Keywords
C5 - C6 root avulsion - shoulder function - distal nerve transfers
Introduction
Restoration of shoulder abduction and external rotation are important goals in the
rehabilitation of patients with devastating brachial plexus injuries. In C5 and C6
root avulsions, anatomical reconstruction is not possible and nerve transfers offer
far superior results over tendon/muscle transfers or shoulder arthrodesis.[1] Suprascapular and axillary are the target nerves in the restoration of shoulder
function. Suprascapular neurotization also aims at restoration of external rotation
through reinnervation of the infraspinatus muscle. Reinnervation of the deltoid (axillary
nerve) allows a greater range of shoulder abduction and also improves the flexion
and extension at the glenohumeral joint. In C5 and C6 root avulsion injury, the serratus
anterior muscle is dysfunctional to a variable extent and, at times, presents with
considerable winging of scapula. These cases may warrant neurotization of the long
thoracic nerve to maximize shoulder abduction.
Patients and Methods
Between February 2009 and December 2012, 30 patients presenting with upper brachial
plexus injuries ([Fig. 1]) were subjected to magnetic resonance myelography and electromyographic studies.
Presence of pseudomenigoceles and fibrillation waves supported the evidence of C5
and C6 root avulsions. Patients were operated 3 to 9 months after injury. The average
denervation period was 5.6 months ([Table 1]). Each patient was explored under general anesthesia with a short reverse “C”-shaped
incision. Root avulsions were indicated either by an absence of C5 and C6 roots in
the scalene triangle or presence of scarred, thinned-out, and flimsy nerve segments
that failed to respond to an electrical stimulus. Multiple nerve transfers were performed
to reinnervate the prime abductors and external rotators of the shoulder ([Fig. 2]). In four patients with winged scapula (case numbers 6, 17, 20, and 27 in [Table 1]), an additional nerve transfer was performed to restore the serratus anterior muscle
function by transferring a part of the thoracodorsal nerve into the long thoracic
nerve ([Fig. 3]).
Fig. 1 Upper brachial plexus injury with winged scapula.
Fig. 2 Distal nerve transfers to suprascapular and axillary nerves (anterior branch).
Fig. 3 Transfer of lateral branch of thoracodorsal nerve to long thoracic nerve.
Table 1
Functional outcomes of distal nerve transfers in shoulder function (n = 30)
|
Case number
|
Age
|
Denervation period (mo)
|
Follow-up (mo)
|
Abduction (degree)
|
Abduction strength (MRC grade)
|
External rotation (degree)
|
|
1
|
19
|
4
|
30
|
170
|
M4
|
70
|
|
2
|
21
|
3
|
24
|
150
|
M3
|
50
|
|
3
|
28
|
6
|
24
|
Stable shoulder with no active abduction
|
Nil
|
Nil
|
|
4
|
21
|
5
|
28
|
160
|
M3
|
60
|
|
5
|
18
|
4
|
36
|
170
|
M4
|
70
|
|
6[a]
|
29
|
4
|
26
|
160
|
M3
|
40
|
|
7
|
20
|
7
|
28
|
110
|
M3
|
Nil
|
|
8
|
31
|
3
|
24
|
140
|
M3
|
50
|
|
9
|
23
|
8
|
28
|
110
|
M3
|
Nil
|
|
10
|
19
|
4
|
28
|
160
|
M4
|
70
|
|
11
|
26
|
7
|
36
|
140
|
M3
|
40
|
|
12
|
29
|
9
|
24
|
100
|
M3
|
Nil
|
|
13
|
27
|
6
|
28
|
130
|
M3
|
40
|
|
14
|
24
|
4
|
26
|
140
|
M3
|
50
|
|
15
|
19
|
6
|
48
|
150
|
M3
|
50
|
|
16
|
35
|
7
|
24
|
90
|
M3
|
Nil
|
|
17[a]
|
24
|
4
|
28
|
150
|
M3
|
60
|
|
18
|
27
|
6
|
24
|
160
|
M3
|
50
|
|
19
|
32
|
4
|
30
|
Stable shoulder with no active abduction
|
Nil
|
Nil
|
|
20[a]
|
21
|
5
|
28
|
160
|
M4
|
60
|
|
21
|
25
|
7
|
26
|
110
|
M3
|
Nil
|
|
22
|
30
|
6
|
38
|
170
|
M4
|
70
|
|
23
|
27
|
5
|
30
|
150
|
M3
|
40
|
|
24
|
29
|
8
|
24
|
110
|
M3
|
Nil
|
|
25
|
32
|
4
|
26
|
Stable shoulder with no active abduction
|
Nil
|
Nil
|
|
26
|
21
|
6
|
24
|
140
|
M3
|
40
|
|
27[a]
|
19
|
4
|
20
|
170
|
M4
|
70
|
|
28
|
32
|
7
|
24
|
90
|
M3
|
Nil
|
|
29
|
25
|
5
|
26
|
120
|
M3
|
30
|
|
30
|
22
|
8
|
24
|
90
|
M3
|
Nil
|
a These patients presenting with winged scapula required an additional nerve transfer,
that is, transfer of the lateral branch of thoracodorsal nerve into the long thoracic
nerve.
Transfer of Distal Part of Spinal Accessory Nerve into Suprascapular Nerve
The patient was kept in semilateral position with an assistant holding the arm up
in 90-degree abduction. An incision was made parallel to the spine of scapula. After
division of the trapezius muscle fibers, the space between it and the supraspinatus
muscle was opened.
The spinal accessory nerve coursing on the undersurface of the trapezius muscle was
carefully isolated from the thin vessels and dissected further down along the medial
border of scapula. Working laterally, supraspinatus muscle was retracted downward
to expose the transversally oriented suprascapular ligament along the superior border
of scapula. After gaining control over the suprascapular vessels, the ligament was
divided and underlying suprascapular nerve was identified in the adipose tissue. The
nerve was divided proximally and sutured to the spinal accessory nerve with 10–0 nylon
suture or fibrin glue ([Fig. 2]).
Transfer of Long Head Triceps Branch of Radial Nerve into Anterior Branch of Axillary
Nerve
In supine position a curvilinear incision was made along the posterolateral aspect
of the arm. The radial nerve was exposed in the triangular space and its branch to
the long head of triceps was identified. The axillary nerve with its anterior and
posterior branches was identified in the quadrilateral space. The long head triceps
branch was sutured to the anterior branch of the axillary nerve with 10–0 nylon suture
or fibrin glue ([Fig. 2]).
Transfer of Lateral Branch of Thoracodorsal Nerve into Long Thoracic Nerve
With a longitudinal incision in semilateral position, the thoracodorsal nerve was
identified along the anterior border of the latissimus dorsi muscle in the posterior
axillary line. The dominant branch, usually the lateral, was traced distally and sectioned
close to the muscle. The long thoracic nerve was identified and divided high in the
axilla. The thoracodorsal branch was sutured to the long thoracic nerve with 10–0
nylon suture or fibrin glue ([Figs. 3], [4]).
Fig. 4 Surgical incisions.
Additional nerve transfers in restoration of elbow flexion consisted of ulnar and
median nerve fascicular transfer to biceps and brachialis branches of the musculocutaneous
nerve.
Postoperative Care
Postoperatively the operated arm was strapped to the chest for a period of 4 weeks.
Mobilizing exercises and electrical stimulation were begun thereafter. The shoulder
function was clinically assessed by measuring the abduction and external rotation
with a goniometer. Abduction strength was measured on the Medical Research Council
(MRC) scale. Clinical evaluations were performed at 3-month intervals for a period
of 24 to 48 months (average: 32 months).
Results
The brachial plexus injury was a result of motorcycle accidents in 27 patients, four-wheeler
accidents in 2 patients, and a fall from a height in 1 patient. All patients were
males. The mean age of the patients was 25.1 years (range: 18–35 years), and the denervation
period ranged from 3 to 9 months (mean: 5.5 months). MRC scale was used to assess
the preoperative muscle power of the target muscles. Preoperative shoulder abduction
and external rotation were graded as 0 degree. Deltoid, supraspinatus, and infraspinatus
muscles were assessed as M0. There was M5 power in the trapezius muscle and M4 in
the triceps and latissimus dorsi muscles.
Results of Distal Nerve Transfers
Shoulder abduction was restored in 27 (92.86%) patients whereas external rotation
could be reinstated in 19 (64.28%). An initial evidence of restoration of shoulder
abduction appeared at 30 ± 4 weeks. The degree of restoration of shoulder abduction
ranged from 90 to 170 degrees (average 118 degrees); 21 scored M3 and 6 scored M4
on MRC grade. Three patients in whom abduction could not be elicited on clinical examination
were, however, symptomatically better in terms of stability of the shoulder joint
and absence of pain.
External rotation was restored in 19 cases and the range of external rotation varied
from 30 to 70 degrees (average 53 degrees).
At the final follow-up, winging of scapula had improved in three of four patients
following reinnervation of serratus anterior muscle. Surgical outcomes are depicted
in [Table 1] and [Fig. 5].
Fig. 5 Restoration of good range of active shoulder abduction and external rotation.
Postoperative Follow-up
All patients were evaluated at 3-month intervals for a period of 24 to 48 months (average:
27.8 months). At 6-month follow-up, the trapezius muscle power was assessed as M4
in 27 cases and M3 in 3 cases. Muscle power in triceps was downgraded to M3 in all
cases. In four cases in which lateral branch of the thoracodorsal nerve was used to
reinnervate the serratus anterior muscle (case numbers 6, 17, 20, and 27 in [Table 1]), latissimus dorsi muscle power was assessed as M3.
Discussion
Restoration of shoulder function is an important goal in the management of devastating
brachial plexus injuries. In C5 and C6 root avulsion injury, anatomical reconstruction
of the plexus is not feasible and nerve transfer to the suprascapular and axillary
nerves is a viable option in restoration of shoulder function.
A direct nerve transfer between the spinal accessory nerve and suprascapular nerve
produces an average of 45 degrees of shoulder abduction (range from < 20 to 80 degrees).[1] The recovery in external rotation is variable depending on the number of axons ultimately
reaching to the infraspinatus muscle. Conventionally the spinal accessory nerve is
transferred to the suprascapular nerve by an anterior supraclavicular approach. An
anterior coaptation has certain limitations: in severe traction injuries suprascapular
nerve may be retracted retro/infraclavicularly and its coaptation with spinal accessory
nerve may necessitate a nerve graft; proximal transfer may denervate a significant
part of the trapezius muscle; and distal injury to the suprascapular nerve, though
rare, may be overlooked. A posterior transfer near the suprascapular notch is in close
proximity to the target muscles. This possibly facilitates an early reinnervation,
as suggested in one of the study.[2] In the series reported, clinically active shoulder abduction was restored in 27
patients. Three patients lacked active abduction, but shoulder was stable and free
from pain.
A simultaneous nerve transfer to the axillary nerve yields much better results when
adequate donors are available.[1]
[3]
[4]
[5] In anterior neurotization of axillary nerve, a considerable mismatch in the sizes
of donor and recipient nerves results in dilution of nerve fibers entering the deltoid
muscle.[5] A posterior transfer of the long head triceps branch into the anterior branch of
axillary nerve in the quadrilateral space selectively maximizes the donor axonal input
into a single muscle (deltoid).[6]
[7]
C5 and C6 root avulsion injury at times presents with considerable weakness of serratus
anterior muscle. The serratus anterior muscle, innervated by the long thoracic nerve,
originates from the external surfaces of the first eight ribs and is inserted to the
costal surface of the scapula. This muscle stabilizes the scapula against the chest
wall and is an important complement to deltoid function in shoulder abduction. In
the serratus anterior muscle palsy arm can no longer be lifted higher than 90 degrees.
With significant denervation, the scapula is tilted superiorly and medially and its
inferior pole rotated medially. In cadaveric studies in 38 dissections, Wang et al[9] have reported different derivations of the long thoracic nerve: C4–7, C5–7, C5 and
C7, C5–7, C5–C8, C6, and C7, and branch from C6. This may explain the varying extent
of winging observed with different grades of injury. The anatomic study of the thoracodorsal
and long thoracic nerves have shown that the lateral branch of the thoracodorsal nerve
has an adequate length and sufficient number of axons for a direct transfer to the
long thoracic nerve.[10] In the present series, four patients with winged scapulae underwent simultaneous
neurotization of the serratus anterior muscle with a branch of the thoracodorsal nerve.
In three of four patients, winging of the scapula improved with restoration of shoulder
function.
In this study, patients with C5 and C6 root avulsion injury underwent distal nerve
transfers close to the target muscles and exhibited a good outcome in shoulder function.
