Keywords
Brachial plexus - Brachial artery - Cephalic vein
Background
Anatomy of brachial plexus and axillary artery (AA) is complicated, subjected to a
wide variety of variations and of major importance for many pathological and surgical
conditions. Embryologic explanation of its development is difficult. Clinical sequelae
of variations in the area are often unpredictable but of major importance. Many authors
[[1],[2],[3]
[4]] have studied and provided analytical descriptions of Brachial Plexus, AA and their
relationship.
In this study an unusual combination of arterial, venous and neural variations concerning
axillary and brachial region is described. Variations are analyzed both separately
and as a pattern and examined in the light of their clinical and embryological significance.
Classification with reference to widely used classification systems of the area is
also attempted. Literature is briefly reviewed and anatomical, embryological and clinical
questions raised are discussed.
Case presentation
During dissection of the neck, right axillary and brachial region of a male cadaver
at the Laboratory of Anatomy, Faculty of Medicine, National and Kapodistrian University
of Athens, Greece an unusual combination of arterial, venous and neural variations
was identified. Primary dissection was performed by undergraduate students and further
dissection by authors. Variations were described, photographed and measured.
Brachial plexus took origin from C5-T1 roots. No contribution of C4 or T2 roots was
encountered. The C5 and C6 roots united in an unusually short Upper Trunk (UT) which
immediately divided into its anterior division (AD [UT]) and posterior division (PD
[UT]). Suprascapular nerve took origin from UT. The C7 root continued typically as
Medial Trunk (MT) and divided into its anterior (AD [MT]) and posterior division (PD
[MT]). The C8 root divided into anterior and posterior divisions (PD [C8]) before
uniting with T1 root. Anterior division of C8 root united with T1 root and together
formed Inferior Trunk (IT). The AD [UT] and AD [MT] did not unite thus no Lateral
Cord (LC) was formed. The AD [UT] divided into Musculocutaneous Nerve (MCN) and lateral
root of median nerve (LR [MN]). The AD [MT] gave off lateral pectoral nerve and then
united with LR [MN]. The IT, which since C8 root had divided before union with T1
is also AD [IT], continued into medial cord as usually described and later divided
into medial root of median nerve (MR [MN]) and Ulnar Nerve (UN). Medial Brachial Cutaneous
Nerve (MBCN) was one of its branches. The PD [C8] united with PD [MT] and these two
united later with PD [UT] so to form posterior cord (PC). The MCN was formed by AD
[UT] and thus did not contain C7 fibers while Median Nerve (MN) and UN were formed
as usual. The PC did not contain T1 fibers. After this level, nerves continued their
course and distribution normally in humerus, forearm and hand. No other variations
of the branches of the brachial plexus were encountered.
Transverse cervical artery passed above all branches of the brachial plexus. Suprascapular
and deep scapular artery passed between AD [UT] and MT. No other variations concerning
neural elements of humeral, axillary and neck region were encountered.
The AA at the level of the union of the two root of the MN, also known as ansa medianis,
divided into two branches. Superior Thoracic Artery (STA) occurred and coursed normally.
Pectoral artery of Thoracoacromial Artery (PA [TA]) occurred before the division.
After the division, two branches occurred, one that continued as AA and another that
passed superficial to Ansa Medianis. The AA gave off the other branches of Thoracoacromial
Artery (TA), namely clavicular, deltoid and acromial and also Subscapular artery (SuCA)
that later trifurcated into lateral thoracic artery (LTA), Circumflex Scapular Artery
(CSA) and Thoracodorsal Artery (TDA). Then it gave origin to Anterior Circumflex Humeral
Artery (ACHA), Posterior Circumflex Humeral Artery (PCHA) and ended as deep brachial
artery (dBA). The other branch continued superficial to MR [MN], then in front of
MN and finally reached the normal position and course of Brachial Artery at about
the middle of the humerus. Taking in consideration its origin, course and branches
we considered it a Superficial Brachial Artery (SBA). Immediately after SBA’s branching
point, it gave a small branch that coursed towards inferior surface of pectoralis
major muscle and thus corresponded to inferior pectoral artery (IPA). Apart from that
it gave origin to only muscular branches and bifurcated into Radial and Ulnar Artery.
A highly diagrammatic presentation of typical anatomy is provided at [Figure 1] and that of the variation is illustrated at [Figure 1] while a photo at [Figure 2]. No other variations concerning arterial system were encountered at axillary, branchial
and forearm region.
Figure 1 Schematic representation of brachial plexus and artery in normal and variant
form. UT: Upper trunk; MT: Medial Trunk; IT: Inferior Trunk, AD [UT]: Anterior division
of Upper Trunk; AD [MT]: Anterior division of Middle Trunk; AD [IT]: Anterior division
of Inferior Trunk; PD [UT]: Posterior division of Upper Trunk; PD [MT]: Posterior
division of Middle Trunk; PD [IT]: Posterior division of Inferior Trunk; PD [C8]:
Posterior division of C8; MC Medial Cord; PC: Posterior cord; MR [MN]: Middle root
of median nerve; LR [MN]: Lateral root of median nerve; MCN: Musculocutaneous Nerve;
MN: Median Nerve; UN: Ulnar Nerve; RN: Radial Nerve; AN: Axillary Nerve; SCN: Suprascapular
Nerve; MBCN: Medial Brachial Cutaneous Nerve; LPN: Lateral pectoral nerve; MPN: Medial
Pectoral Nerve; SA: Subclavian Artery; AA: Axillary Artery; SBA: Superficial Brachial
Artery; dBA: Deep Brachial Artery; DSC: Deep Scapular Artery; SCA: SupraScapural Artery;
STA: Superior Thoracic Artery; TA: Thoracoacromial Artery; CA: Clavicular Artery;
DA: Deltoid Artery; AcA: Acromial Artery; SuSA: SubScapular Artery; LTA: Lateral Thoracic
Artery; TDA: Thoracodorsal Artery; CSA: Circumflex Scapular Artery; ACHA: Anterior
Circumflex Humeral Artery; PCHA: Posterior Circumflex Humeral Artery; IPA: Inferior
Pectoral Artery.
Figure 2 Cadaveric photo of variation of brachial plexus and axillary artery variations. UT: Upper trunk; MT: Medial Trunk; IT: Inferior Trunk; AD [UT]: Anterior division
of Upper Trunk; AD [MT]: Anterior division of Middle Trunk; AD [IT]: Anterior division
of Inferior Trunk; PD [UT]: Posterior division of Upper Trunk; PD [MT]: Posterior
division of Middle Trunk; PD [C8]: Posterior division of C8; MC: Medial Cord; PC:
Posterior cord; MR [MN]: Middle root of median nerve; LR [MN: Lateral root of median
nerve; MCN: Musculocutaneous Nerve; MN: Median Nerve; UN: Ulnar Nerve; RN: Radial
Nerve; AN: Axillary Nerve; SCN: Suprascapular Nerve; MBCN: Medial Brachial Cutaneous
Nerve; LPN: Lateral pectoral nerve; MPN: Medial Pectoral Nerve; SA: Subclavian Artery;
SCA: Suprascapular Artery; DSC: Deep Scapular Artery; AA: Axillary Artery; SBA: Superficial
Brachial Artery; dBA: Deep Brachial Artery; DSC: Deep Scapular Artery; TCA: Transverse
Cervical Artery; STA: Superior Thoracic Artery; TA: Thoracoacromial Artery; PA [TA]
Pectoral Branch of Thoracoacromial Artery; SuSA: Subscapular Artery; LTA: Lateral
Thoracic Artery; TDA: Thoracodorsal Artery; CSA: Circumflex Scapular Artery; IPA:
Inferior Pectoral Artery; ACHA: Anterior Circumflex Humeral Artery; PCHA: Posterior
Circumflex Humeral Artery.
The Cehpalic Vein (CV) was absent. Superficial radial surface of the forearm and brachial
region was drained by two veins that had oblique course, upwards and downwards respectively,
and ended as branches of the basilica vein ([Figure 3]).
Figure 3 Cadaveric photo of cephalic vein abscence. BV: Basilic Vein; MCV: Middle cubital vein; OV (F): Oblique vein draining forearm;
OV (H): Oblique vein draining humeral region.
Some of these variations have already been described separately. However, to the best
of our knowledge, there has never been described such a combination of arterial and
neural variations, not to mention the absence of the CV.
Discussion
Variations in brachial plexus formation are common and complicated. Their frequency
reaches 54% and their degree of complexity is such that makes every systematization
effort very difficult [[5]]. In 1918 Kerr [[1]] in an attempt to classify brachial plexus variations organized them in 3 groups
and 7 subgroups with respect to contribution of C4 and T2 root (groups) and participation
of roots in the formation of cords (subgroups). Taking in consideration these characteristics,
pattern described here corresponds to type E, i.e. contribution of C5, C6, C7, C8
and T1 roots with LC “formed” from C5, C6 and C7 root and medial cord from C8 and
T1 roots. (29.14%). He also described the frequency of certain variations in brachial
plexus. Extending further his investigation, he described a number of rare variations
corresponding to brachial plexus elements arrangement and described 29 interesting
and difficult to classify cases. According to Kerr non - formation of LC has a frequency
of 3%. The C8 root dividing before uniting with T1 root has a frequency of 3.5% and
union of posterior division of Inferior Trunk and PD [MT] before union with PD [UT]
accounts for 14%. The latter two variations are combined in only 1 case in Kerr’s
research. Taking in consideration all 3 cases, our case does not correspond precisely
to any of Kerr’s cases, not accounting arterial and venous variations. Other authors
[[6]] agree that non formation of LC accounts for 3%. Various researchers investigated
morphometry of brachial plexus. Significance of such measurements is difficult to
evaluate due to arrangement of connective and neural tissue [[1]] and of uncertain clinical importance.
Precise embryologic explanation of brachial plexus variations is not fully understood.
It is known that embryonic somites, carrying their innervation, migrate to the limbs
and Brachial Plexus is formed latter. In fetal life brachial plexus appears as a radicular
cone that latter divides into ventral and dorsal branches [[7]]. Formation of brachial plexus is interconnected with axillary artery formation
and variations between them coexist and interfere, as in our case. Variations of brachial
plexus and axillary artery coexist in at least 8% of the cases. Occurrence of axillary
artery from 6th or 8th intersegmental artery or variations in its branches is of importance
for brachial plexus final form although the exact way remains obscure [[2]].
Functional significance of brachial plexus variations is not known either. Taking
in consideration its embryologic formation, especially the fact that innervation of
somites by neurotomes is established before formation of brachial plexus they might
are not always important. In our case the only evident change is lack of C7 root innervation
at MCN and lack of T1 root innervation at PC. Brachial plexus is formed by an extremely
large number of fascicles that combine and recombine as we proceed more distal. Analysis
at microscopic level has proved that C7 contribution at MCN and T1 at PC is minimal
or absent. However variations of brachial plexus, even if they do not alter terminal
nerves, can be useful in explaining various neuropathies or neurological deficits
[[4],[5],[7]]. It has been stated that a number of variations of UT in its formation pattern,
course and relative position to anterior scalene muscle might predispose to appearance
of thoracic outlet syndrome [[8]].
Occurrence of arteries near or between elements of brachial plexus is high reaching
23% [[9]]. In our case an interesting combination of upper limb’s variations was observed.
First the existence of SBA as a branch of AA was observed, giving off as only branch
the IPA Also the LTA originated from SuCA. Last but not least the TA was absent and
its branches arose directly from the second part of the axillary artery. The most
frequent anatomic variations of the axillary artery are the persistent SBA, high division
of the brachial artery, radial artery and ulnar artery [[10],[11],[12],[13]]. SBA is a common variation. Lippert and Pabst calculate it at about 22% but especially
the SBA deriving from the AA only at 4% [[14]]. As for the LTA originating with the SuSA artery it is also a quite common variation
accounting for 10% [[14]]. Kodama’s study noticed a frequency of IPA originating from SBA approximately at
8,7%. Whenever or not the SBA is combined with the IPA existence, it is noteworthy
that the latter artery never happens to ramify from typical brachial artery which
lies deep to the median nerve. Same mechanisms that induce its existence might also
induce SBA’s existence. Moreover he suggested that the IPA might be a derivative of
or a trigger for SBA morphogenesis [[15]]. Finally, absent TA and origin of its branches directly from the AA is described
with a frequency of about 11.25% [[16]].
When mentioning the upper limb, in particular the vascular system and its variations,
it is necessary to discuss the embryology of the region. Originally the Subclavian
Artery (SA) extends to the wrist, where it terminates by dividing into terminal branches
for the fingers, later becoming interosseous and median artery. In embryos 21 mm long
the SBA develops in the axillary region and traverses the medial surface of the arm
ending to the posterior surface of the wrist. When the embryo reaches the length of
about 23 mm, the median artery undergoes retrogression, becoming a small, slender structure.
The SBA is a consistent embryonic vessel that plays an important role in the normal
arterial morphogenesis of the upper limb. At the elbow, an anastomotic branch between
the brachial artery and the SBA becomes enlarged sufficiently to form the distal portion
of the latter, the radial artery. Radial artery soon becomes a major artery of the
forearm while the proximal portion of the SBA atrophies correspondingly.
Every vascular variation can be traced back to an embryological origin. Jurjus [[10]] mentioned six explanations for the variations observed:
-
The choice of unusual paths in the primitive vascular plexus.
-
The persistence of vessels which are normally obliterated.
-
The disappearance of vessels which are normally retained.
-
An incomplete development.
-
The fusion and absorption of parts which are normally distinct.
-
A combination of factors leading to an atypical pattern normally encountered.
Superficial surface of the forearm is drained by CV and basilica vein, united by median
cubital vein. The CV ascends in front of the elbow superficial to a groove between
the brachioradialis and biceps, crosses superficial to the lateral cutaneous nerve
of the forearm, ascends lateral to biceps and between pectoralis major and deltoid,
where it adjoins the deltoid branch of the TA. Entering the infraclavicular fossa
it passes behind the clavicular head of pectoralis major, it pierces the clavipectoral
fascia, crosses the AA and joins the axillary vein just below clavicular level. It
may connect with the external jugular vein by a branch crossing anterior to the clavicle
[[14],[17]].
Numerous variations in the course and terminal drainage of the cephalic vein have
been described including persistence of the jugulocephalic vein [[18]], absence of cephalic vein [[19],[20],[21],[22],[23]], cephalic vein draining into the external or internal jugular vein, cephalic vein
draining into the subclavian vein or into the junction of subclavian and internal
jugular vein, cephalic vein draining into the basilic vein [[24]] and accessory cephalic vein [[25]]. Concerning frequency of the absence of the cephalic vein, Loukas et al. [[19]] report 5% Le Saout et al. [[20]] report 19.7%, De Rosa [[21]] et al. report 5.3% and Yeri L.A. et al. [[22]] report 8.2%.
During embryonic life principle arm vein remains in caudal or ulnar positions and
joins the lateral thoracic (thoracoepigastric) vein to form the primitive subclavian
trunk. A small cranial tributary of this trunk develops into a primitive cephalic
vein and follows the radial border of the arm, becoming continuous with the ulnar
vein by way of the marginal vein outlining the hand plate. The proximal end of this
new vein, namely the cephalic vein, curves cranially around the superficial aspect
of the primordium of the clavicle. This arched part of the vessel has been called
the jugulocephalic vein [[18]]. Sometimes the median cubital vein is large, transferring most blood from the cephalic
to the basilica vein; the proximal cephalic vein is then absent- as in our case- or
much diminished [[26]].
The clinical importance of the described axillary variation is of utmost significance
for surgeons, cardiologists and vascular specialists but also for diagnostic reasons.
It is specially relevant in cases of arteriovenous fistulae, aneurysms and abscesses
drainage in region of axilla, arm and cubital fossa [[27]]. In angiographic studies preceding coronary artery bypass surgery such aberrant
anatomy should be timely confirmed to reduce the incidence of iatrogenic injuries.
An abnormal SBA as in this case may be mistaken for basilic vein during cannulation
[[28],[29]]. If certain drugs are injected into these vessels, the result might be disastrous:
gangrene with subsequent partial or total loss of the hand [[28]]. Axillary and brachial artery variations are relevant in shoulder, arm and forearm
surgery, in fractures and dislocations. What is more, diagnostically this type of
variation may disturb the evaluation of angiographic images. Awareness of such abnormal
axillary vasculature is crucial in use of superficial brachial artery flap in plastic
surgery and protection of axillary artery in breast cancer surgery. Finally, accurate
knowledge of the relationships and course of these major arterial conduits, and particularly
of their variation patterns, is of considerable practical importance in the conduct
of reparative surgery in the arm, forearm, and hand. Otherwise, less critical knowledge
of anatomy might lead to hazards in surgery of the upper extremity [[30]].
Central venous access via the upper extremity veins is used in various procedures
because it is easy to perform, convenient for the patients and has low complications
rate. The relatively low mobility of the central veins of the upper extremity and
the neck also affords low mechanical stress on the indwelling hardware. The cephalic
vein cutdown is reported to has low complication rates particularly when compared
with subclavian vein cannulation. Also cephalic vein cutdown poses no risk of pneumothorax.
This technique is widely used for the placement of pacing and defibrillation leads
and chronic indwelling venous catheters. It is obvious that the absence of the cephalic
vein would obviate the need for an approach through a more proximal vein (axillary,
subclavian) to obtain central venous access, a technique that entails comperatively
increased morbidity rates. [[31]] Currently there are neither simple diagnostic techniques for the location of such
persons nor specific indications for the use of more sophisticated ones (eg, phlebography)
thus a high rate of clinical suspicion is necessary in case of intervention need in
cephalic vein area.
Conclusions
Deep knowledge of anatomy of Brachial Plexus is necessary for an extremely large number
of procedures including direct trauma, fractures, obstetrical wounds and a wide variety
of neuropathies. Methods of preoperative evaluation of brachial plexus include electromyography,
somatosensory evoked potentials myelography, computerized tomography, myelo Computerized
Tomography, magnetic resonance imaging, and magnetic resonance neurography. Profound
knowledge is also necessary for success of regional anaesthesia with ultrasound guidance
[[9]] Although not all variations can be encountered, knowledge of the possibility of
their existence raised a high level of suspicion that helps neurologists, orthopaedic
surgeons, surgeons and neurosurgeons avoid unnecessary mistakes and thus provide best
possible care and ensure patients’ interests.
Consent
Since this is a cadaveric study, no special consent form is necessary.
Abbreviations
AD [UT]:
Anterior division of upper trunk
AD [MT]:
Anterior division of middle trunk
AD [IT]:
Anterior division of inferior trunk
PD [UT]:
Posterior division of upper trunk
PD [MT]:
Posterior division of middle trunk
PD [IT]:
Posterior division of inferior trunk
PD [C8]:
Posterior division of C8
MR [MN]:
Middle root of median nerve
LR [MN]:
Lateral root of median nerve
MCN:
Musculocutaneous nerve
MBCN:
Medial brachial cutaneous nerve
LPN:
Lateral pectoral nerve
MPN:
Medial pectoral nerve
SBA:
Superficial brachial artery
dBA:
deep brachial artery
DSC:
Deep scapular artery
SCA:
SupraScapural artery
STA:
Superior thoracic artery
TA:
Thoracoacromial artery
LTA:
Lateral thoracic artery
TDA:
Thoracodorsal artery
CSA:
Circumflex scapular artery
ACHA:
Anterior circumflex humeral artery
PCHA:
Posterior circumflex humeral artery
IPA:
Inferior pectoral artery
OV (F):
Oblique vein draining forearm
OV (H):
Oblique vein draining humeral region
Competing interests
The authors declare that they have no competing interests.
Authors’ contribution
TT had the study concept and design. AM participated in dissection, analysis and interpretation
of data. VM participated in dissection, analysis and interpretation of data. DV participated
in dissection, analysis and interpretation of data. EOJ participated in drafting of
the manuscript. PS had the Critical revision of the manuscript for important intellectual
content. All authors’ read and approved the final manuscript.
Cite this article as: Troupis et al.: Report of an unusual combination of arterial, venous and neural variations in a
cadaveric upper limb. Journal of Brachial Plexus and Peripheral Nerve Injury 2014 9:2.
