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SHOULDER
Distribution of the axillary nerve to the subacromial bursa
and the area around the long head of the biceps tendon
H. Nasu •A. Nimura •K. Yamaguchi •
K. Akita
Received: 2 December 2013 / Accepted: 29 May 2014
ÓSpringer-Verlag Berlin Heidelberg 2014
Abstract
Purpose Patients with a shoulder disorder often complain
of pain on the anterior or lateral aspect of the shoulder.
Such pain has been thought to originate from the supra-
scapular nerve. However, taking into consideration the
distinctive course of the axillary nerve, the axillary nerve is
likely to supply branches to the structure around the
shoulder joint. This study was conducted to clarify the
division, course, and distribution of the branches which
originate from the axillary nerve and innervate structures
around the shoulder joint.
Methods The division, course, and distribution of the
branches which originate from the axillary nerve and
innervate structures around the shoulder joint were exam-
ined macroscopically by dissecting 20 shoulders of 10
adult Japanese cadavers.
Results The thin branches from the anterior branch of the
axillary nerve were distributed to the subacromial bursa
and the area around the long head of the biceps tendon. The
branches from the main trunk of the axillary nerve or the
branch to the teres minor muscle were distributed to the
infero-posterior part of the shoulder joint.
Conclusion The pain on the anterior or lateral aspect of
the shoulder, which has been thought to originate from the
suprascapular nerve, might be related to the thin branches
which originate from the axillary nerve and innervate the
subacromial bursa and the area around the long head of the
biceps tendon.
Clinical relevance These results would be useful to
consider the cause of the shoulder pain or to prevent the
residual pain after the biceps tenodesis.
Keywords Axillary nerve Subacromial bursa
Long head of the biceps Capsule Distribution
Macroscopic anatomy
Introduction
Patients with a shoulder disorder often complain of pain on
the lateral aspect of the shoulder. Such lateral shoulder pain
has been proposed to originate from some lesions on the
subacromial bursa, rotator cuff, or capsule [18,19]; it is
considered as a referred pain. However, the mechanism
how the lateral shoulder pain is referred to the lesions has
not been elucidated. Further, the division and courses of
nerve fibres that are distributed to the lateral aspect of the
shoulder have not been clarified.
Some patients also complain of pain on the anterior
aspect of the shoulder. The anterior shoulder pain is usually
caused by a lesion of the long head of the biceps tendon
[16,24,30]. Recently, the origin of the pain has been
considered to be due to biochemical substances interacting
with nociceptors in and around the tendon. Therefore, the
sympathetic innervation of the long head of the biceps
tendon has been investigated histochemically [2,13,25].
However, the manner of division and course of nerve fibres
innervating the structures around the long head of the
biceps tendon have not been clarified macroscopically.
The suprascapular nerve provides sensory fibres to 70 %
of the shoulder joint [21]. The suprascapular nerve is typ-
ically distributed to the posterior shoulder joint capsule,
coracoclavicular ligament, coracohumeral ligament,
H. Nasu A. Nimura K. Yamaguchi K. Akita (&)
Department of Clinical Anatomy, Graduate School of Medical
and Dental Sciences, Tokyo Medical and Dental University,
1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8510, Japan
e-mail: akita.fana@tmd.ac.jp
123
Knee Surg Sports Traumatol Arthrosc
DOI 10.1007/s00167-014-3112-4
subacromial bursa, and acromioclavicular joint capsule [3].
Therefore, lateral or anterior shoulder pains have been
thought to mainly originate from the suprascapular nerve.
The axillary nerve extends to the lateral and anterior
aspect of the shoulder, and has the distinctive characteristic
of surrounding the humerus from posterior to anterior. It
originates from the posterior cord of the brachial plexus,
divides into the anterior branch and the posterior branch,
and is distributed to the deltoid muscle, teres minor muscle,
and the skin on the posterolateral aspect of the shoulder [1,
4,8,14,26]. The axillary nerve also has an articular
branch. The articular branch arises from the origin of the
axillary nerve and enters the inferior part of the shoulder
joint capsule [10,29]. With regard to surgical exposure,
innervation patterns of the axillary nerve to the inferior
joint capsule have been discussed in depth [3,9]. However,
taking into consideration the course of the axillary nerve,
we hypothesized that it has the potential to supply other
branches to the humerus or structures around the shoulder
joint. This was a new viewpoint on branches of the axillary
nerve. The presence of these branches might provide
insight into the correct diagnosis of the pain on the lateral
or anterior aspects of the shoulder.
The aim of this study was to clarify the division, course, and
distribution of the branches which originate from the axillary
nerve and innervate structures around the shoulder joint.
Materials and methods
All of the cadavers used in this study were donated to
Tokyo Medical and Dental University. Before death, all of
the donors had voluntarily expressed their will of donating
their own body for anatomical education and study. This
system is established in Act on Body Donation for Medical
and Dental Education in Japan. Our study completely
complied with the law.
A total of 20 shoulders of 10 adult Japanese cadavers (eight
male and two female cadavers) were dissected in this study.
The age range was 70–91-year old (average age: 82-year old).
Cadavers were fixed in 8 % formaldehyde and preserved in
30 % ethanol. This study was conducted under a stereomi-
croscope (magnification: 129, Operation Microscope
OLYMPUS OME-1000, Olympus Optical, Tokyo). Findings
were recorded by drawings and photographs in each case.
First, the brachial plexuses in the neck and muscles around
the shoulder joint were identified. The anterior part of the
deltoid muscle, which originated from the clavicle, was
dissected from the clavicle and carefully reflected laterally.
Then, the pectoralis major muscle, the trapezius muscle, the
pectoralis minor muscle, the coracobrachialis muscle, the
short head of the biceps brachii muscle, the latissimus dorsi
muscle, the teres major muscle, and the long head of the
triceps brachii muscle were removed. The clavicle was cut at
the middle third. The posterior cord of the brachial plexus
was identified, and the origin of the axillary nerve was
exposed. Then, the branches of the axillary nerve were
identified as follows: the branch to the posterior part of the
deltoid muscle, the branch to the teres minor muscle, the
superior lateral brachial cutaneous nerve, the articular
branch, and the anterior branch which was usually distrib-
uted to the middle and anterior part of the deltoid muscle. The
branching pattern of the axillary nerve was examined.
Second, a thin branch from the anterior branch of the
axillary nerve was identified, while the connective tissue
was removed between the reflected anterior part of the
deltoid muscle and the humerus. An identified thin branch
was pursued to both the origin of the anterior branch and
the distributed area. The origin, course, and distribution of
the thin branch were investigated. In addition, the origin,
course, and distribution of the articular branch, which
originated from a main trunk of the axillary nerve or a
branch to teres minor, were also examined.
The distribution of the thin branch was categorized into
three areas: the subacromial bursa, the connective tissue
around the long head of the biceps tendon, and the int-
ertubercular sulcus. The number of shoulders in which the
thin branch was distributed to each area was counted and
summarized in a table. In the same manner, the distribution
of the articular branch was also categorized into three
areas: the inferior capsule, the posterior capsule, and the
long head of the triceps tendon. The number of shoulders in
which the articular branch was distributed to each area was
counted and summarized in a table.
Results
The axillary nerve bifurcated into an anterior branch and a
posterior branch at the infero-lateral part of the subscapu-
laris muscle. The anterior branch went around the humerus
from posterior to anterior and gave off numerous branches
which supplied to the middle and anterior parts of the
deltoid muscle. The posterior branch trifurcated into the
branch to the teres minor muscle, the branch to the pos-
terior part of the deltoid muscle, and the superior lateral
brachial cutaneous nerve in the quadrilateral space (Fig. 1).
In addition to these muscular or cutaneous branches, the
axillary nerve divided into some branches which were
distributed to the following structures around the shoulder
joint in all specimens.
Distribution to the subacromial bursa
In 12 of 20 shoulders, the anterior branch gave off a thin
branch to the subacromial bursa (Fig. 2). As the anterior
Knee Surg Sports Traumatol Arthrosc
123
branch ran through the middle part of the deltoid muscle, it
gave off the thin branch. This thin branch ran in the
direction towards the humerus rather than entering the
deltoid muscle. It ascended on the surface of the humerus,
pierced a thin fascia, and was distributed to the
subacromial bursa on the lateral or anterolateral aspect of
the shoulder.
Distribution around the long head of the biceps
In 8 of 20 shoulders, a thin branch originated from the
anterior branch and was distributed around the long head of
the biceps tendon. The thin branch bifurcated into an
ascending twig and a descending twig along the lateral
border of the long head of the biceps tendon. It was dis-
tributed to the connective tissue of the long head of the
biceps tendon such as the tendon sheath or the transverse
humeral ligament (Fig. 3a, b). In 3 out of 8 shoulders, the
thin branch ascended and pierced the cortical bone of the
humerus at the superolateral portion of the intertubercular
sulcus (Fig. 3c, d).
Distribution around the infero-posterior part
of the shoulder joint
In 16 of 20 shoulders, a branch was distributed to the
inferior part of the joint capsule. In 15 shoulders, it origi-
nated from the main trunk of the axillary nerve on the
surface of the subscapularis muscle (Fig. 4a). In one
specimen, it originated from the branch to the teres minor
muscle.
In three shoulders, a branch innervated the posterior part
of the joint capsule in addition to the inferior part. The
branch was given off by the branch of the teres minor
muscle, ascended beneath the teres minor muscle, and
entered the posterior part of the joint capsule (Fig. 4b).
In another three shoulders, the branch also supplied to the
posterolateral aspect of the long head of the triceps tendon
(Fig. 4c). It originated from the branch to the teres minor
muscle, passed along the lateral border of the long head of
the triceps tendon, and entered its the posterolateral aspect.
In the dissection series of the current study, the distri-
bution patterns of all specimens to the areas described
above are summarized in Table 1.
Discussion
The most important finding of the present study was that
the anterior branch of the axillary nerve was distributed to
the subacromial bursa, the connective tissue around the
long head of the biceps tendon, and the cortical bone of the
humerus at the superolateral portion of the intertubercular
sulcus. This result supports our hypothesis that the axillary
nerve has branches to the humerus or the structures around
the shoulder joint.
Some histochemical studies on the subacromial bursa
showed that the subacromial bursa had more free nerve
Fig. 1 Overall view of the division of the axillary nerve in an anterior
view of the right shoulder. The deltoid muscle (DEL) is detached and
reflected laterally. The axillary nerve (Ax) bifurcated into the anterior
branch (Ant) and the posterior branch (Pos) at the infero-lateral part of
the subscapularis muscle (SSC). The anterior branch ran anterior-
wards from behind the humerus and supplied branches to the anterior
and middle parts of DEL. The posterior branch trifurcated into the
branch to the teres minor muscle (black circle), the branch to the
posterior part of the deltoid muscle (black triangle), and the superior
lateral brachial cutaneous nerve (black square)
Fig. 2 Distribution to the subacromial bursa. The region surrounded
by the white outline in the anterolateral view of the left shoulder is
magnified. The deltoid muscle (DEL) is reflected laterally. The
anterior branch (black arrow) gave off a thin branch (open
arrowhead) to supply the subacromial bursa (SAB)
Knee Surg Sports Traumatol Arthrosc
123
endings than proprioceptors [12,17,23]. These sensory
branches have been considered to come from the supra-
scapular nerve [3,6,27]. However, we found that the
axillary nerve was distributed to the subacromial bursa.
This result suggests that the axillary nerve is involved with
sensation in the subacromial bursa, like the suprascapular
nerve. Further, the distribution area of the axillary nerve in
the subacromial bursa was located on the lateral or anter-
olateral aspect of the shoulder. We suppose that the pain of
the lateral aspect of shoulder from the subacromial bursitis
might originate from both the suprascapular nerve and the
axillary nerve.
Alpantaki et al. [2] showed that the sensory and sym-
pathetic fibres innervating the long head of the biceps
tendon were distributed to its origin predominantly. How-
ever, we observed that the axillary nerve was widely dis-
tributed to the connective tissue around the long head of the
biceps tendon. Rauber [20] and Wrete [29] also showed
that a branch of the axillary nerve was distributed around
the long head of the biceps tendon. The branch, which
originated from the main trunk of the axillary nerve, passed
deep to the long head of the biceps tendon from the medial
side to the lateral side. In the present study, we observed
that the branch originated from the anterior branch and ran
along the lateral side of the long head of the biceps tendon.
This is a new finding about the distribution of the axillary
nerve in a macroscopic study. As a clinical relevance, the
wide distribution of the axillary nerve might contribute to
the anterior shoulder pain with a lesion of the long head of
the biceps tendon.
Additionally, we observed that the branch from the
anterior branch of the axillary nerve pierced the cortical
bone of the humerus at the superolateral portion of the
intertubercular sulcus. Many studies have reported cases of
the persistent post-operative pain after biceps tenodesis [5,
7,11,16,28]. In particular, the proximal fixation led to
more persistent post-operative pain at the intertubercular
sulcus than the distal fixation [15,22]. The proximal part
might correspond to the area in which the branch pierced
into the cortical bone. We suppose that the branch could be
Fig. 3 Distribution around the
long head of the biceps tendon.
The region surrounded by the
white outline in the anterolateral
view of the right shoulder is
magnified. The deltoid muscle
(DEL) is reflected laterally. aA
thin branch (open arrowhead)
originated from the anterior
branch and ascended or
descended along the lateral
border of the long head of the
biceps tendon (asterisk). The
thin branch was distributed to
the connective tissue around the
long head of the biceps tendon
such as the tendon sheath
(circles) or the transverse
humeral ligament (star).
bIllustration of the findings of
a.cThe transverse ligament
was cut and opened bilaterally
(stars) at the approach point of
the long head of the biceps
tendon (asterisk) to the
intertubercular sulcus. The thin
branch originated from the
anterior branch and ascended to
pierce the cortical bone of the
humerus at the superolateral
portion of the intertubercular
sulcus (circles). dIllustration of
the findings of c
Knee Surg Sports Traumatol Arthrosc
123
related to the residual pain after the biceps tenodesis, and
knowledge about the course and distribution of the branch
might be helpful for the prevention of the residual pain.
Although the main nerve distributed to the posterior part
of the joint capsule was the suprascapular nerve, Aszmann
et al. [3] reported that a small branch from the branch to the
Fig. 4 Distribution around the infero-posterior part of the shoulder
joint. The region surrounded by white outline in each view is
magnified. aInferior view of the right shoulder is shown. The main
trunk of the axillary nerve (arrow) gave off a branch (open
arrowheads) which supplied the inferior part of the joint capsule
(star). bPosterior view of the right shoulder is shown. The teres
minor muscle (TMI) and the infraspinatus muscle (ISP) were detached
from the scapula and reflected laterally. The long head of the triceps
tendon was cut at its insertion (asterisk). A branch (open arrowheads)
that was gave off by the branch to the teres minor muscle (black
arrowhead) was distributed to the posterior part of the joint capsule
(star). cPosterior view of the left shoulder is shown. TMI was
reflected laterally. The long head of the triceps tendon was cut at its
insertion (asterisk). A thin branch (open arrowheads) that originated
from the branch to the teres minor muscle (black arrowhead) was
distributed to the long head of the triceps tendon. Ant anterior branch,
SSC subscapularis muscle
Table 1 Distribution areas of the branch from the axillary nerve and the number of shoulders in which the branch was observed
From anterior branch From main trunk of axillary nerve or branch to teres
minor muscle
Subacromial bursa Area around LHB Intertubercular sulcus Inferior capsule Posterior capsule LHT
Number of shoulders 12 8 3 16 3 3
LHB long head of the biceps tendon, LHT long head of the triceps tendon
Knee Surg Sports Traumatol Arthrosc
123
teres minor muscle entered the long head of the triceps
tendon and the adjacent capsule in 28 %. We also found
that a branch from the branch to the teres minor muscle was
distributed to the posterior part of the joint capsule or the
long head of the triceps tendon in 30 %. This finding was
consistent with the result reported by Aszmann et al. [3].
Gardner [10] proposed that if one articular branch did not
exist, other articular branches would develop. We also
speculate that the axillary nerve, in addition to the supra-
scapular nerve, might play dominant roles in innervation of
structures around the shoulder joint and that the supra-
scapular and the axillary nerve could compensate for each
other for lack of distribution area.
This study is limited by the fact that it analysed only a
macroscopic approach. Although we have mainly dis-
cussed the pain based on the past histochemical studies, a
histochemical study is necessary to demonstrate which
receptors are present in the terminal of the thin branches
from the axillary nerve. In addition, we investigated only
the axillary nerve. If the thin branch from the axillary nerve
is poor or empty, other nerves will compensate for the
region. Further macroscopic study about other nerves is
necessary to show shoulder innervation in full detail.
Conclusion
The thin branches from the anterior branch of the axillary
nerve were distributed to the subacromial bursa and the
area around the long head of the biceps tendon. We con-
clude that the pain on the anterior or lateral aspect of the
shoulder, which has been considered to originate from the
suprascapular nerve, might be related to the thin branches
originating from the axillary nerve.
Acknowledgements This study was partly supported by a Grant-in-
Aid for Young Scientists (B) from the Ministry of Education, Culture,
Sports, Science and Technology (No. 90622556).
References
1. Aiyama S, Kihara S (1973) On the cutaneous branches of the
axillary nerve with special reference to their topographic relation
to the deltoid muscle. Hirosaki igaku 24:413–423 (in Japanese
with English abstract)
2. Alpantaki K, McLaughlin D, Karagogeos D, Hadjipavlou A,
Kontakis G (2005) Sympathetic and sensory neural elements in
the tendon of the long head of the biceps. J Bone Joint Surg Am
87:1580–1583
3. Aszmann OC, Dellon AL, Birely BT, McFarland EG (1996)
Innervation of the human shoulder joint and its implications for
surgery. Clin Orthop Relat Res 330:202–207
4. Ball CM, Steger T, Galatz LM, Yamaguchi K (2003) The pos-
terior branch of the axillary nerve: an anatomic study. J Bone
Joint Surg Am 85:1497–1501
5. Boileau P, Krishnan SG, Coste JS, Walch G (2002) Arthroscopic
biceps tenodesis: a new technique using bioabsorbable interfer-
ence screw fixation. Arthroscopy 8:1002–1012
6. Ebraheim Ebraheim NA, Whitehead JL, Alla SR, Moral MZ,
Castillo S, McCollough AL, Yeasting RA, Liu JNA (2011) The
suprascapular nerve and its articular branch to the acromiocla-
vicular joint: an anatomic study. J Shoulder Elbow Surg 20:13–17
7. Elser F, Braun S, Dewing CB, Giphart JE, Millett PJ (2011)
Anatomy, function, injuries, and treatment of the long head of the
biceps brachii tendon. Arthroscopy 27:581–591
8. Frohse F, Fra
¨nkel M (1908) M. deltoideus. Schultermuskeln. In:
Von Bardeleben K (ed) Die muskeln des menschlichen armes.
Gustav Fischer, Jena, pp 27–39
9. Gelber PE, Reina F, Monllau JC, Yema P, Rodriguez A, Caceres
E (2006) Innervation patterns of the inferior glenohumeral liga-
ment: anatomical and biomechanical relevance. Clin Anat
19:304–311
10. Gardner E (1948) The innervation of the shoulder joint. Anat Rec
102:1–18
11. Hsu AR, Ghodadra NS, Provencher MT, Lewis PB, Bach BR
(2011) Biceps tenotomy versus tenodesis: a review of clinical
outcomes and biomechanical results. J Shoulder Elbow Surg
20:326–332
12. Ide K, Shirai Y, Ito H, Ito H (1996) Sensory nerve supply in the
human subacromial bursa. J Shoulder Elbow Surg 5:371–382
13. Khan KM, Cook JL, Maffulli N, Kannus P (2000) Where is the
pain coming from in tendinopathy? It may be biochemical, not
only structural, in origin. Br J Sports Med 34:81–83
14. Loukas M, Grabska J, Tubbs RS, Apaydin N, Jordan R (2009)
Mapping the axillary nerve within the deltoid muscle. Surg
Radiol Anat 31:43–47
15. Lutton DM, Gruson KI, Harrison AK, Gladstone JN, Flatow EL
(2011) Where to tenodese the biceps: proximal or distal? Clin
Orthop Relat Res 469:1050–1055
16. Mazzocca AD, Rios CG, Romeo AA, Arciero RA (2005) Sub-
pectoral biceps tenodesis with interference screw fixation.
Arthroscopy 21:896.e1–896.e7
17. Morisawa Y, Uemura H, Michinaka Y, Hasegawa S, Yamamoto
H (1997) A morphological study of the mechanoreceptors in the
rotator cuff, the subacromial bursa and the coracoacromial liga-
ment. Kansestu geka 16:917–922 (in Japanese)
18. Murakami M, Yoshikawa G, Tarumoto R, Dohi J (1997) Sensory
nerve endings of the capsule and pain onset mechanism in the
shoulder joint. Kansestu geka 16:923–930 (in Japanese)
19. Ochiai N, Sato S, Sugioka K, Kenmoku T, Saisu T, Fujita K,
Mastuki K (2010) Lateral side of the shoulder pain due to the
shoulder pathology. Katakansestu 34:569–573 (in Japanese with
English abstract)
20. Rauber A (1870) II. Die Nerven des Oberarmknochens. In: Ra-
uber A (ed) Ueber die Knochen-Nerven des Oberarms und
Oberschenkels. Caesar Fritsch, Mu
¨nchen, pp 13–15
21. Ritchie ED, Tong D, Chung F, Norris AM, Miniaci A, Vairava-
nathan SD (1997) Suprascapular nerve block for postoperative
pain relief in arthroscopic shoulder surgery: a new modality?
Anesth Analg 84:1306–1312
22. Sander B, Lavery K, Pennington S, Warner JJP (2008) Biceps
tendon tenodesis: success with proximal versus distal fixation.
Arthroscopy 24:e9
23. Soifer TB, Levy HJ, Soifer FM, Kleinbart F, Vigorita V, Bryk E
(1996) Neurohistology of the subacromial space. Arthroscopy
12:182–186
24. Szabo
´I, Boileau P, Walch G (2008) The proximal biceps as a
pain generator and results of tenotomy. Sports Med Arthrosc
16:180–186
25. Tosounidis T, Hadjileontis C, Triantafyllou C, Sidiropoulou V,
Kafanas A, Kontakis G (2013) Evidence of sympathetic
Knee Surg Sports Traumatol Arthrosc
123
innervation and a1-adrenergic receptors of the long head of the
biceps brachii tendon. J Orthop Sci 18:238–244
26. Uz A, Apaydin N, Bozkurt M, Elhan A (2007) The anatomic
branch pattern of the axillary nerve. J Shoulder Elbow Surg
16:240–244
27. Vorster W, Lange CP, Brie
¨t RJ, Labuschagne BC, du Toit DF,
Muller CJ, de Beer JF (2008) The sensory branch distribution of
the suprascapular nerve: an anatomic study. J Shoulder Elbow
Surg 17:500–502
28. Wittstein JR, Queen R, Abbey A, Toth A, Moorman CT III
(2011) Isokinetic strength, endurance, and subjective outcomes
after biceps tenotomy versus tenodesis: a postoperative study.
Am J Sports Med 39:857–865
29. Wrete M (1949) The sensory pathways from the shoulder joint.
J Neurosurg 6:351–360
30. Zhang Q, Zhou J, Ge H, Cheng B (2013) Tenotomy or tenodesis
for long head biceps lesions in shoulders with reparable rotator
cuff tears: a prospective randomised trial. Knee Surg Sports
Traumatol Arthrosc. doi:10.1007/s0016701325878
Knee Surg Sports Traumatol Arthrosc
123