Human cadaveric study of subscapularis muscle innervation and

advertisement
Human cadaveric study of subscapularis muscle innervation
and guidelines to prevent denervation
James C. Kasper, MD,a John M. Itamura, MD,b James E. Tibone, MD,b Scott L. Levin, MD,c
and Milan V. Stevanovic, MD, PhD,b Santa Maria and Los Angeles, CA, and Durham, NC
The upper and lower subscapular nerves provide
innervation to the subscapularis muscle. However, the
axillary nerve may provide a significant innervation to
the lower portion of the muscle. The prevalence and
patterns of anomalous innervation of the subscapularis
muscle were studied to determine if these variations
increased the risk of muscle denervation during open
shoulder surgery. Twenty human cadaveric shoulders
were dissected, and the innervation to the subscapularis
was defined. The distance from the nerve insertion to the
shoulder joint was measured in neutral and maximal
external rotation. In the most common variation, the
lower subscapular nerve arose from the axillary nerve (5
specimens; 25%). Although external rotation of the
shoulder brought the nerve insertion significantly more
lateral (35.2 to 16.9 mm, P < .001), the origin of the
nerve had no significant effect on nerve proximity to the
joint. The closeness of the nerve insertions to the shoulder
joint warrants care during an anterior approach to the
shoulder and dissections on the anterior surface of the
muscle. Subscapularis nerve damage or denervation
may cause unexplained joint instability and
subscapularis dysfunction. (J Shoulder Elbow Surg
2008;17:659-662.)
T
he subscapularis muscle is the largest muscle in the
rotator cuff, and its role in shoulder function and in
the passive and dynamic stability of the joint has
been well described.3,13,14 This muscle is commonly
encountered during open shoulder surgery. Routine
approaches involve splitting the muscle in line with its
fibers or detaching it at the insertion. Well-known to
be at risk during surgery about this muscle are the axillary nerve and posterior circumflex humeral artery at its
From aCentral Coast Orthopedics, bUSC Orthopaedic Surgery
Associates, and cDuke Plastic and Reconstructive Surgery.
Reprint requests: James C. Kasper, MD, Central Coast Orthopedics,
2342 Professional Pkwy, Ste 200, Santa Maria, CA 93455
(E-mail: orthodoc@gmail.com).
Copyright ª 2008 by Journal of Shoulder and Elbow Surgery
Board of Trustees.
1058-2746/2008/$34.00
doi:10.1016/j.jse.2007.11.013
inferior margin and the infraclavicular brachial plexus
and axillary artery medially.2,5,11 Various chronic,
postsurgical, and traumatic conditions can lead to
scarring and retraction of the subscapularis muscle,
making surgery in this area even more difficult. Inadvertent damage to the subscapular nerves may lead
to denervation of the subscapularis muscle and unexplained instability or loss of function of the shoulder.
The most commonly described innervation to the
subscapularis muscle includes the upper subscapular
and the lower subscapular nerves, both originating
from the posterior cord of the brachial plexus (Figure 1). Numerous studies, however, have documented
significant variability in this pattern for both the upper
and lower nerves.7,8,15 The upper nerve most commonly originates from the posterior cord, but it frequently arises as more than one branch. Cadaveric
studies have shown even greater variability of the
lower subscapular nerve. This nerve has been reported to arise as 1 or multiple branches from the posterior cord, axillary nerve, or thoracodorsal nerve
(Figures 2 and 3). In particular, this nerve originates
from the axillary nerve in 9% to 55% of cases as 1
or more branches.7,8,15
The purpose of the present study was to determine
the prevalence and patterns of anomalous innervation
of the subscapularis muscle and to determine if these
variations would place the nerves at greater risk during open shoulder surgery.
MATERIALS AND METHODS
Dissections were done in 16 shoulders from 8 whole fresh
cadavers and 4 shoulders from frozen cadaveric forequarters. The 20 specimens consisted of 10 right and 10 left
shoulders from a total of 10 cadavers. The same approach
was used in each specimen, which included developing
the deltopectoral interval and releasing the pectoralis major
muscle from its origin at the clavicle. Next, the conjoined tendon and the pectoralis minor tendon were reflected from the
coracoid process to expose the brachial plexus and subscapularis muscle. The axillary nerve was identified at the inferior border of the subscapularis muscle and traced back to
the posterior cord of the brachial plexus. The branches innervating the subscapularis muscle were then tagged and
traced back to their origin. The innervation pattern of each
specimen was recorded, and variations were noted.
659
660
Kasper et al
Figure 1 This subscapularis muscle drawing shows the upper and
lower subscapular nerves originating from the posterior cord of
the brachial plexus. The lateral and medial cords of the brachial
plexus have been removed for better visualization.
J Shoulder Elbow Surg
July/August 2008
Figure 3 This subscapularis muscle drawing shows the origin of upper subscapular nerve from the posterior cord and the lower subscapular nerve from the thoracodorsal nerve. The lateral and
medial cords of the brachial plexus have been removed for better visualization.
the joint was marked with a pin on the anterior surface of
the subscapularis muscle. Measurements were recorded to
determine the distance from the muscular innervation by
the lower subscapular nerve to the glenohumeral joint. The
humerus was placed in maximal external rotation, and
a pin was again placed through the subscapularis in the center of the glenohumeral joint. Measurements were repeated
for each specimen in this position.
Statistical analysis
Our data consisted of measurements of the distance from
the site of the lower subscapular nerve innervation to the glenohumeral joint. These measurements were taken in both
neutral and maximal external humeral rotation. The mean
distance for all the specimens was compared using a Wilcoxon signed-rank test. We also grouped the data by innervation pattern and compared the distances in each position
between groups using a 2-sample t test. Values of P ¼ .05
were considered significant.
Figure 2 This subscapularis muscle drawing shows the origin of upper subscapular nerve from the posterior cord and the lower subscapular nerve from the axillary nerve. The lateral and medial
cords of the brachial plexus have been removed for better visualization.
The muscular insertion of the upper and lower subscapular nerves, as well as any additional branches, were marked
with a pin. When the nerves branched out around the site of
insertion, the closest branch to the glenohumeral joint was
chosen and marked. The humerus was placed in neutral rotation with no abduction, and the glenohumeral joint was
palpated deep to the subscapularis muscle. The center of
RESULTS
The 20 specimens revealed significant variability in
the innervation pattern of the subscapularis muscle.
Ten specimens (50%) had the most commonly described anatomy, consisting of a dominant upper subscapular nerve, 1 thoracodorsal nerve (or middle
subscapular nerve), and 1 lower subscapular nerve,
all originating from the posterior cord of the brachial
plexus. In relation to the upper subscapular nerve, 4
specimens had 2 distinct branches to the subscapularis, which originated from the posterior cord proximal
to the thoracodorsal nerve. On the basis of their origin
Kasper et al
J Shoulder Elbow Surg
Volume 17, Number 4
and entrance into the muscle, we concluded that these
represented 2 upper subscapular branches in all 4
cases.
Twelve of the 20 specimens had a single lower subscapular nerve arising from the posterior cord distal to
the thoracodorsal nerve origin; however, the remaining lower subscapular nerves showed considerable
variability. One specimen had 2 lower subscapular
nerve branches arising from the posterior cord. Two
specimens had a single lower subscapular nerve coming from the thoracodorsal nerve, and in 5 specimens,
the lower subscapular nerve arose from the axillary
nerve. Two cases, which had the lower subscapular
nerve arising from the axillary nerve, had 2 separate
lower subscapular nerve branches.
For all specimens, the distance from site of the lower
subscapular nerve entrance into the muscle to the glenohumeral joint was 35.2 mm (range, 23-48 mm) with
the humerus in neutral rotation and 16.9 mm (range,
0-28 mm) with the humerus in maximal external rotation. This difference was statistically significant (P <
.001). In the specimens with a lower subscapular
nerve arising from the posterior cord (group 1), these
distances were 35.9 mm for neutral rotation and 18.5
mm for external rotation. In the specimens in which the
nerve came from the axillary nerve (group 2), these
distances were 36.6 mm for neutral rotation and
15.8 mm for external rotation (Tables I and II).
When the data from groups 1 and 2 were compared,
no statistical difference was found between the groups
in neutral or external rotation in the difference between the distance from the site of the nerve entering
the muscle to the glenohumeral joint (P ¼ .83 and
P ¼ .20). Therefore, regardless of where the lower
subscapular nerve began, the innervation site of the
muscle is statistically similar.
DISCUSSION
The subscapularis is generally regarded as a single
muscle innervated by the upper and lower subscapular nerves. However, the differing anatomy and innervation patterns of the superior and inferior portions of
this muscle have led many authors to make a distinction
between these 2 parts. Klapper et al9 described the
tendinous bands of the muscle and found that the superior two-thirds coalesced into a tendinous insertion at
the lesser tuberosity, whereas the inferior one-third remained muscular at its insertion.1 This interval is also
routinely exploited in anterior approaches to the shoulder when the muscle is split in line with its fibers at the
junction of the superior two-thirds and inferior onethird.6 McCann et al10 studied the subscapularis muscle using electromyography and found that the upper
and lower portions of the muscle exhibit differential
activity depending on shoulder position.
661
Table I Distance from insertion of lower subscapular nerve to
glenohumeral joint with the humerus in neutral external rotation and
0 of abductiona
Distance in neutral
humeral rotation (mm)
Anatomy
No.
Mean
SD
SE
Normal (group 1)
Axillary (group 2)
13
5
35.9
36.6
6.25
4.98
1.73
2.23
SE, Standard error; SD, standard deviation.
a
P ¼ .83, 2-sample t test.
Table II Distance from insertion of lower subscapular nerve to
glenohumeral joint with the humerus in maximal external rotation and
0 of abductiona
Distance in max external
humeral rotation (mm)
Anatomy
No.
Mean
SD
SE
Normal (group 1)
Axillary (Group 2)
13
5
18.5
15.8
6.70
1.92
1.86
0.86
SE, Standard error; SD, standard deviation.
a
P ¼ .20; 2-sample t test.
Many articles have reported a variable pattern of
innervation of this inferior portion of the muscle.
Kerr8 described the innervation of the subscapularis
extensively and referred to the lower subscapular
nerve as the axillary subscapular nerve due to its innervation of the axillary border of the muscle. Kerr found
that the lower subscapular nerve arose from axillary
nerve in 55% of his dissections. In a similar anatomic
analysis by Kato,7 the origin was from the axillary
nerve in 23% of cases. A cadaver study by Yang et
al15 found this pattern in 1 of 11 specimens. Our
own surgical experience has revealed a similar variable origin of the lower subscapular nerve and prompted the current study. We postulated that a more distal
origin of the nerve might bring the nerve supply closer
to the surgical field, placing it at greater risk during
surgery.
We found considerable variability in the origin of
the lower subscapular nerve. Specifically, the nerve
arose from the axillary nerve in 5 of 20 specimens
(25%), consistent with the findings of Kerr and Kato.
We also found that the nerve came from the thoracodorsal nerve in 2 cases, but we did not believe this
was a large enough group to allow statistical comparison. In comparing the distance from the shoulder joint
to the innervation site of the lower subscapular nerve,
we found no difference between the group with normal anatomy and the group with the nerve arising
from the axillary nerve. This held true in both neutral
662
Kasper et al
and maximal external humeral rotation. Therefore, although the pattern of innervation of the inferior portion
of the subscapularis muscle has a high rate of variability, this does not seem to place the nerve supply at
greater risk during surgical dissection.
As expected, we were able to show that the innervation site of the muscle passes significantly closer to
the glenohumeral joint when the arm is in maximal
external rotation. This was true for all specimens and
when the groups were analyzed independently. The
mean distance from the point of innervation to the joint
decreased from 35.2 mm to 16.9 mm with maximal
external rotation (P <.001). This is in line with the findings of Yang et al,15 who showed a similar significant
decrease. This led them to recommend caution when
dissecting medial to the glenohumeral joint, especially
with the humerus in external rotation or while applying
traction to a detached subscapularis tendon.15
The current study, as well as the work by Yang et
al,15 reveals that the subscapularis muscle innervation
is close to the surgical field during a routine anterior
approach to the shoulder. Inadvertent damage to
these nerves may result in problems with shoulder function and stability. An interesting finding in a study by
Flatow et al12 was the documented loss of subscapularis function after total shoulder arthroplasty. They used
the lift-off and belly-press tests, as well as the patients’
ability to tuck in a shirt, to determine the integrity of the
subscapularis muscle after arthroplasty. They reported
a 69% rate of subscapularis dysfunction, despite meticulous attention to subscapularis repair. The source
of this dysfunction could not be determined because
electromyography and advanced imaging studies
were not done. In addition, recent work by Gerber
et al4 has documented fatty infiltration of the subscapularis muscle in almost half of their patients treated with
osteotomy of the lesser tuberosity for total shoulder
replacement. This finding occurred despite radiographic evidence of bony healing of the tuberosity.
They speculated that inadvertent neurologic injury
might have accounted for this phenomenon.
In summary, the subscapularis muscle has a highly
variable pattern of innervation. The most common variation of the lower subscapular nerve is as a branch of
the axillary nerve, yet this does not seem to place
the nerve at greater risk during surgery. Nonetheless,
the subscapular nerves innervate the muscle close to
the glenohumeral joint, and inadvertent damage
may account for unexplained shoulder dysfunction
after surgery. Care should be taken when dissecting
J Shoulder Elbow Surg
July/August 2008
around or releasing the subscapularis muscle belly,
especially with the shoulder in external rotation. In addition, dissection should not be done on the anterior
surface of the subscapularis muscle belly medial to
the glenohumeral joint. Dissection in this area may
lead to inadvertent neurologic damage and subsequent disability. Further research is needed in the field
of total shoulder arthroplasty to determine if postoperative subscapularis dysfunction is due to denervation
of the muscle at the time of surgery.
REFERENCES
1. Cleeman E, Brunelli M, Gothelf T, Hayes P, Flatow EL. Releases of
subscapularis contracture: an anatomic and clinical study. J Shoulder Elbow Surg 2003;12:231-6.
2. Cuomo F, Checroun A. Avoiding pitfalls and complications in total
shoulder arthroplasty. Orthop Clin North Am 1998;29:507-18.
3. DePalma AF, Cooke AJ, Prabhakar M. The role of the subscapularis in recurrent anterior dislocations of the shoulder. Clin Orthop
Relat Res 1967;54:35-49.
4. Gerber C, Yian EH, Pfirrmann CAW, Zumstein MA, Werner CML.
Subscapularis muscle function and structure after total shoulder replacement with lesser tuberosity osteotomy and repair. J Bone Joint
Surg Am 2005;87:1739-45.
5. Ho E, Cofield RH, Balm MR, Hattrup SJ, Rowland CM. Neurologic
complications of surgery for anterior shoulder instability. J Shoulder
Elbow Surg 1999;8:266-70.
6. Jobe FW, Giangarra CE, Kvitne RS, Glousman RE. Anterior capsulolabral reconstruction of the shoulder in athletes in overhand
sports. Am J Sports Med 1991;19:428-34.
7. Kato K. Innervation of the scapular muscles and its morphological
significance in man. Anat Anz 1989;168:155-68.
8. Kerr A. Brachial plexus of nerves in man: the variations in its formation and branches. Am J Anat 1918;23:285-395.
9. Klapper RC, Jobe FW, Matsuura P. The subscapularis muscle and
its glenohumeral ligament-like bands. A histomorphologic study.
Am J Sports Med 1992;20:307-10.
10. McCann P, Cordasco F, Ticker J. An anatomic study of the subscapular nerves: a guide for electromyographic analysis of the subscapularis muscle. J Shoulder Elbow Surg 1994;3:94-9.
11. McFarland EG, Caicedo JC, Guitterez MI, Sherbondy PS, Kim TK.
The anatomic relationship of the brachial plexus and axillary artery
to the glenoid. Implications for anterior shoulder surgery. Am
J Sports Med 2001;29:729-33.
12. Miller SL, Hazrati Y, Klepps S, Chiang A, Flatow EL. Loss of subscapularis function after total shoulder replacement: A seldom recognized problem. J Shoulder Elbow Surg 2003;12:29-34.
13. Symeonides PP. The significance of the subscapularis muscle in the
pathogenesis of recurrent dislocation of the shoulder. J Bone Joint
Surg Br 1972;54:476-83.
14. Turkel SJ, Panio MW, Marshall JL, Girgis FG. Stabilizing mechanisms preventing anterior dislocation of the glenohumeral joint.
J Bone Joint Surg Am 1981;63:1208-17.
15. Yung S4-W, Lazarus MD, Harryman DT. Practical guidelines to
safe surgery about the subscapularis. J Shoulder Elbow Surg
1996;5:467–70.
Download