 28]. One of the frequently cited views is that these accessory thoracic muscles are remnants of the panniculus carnosus [2, 8, 11, 16], the cutaneous skeletal muscle sheets found in mammals such as cats, dogs, rodents, horses and to a certain extent in some primate species [11, 12]. Rostrally, the panniculus carnosus attaches to the humerus via the fascia deep to the pectoralis muscles, and caudally inserts beneath the dermis of the back and flank regions [11, 12, 25]. The observations that accessory thoracic muscles such as the sternalis, pectoralis quartus, and AA, are often found physically connected to each other [1, 4, 7, 8] may reflect the close phylogenetic relationship proposed between the panniculus carnosus and pectoral muscles [8, 11, 16].
An alternative origin of the pectoralis quartus has been also proposed in literature. Based on comparative anatomical studies that show concurrent presence of the pectoralis quartus and the panniculus carnosus in several mammalian species, the view that the pectoralis quartus is a segmented portion of the lower part of the pectoralis major, not a vestigial rudiment of the panniculus carnosus, has been described [3]. In this view, the pectoralis quartus is considered as a variation of the pectoralis major, to a certain extent similar to the pectoral fascicles found deep to the pectoralis major, which were identified in Case 2 of the current report. Deep accessory pectoral fascicles have been reported in primates such as chimpanzees and bonobos as a common occurrence [18]. In the same report, the authors also identified similar accessory pectoral fascicles in two human cadavers [18]. Independently, an accessory head of the pectoralis major muscle has been reported [13]. The bilateral paired accessory pectoral fascicles reported in Case 2 of the current report appears to be a rarer presentation of these muscles since the reports cited above described only unilateral accessory pectoral fascicles.
The source of the relatively common occurrence of accessory muscles of the pectoralis major and the latissimus dorsi may lie in the complex migration pattern taken by their myogenic precursor cells. Recent investigation on embryonic origins of the pectoral and latissimus dorsi muscles revealed that these superficial shoulder girdle muscles arise through the two-step process, referred to as the “in-out” mechanism, in which the myogenic precursors first migrate into the forelimb bud from the thoracic somites and then return to the trunk region to complete the muscle development [19, 27]. This complex developmental process may possibly lead to varied migration paths among the precursors, giving rise to accessory pectoral muscles associated with the pectoral and latissimus dorsi muscles.
Because the accessory thoracic muscles discussed above are common in the general population and closely associated with clinically important structures such as the neurovascular bundles and lymph nodes in the axillary region, awareness of their implications to medical procedures such as surgery and potential chronic conditions is warranted [6, 23]. For instance, potential interference of the AA and the pectoralis quartus with sentinel lymph node biopsy and axillary lymphadenectomy have been discussed [10, 17, 21]. Also, compression on the neurovasculature in the axilla by the AA may be involved in conditions such as a thoracic outlet syndrome [5] and can cause deep vein thrombosis [15]. The accessory pectoral muscles closely associated with axilla, therefore, have significant implications for regularly performed surgical procedures in the axillary region and chronic conditions affecting the axillary neurovasculature.
CONCLUSIONS
In this report, we examined 48 donors and found 4 cases of AA (8.3%) in an ethnically diverse donor population. Additional thoracic accessory muscles were identified, a pectoralis quartus associated with bilateral AAs and bilateral paired pectoral fascicles associated with a unilateral AA. Since these thoracic accessory muscles are in close proximity to the axillary lymph nodes and neurovasculature, the relatively common occurrence of these variations merits awareness.
Acknowledgements
The authors are grateful to the staff of the UC Davis Body Donation Programme for their support and wish to express gratitude to the individuals who donated the bodies for the advancement of medical education and research.
