A Short Scenario for Restoration of Reasonable Limb Function in Adults after Upper Brachial Plexus Injuries Using Neurotization and Combined Muscle Transfers

Brachial plexus injury is a considerably disabling
problem which has different strategies to
deal with. The strategies of management of children
and adults' plexus injury differ greatly for many
factors. The nerve axons have to travel a considerably
shorter distance as well as the regeneration
power of the nerve axons is far greater in children
[1]. These relative privileges enable extensive plexus
reconstruction in children more than adults'
palsies in these it may be rarely feasible [2].
In the other hand, physical, psychological and
hard nursing supporting care for those adult patients
add more difficulties especially for the prolonged
periods of seeking medical and surgical management.
Unfortunately, this may result in economic
and psychological troubles and force some patients
to give up seeking the medical care.
Timefactors are crucial for the sound management
for these patients. Time delay can result in
a non-achievable chance loss as the neuromuscular
end plates showed an eventual loss within 20 to
24 months following muscle denervation [3].
Many waiting periods are really subtracted
from the remaining time before these permanent
changes in the motor end plates within the denervated
muscles. This loss affects greatly the scenario
of functional improvement.
These periods of delay are such as waiting
intervals for management of associated injuries
like fractures and post-injury spontaneous recovery
periods. Also, patient evaluation, investigations,
decision making, availability of suitable facilities,
skilled personnel and even periods of ongoing
recovery after a trial of primary repair may result
in much time loss.
Functionally, the flexion of the elbow is the
main motor function moderator of the upper limb
and considered the most precious [4]. The second
important function is the abduction of the shoulder
as the loss of power to abduct the arm is an incapacitating
condition [5].
C5C6 brachial plexus injury generally affects
shoulder abduction and elbow flexion causing
disabilities and deformities of both the biceps and
deltoid muscles. However, if C7 has been injured
with C5,6the triceps muscle would have been
affected and the wrist extension may be affected
as well [2,6]. For managing adult upper brachial
plexus palsy, many strategies should be discussed
with the patients according to their disabilities.
Primary plexus repair, nerve transfer, functional
muscle transfer and other musculoskeletal approaches
may be followed according the suitability,
merits and disadvantages of each [2].
In this study we aim to evaluate a relatively
short management scenario (totally 6 to 10 months)
for adults' upper brachial plexus palsybetween 3
and 15 months of injury. The study used a multimodal
management approach as a combination
between nerves transfer to the biceps and rotator
calf muscles in its first stage surgery followed by
multiple muscle transfers in the shoulder in the
second stage.
PATIENTS AND METHODS
Between March 2013 and June 2015, six adult
patients, referred to Zagazig University Hospitals,
suffering from upper brachial plexus injuries were
operated upon in two stages. Those patients (1
396 Vol. 42, No. 2 /A Short Scenario for Restoration of Reasonable Limb Function
women and 5 men) were having a history of injury
between 3 and 15 months with no clinical or electroneuromyographic
(ENMG) improvement of biceps
and deltoid muscles. The first stage may be exclusively
done urgently without the initial three months
conservation periodfor patients having preganglionic
upper plexus injuries diagnosed by imaging
(MRI) or ENMG.
In the first stage, two nerve transfers were
performed in the same setting:
- Neurotization of suprascapular nerve (using a
branch of spinal root of the accessory nerve to
the suprascapular nerve).
- Oberlin nerve transfer [4] (transfer of two nerve
fascicles from the ulnar nerve to biceps branch
of the musculocutaneous nerve to reinnervate
the biceps muscle).
After three to four months of the first stage, the
following conditions should be fulfilled to continue
to the second stage:
• Trapezius strength level should be 5 by MRC
scale.
• Complete deltoid paralysis confirmed by electroneuromyography
(ENMG).
• Passive shoulder joint abduction should be 80
degree or more.
After fulfillment of these conditions, the patients
were operated in the second stage for combined
muscles transfers in the same setting:
- Trapezius transfer to the humerus.
- Combined latissimus dorsi transfer with teres
major transferto rotator calf of the shoulder.
Fig. (1): First stage; suprascapular nerve neurotization by the distal part of the spinal accessory nerve followed by transfer of two
nerve fascicles from the ulnar nerve to biceps branch of the musculocutaneous nerve to reinnervate the biceps muscle.
Second stage: Elevation of trapezius insertion by division of the acromion base, disinsertion of the tendons of latissimus
dorsi and teres major and transfer to the rotator calf and then fixation of the acromion by screws in the humerus.
First Stage Second Stage
Egypt, J. Plast. Reconstr. Surg., July 2018 397
Operative Techniques:
First stage surgery:
The surgeon should clarify to the anesthesiologist
to avoid systemic paralytics prior to anesthetic
induction to allow proper intraoperative use of the
nerve stimulator. Surgical loupes or operating
microscope should be used according to the surgeon
preference. The patient is put in supine position
with his arm abducted 90 degree on an arm Table.
A 1/200000 epinephrine solution may be infiltrated
in the operative site without any local anesthetic.
A supraclavicular transverse incision to skin and
dissection of the fascia is made. Under the omohyoid
muscle, the suprascapular (the recipient) nerve
is identified and taken by a tape to be cut in a
healthy segment close to its origin from the upper
trunk of the brachial plexus. By following the
transverse cervical artery to its entry site in the
trapezius muscle, the spinal accessory nerve is
searched for at this location, by use of nerve stimulator,
which helps to distinguish it from cervical
plexus branches. The nerve is then traced distally
under the middle and lower trapezius beyond its
branches. The large branches of the transverse
cervical vessels are carefully divided and the nerve
is stimulated again to be reconfirmed and divided
as distal as possible. The nerve is then elevated to
be anastomosed with the distant cut end of therecipientsuprascpular
nerve. Both donor and recipient
nerves are anastomosed by fibrin glue and microsutures
and closure of the cervical wound. In the
upper medial arm, along the bicipital groove, other
incision is done with dissection through subcutaneous
tissue and fascia. The medial antebrachial
nerve should be identified and protected. The
median nerve is centered on the brachial artery
and the ulnar nerve is identified medially. The
biceps muscle is elevated laterally to follow the
musculocutaneous nerve proximally and its branches.
The musculocutaneous has three branches; a
branch to the biceps (BBi) courses laterally and
separates from the musculocutaneous nerve proximally
and another branchto the brachialis (BBr)
courses medially and lateral antebrachial nerve
continues distally. Firstly, we test these branches
using the nerve stimulator to confirm the absence
of any muscle activity. The biceps branch is dissected
proximally allowing more length for the
anastomosis as proximal as possible (the recipient).
The ulnar nerve is dissected more distally with
opening of its epineurium and separation of a group
of fascicles by a fine, microscopic technique. By
using the nerve stimulator, we select two fascicles
(the donor) with pure wrist flexion action that often
located on the lateral or central fascicles. The donor
and recipient fascicles are dissected properly and
cut after making sure that the anastomosis would
not be under tension. The two ends are coaptated
and anastomosed by fibrin glue and micro-sutures.
The wound is closed in layers with soft drain and
wrapped with bulky gently compressive dressing.
Then, the limb is put in an arm sling for 3 weeks.
Re-education and electrotherapy is done from the
endof the second month till the second stage surgery.
Second stage surgery:
The patient is placed in a lateral position and
a skin incision along with the anterior, lateral, and
posterior deltoid origin then continue posteriorly
on the back of the shoulderthen along with the
posterior axillary fold. Elevation of the insertion
of the trapezius by dividing the root of acromion
and the lateral end of the clavicle lateral to the
coracoclavicular ligaments,using a Gegli saw, with
release of the remaining insertion of the trapezius
from the clavicle and the spine of the scapula. The
proximal humerus is exposed by undermining the
deltoid. Latissimus dorsi and teres major tendons
are disinserted from the humerus with putting the
humerus in 90 degree of abduction and full external
rotation. This position should be kept until the
limb be put in an airplane splint immediately
postoperatively. In this position, latissimus dorsi
tendon is fixed to rotator calf (two non-absorbable
sutures at least or by using an anchor fixator to the
humerusbone to obtain a reliable fixation) and
teres major muscle is rerouted and reattached to
the latissimus dorsi tendon with an appropriate
extra-articular musculotendinous lengthening. The
acromial fragment with its insertion of trapezius
is then transferred and fixed by two 4.5mm screws
to the humerus after roughening the attachment by
an osteotome. The fixation is done with the arm
in 90 degree arm abduction and full external rotation.
A radiograph is then taken to check the proper
fixation position followed by suturing the deltoid
over the trapezius as proximal as possible, to
enforce the trapezius transfer and the potential
deltoid reinnervation recovery if any. The skin
isthen closed with a suction drain. After operation,
the arm is immobilized at 80º of abduction and
full external rotation in an airplane splint for 10
weeks with gradual weaning of the splint for another
two weeks then gradual therapy is started
(Fig. 4).
The patients were evaluated for shoulder joint
stability i.e. clinically and radiologically, shoulder
pain, back pain, scoliosis and gait changes (Table
1).
The patients' results were reported just before
the first stage, before the second stage i.e. about
398 Vol. 42, No. 2 /A Short Scenario for Restoration of Reasonable Limb Function
3 months after the first stage, 3 months after the
second stage and 6 months after the second stage.
Fig. (2): Operative technique of the trapezius, latissimus dorsi and teres major transfer. A- Preoperative marking. B- Skin incision
along with the anterior, lateral deltoid origin, back of the shoulder and posterior axillary fold. C,D,E. division of the
origin of the deltoid from acromion, disinsertion of L.D. and T.M from the humerus and bone division of the acromion
base and lat. clavicle. F,G,H,I. transfer of the L.D. to rotator. calf, T.M. to L.D. tendon, acroion fixation by screws to
tumerus and closure.
RESULTS
Six patients were studied in the current study
(5 males and one female) with ages ranging from
18 to 42 years. The time intervals between injury
and surgery were from 3 to 15 months.
Shoulder joint instability were detected as early
as 5 months after injury however shoulder pain
was reported in half number of patients of the
study. Scoliosis and gait changes were present in
all patients included in the study.
In the six patients, as shown in the Tables (2,3),
four types of movementshave been evaluated;
shoulder abduction, external rotation, shoulder
flexion and elbow flexion according to the angle
of the movement against gravity. Furthermore,
according to Medical Research Council scale
(MRC), elbow flexion was evaluated. MRC scale
is amuscle power scoring system ranging from 0
to 5; 0 no contraction, 1 flicker or trace of contraction,
2 active movement with gravity eliminated,
3 active movement against gravity, 4 active movement
against gravity and resistance and 5 normal
power. During evaluation of the external rotation
of the shoulder, the arm is hanged in 90degree
abduction with the elbow is put in 90 degree flexion
(neutral position) and the patient is asked to rotate
the arm by elevating the forearm from the horizon
and the degree of the external rotation is evaluated
by the forearm elevation. Also, the wrist and hand
muscles were evaluated before and after.
The first and second stages and the trapezius
power were mandatory confirmed to have a normal
power (MRC5) and the passive abduction of the
shoulder was exceeding 80 degree as a preliminary
condition for the second stage.
The six patients were operated for Obrelin
procedure by using 2 ulnar nerve fascicles transferred
to the biceps muscle. By the end of the tenth
post-operative month, half of patients have regained
M4 elbow flexion and the remaining patients have
been M3. These improvements have been primarily
noticed by the end of the third month postoperatively.
The range of elbow flexion has increased
throughout the follow up visits to reach 120 degree
against gravity (mean 112 degree) with no noticeable
deficit in the hand function as a donor site
morbidity. (Table 2) (Fig. 3).
After the second stage, the patients were put
in airplane splint for ten weeks complete splinting
and two weeks of gradual weaning. Within six
months from the second stage, shoulder abduction
ranged from 80 to 120 degree (mean 98 degree)
with the forward shoulder flexion was ranging
from 50 to 90 degree (mean 77 degree) and external
rotation was ranging from 10 to 70 degree (mean
47 degree). (Table 3) (Fig. 4).
Egypt, J. Plast. Reconstr. Surg., July 2018 399
Fig. (4): Post-operative views of the second stage surgery with improvement of the shoulder abduction (110°), flexion (90°)
and external rotation (50°) in addition to more improving of the elbow flexion. The hand has not been affected by ulnar
fascicles donation (no fingers clawing). The splinting of the limb in the airplane splint and gradual exercises for
weaning from splint are also shown.
Fig. (3): Pre-operative views of the first stage surgery with complete paralysis of shoulder abduction and elbow flexion. Preoperative
views of the second stage surgery with improvement of the elbow flexion (100°) and partial improvement
of the right shoulder abduction (reinnervation of the biceps and supraspinatus muscles in the first stage).
Before First Stage
Before Second Stage
400 Vol. 42, No. 2 /A Short Scenario for Restoration of Reasonable Limb Function
Table (2): Examination of elbow flexion before and after transfer of two fascicles from ulnar nerve to branch of biceps and
compared in four intervals the results are presented in MRC scale and angle of flexion against gravity.
Case
No.
1
2
3
4
5
6
Month 6-7
3 months postoperative
of 2nd
stage
6 months postoperative
of
2nd stage
18y. male
22y. female
36y male
33y. male
42y. male
41y. male
Age &
Gender
Month 0
Pre-operative
of 1st stage
3
3
3
3
2
3
MRC
0
0
0
0
0
0
Flexion
angle
Pre-operative
of 2nd stage
90
100
50
70
0
40
Flexion
angle
0
0
0
0
0
0
MRC
Month 3-4
110
120
80
100
90
100
Flexion
angle
MRC
4
3
4
3
3
4
Month 9-10
110
120
100
110
110
120
Flexion
angle
4
3
4
3
3
4
MRC
Table (1): Patients ages, gender, general signs, investigations, operative times and complications.
Case
No.
1
2
3
4
5
6
–
+
+
+
+
+
Shoulder
joint
instability
Shoulder
joint pain
–
+
–
+
+
–
Gait
changes
+
+
+
+
+
+
Preoperative
investigations
Highly
suspicious to
C5.6 avulsion
C5,6 avulsion &
C7 rapture
C5,6,7 Rapture
C5,6 avulsion
C5,6 avulsion,
C7 rapture
C5,6 avulsion and
C7 rapture
First Stage
operative
time
240min.
210min.
180min.
170min.
180min.
200min.
Early post-operative
Complications of
1st stage
(wound infection,
hematoma, severe pain)
_
_
_
_
_
_
18y. male
22y. female
36y male
33y. male
42y. male
41y. male
Age &
Gender
Time interval
between injury
and 1st stage
surg.
3m.
12m.
7m.
15m.
10m.
5m.
Interval
between
the two
stages
3m.
3m.
4m.
3m.
4m.
3m.
220min.
160min.
180min.
170min.
250min.
180min.
Second
stage
operative
time
Operative
blood loss
in the second
stage
250ml.
250ml.
400ml.
250ml.
400ml.
400ml.
Post-operative
Complications of 2nd
stage (wound infection,
hematoma, severe pain,
Bone loosening
Soft tissue loosening
of transfer)
–
–
–
Soft tissue
loosening
of transfer
Scoliosis
+
+
+
+
+
+
Egypt, J. Plast. Reconstr. Surg., July 2018 401
Table (3): Shoulder muscle examination compared in four intervals; month zero (pre-operative of 1st stage), month 3-4 (pre-operative of 2nd stage), month 6-7 (after finishing the
limb splining 3 months post-operative of 2nd stage) and month 9-10 (6 months post-operative of 2nd stage).
Case
No.
1
2
3
4
5
6
18y. male
22y. female
36y male
33y. male
42y. male
41y. male
Age &
Gender
0
0
0
0
0
0
Month
0
Preoperative
of
1st stage
15
0
0
15
0
15
Preoperative
Month
3-4
100
100
90
100
110
80
Month
6-7
3 months
postoperative
of
2nd stage
110
120
95
70
110
80
6 months
postoperative
of
2nd stage
Month
9-10
Shoulder abduction
90
40
60
40
90
90
Month
6-7
3 months
postoperative
of
2nd stage
90
90
70
50
90
70
6 months
postoperative
of
2nd stage
Month
9-10
Preoperative
of
2nd stage
Month
3-4
0
0
0
0
0
0
Month
0
Preoperative
of
1st stage
0
0
0
0
0
0
Month
6-7
3 months
postoperative
of
2nd stage
60
50
40
60
80
60
6 months
postoperative
of
2nd stage
Month
9-10
70
30
60
10
70
50
Month
0
Preoperative
of
1st stage
0
0
0
0
0
0
0
0
0
0
0
0
Month
3-4
Preoperative
of
2nd stage
Shoulder flexion External rotation (in abduction)
DISCUSSION
Functionally, the flexion of the elbow is the
main motor function of the upper limb and considered
the most precious [4]. The second important
function is the abduction of the shoulder and the
loss of power of the arm abduction is an incapacitating
condition [5].
C5C6 injury generally affects shoulder abduction
and elbow flexion causing marked disabilities
and deformities of both the biceps and deltoid [6].
However, if C7 has been injured with C5, 6 the
triceps muscle would have been affected and the
wrist extension may be affected as well [2,6].
By target-based analysis of thesedisabilities,
the primary goal in managing their cases is the
combined regaining of both elbow flexion, shoulder
stability and shoulder abduction otherwise the
results would be considered by the patient as unfavorable.
Also, other secondary goals are necessary
to achieve like shorting themanagement time and
regaining adequate shoulder external rotation.
For many surgeons, whenever the time is feasible,
the primary nerve repair is considered to
have the most priority over the other options in
order to deal with the injuries primarily wheneverfeasible
asearly as possible [2]. Unfortunately,
this statement is not the rule in adult brachial plexus
palsies and traditional brachial plexus exploration
and reconstruction may result in poor functional
outcomes [6].
Oberlin's used a nerve transfer from ulnar nerve
to biceps muscle in 1994 as an alternative way to
regain the biceps function [4]. Leechavengvongs
in 1998 reported restoration of biceps function and
elbow flexion MRC power M3 to M4 with the
same technique [7]. Furthermore, Mackinnon's
added other fascicular neurotization of the brachialis
muscle from the ulnar nerve with even better
results [8,9]. Currently, the transfers performed by
those surgeons are gaining more popularity as their
works have created an exciting new strategy in
management of brachial plexus palsy [2]. This
strategy has carried out much quick reinnervation
with higher chances of success [4,10].
In the current study, 6 patients were operated
upon using Obrelin procedure by transferring two
ulnar nerve fascicles selected by a nerve stimulator.
These fascicles usually have beentaken from the
fascicles supplying the wrist flexors and transferred
to the biceps muscle. In the third post-operative
month the flickers or good flexion power have
402 Vol. 42, No. 2 /A Short Scenario for Restoration of Reasonable Limb Function
been primarily noticed. By the end of the tenth
month, half of patients have regained M4 elbow
flexion and the remaining patients have been M3.
Furthermore, the range of elbow flexion has increased
throughout the follow-up visits to reach
120 degree against gravity and mild resistance
(mean 112 degree) with no noticeable deficit in
the hand function as a donor site morbidity. Sungpet
[11] reported the most favorable results by obtaining
MRC 3 or more within 3.3 months in thirty four
out of thirty-six patients when he innervated the
biceps by a single fascicle of the ulnar nerve. Also,
the hand function of this series was not compromised
through a prolonged follow-up period [11].
The present study assumes that waiting for long
graft repair in upper brachial plexus injuries for
restoration the shoulder abduction is not the best
choice. In consistent to our assumption, somsak
[12] invented a nerve transfer to the deltoid from
the nerve of the long head of the triceps muscle.
However, although this is a useful addition for the
management of the brachial plexus injuries it is
not suitable for delayed cases or injured C7 asdonor
branchwould be non-functioning. Also, it would
improve the deltoid function only with no effect
on external rotation.
Although, secondary procedures are generally
usedafter full neurological management and adequate
physiotherapy [2,13,14,15]. In this study, only
regarding the shoulder joint, we assume that it is
not an evidence base attitude. Muscle transfer is
relatively simple techniques with high incidence
of success and comparable functional results. Trapezius,
rhomboid muscles and levator scapulae, in
96% of cases, are usually healthy and available
for transfer [16]. Aziz, Singer and Wolff [17] when
studied trapezius transfer after brachial plexus
palsy, reported that it is a simple procedure with
functional improvement regarding the shoulder
abduction, pain elimination, joint stability and can
be performed in combination with other muscles
transfer to maximize the limb function [16,17]. Also,
he argues that trapezius transfer was compatible
with any progression of the function of the other
shoulder muscles [17].
In the current study, we used in the first stage
reinnervation of suprascapular nerve of the infraspinatus
and supraspinatus muscles nerve in association
with Oberlin neurotization of biceps muscle.
The second stage a combined muscle transfer
(trapezius muscle to the humerus plus latissimus
dorsi to rotator calf and teres major muscle augmenting
this muscle function). By combination
between the two stages we could combine two fast
track methods.
In the present study, by combining muscles
transfer, shoulder abduction ranged from 80 to 120
degree (mean 98 degree) with the mean of shoulder
flexion 77 degree and external rotation 47 degree
after six months follow-up period.
In consistent to the current study, Gilbert et al.,
[18] concluded that trapezius transfer and latissimus
dorsi rerouting resulted in good results. However,
Saha [24] confirmed that when transfer of a single
muscle to replace the deltoid the angle of abduction
did not exceed 90º Chen et al., [19] and Terzis and
Kokkalis [20]. combinedlatissimus dorsi andteres
major transfer to the rotator calf muscles with the
trapezius muscle transfer with significant global
shoulder function improvement. Average abduction
of 120 degree was reported by Narakas [21]. with
trapezius transfer with latissimus dorsi, teres major
and levator scapulae. Also, Karev [22] obtained a
full range of movementin a patient by the same
technique. Chun-lin and Yong-hua [23] reported
seven cases of pectoralis major transfers with
additional trapezius transfer.
Conclusion: Multimodal association between
distal nerves transfer followed by combined transfer
of trapezius, latissimus dorsi and teres major muscles
provides an effective and relatively short
management scenario for upper brachial plexus
injuries in adult patients.