A coincidental variation of the axillary artery: the brachioradial artery and the aberrant posterior humeral circumflex artery passing under the tendon of the latissimus dorsi muscle.
The development of the upper limb arteries is not a simple process and is closely related to the bone development . The brachioradial artery (arteria brachioradialis, BrA) is the most common variation of the arteries of the upper limb. Anatomically, the BrA is the radial artery (arteria radialis, RA), featuring a "high origin", which means that the RA originates not as a terminal branch of the brachial artery (arteria brachialis, BA) by bifurcation within the cubital fossa (fossa cubitalis), but more proximal, either from the BA anywhere along the course of the arm, or directly from the axillary artery (arteria axillaris, AA). The course of the BrA is then either similar to the BA, i.e. it descends along the proper brachial artery, situated more ventrally and laterally, or more rarely, it can get more superficial and cross the median nerve (nervus medianus) ventrally; then it should be termed as the superficial brachioradial artery (arteria brachioradialis superficialis)[1,2]. The incidence of the BrA is reported to be 13.8% on average . The posterior humeral circumflex artery (arteria circumflexa humeri posterior, PHCA) stems from the AA at the distal border of the subscapularis (musculus subscapularis) from the proximal segment of the infrapectoral (last, third) part of the AA and runs dorsally into the quadrangular space (foramen humerotrici-pitale, spatium axillare laterale) together with the axillary nerve (nervus axillaris). The PHCA curves around the surgical neck of humerus to supply the shoulder joint, the deltoid (musculus deltoideus), the teres major, the teres minor and the long and lateral head of triceps. The PHCA can anastomose with the deltoid branch of profunda brachii artery (ramus deltoideus arteriae profundae brachii), the largest branch from the BA, given off not far from the arbitrary beginning of the BA (at the level of the distal margin of the artery passing under the tendon of the latissimus dorsi muscle teres major) in the very proximal arm. The PHCA can further anastomose with the deltoid branch of thoracoacromial artery (ramus deltoideus arteriae thoracoacromialis) and the acromial branches of suprascapular artery (rami acromiales arteriae suprascapularis).
The terminology applied strictly follows the last revision of the Latin anatomical nomenclature, as analyzed in our previous papers [4-6]. The terms from variant anatomy follow the recommendation of Rodriguez-Niedenfuhr .
MATERIALS AND METHODS
The body of a 68-years-old female donor, injected and fixed with the classical formaldehyde method, was routinely dissected at the Department of Anatomy, Third Faculty of Medicine, Charles University in Prague, Czech republic, as a part of larger study concerning 214 limbs. Both upper limbs were carefully dissected from the axillary fossa as far as the distal palm. Two arterial variations close to each other were observed and documented, present only unilaterally, in the left limb.
The project has been approved by a Ethics Commission of the Third Faculty of Medicine, Charles University in Prague and that it conforms to the provisions of the Declaration of Helsinki in 1995 (as revised in Edinburgh 2000) and all human subjects gave written informed consent and donors anonymity has been preserved.
The proximal variant registered was the posterior humeral circumflex artery, stemming from an abnormal site (see Figure 1).
It originated from a trunk (profundocircumflex trunk; truncus profundocircumflexus), a short and thick vessel (caliber 6mm) which bifurcated into the proximally ascending PHCA (caliber 5mm) and distally descending PBA (caliber 5mm). The origin site for PHCA was shifted distally from the infrapectoral part of the AA to the very proximal part of the BA, immediately below the inferior margin of the insertion muscle tendons. The short profundocircumflex trunk ran horizontally and laterally. Thus, the PHCA could not pass through its usual topographical site - the quadrangular space (foramen humerotricipitale)- but after leaving the trunk, it coursed underneath the fused tendons of the proximal teres major and distal latisssimus dorsi. Then it turned up and ascended behind the tendon to the usual position at the level of the quadrangular space, where it ramified and entered the deltoid.
The profunda brachii artery was given off from the trunk bifurcation distally, approached the radial nerve (nervus radialis), crossing the AA and BA dorsally, and together they entered the space between the heads of the triceps brachii.
All the arteries were accompanied by corresponding veins. The caliber of the axillary vein was 10mm, that of the venous profundocircumflex trunk was 8mm, and both tributaries (posterior humeral circumflex vein and profunda brachii vein) were 6mm wide.
The latter (distal) variant was the brachioradial artery stemming from the BA (caliber 6mm) shortly (3cm) after the origin of the profundocircumflex trunk (see Figure 2).
It followed the same course as the BA, 6mm wide, descended medially, passed under the median nerve and was situated between the median and ulnar nerve (nervus ulnaris). It approached the medial cutaneous nerve of forearm (nervus cutaneus medialis antebrachii) and the basilic vein (vena basilica) and together they coursed distally as far as the interepicondylar line. Here, the BrA entered the cubital fossa, left the basilic vein and the medial cutaneous nerve of forearm for the depth, where it immediately joined the median nerve and re-crossed it to the lateral side; in this case superficially, though. Then it passed under the whole tendon of the biceps brachii (musculus biceps brachii) and emerged on the lateral side of the forearm. From here, it ran as the usual radial artery as distal as the palm to from the deep palmar arch (arcus palmaris profundus). As for the veins, they followed the textbook pattern (except those accompanying the variations mentioned), i.e. they were doubled from periphery as far as the axillary vein and featured no principal derivation form usual arrangement.
Other arteries of the upper limb dissected featured no other variations.
Our finding depicts a case of coincidental variation. But regarding the embryological background, both variants are a combined sequence of one development abnormality, as explained below.
First, we concentrate on the PHCA passing under the fused tendons of the teres major (musculus teres major, TM) and the latissimus dorsi (musculus latissimus dorsi, LD). This variant is rather neglected in the anatomical reference literature, in case the authors listed the PHCA running under the tendons, it is usually a brief note stating its possible existence. One of the few studies concerning this topic in particular and the most thorough one was performed by Adachi, is based on 398 AA and was published in 1928 as a part of his famous book "Das Arteriensystem der Japaner" . The variant of the PHCA coursing below the tendons of the TM and LD was observed 63 times. The incidence was 15.8% of cases in this study.
Adachi described and classified four different groups of PHCA passing under the tendons and designated them as types D, E, F, and G in his larger concept of the branching pattern. The classification is based upon the origin of the PBA and the radial and medial collateral artery (arteria collateralis radialis et media)--see Table 1.
Several other authors reported on this variant in their larger studies, stating the incidence between 2.8% and 11.3% of cases [7-11,15]. Some of them mention just one of the muscles but exactly the PHCA turns around the fused tendons of both muscles--see Table 2.
Such variant can be denominated as the subtendinous posterior humeral circumflex artery (arteria circumflexa humeri posterior subtendinea), conjoint with the profundocircumflex trunk (truncus profundocircumflexus) to describe all the peculiarities and to avoid any possible misnomers.
Second, the latter variant, concerning the unusually proximally shifted origin of the RA, is not a rare arterial variation of the upper limb. Such a vessel should be denominated as the brachioradial artery (arteria brachioradialis), if we follow a classification proposed by Rodriguez-Niedenfuhr et al. , which we consider marvelous, simple and intelligible.
There are two different types of the BrA. If the artery courses superficially to the muscles of the forearm, it should bear the name of the superficial brachioradial artery (arteria brachioradialis superficialis, SBrA), but if the artery stays deep to the muscles (as usual RA), it should be denominated as the brachioradial artery only [2,3]. The precise definition of the BrA runs as follows: It is abnormal RA originating proximal to the interepicondylar line, either from the AA or the BA [12,13]. The "radial artery with high origin" is an often used synonym for this variant, but it is not an appropriate one and should be omitted and/or excluded . Due to a long distance between the axillary and cubital fossae, the exact location of the origin of the BrA (and the SBrA) can be classified into four groups see Table 3. Our case of the BrA ranks into the Group 4 - the RA stemming from the proximal part of the BA.
Rodriguez-Niedenfuhr et al. performed in 2001 a deep and thorough survey of the upper limb arterial variants and summarized that the BrA was present in 13.8% of cases . But the pattern, in which the RA originates directly from the AA, is present in 3.12% of cases only. That is why we have performed another literature survey and now we can conclude that this variant pattern is present in 1.25% of cases  and in 2.33% of cases in our dissection study. The general incidence of the BrA and the origin site are summarized in the Table 4.
Many authors in the 19th and even in the 20th century did not distinguish between the superficial brachial artery (which is an embryological precursor of the BrA) and the BrA itself. Thus, they erroneously mix both variants into one group and the data are not statistically reliable for both variants separately.
The clinical relevance of knowledge of such anatomical variant consists in more aspects.
The superficially located artery brings an elevated danger of heavy bleeding in all unexpected situations, due to its very close relationship to the skin and possible injury in any superficial cut in both the arm and forearm.
The anatomical knowledge of the BrA is worth during the transradial catheterization procedures, due to the possible narrower caliber of BrA. Such reduction of the caliber of one the main arterial trunks of the upper limb (much more frequent than in usual radial and brachial arteries, being less than 2mm) can interrupt and disable the successful intervention during the transradial catheterization, used for example for diagnostic and therapeutic procedures on co-ronary arteries, such as the coronary angiography and percutaneous coronary intervention (now preferred as a method of choice).
The superficial BrA (if not having the reduced caliber) can serve as a longer graft for aortocoronary bypasses than the usual radial artery.
The PHCA with different course can be harmed during injuries or/and surgical procedures concerning the surgical neck of humerus and the area around the proximal growth plate of humerus. It can also serve as a collateral in case of thrombotic closure of the axillary artery.
Both arterial variants have to be respected in radiodiagnostic, surgical and traumatologic procedures within the axilla and the arm.
Finally, the embryological background has to be discussed. The distal part of the right subclavian artery as well as the whole left subclavian artery comes from the seventh intersegmental artery (arteria intersegmentalis septima sinistra). The bud of the upper limb is supplied by the branches of this vessel, forming the axial artery (arteria axialis), which later gives rise to the AA, the BA, the ulnar artery, the RA, etc. The BrA (the variant concerning the RA with more proximal ("high") origin) is based on the embryological abnormality, termed the superficial brachial artery (arteria brachialis superficialis). The superficial brachial artery arises from persistence of more than one cervical intersegmental artery, which can enlarge and does not perish [22-27].
The knowledge of such arterial variant coincidence is crucial for the catheterization approach using the radial artery in coronary interventions, for the by-pass grafting in coronary vascular surgery and in surgery of humerus.
Special thanks to Mirka Plecita and Vladimir Musil for the technical and bibliographic support.
DECLARATION OF INTEREST
The authors declare that they have no conflict of interest and no financial interests.
 Rodriguez-Niedenfuhr M, Burton J, Deu J, Sanudo JR. Development of the arterial pattern in the upper limb of staged human embryos: normal development and anatomic variations. J Anat 2001; 199:407-417.
 Kachlik D, Konarik M, Baca V. Vascular patterns of upper limb: an anatomical study with accent on superficial brachial artery. Bosn J Basic Med Sci 2011; 11:4-10.
 Rodriguez-Niedenfuhr M, Vazquez T, Nearn L, Ferreira B, Parkin I, Sanudo JR. Variations of the arterial pattern in the upper limb revisited: a morphological and statistical study, with a review of the literature. J Anat 2001; 199:547-566.
 FCAT. Terminologia anatomica. Stuttgart: Thieme Verlag; 1998.
 Kachlik D, Baca V, Bozdechova I, Cech P, Musil V. Anatomical terminology and nomenclature: Past, Presence and Highlights. Surg Radiol Anat 2008;30:459-466.
 Kachlik D, Bozdechova I, Cech P, Musil V, Baca V. Mistakes in the usage of anatomical terminology in clinical practice. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2009; 153:157-162.
 Adachi B. Das Arteriensystem der Japaner. Kyoto: Maruzen; 1928; 285-356.
 Coulouma P, Bastien P, Garraud R. Sur cinq cas d' artere cubitale superficielle naissant par bifurcation precoce du tronc axillo-humeral. Echo Med Nord 1934; 2:613-619.
 Skopakoff C. Uber die Variabilitat Ab- und Verzweigung der A. brachialis superficialis. Anat Anz 1959; 106:356-368.
 Keen JA. A study of the arterial variations in the limbs with special reference to symmetry of vascular patterns. Am J Anat 1961; 108:245-261.
 Olinger A, Benninger B. Branching patterns of the lateral thoracic, subscapular, and posterior circumflex humeral arteries and their relationship to the posterior cord of the brachial plexus. Clin Anat 2010; 23:407-412.
 Golan J, Kaus M, Szwarc P. High origin of the ulnar and radial arteries in human. Folia Morphol (Warsz) 1994; 53:37-48.
 Rao PV, Chaudhary SC. Superficial brachial artery terminating as radial and superficial ulnar arteries: a case report. Centr Afr J Med 2001; 47:78-80.
 Anatomy Atlases: Illustrated Encyclopedia of Human Anatomic
Variation, Opus II, Cardiovascular System, Arteries, Upper Limb, Brachial Artery [Internet]. c1995-2014. [cited 2014-08-22]. Available from: http://www.anatomyatlases.org/AnatomicVariants/ Cardiovascular/Text/Arteries/Brachial.shtml.
 Kachlik D, Konarik M, Cupka T, Knize J, Baca V. An unusual course of the arteria circumflexa humeri posterior. Surg Radiol Anat 2009; 31:158-159.
 Quain R. Anatomy of the arteries of the human body. London: Taylor and Wolton, 1844326-337.
 Muller E. Beitrage zur Morphologie des Gefasssystem. Die Armarterien des Menchen. Anat Hefte 190332: 377-575.
 McCormack LJ, Cauldwell EW, Anson BJ. Brachial and antebrachial arterial patterns: a study of 750 extremities. Surg Gynecol Obstet 1953; 96:43-45.
 Weathersby HT Anomalies of brachial and antebrachial arteries of surgical significance. South Med J 1956; 49:46-49.
 Rodriguez-Baeza A, Nebot J, Ferreira B, Reina F, Perez J, Sanudo JR, Roig M. An anatomical study and ontogenetic explanation of 23 cases with variations in the main patterns of the human brachio-antebrachial arteries. J Anat 1995; 187:473-479.
 Topol EJ, Teirstein PS. Textbook of Interventional Cardiology, 6th ed. Philadeplphia: Elsevier Saunders; 2011.
 Singer E. Embryological patterns persisting in the arteries of the arm. Anat Rec 1933; 55: 406-413.
 Jurjus AR, Correa-De-Aruaujo R, Bohn RC. Bilateral double axillary artery: embryological basis and clinical implications. Clin Anat 1999; 12:135-140.
 Karlsson S, Niechajev IA. Arterial anatomy of the upper extremity. Acta Radiol (Stockholm) 1982; 23: 115-121.
 Evans HM. The development of the vascular system. In; Keibe F, Mall FP (eds). Manual of human embryology. Vol. 2. Philadelphia: J.B. Lippincott; 1912; 570-709.
 Senior HD. A note on the development of the radial artery. Anat Rec 1926; 33:220-221.
 Maraspin LE. A report of an anomalous bifurcation of the right axillary artery in man. Vasc Surg 1971; 5:133-136.
Marek Konarik (1), David Kachlik (1,2) *, Vaclav Baca (1,2)
(1) Department of Anatomy, Third Faculty of Medicine, Charles University in Prague, Ruska 87, Praha 10, 100 00, Czech Republic. (2) Department of Health Care Studies, College of Polytechnics Jihlava, Tolsteho 16, Jihlava, 586 01, Czech Republic
* Corresponding author: David Kachlik, Department of Anatomy, Third Faculty of Medicine, Charles University in Prague, Ruska 87, Praha 10, 100 00, Czech Republic Tel: +420267102508 Fax: +420267102504 E-mail: firstname.lastname@example.org
Submitted: 15 February 2014 / Accepted: 03 August 2014
TABLE 1. Overview of the branching types of the PBA according to Adachi , combined with the PHCA passing under the fused tendons of the TM and LD. Type Origin of PHCA and PBA Number of cases D PBA originates from AA 5 times in 398 cases E PBA originates from PHCA (common 398 cases trunk) and then PBA bifurcates into medial and radial collateral artery F No regular PBA: Medial and radial 17 times in collateral artery originates 398 cases from PHCA G No regular PBA: Radial collateral 15 times in artery originates from PHCA and 398 cases medial collateral artery originates directly from AA/BA Type Origin of PHCA and PBA Frequency D PBA originates from AA 1.3% E PBA originates from PHCA (common 6.5% trunk) and then PBA bifurcates into medial and radial collateral artery F No regular PBA: Medial and radial 4.3% collateral artery originates from PHCA G No regular PBA: Radial collateral 3.8% artery originates from PHCA and medial collateral artery originates directly from AA/BA TABLE 2. List of studies reporting on the PHCA passing under the tendons of the TM and LD Author Total Number of Frequency limbs cases Adachi (1928)  398 63 15.8% Coulouma (1934)  284 8 2.8% Skopakoff (1959)  610 69 11.3% Keen (1961)  104 3 2.9% Olinger (2010)  166 14 8.4 Kachlik (2009)  130 11 8.8% Konarik (2014) 214 23 10.7% TABLE 3. Classification of BrA (and SBrA) according to its origin  Group Location Frequency 1 Distal third of brachial artery 3.9% 2 Middle third of brachial artery 7.7% 3 Proximal third of brachial artery 65.4% 4 Infrapectoral (distal) part 23% of axillary artery TABLE 4. The origin site and incidence of the SBrA and BrA as a whole Author Number Total Origin of cases frequency from AA Quain (1844)  429 30% * -- Muller (1903)  300 25.8% * -- Adachi (1928)  1198 31% * -- McCormack (1953)  750 15% * -- Wheatersby (1956)  408 15.6% -- Rodriguez-Baeza (1995)  150 16.7% * -- Skopakoff (1959)  610 19.7% * 9% Keen (1961)  284 12.3% * 5.9% Rodriguez-Niedefuehr 384 13.8% * 3.25% (2001)  Kachlik (2009)  130 (#) 1.25% Konarik (2014) 214 14.5% 2.33% * Most of the authors do not distinguish between the origin site of the SBrA or BrA, (#) The brachial artery was not a part of research; data were beyond our study outlines
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|Author:||Konarik, Marek; Kachlik, David; Baca, Vaclav|
|Publication:||Bosnian Journal of Basic Medical Sciences|
|Date:||Nov 1, 2014|
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