Vascular patterns of : an anatomical study with accent on superfi cial brachial

David Kachlik 1*, Marek Konarik 1, Vaclav Baca 1

1 Charles University in Prague, Third Faculty of Medicine, Department of Anatomy, Ruská 87, Praha 10, 100 00, Czech Republic

Abstract

Th e aim of the study was to evaluate the terminal segmentation of the and to present four cases of anomalous branching of the axillary artery, the superfi cial (arteria brachialis superfi cialis), which is defi ned as the brachial artery that runs superfi cially to the median nerve. Totally,  cadaveric upper embalmed by classical formaldehyde technique from collections of the Department of Anatomy, Th ird Faculty of Medicine, Charles University in Prague, were macroscopically dissected with special focus on the branching ar- rangement of the axillary artery. Th e most distal part of the axillary artery (infrapectoral part) terminated in four cases as a bifurcation into two terminal branches: the superfi cial brachial artery and profunda brachii artery, denominated according to their relation to the median nerve. Th e profunda brachii artery primarily gave rise to the main branches of the infrapectoral part of the axillary artery. Th e superfi cial brachial ar- tery descended to the where it assumed the usual course of the brachial artery in two cases and in the other two cases its branches (the radial and ulnar ) passed superfi cially to the fl exors. Th e incidence of the superfi cial brachial artery in our study was  of cases. Th e reported incidence is a bit contradictory, from . to  of cases. Th e anatomical knowledge of the axillary region is of crucial impor- tance for neurosurgeons and specialists using the radiodiagnostic techniques, particularly in cases involving traumatic injuries. Th e improved knowledge would allow more accurate diagnostic interpretations and surgical treatment. ©  Association of Basic Medical Sciences of FBIH. All rights reserved

KEY WORDS: anatomical variations, axillary artery, profunda brachii artery, superfi cial brachial artery.

Introduction accepted concept describing the beginning of the AA as pass- ing under the clavicle and the end of the distal border of pec- Th e superfi cial brachial artery (arteria brachialis superfi cia- toralis major muscle. Th e whole AA can be divided into three lis, SBA) is not a rare vascular variation of the superior ex- segments [-], which we propose to denominate according tremity. It was already reported and defi ned by Adachi [] to their relation to the pectoralis minor muscle (Table ). as the brachial artery running superficially to the median Th e textbook description regarding the branching pattern of nerve. However, according to recent findings, the defini- the AA refers to it as an artery possessing  principal branch- tion regarding the course of the SBA in relation to the me- es: (arteria thoracica superior), thora- dian nerve is not so stringent. Rodriguez-Niedefűehr recalled coacromial artery (arteria thoracoacromialis), lateral thoracic attention to the SBA and stated that “its course is rather artery (arteria thoracica lateralis), (arteria superficial”. The SBA then descends as far as the cubital subscapularis) and both the anterior and posterior circum- fossa where it bifurcates as the proper brachial artery into flex arteries (arteria circumflexa humeri anterior et poste- both the radial and ulnar arteries and their branches []. rior, ACHA and PCHA) [,]. But many authors disagree To understand the anatomy and terminology of the with the above mentioned data: De Garis reported the span SBA, its relations and developmental background prop- of branch numbers to be - and documented the most erly, it is necessary to mention first some basic facts frequent pattern to be  branches []; Trotter published a regarding the axillary artery (arteria axillaris, AA). study in which a diff ering frequency for both men () and Th e extent of the AA is set by diff erent structures as reported women () was documented []; Huelke suggested the in our previous publication []. We followed the prevailingly normotype with  independent branches (incidence of  of cases), including the upper subscapular artery, described in * Corresponding author: David Kachlik; Charles University in Prague,  of cases, following the course of the subscapular nerve to Third Faculty of Medicine, Department of Anatomy; Ruská 87, Praha 10, 100 00, Czech Republic; Telephone: +420267102508, the subscapular muscle (corresponding to the largest ramus Fax: +420267102504; e-mail: [email protected] subscapularis), and, simultaneously, he reported the most fre- Submitted 23 September 2010/ Accepted 23 December 2010 quent pattern to be  branches (present in . of cases) [].

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TABLE 1. The proposal of arbitrary segmentation of the axillary artery, based on the clinical-anatomical approach

Segment Extent Branches suprapectoral part from clavicle to proximal border superior thoracic artery (pars suprapectoralis) of pectoralis minor muscle retropectoral part limited by width of pectoralis minor muscle, (pars retropectoralis) located dorsally and covered by its belly subscapular artery infrapectoral part From distal border of pectoralis minor muscle to distal border of anterior humeral cicumfl ex artery (pars infrapectoralis) pectoralis major muscle (or surgical neck of humerus) posterior humeral cicumfl ex artery

Materials and Methods (aged ). Th e AA terminated as a trifurcation into three large branches: superfi cial brachial artery, profunda brachii artery One hundred and thirty preparations of upper limbs of the ca- (arteria profunda brachii, deep artery of , incorrectly daverous material (Czech population, Caucasian race, - “deep brachial artery”, PBA), and subscapular artery (Figure ). years old,  males,  females), fi xed with classical formalde- The thoracoacromial and superior thoracic artery origi- hyde method, were dissected at the Department of Anatomy nated from the suprapectoral part of the axillary artery; the of the Th ird Faculty of Medicine, Charles University in Prague. retropectoral part gave rise to the lateral thoracic artery. Th e atypical courses of SBA were followed and registered. The remaining branches, which under normal conditions ramify from the infrapectoral part of the AA, branched Results from the PBA, with the exception of the subscapular artery, which was a branch of the unique AA terminal trifurcation. The four different arterial branching patterns of the The profunda brachii artery gave rise not only to both AA, concerned the superficial brachial artery, were ob- circumflex humeral arteries but also to the acces- served. All four patterns deviated from the above men- sory (arteria thoracodorsalis ac- tioned textbook pattern, scilicet in various sites of origin, cessoria) and terminated as the medial and radial col- course, arrangement of terminations, branches, and calibre. lateral arteries (arteria collateralis media et radialis). The SBA descended in front of the medi- Case : an nerve and proceeded to branch into both Th is case presented a very unique type of branching pattern the ulnar and radial arteries in the cubital fossa. of the AA. It was observed in the left arm of a female cadaver Th e length of the AA from its origin (the inferior border of

AB

FIGURE 1. The real (A) and schematic (B) situation of the Case 1. AA – axillary artery, ACHA – anterior circumfl ex humeral artery, BBM – biceps brachii muscle, CSA – circumfl ex scapular artery, LTA – lateral thoracic artery, MCA – medial collateral artery, MN – median nerve, PBA – profunda brachii artery, PCHA – posterior circumfl ex humeral artery, RCA – , RN – radial nerve, BAS – super- fi cial brachial artery, SsA – subscapular artery, STA – superior thoracic artery, TaA – thoracoacromial artery, TdA – thoracodorsal artery, TdAA – accessory thoracodorsal artery, * – common trunk for circumfl ex humeral arteries.

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A B

FIGURE 2. The real (A) and schematic (B) situation of the Case 2. AA – axillary artery, PBA – profunda brachii artery, PCHA – posterior circumfl ex humeral artery, SBA – superfi cial brachial artery, SsA – subscapular artery, LTA – lateral thoracic artery, STA – periorsu thoracic artery, 1 – common trunk (No. 1) for LTA and STA, 2 – common trunk (No. 2) for PBA, PCHA and SsA, 3 – common trunk (No. 3) for PCHA and SsA.

AB

FIGURE 3. The real (A) and schematic (B) situation of the Case 3. AA – axillary artery,,ACHA – anterior circumfl ex humeral artery, LTA– lateral thoracic artery, PBA – profunda brachii artery, PCHA – posterior circumfl ex humeral artery, SBA – superfi cial brachialartery, SsA – subscapular artery, STA – superior thoracic artery, 4 – common trunk (No.4) for circumfl ex humeral arteries and PBA.

A B

FIGURE 4. The real (A) and schematic (B) situation of the Case 4. AA – axillary artery, ACHA – anterior circumfl ex humeral artery, AV – axil- lary vein, LTA – lateral thoracic artery, MN – median nerve, PBA – profunda brachii artery, PCHA – posterior circumfl ex humeral artery, SBA – superfi cial brachial artery, SsA – subscapular artery, STA – superior thoracic artery, UN – ulnar nerve, 5 – common trunk for (No.5) for circumfl ex humeral arteries and PBA.

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TABLE 2. The caliber of arteries in the aforementioned cases of the humerus (crista tuberculi minoris humeri). Th e infra- Artery Case 1 Case 2 Case 3 Case 4 clavicular part of the AA terminated  mm distally to the Axillary artery 9 mm 8 mm 8 mm 9 mm arbitrary beginning of the AA with a bifurcation into the SBA Th oracoacromial artery 5 mm 5 mm 4 mm 4 mm and a common trunk (No. ). Th e SBA descended along the Subscapular artery 6 mm 4 mm 4 mm 4 mm arm and terminated as a bifurcation into the radial and ulnar Profunda brachii artery 5 mm 4 mm 5 mm 5 mm arteries at the level of the interepicondylar line. Both the ra- Posterior circumfl ex humeral artery 4 mm 4 mm 4 mm 4 mm dial and ulnar arteries were located superfi cially to the fl exor Superfi cial brachial artery 6 mm 5 mm 5 mm 5 mm muscles of the forearm and distally they rejoined their “com- Lateral thoracic artery 3 mm 3 mm 3 mm 3 mm mon” textbook position. Th e common trunk (No. ) gave rise Superior thoracic artery 3 mm 4 mm 3 mm 3 mm to the profunda brachii artery immediately and continued Circumfl ex scapular artery 4 mm 4 mm 3 mm 4 mm as a common trunk (No. ) to terminate  mm farther as a Th oracodorsal artery 3 mm 3 mm 3 mm 3 mm bifurcation into the subscapular artery and posterior circum- Accessory thoracodorsal artery 3 mm - - - fl ex humeral artery. Th e PBA ran distally without any other Anterior circumfl ex humeral artery 2 mm 2 mm 2 mm 2 mm deviation. Th e subscapular artery ramifi ed (as is the textbook Radial collateral artery 3 mm - - - pattern) into the circumfl ex scapular artery and thoracodor- Medial collateral artery 3 mm - - - sal artery, which entered the  mm Common trunk No. 1 - 6 mm - - from the point of muscle insertion into the humerus. Th e ob- Common trunk No. 2 - 5 mm - - Common trunk No. 3 - 5 mm - - served case presented the latissimus dorsi muscle being sup- Common trunk No. 4 - - 5 mm - plied by two diff erent large regular branches of the AA: the Common trunk No. 5 - - - 5 mm lateral thoracic artery and the thoracodorsal artery (Figure ).

Case : clavicle) to its trifurcation was  mm. A large subscapu- The third case also represented a combined variation of lar artery ran for  mm from the trifurcation to its ter- the SBA and another vascular variation of the AA branch- minal bifurcation into the thoracodorsal artery (arteria ing pattern: a common trunk for the anterior and posterior thoracodorsalis) and circumflex scapular artery (arteria circumflex humeral arteries and the PBA (Figure ). The circumflexa scapulae). Immediately after stemming from variation was observed in the left arm of a female cadaver the termination of the AA, the PBA gave rise to the acces- (aged ). Th e fi rst two parts of the AA did not feature any sory thoracodorsal artery for the latissimus dorsi muscle, deviation from the textbook pattern; however, the infra- which thus received the arterial blood from two different clavicular part of the AA gave rise to the subscapular artery, sources. A common trunk for both the anterior and pos- which  mm distally ramified into a common trunk (No. terior circumflex humeral arteries, which stemmed from  - for ACHA, PCHA, and PBA) and SBA. The SBA de- the PBA  cm from its origin, was also observed. After giv- scended along the arm and coursed superfi cially to the me- ing rise to this common circumfl ex humeral trunk, the PBA dian nerve and, in the area of interepicondylar line, divided bifurcated into the medial and radial collateral artery. For into the ulnar and radial arteries. Th e rather long common the caliber of all the aforementioned arteries, see Table . trunk (No. ) terminated after  mm with a trifurcation.

Case : Case : Th e second case of the abnormal branching pattern of the The last case represented a typical AA branching pattern AA included again the SBA and another associated variation. associated with SBA (Figure ). The first two parts of the It was observed in the right arm of a female cadaver (aged AA did not show any deviation from normal textbook pat- ). Th e retropectoral part of the AA featured a common terns; however, the third part terminated with a bifurcation trunk (No. ) which bifurcated and gave rise to the superior into the SBA and a common trunk (No. ) for the PCHA, thoracic artery and the lateral thoracic artery. Th e common PBA, and the subscapular artery. The subscapular artery trunk (No. , being  mm wide and  mm long) stemmed then continued without any other variation. The caliber  mm distally to the arbitrary beginning of the AA. Th e su- of the common trunk (No. ) was quite large –  mm. Th e perior thoracic artery adhered to the lateral thoracic wall and SBA descended along the arm, ran superfi cially to the me- supplied prevailingly the upper part of the serratus anterior dian nerve and terminated in the cubital fossa with a bifur- muscle. Th e lateral thoracic artery descended towards the cation into the ulnar and radial arteries at the level of the latissimus dorsi muscle and entered the muscle  mm far interepicondylar line. Both of these arteries ran along the from the muscle insertion to the crest of the lesser tubercle forearm superficially to the flexor muscles (as in Case ).

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Discussion then retakes its position of the “usual” brachial artery in the distal arm and the region by bifurcating into the Th e defi nition of the superfi cial brachial artery was set for the radial and ulnar arteries. Nevertheless, frequently, it runs fi rst time by Adachi in  and runs as follows: “Th e super- rather superficially, i.e. its terminal branches also follow fi cial brachial artery is the brachial artery that runs superfi - this superficial course in relation to the forearm muscles. cially to the median nerve.” []. On the contrary, the profunda As for the nomenclature, it is necessary to mention a clas- brachii artery always descends dorsally to the median nerve, sification set by Bergman et al. [], who proposed differ- i.e. deeper from the surface. In such a case, all the branches ent new terms. But we strictly recommend to follow the from the infraclavicular part of the AA (ACHA, PCHA and clear and simple nomenclature as published by Rodríguez- the subscapular artery) are branches from the proximal part Niedenführ et al. in  [] due to easy and non-problem- of the profunda brachii artery, which caliber is then evidently atic communication between experts worldwide [,]. larger. Th is variant is the only one listed in the Terminolo- The embryological background of these variations in the gia Anatomica, as the item A... at page No.  []. vasculature of the upper limb may be explained as abnor- Th e most interesting case out of those aforementioned ones mal deviations in the normal vascular patterns. Th e proxi- was the Case , featuring the terminal trifurcation of the mal part of the right subclavian artery arises from the right AA. Th e artery ramifi ed into the PBA, SBA and subscapular aortic arch and the distal part of the artery is derived from artery. In reference literature, only one similar case has ever the right seventh intersegmental artery. The left subcla- been reported, mentioned by De Garis and classifi ed as the vian artery has a diff erent embryological background with “G” pattern []. When both cases were compared, two no- the entire artery being formed from the seventh inter- table differences were identified between the “G” pattern segmental artery. The AA and its branches are derived and our Case . At fi rst, there was no posterior circumfl ex from the axial artery, being a distal continuation of the humeral artery passing under the tendons of the teres minor seventh intersegmental artery on both sides of the body. and latissimus dorsi muscles. At second, there was another Every vascular variation can be traced back to an em- variation in the arrangement of the branching pattern of bryological origin. Arey and Jurjus mentioned six the third part of the AA. De Garis described a terminal bi- explanations for the variations observed [,]: furcation into the SBA and a short common trunk which . The choice of unusual paths in the primitive vascular gave rise to the PBA and the subscapular artery; this diff ers plexus. from our Case , which featured a terminal trifurcation []. . Th e persistence of vessels which are normally obliterated. Moreover, the PBA, immediately after stemming from the . Th e disappearance of vessels which are normally retained. termination of the AA, gave rise to the accessory thoracodor- . An incomplete development. sal artery, supplying the latissimus dorsi muscle. Th is varia- . Th e fusion and absorption of parts which are normally tion can be denominated as the “inferior thoracodorsal ar- distinct. tery” as well, in order to distinguish it from the proper artery . A combination of factors leading to an atypical pattern situated more proximally. Such fi nding is of a great clinical normally encountered. relevance due to the wide use of the latissimus dorsi mus- cle as a fl ap in the plastic and reconstructive surgery. Such When mentioning the upper limb, in particu- double main pedicle of the muscle can either aggravate the lar its vascular system, it is necessary to dis- fl ap harvesting or can be useful for splitting the donor fl ap cuss the embryology of the region [,]. for more acceptor sites. In our previous study, the frequency The most interesting fact is that the arterial system of the of the accessory thoracodorsal artery was  of cases []. upper limb develops as a capillary network at Day  (- In the Case , the latissimus dorsi muscle was supplied mm bud of the future upper limb begins to form), con- by two diff erent large regular branches of the AA as well: nected to the axial artery, which pierces the condensed the lateral thoracic artery and the thoracodorsal artery. nervous tissue within future axilla at Day  – the circu- In the Case , the present common trunk for the posterior latory system of the bud can be characterized as a capil- circumfl ex humeral artery and profunda brachii artery be- lary network. On Day , the SBA is defined and, on Day longs to quite frequently reported variations,  [,,]. , the entire limb acquires a mature appearance. The In the case of SBA existence, the profunda brachii artery distal section of the is completely developed replaces the proximal part of the brachial artery. It can be and the connections with deeper parts of the vascular completed with the variations of the infraclavicular part systems (deviations of the axial artery) are now degener- of the AA, with “common” branches stem, in the case of ated. Th e SBA and the brachial artery are anastomosed, the SBA, mainly from the profunda brachii artery. The SBA radial artery is now established as a major branch of the

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TABLE 3. Incidence of the superfi cial brachial artery in various studies. the SBA successfully degenerates. Th e distal part of the SBA Number of Dissected develops into the radial artery and median artery (arteria co- Author (Year) Number Specimens mitans nervi mediani) and serves as the developmental base Quain (1844) [28] 429 0.2% for the majority of arterial variations in the upper limb []. Gruber (1848) [29] 1200 0.4% All the embryological and developmental facts discussed in- Poirier (1886) [30] **** 6% dicate that the SBA is an important variant. Th e Table  sum- Müller (1903) [22] 100 1% Linell (1921) [31] - 6% marizes the most important studies concerning the SBA and De Garis (1928)** [10] 512 4.6% its reported incidence. A particularly interesting phenom- Adachi (1928) [1] 1198 3.1% enon can be traced throughout the years of the studies. Origi- Miller (1939) [21] 100 3% nally, the SBA was observed in only - of cases; however, Treves (1947) [32] - 15% later studies, published in ’s, reported its frequency to be McCormack (1953) [33] 750 0.12% - of cases. In the last  years, the incidence has been Lanz (1959) [25] - 25% documented to be only - (Table ). Th e reasons for this Skopakoff (1959) [34] 610 19.7% Keen (1961) [35] 284 3.6% (12.3%*) sinusoid characteristic of the result incidence can be attrib- Fuss (1985) [36] 200 17% uted to new specifi cation guidelines, classifi cation of the vari- Lippert (1985) [37] *** 22% ations and melioration in study methods, which have been Rodriguez-Baeza (1995) [27] 160 11.9% improved thanks to the conclusions of the previous fi ndings Kapur (2000) [38] - 5% and observations. Adachi defi ned the SBA as coursing super- Prasada Rao (2001) [39] 24 4.2% fi cially to the median nerve and Rodriguez-Niedefűehr stated, Rodriguez-Niedefűehr (2001) [40] 384 4.9% more than  years later, that it ran “rather superfi cially” [,] Patanik (2002) [23] 49 6% Rodriguez-Niedefűehr. (2001)*** [2] 168 7.7% Conclusion Kachlík (2010) 130 5% *Comprises three diff erent variants: the superfi cial brachial artery (3.6%), brachiora- dial artery = high origin of radial artery (5.9%) and brachioulnar artery = high origin of (2.8%) in one group. ** The superfi cial brachial artery is more frequent We reported, for the fi rst time, the trifurcation of the axillary in Afro-Americans (13.4%) than in white race (4.6%). *** Research based on literature artery (into the superfi cial brachial artery, profunda brachii review artery and subscapular artery), combined with an accessory forearm vascular system and the SBA begins to fade away. thoracodorsal artery (stemming from the PBA) and the super- Th e structures involved in the development of the AA are fi cial brachial artery. Th e SBA descended in front of the me- derived from the seventh intersegmental artery, where- dian nerve and proceeded to branch into both the ulnar and as the thoracodorsal-subscapular trunk corresponds radial arteries in the cubital fossa at the level of the interepi- to the ninth intersegmental artery. The regular persis- condylar line. It is a remnant of the complex development tence of the ninth intersegmental artery was observed of the arm and forearm arterial supply, persisting in various by Miller in primates and Lemur and Galago gorillas []. forms in approximately - of cases. It can be concluded that It is generally admitted that anomalies in the arrange- it is quite frequent arterial variant of the upper limb vascula- ment of the branches of the brachial plexus are second- ture. Th e anatomic knowledge of the axillary region is of cru- ary to an aberrant distribution of the AA [,,]. cial importance not only for neurosurgeons, but for all those The SBA is presented as a concentration of vascular ele- involved in radiodiagnostics, particularly in cases involving ments in the area close to the proximal portion of the bra- traumatic injuries, as improved knowledge would allow more chial artery, or, more precisely, to the infraclavicular part of accurate diagnostic interpretation and surgical treatment. the AA. The consecutive branching of the SBA is divided into a superficial antebrachial medial and superficial ante- Declaration of Interest brachial lateral arteries. The latter of the aforementioned arteries runs distally as the defi nitive radial artery. Th e for- Th e authors state that there is no confl ict of interest. mer one bifurcates into the median and ulnar branches, anastomosing with certain segments of the primitive axial References artery [-]. The only regularly persisting branch of the SBA is the main section of the radial artery []. Th e ulnar [] Adachi B. Das Arteriensystem der Japaner, Maruzen, Kyoto, ; pp. -. and common interosseous arteries (arteria interossea com- [] Rodríguez-Niedenführ M, Vázquez T, Nearn L, Ferreira B, Parkin munis) are set by the distal portions of the primitive axial I, Sañudo JR. Variations of the arterial pattern in the upper limb artery. Consequently, a process of degradation begins. Due revisited: a morphological and statistical study, with a review of the literature. J Anat ; : -. to diff erent hemodynamic conditions, the proximal part of

BOSNIAN JOURNAL OF BASIC MEDICAL SCIENCES 2011; 11 (1): 9-10  DAVID KACHLIK ET AL.: VASCULAR PATTERNS OF UPPER LIMB: AN ANATOMICAL STUDY WITH ACCENT ON SUPERFICIAL BRACHIAL ARTERY

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 BOSNIAN JOURNAL OF BASIC MEDICAL SCIENCES 2011; 11 (1): 10-10