Int J. MorphoL, 25(2) :357-361,2007.

Multiple Variations in the Axillary Arterial Tree Relevant to Plastic Surgery: A Case Report

Variaciones Múltiples de las Ramas de la Arteria Axilar Relevantes para la Cirugía Plástica. Reporte de Caso

*Orhan Magden; **Nuket Gocmen-Mas & ***Baris Caglar

*Prof., M.D., Ph.D Dokuz Eylül University Faculty of Medicine Department of Anatomy, 35100 Inciralti- Izmir Turkey.
** M.D., Ph.D. Baskent University Faculty of Medicine Department of Anatomy. 06530 Baglica - Etimesgut/ Ankara Turkey.
*** M.D. Baskent University Faculty of Medicine Department of Plastic & Reconstructive Surgery

Dirección para correspondencia

SUMMARY: While dissecting the body of a 59 years old male cadaver we observed "abnormal" branching pattern of the axillary artery and unusual vascular pedicles of the serratus anterior muscle. The serratus anterior branch originated directly first part of the axillary artery as the first branch. The lateral thoracic and thoracodorsal arteries arose together from the third part of the axillary artery as "a lateral thoracic-thoracodorsal"common trunk. The superior thoracic artery was out of the position. The circumflex scapular artery originated directly the third part of the axillary artery. The subscapular artery was not present.

KEY WORDS: Axillary artery; Common trunk; Serratus anterior branch; Unusual vascular pedicle.

RESUMEN: Durante la diección de un cadáver de un hombre de 59 años de edad observamos un padrón «anormal» de las ramas de la arteria axilar e inusual pedículo vascular para el músculo serrato anterior. La rama para el músculo serrato anterior se originaba directamente de la primera parte de la arteria axilar como la primera rama. Las arterias torácica lateral y toracodorsal se originaban juntas de tronco común de la tercera parte de la arteria axilar como «arteria torácica lateral-toracodorsal». La arteria torácica superior estaba fuera de la posición. La arteria circunfleja escapular se originaba directamente de la tercera parte de la arteria axilar. La arteria subescapular no estaba presente.

PALABRAS CLAVE: Arteria axilar; Tronco común; Rama para el el músculo serratus anterior; Unusual pedículo vascular.

INTRODUCTION

There are many variations in the branching patterns of the axillary artery (Moore, 1999; Valnicek et al.2004; Pandey, 2004). Such variations are significant because a large number of diagnostic or therapeutic invasive procedures such as ligation of injured arteries, angiographic studies of the axillary vessels, and axillary aneurysms are carried out on the axillary artery. It is also considerable to avoid possibility of brachial plexus or arterial damages during surgical interventions such as the serratus anterior flap surgery (Goldberg et al.1990; Moore; Valnicek, et al.)

The serratus anterior muscle can be used as a pedicled functional muscle flap, musculocutaneous flap, osseofasciocutaneous flap, combined serratus-latissimus flap, serratus fascia flap, microvascular free flap. Entire muscle can be used as flap but this will result in severe winging of scapula, to prevent this condition and to maintain function it is very important to preserve at least upper five or preferably six digitations and their innervation's and, only lower three or four slips should be harvested as a flap. In general the upper two or three slips of serratus are based on the lateral thoracic pedicle and rest parts are based on thoracodorsal pedicle. For this reason pedicle of choice for elevation of flap either as standart flap or for microvascular transplant is the thoracodorsal pedicle (Mathes & Nahai, 1997; Moore).

Classically, the axillary artery a continuation of the subclavian artery begins at the outer border of the first rib, ending at the inferior margin of the teres major muscle. The pectoralis minor muscle crosses it and divides it into the first (proximal), the second (posterior) and the third (distal) parts. The first part of the axillary artery is located between the first rib and the superior border of the pectoralis minor muscle. The first branch of the first part is the superior thoracic artery which supplies the first and second intercostal space and the superior part of the serratus anterior muscle. It anastomoses with the intercostal arteries. The second part of the axillary artery lies deep to the pectoralis minor muscle. The lateral cord of the brachial plexus is laterally to the artery, the medial cord is medial to it, and the posterior cord is posterior to it. The second part of the axillary artery has two branches, the thoracoacromial artery, proximally and the lateral thoracic artery, distally. The artery supplies the latissimus dorsi muscle. The third part of the axillary artery has three branches which are named the subscapular, the anterior circumflex humeral and the posterior circumflex humeral arteries. The subscapular artery is the largest branch of the axillary artery which ends as the circumflex scapular and thoracodorsal arteries (Moore).

The serratus anterior muscle is a large muscular sheet curving round the thorax from an extensive multidigital costal attachment to medial scapular border. Its muscular digitations (slips) spring anteriorly from the outer surfaces and superior borders of the upper eight, nine or even ten ribs, and fascia over the intervening intercostals. The long thoracic nerve descending on the muscle's external surface innervates it (Tobin et al.1990) and this nerve has to be spared to preserve function during dissection. The serratus anterior is a type III muscle (has 2 dominant pedicles). First dominant pedicle is lateral thoracic artery which supplies upper three-four slips. Second dominant pedicle is thoracodorsal artery which sends two to four branches to the muscle supplying fifth-tenth slips. The lateral thoracic artery arises directly from the second part of the axillary artery. The thoracodorsal artery is the continuation of the subscapular artery (Mathes & Nahai; Grotting, 1998).

Data about axillary vascular tree and pedicle of the serratus anterior muscle will be valuable the anatomical knowledge which may be provided non complicated medical interventions and surgical approaches of this region especially in case of reconstructive surgery.

CASE REPORT

The multiple variations in branching of the axillary artery were determined during a routine dissection of a 59 years old formalin-preserved male cadaver on the right side in the axillary region by using fine surgical instruments under X4 loupe magnification.

A subcostal to mid axillary incision was made and skin and subcutaneous tissue were separated to expose the axillary vessels and the serratus muscle, unilaterally. Pectoralis major and minor muscles were reflected and the clavipectoral fascia removed together with the axillary sheath which surrounded the axillary vessels and the brachial plexus. With forceful contraction anterior margin of latissimus dorsi muscle and lateral border of pectoralis major muscle are marked. The anterolateral portion of serratus and its skin island lie in this triangle. An incision is made diagonally across the axilla and extended for several centimeters inferiorly in the space between the anterior and posterior axillary line, the serratus anterior muscle was exhibited by preserving neurovascular structures. When thoracodorsal pedicle is identified, the desired number of slips of muscle is dissected. These digitations are divided anteriorly from their rib origin and dissected from anterior to posterior toward the scapula. Posteriorly muscles are divided and the flap elevated from below upward and mobilized to recipient site.

The muscle has been evaluated in three zones as origin zone, central zone and insertion zone to define neurovascular supplying. All vessel diameters were measured with 3-mm micrometer with 0.1 markings. Nerve dimensions (length, course and which slips they served) were measured. To determine harvesting area of the serratus anterior muscle, attention was then turned to arterial pattern and supply. The branching pattern was recorded and the supply to the each slip was determined. Terminal branches were followed into the muscle until their external diameters are less than 1 mm. The specimen was photographed. The following parameters regarding the branches of axillary artery were evaluated: (1) Locations; (2) origins; (3) diameters of the branches at their origin; (4) length of the branches; (5) courses; (6) distance between origin of the branches and lateral margin of the first rib; (7) anastomosing and crossing patterns of the branches; (8) relations with the adjacent structures; (9) innervations and (10) the blood supplying patterns of the serratus anterior slips according to the muscle zones. The findings are as follows:

In the case, it was encountered various anomalies of the branching pattern of the axillary artery such as the serratus anterior branch which was the pedicle of serratus anterior muscle; the thoracodorsal artery which was the pedicle of the latissimus dorsi muscle; the lateral thoracic artery which was the pedicle of the serratus anterior, the pectoralis major, the pectoralis minor and the subscapular muscles. An aberrant independent origin of the serratus anterior branch as the first branch which originated directly from the first part of the axillary artery was presented. The distance between origin point of the serratus anterior branch and the lateral margin of the first rib was 20 mm. At the level of origin diameter of the branch was mean 1.8 mm. The branch passed from the origin point through the central third of the muscle and supplied the inferior part of the serratus anterior. It gave off the small branches which arose on average 18 mm from the origin point, supplied the first external intercostal muscle. The mean length of the vascular pedicle of serratus anterior branch which harvested from origin point through the junction of the slips 5 and 6 was 15.3 cm; the mean diameter at the level of the junction of slips 5 and 6 was 1.1 mm. There were four common slip arteries which arose from the serratus anterior branch anteriorly and three common slip arteries arose from the muscle posteriorly.

It was found that the superior thoracic artery was out of position. The artery was originated from the first part of the axillary artery as the second branch. Then, the thoracoacromial artery directly originated from the second part of the axillary artery. The lateral thoracic and thoracodorsal arteries arose together from the second part of the axillary artery as a common trunk (Fig. 1). This "lateral thoracic-thoracodorsal" common trunk originated 58 mm distance from the lateral margin of the first rib. The distance between origin of the common trunk and its dividing point was 20 mm. At the level of origin diameter of the common trunk was mean 2.4 mm. Data about the lateral thoracic and thoracodorsal arteries was obtained as well. At the level of origin diameter of the lateral thoracic artery was mean 1.7 mm and mean length of the artery was 13.2 cm. It crossed anterior to the long thoracic nerve after 15 mm distance from the origin and lain between insertion zone and central zone of the serratus anterior muscle. One of the anterior branches anastomosed the intercostal artery in the third intercostal space. At the level of origin diameter of the thoracodorsal artery was mean 1.9 mm; mean length of the artery was 16.5 cm and it crossed posterior to thoracodorsal nerve 41 mm distance from the coracoid process.

Fig. 1. Anomalous axillary artery tree is presented. The serratus anterior vascular branch (BS) as the first branch (newly reported anomaly), the lateral thoracic-thoracodorsal common trunk (TLT) and the circumflex scapular artery arise directly from the axillary artery (CSA). The branches which supply the first external intercostal muscle are indicated by plus signs, the common slip arteries which arise from the serratus branch are indicated by asteriks. AA. Axillary artery; BS. Branch to serratus anterior muscle; STA. Superior thoracic artery; TLT. Lateral thoracic-thoracodorsal trunk; LTA. Lateral thoracic artery; TDA. Thoracodorsal artery; CSA. Circumflex scapular artery; LTN. Long thoracic nerve; TDN. Thoracodorsal nerve; ASM. Anterior serratus muscle; PMM. Pectoralis major muscle; PMiM. Pectoralis minor muscle; LDM. Latissimus dorsi muscle; SSM. Subscapular muscle; FR. First rib; C. Clavicle.

The circumflex scapular artery originated directly from the third part of the axillary artery. The subscapular artery was not present. The anterior circumflex humeral and posterior circumflex humeral arteries originated directly from the third part of the axillary artery. The veins accompanied the arteries of the serratus anterior muscle and the branches to their distal-most extent.

The superior and the middle part of the serratus anterior muscle were supplied by the lateral thoracic artery as the lateral thoracic-thoracodorsal common trunk which originated from the axillary artery. The inferior part of the serratus anterior muscle was supplied by the serratus anterior branch which was the first branch of the first part of the axillary artery. The veins accompanied with the arteries.

The long thoracic nerve which innervated the serratus anterior muscle arose from the ventral rami of 5-7 cervical spinal nerves. Each three ventral rami came together after 13 cm distance from the origin. The whole length of the nerve was 26.8 cm; distance between the level of C7 and the junction of the slips 5 and 6 was 13.8 cm. The nerve crossed anterior to serratus anterior branch after 21 cm. The nerve lain on central zone of the serratus anterior muscle; then it bifurcated into the two branches at the level of the fourth intercostal space. Afterwards, the fascicules of the nerve accompanied with anterior sub branches of the serratus anterior branch. The diameter of the long thoracic nerve was measured at the level of C7, at the level of the junction of slips 5 and 6, at the level of the junction of slips 8 and 9; as 1.6 mm, 1.3 mm and 0.6 mm, respectively.

DISCUSSION

Variations of axillary artery are significant for clinicians either for the diagnostic interventions or the surgical approaches. More recent cadaver studies have attempted to characterize the serratus muscle and neurovascular supply to aid in its usage as a flap. The serratus anterior flaps have favorable characteristics owing to anatomically convenient and consistent vascular pedicle for use in especially extensive face, hand and extremity defect reconstructions (Valnicek et al; Godat, 2004). Recognition of any vascular variation is very important to select the appropriate pedicle for flap survival (Mathes & Nahai; Moore).

The blood supply to the serratus anterior muscle typically originates as branches from the lateral thoracic artery (Moore). But in the literature, it was defined four patterns of subscapular vascular tree which supplied the serratus anterior muscle. In the first pattern, the subscapular artery gave off the circumflex scapular and the thoracodorsal arteries. The subscapular artery sent 1 to 3 branches to the serratus anterior muscle. This pattern was represented 95 % to 98 % of cases. In the second pattern, the thoracodorsal artery which arose from the subscapular artery sent the branches to the serratus anterior muscle was represented 1 % to 3 % of cases. In the third pattern, the thoracodorsal and the serratus anterior branches originated separately from the subscapular artery was represented less than 1 % of cases. In the fourth pattern the subscapular artery gave off the serratus anterior branches. The thoracodorsal artery originated directly from the axillary artery. The circumflex scapular artery not visualized. This pattern was represented in 1 case (Goldberg). In the present case, different type of arterial pattern was found. It was defined multiple anomaly in the branching axillary artery. Accordingly, it was found that the serratus anterior vascularbranch as the first branch, the lateral thoracic- thoracodorsal common trunk and the circumflex scapular artery arose directly from the axillary artery.

Classically, the superior thoracic artery which branches from the first part of axillary artery anastomoses with the intercostal arteries (Moore). There were many variations about superior thoracic artery in literature (Pandey, 2004). In the present case, the superior thoracic artery was found out of the position. Differing from the knowledge of the classical textbook (Moore), it was originated from the first part of the axillary artery as the second branch. Instead of the superior thoracic artery, an aberrant independent origin of the serratus anterior branch as the first branch which originated directly from the first part of the axillary artery was presented. The origin point of the serratus anterior branch, surgical reference points, diameter, course of the branch and supplying area were determined. It was defined; the branch passed from the origin point through the central third of the serratus anterior muscle and supplied the inferior part of it.

Many authors declared that the serratus anterior branch originated directly from subscapular artery from the proximal third of the axillary artery and thoracodorsal artery arose separately from the distal third of the axillary artery as variations in the case (Goldberg et ah; Tobin et al.). But in the present case, the subscapular artery was not present.

Normally, the second part of the axillary artery has two branches, the thoracoacromial artery proximally and lateral thoracic artery distally (Moore). Similar with the knowledge of the textbook it was found that, the thoracoacromial artery originated directly from the second part of the axillary artery. There was not any variation related with thoracoacromial artery. Classically, the long thoracic artery which is arises directly from the second part of the axillary artery courses along the thoracic wall superficial to the serratus anterior muscle and branches of the artery harvest on the muscle (Moore). Instead of separate origin of the lateral thoracic artery, the thoracodorsal and lateral thoracic arteries arose together from the second third of the axillary artery as the common trunk. We suggested naming this vessel "a lateral thoracic- thoracodorsal" common trunk. It was declared that the thoracodorsal artery was a branch of the subscapular artery in 97% of the cases by Goldberg et al. (Goldberg et al.) and 94% of the cases by Roswell et al. In 24%> of dissections the thoracodorsal artery gave off two branches to the serratus anterior muscle; one of them was 1 mm in diameter and the other one was on average 2 mm in diameter (Roswell et al.).

In the present case all of the branches which supplied the serratus anterior muscle had diameter of more than 1.0 mm and each had average diameters large enough for anastomosis, so we considered that these branches were reliable to use as the pedicles of flaps. Similar with the authors, it was determined that these arteries have satisfactory size for using the serratus anterior muscle flap.

The knowledge of these variations is of the anatomical and surgical interest. These results confirm the anatomical reliability of the serratus anterior flaps to eliminate in ambiguity due to variations of the axillary vascular tree. Hence, the knowledge about the variations of axillary arterial tree could provide to prevent the branches of the axillary artery during raising serratus anterior flaps and understanding of adjacent region the anatomic characteristics of this region. Our findings may give a contribution about the surgery procedures of the defects by providing easy anastomosis, normal anatomical reorganization, easing operative period and also provide anatomic information, guidance and will support the literature.

REFERENCES

Godat, D. M. et al. Detailed neurovascular anatomy of the serratus anterior muscle: Implications for a functional muscle flap with multiple independent force vectors. Plast. Reconstr. Surg., 114: 21-9, 2004.

Goldberg, J. A. et al. An aberrant independent origin of the serratus anterior pedicle. Ann. Plast. Surg., 25:487-90, 1990.

Grotting, J. C. Microvascular free transfer of the serratus anterior muscle. Grabb 's Encylopedia of Flaps, Head and Neck. Philadelphia-New York, Lippincott-Raven, 1998.

Mathes, S. J. & Nahai, F. Reconstructive Surgery Principles, Anatomy & Technique. New York, Livingston, 1997.

Moore, L. K. & Dalley, A. F. Anatomy. 4. Ed. Philadelphia, Lippincott Williams & Wilkins, 1999.

Pandey, S. K. & Shukla, V. K. Anatomical variation in origin and course of the thoracoacromial trunk and its branches. J. Nepal Med. Coll., 6:88-91,2004.

Roswell, A. R. et al. The anatomy of the subscapular-thoracodorsal arterial system: study of 100 cadaver dissections. Br J. Plast. Surg., 57:574-6, 1984.

Tobin, G. R. et al. Mandibular-facial reconstruction with segmental split serratus anterior composite flaps. Clin. Plast. Surg., 77:663-72, 1990.

Valnicek, S. M. et al. The subscapular arterial tree as a source of microvascular arterial grafts. Plast. Reconst. Surg., 113: 2001-5, 2004.

Received: 15-03-2007 Accepted: 16-04-2007

Correspondence to:

Nuket Gocmen-Mas PhD MD
Baskent University School of Medicine
Department of Anatomy
06530 Baglica /Ankara
TURKEY
Tel: +90 312 234 10 10/1524 Fax:+90 312 234 11 80
Email: nuketgocmen@yahoo.com