Abstract
Background: The transfer of one or more ulnar nerve fascicles to the
nerve to the biceps can restore elbow flexion in patients with upper brachial
plexus palsy. The purposes of the present retrospective study were to evaluate
the results of this procedure, to measure the delay in reinnervation of the
biceps muscle, and to define the indications for a secondary Steindler
flexorplasty.
Methods: Thirty-two patients with an upper nerve-root brachial
plexus injury were reviewed at an average of thirty-one months after the nerve
fascicle transfer. The average age of the patients was twenty-eight years. The
average time between the injury and the operation was nine months. Patients
were evaluated with regard to reinnervation of the biceps, ulnar nerve
function, elbow flexion strength, and grip strength.
Results: The average time required for reinnervation of the biceps
after nerve fascicle transfer was five months. No motor or sensory deficits
related to the ulnar nerve were noted clinically. The average grip strength at
the time of the last follow-up was 25 kg (an improvement of 9 kg compared with
the preoperative value). After the nerve transfer, twenty-four patients
achieved grade-3 elbow flexion strength or better according to the grading
system of the Medical Research Council. A Steindler flexorplasty was performed
as a secondary procedure in ten patients with persistent grade-3 flexor
strength or worse. In eight of these cases, elbow flexion strength improved
after nerve transfer and flexorplasty. Overall, thirty of the thirty-two
patients achieved a good result (grade-4 strength) or a fair result (grade-3
strength).
Conclusions: We recommend this procedure for brachial plexus
injuries involving the C5-C6 or C5-C6-C7 nerve roots. This procedure spares
the C5 nerve root and other nerves for grafting or transfer elsewhere. A
secondary Steindler flexorplasty is indicated for patients who have persistent
grade-3 elbow flexion strength or worse for at least twelve months after nerve
fascicle transfer.
Level of Evidence: Therapeutic study, Level IV (case
series [no, or historical, control group]). See Instructions to Authors for a
complete description of levels of evidence.
The primary aim of surgery in patients with supraclavicular brachial plexus
palsy is the restoration of elbow flexion. In cases of complete palsy, nerve
reconstruction consists of suturing ruptured nerve roots in the neck to
suitable target nerves by nerve-grafting or nerve transfers from outside the
brachial plexus. In cases of upper brachial plexus palsy involving mainly the
loss of shoulder function and elbow flexion, the C5, C6, and, often, C7 nerve
roots are avulsed from the spinal cord, a condition that precludes
nerve-grafting.
In 1994, we described an alternative approach involving the transfer of one
or more fascicles from the intact ulnar nerve to the nerve to the
biceps1. This
technique is supported by several factors. The reinnervation and recovery of
the biceps provides better results than does palliative treatment, which
includes procedures such as a Steindler flexorplasty and transfers of muscles
such as the pectoralis major, pectoralis minor, or latissimus
dorsi2. The closest
normal nerve to the biceps is the ulnar nerve. This proximity allows for a
direct repair (without the need for intervening nerve grafts) that can result
in rapid reinnervation of the
biceps1. The nerve
to the biceps is very small and needs only a thin fascicle for reinnervation.
The selection of a suitable fascicle for transfer is facilitated by
intraoperative electrical stimulation of the ulnar
nerve1-4.
The purposes of the present study were to evaluate the results of this
procedure in a large series of patients and to obtain additional information
regarding the delay in the reinnervation of the biceps muscle, the functional
status of elbow flexion, the consequences of this transfer on the function of
the hand, and the indications for a secondary Steindler flexorplasty.
Between 1990 and 2000, thirty-two patients (twenty-seven men and five
women) presented with an upper brachial plexus injury
(Table I). Twenty-two patients
had a C5-C6-C7 nerve-root lesion, and ten had a C5-C6 nerve-root lesion. The
average age of the patients was twenty-eight years (range, fifteen to
sixty-six years). The average time between the injury and the nerve transfer
was nine months (range, one and one-half to seventy-five months). The median
preoperative delay was six months. In cases of C5-C6 palsy, the preoperative
grip strength was recorded without any stabilization of the wrist. The average
grip strength in this group was 30 kg (range, 8 to 50 kg). In cases of
C5-C6-C7 palsy, in which the wrist and finger extensors were routinely
paralyzed, the measurement of grip strength was performed by the examiner with
manual stabilization of the patient's wrist in 20° of extension. The
average grip strength in this group was 13 kg (range, 6 to 28 kg). For all
thirty-two patients, the mean preoperative grip strength was 18 kg.
Other nerve transfers were done at the same time as the ulnar nerve
transfer to the biceps nerve. These procedures included twenty transfers of
the spinal accessory nerve onto the suprascapular nerve (nineteen patients) or
the axillary nerve (one patient), six transfers of intercostal nerves onto the
nerve to the long head of the triceps (three patients) or the axillary nerve
(three patients), and five transfers of fascicles from the median nerve to the
nerve supplying the brachialis muscle. We also performed seven procedures in
which the C5 nerve root was grafted onto the long head of the triceps (two
patients), the axillary nerve (four patients), or the suprascapular nerve (one
patient). In addition, seven wrist and finger extension transfers, six
external rotation humeral shaft osteotomies, and one shoulder fusion were
performed.
Operative Technique (Fig.
1)
The incision is performed on the anteromedial aspect of the arm, starting 4
cm distal to the acromion and continuing for a length of 12 cm. The
musculocutaneous nerve is approached medially between the biceps and the
coracobrachialis muscles, and the nerve to the biceps is identified. One must
be aware of the numerous variations in the origin and distribution of the
musculocutaneous nerve. Among these variations, the direct origin of the nerve
to the biceps from the median nerve is not uncommon; we noted this variation
in one patient.
The ulnar nerve is approached at the same level and is identified formally
by means of electrical stimulation. Further dissection is performed under
microscopic magnification. One or more branches to the biceps are identified,
split proximally from the musculocutaneous nerve for approximately 2 cm, and
transected. Usually, the vascular pedicle to the biceps has a more transverse
orientation and does not interfere with the dissection of the nerve. The
distal part of the branch to the biceps is then rotated medially toward the
previously dissected ulnar nerve. The epineurium of the ulnar nerve is
incised. One, two, or three fascicles of adequate size are selected, depending
on the size of the nerve to the biceps. We harvested one fascicle in nineteen
cases, two fascicles in ten cases, and three fascicles in three cases.
The fascicles of the ulnar nerve are then subjected to low-intensity
electrical stimulation. The neurostimulator (Stimuplex Dig; B. Braun,
Bethlehem, Pennsylvania) was applied at a low intensity of 0.02 mA.
It is possible to distinguish precisely between sensory and motor
fascicles. Occasionally, one is able to locate fascicles in the extrinsic
flexor muscles that are separate from those supplying the intrinsic muscles of
the hand. In these cases, the fascicles innervating the extrinsic flexors are
selected for transfer. These fascicles are often located anteriorly and
medially within the ulnar nerve. The chosen fascicle or fascicles are
separated from the rest of the ulnar nerve over a distance of 2 cm and are
divided distally. The fascicles are turned laterally and superiorly and are
sutured to the nerve to the biceps with three interrupted 11/0 nylon sutures
under an operating microscope.
Rehabilitation
Postoperatively, the entire upper extremity is immobilized in a
thoracobrachial jersey with the elbow held in 90° of flexion for a period
of three weeks. The jersey is then removed, a simple cuff-and-collar sling is
worn, and passive range-of-motion exercises of the elbow are encouraged for a
period of three weeks. At six weeks, the patient begins a physiotherapy
protocol that includes exercises such as compressing a tennis ball in order to
increase grip strength.
As soon as the earliest contractions in the biceps are seen, the patient is
asked to initiate active supination exercises to increase biceps strength. Our
patients usually continued physiotherapy for nine months after the first
contraction of the biceps muscle was noted.
Evaluation
The elbow flexion strength was recorded periodically in all patients with
use of the grading system of the Medical Research Council until the time of
the last follow-up. A poor result was defined as grade-0, 1, or 2 strength; a
fair result was defined as grade-3 strength; and a good result was defined as
grade-4 or 5 strength. In the group with grade-4 strength, we developed a more
detailed technique for the measurement of strength. With this technique,
various weights were placed in the hand of the patient with the elbow extended
and then the patient was asked to flex the elbow once to 90°
(Fig. 2). The heaviest weight
that could be lifted was recorded in kilograms.
All patients were advised to note the first clinical sign of biceps muscle
contractions, and we palpated the contraction of the biceps during active
elbow flexion to monitor muscle recovery. The deficit in the ulnar nerve was
assessed clinically. We performed clinical motor testing of all muscles,
including the intrinsic muscles of the hand. Two-point discrimination in the
small finger also was measured. We did not use electrodiagnostic tests because
no objective clinical deficit was observed.
Grip strength was assessed with the Jamar dynamometer (Asimow Engineering,
Santa Fe Springs, California).
Nerve Transfers Prior to Steindler Flexorplasty
The average duration of follow-up was thirty-one months (range, nine to
seventy-four months). Twenty patients had a good result (grade-4 strength),
four had a fair result (grade-3 strength), and eight had a poor result
(grade-2 strength or worse); of the eight patients with a poor result, four
had grade-2 strength and four had grade-0 strength. The twenty patients with a
good result had an average elbow flexion strength of 4.2 kg. Of the ten
patients with a C5-C6 lesion, six had a good result, two had a fair result,
and two had a poor result. Of the twenty-two patients who had a C5-C6-C7
lesion, fourteen had a good result, two had a fair result, and six had a poor
result.
When the three patients who were operated on at two years (Cases 6 and 9)
and six years (Case 7) are excluded, twenty-four (83%) of the twenty-nine
remaining patients had a good or fair result.
Delay of Reinnervation
The average time required for the first biceps contraction to be felt by
the patient was five months (range, three to nine months), and the average
time required to achieve grade-3 elbow flexion strength was eight and one-half
months (range, five to thirteen months).
Grip Strength and Deficit in the Ulnar Nerve
The average postoperative grip strength was 36 kg for patients with C5-C6
lesions and 24 kg (with the wrist stabilized) for patients with C5-C6-C7
lesions. The average postoperative grip strength for all patients was 25.3 kg.
The average improvement in grip strength when the preoperative value was
compared with the latest postoperative value was 9 kg, despite the harvesting
of one or more ulnar nerve fascicles.
While three patients reported transient paresthesias in the little finger
for a few weeks postoperatively, these symptoms subsided spontaneously and no
appreciable deficit in ulnar nerve function was identified in any patient at
the time of the most recent follow-up.
Steindler Flexorplasty After Nerve Transfer
A Steindler flexorplasty was only indicated in cases in which the nerve
transfer resulted in the restoration of elbow flexion strength to grade 3 or
less.
Eleven patients underwent a complementary Steindler flexorplasty to
increase elbow flexion strength. One patient (Case 21), who was sixty-six
years old, underwent the nerve transfer and flexorplasty at the same time.
This patient achieved grade-4 elbow flexion strength, was able to lift 9 kg on
the strength test, and had a quite appreciable contraction of the biceps.
For the other ten patients, the average delay between the nerve transfer
and the flexorplasty was nineteen months (minimum, twelve months). Following
the nerve transfer, eight patients had a poor result (including four patients
with grade-2 strength and four with grade-0 strength), and two had a fair
result (grade-3 strength). At an average of twenty-six months after the
flexorplasty, six patients had grade-4 strength (with the ability to lift an
average of 3 kg on the strength test), two had grade-3 strength, and two had
grade-2 strength.
The mean range of active elbow motion was from 30° to 120°, and the
mean range of passive elbow motion was from 10° to 120°.
Overall, grade-3 or 4 elbow flexion strength was achieved in twenty-four
patients after nerve transfer and in eight additional cases after nerve
transfer and flexorplasty. (Two patients had a fair result before the
flexorplasty procedure.)
Other Procedures
For suprascapular nerve palsies, we performed nineteen neurotizations from
the spinal accessory nerve and one grafting procedure involving the C5 nerve
root. Thirteen of these procedures were associated with a good result, with
stabilization of the shoulder and an average postoperative external rotation
of 41°, and seven failed. For axillary nerve palsies, we performed three
neurotizations from intercostal nerves, one neurotization from the spinal
accessory nerve, and four grafting procedures involving the C5 nerve root.
Five of these procedures were associated with a good result, with average
active abduction of 63°, and three were associated with a poor result,
without active abduction. For the nerve to the long head of the triceps, we
performed three neurotizations from intercostal nerves and two grafting
procedures involving the C5 nerve root. All five of these procedures were
associated with a good result, with grade-4 strength of the triceps
muscle.
The first issue that needs to be addressed is the possibility of motor or
sensory deficit in the hand after this procedure. Usually, the patient
complains of some tingling or paresthesias in the little finger for a few days
or weeks after the nerve
transfer1,2.
These symptoms seem to be due to the intraneural dissection, rather than to
the sectioning of some motor fascicles, because they disappear quite rapidly.
Occasionally, the grip strength is slightly reduced in the immediate
postoperative period, perhaps because of the pain resulting from the surgical
approach. After longer follow-up, the grip strength is constantly greater than
that noted preoperatively. In the present series, the mean improvement in grip
strength was 9 kg, despite the harvesting of one or more ulnar fascicles. This
improvement can be explained in one of two ways. First, in cases of upper
nerve root avulsion, lower nerve roots, if injured, might recover with
additional time. Second, in the absence of elbow flexion, the hand is not used
by the patient, thus resulting in a transient weakening of the grip. However,
as elbow flexion and better hand-placement capabilities are recovered, grip
strength is also recovered because of the ability to perform more activities
with the hand. Other authors who have investigated this technique also have
reported no ulnar nerve
morbidity2,4.
Eight patients had a poor result (with grade-2 elbow flexion strength or
less), including three patients (Cases 6, 7, and 9) in whom the preoperative
delay was extremely long. However, the nerve transfer provided a good result
in two patients (Cases 2 and 24) in whom the operation was performed one year
after the injury and a poor result (grade-2 elbow flexion strength) in one
patient (Case 9) who presented twenty-seven months after a failed procedure in
which the C5 nerve root had been grafted onto the musculocutaneous nerve. This
last patient (Case 9) underwent a Steindler flexorplasty nine months after the
nerve transfer, resulting in grade-4 elbow flexion. At the time of the last
follow-up at three years after the time of presentation, the volume and
strength of the biceps were excellent. In our opinion, the flexorplasty was
performed too early after the nerve surgery, before the biceps had had
sufficient time to recover. However, we have to keep in mind that the overall
quality of our results was closely related to the short delay between the
injury and the nerve reconstruction (Fig.
3), as has been reported by authors in association with the use of
other nerve-transfer
procedures5,6.
The higher rate of satisfactory results reported by Sungpet et
al.4, in a study of
thirty-six cases, and Leechavengvongs et
al.2, in a study of
thirty-two cases, may have been due to the shorter preoperative delay in their
series (no more than eight and twelve months, respectively).
Two of the eight patients in the present study who had a poor result had
had a preoperative grip strength of <7 kg. This finding suggests that these
patients had additional nerve lesions at the lower root level. As it is
difficult to determine the final extent of recovery, the decision to perform
the nerve-transfer procedure depends on the time elapsed since the injury
(with shorter times being associated with better results), the age of the
patient (with younger patients tending to have better results), and the
alternative procedures performed. The findings of the present study support
the findings of Brandt and
Mackinnon7, who
recommended nerve transfers over muscle transfers.
Originally, we preferred to reserve this transfer for patients who had
avulsion of the C5, C6, and/or C7 nerve roots in whom direct nerve
reconstruction was not possible. Subsequently, our
results1,3
and those published in the
literature2,4,8,9
prompted us to utilize this technique for all patients who had a C5-C6 palsy
because the results are rapid and are better than those associated with
procedures involving nerve-grafting from the cervical area or other nerve
transfers. There are two main reasons to perform transfer of fascicles from
the ulnar nerve to the nerve to the biceps. First, the ulnar nerve is the
nearest nerve to the bicipital (motor) branch of the musculocutaneous nerve,
and a direct transfer of one or more fascicles from the ulnar nerve to the
branch to the biceps does not waste any donor nerve fibers to the sensory part
of the musculocutaneous nerve as occurs in association with traditional nerve
transfers involving the intercostal nerves, the spinal accessory nerve, or the
phrenic nerve. Second, all of these other nerves are far from the target organ
(the motor end plates of the biceps muscle) as compared with the short
distance between the ulnar fascicles and the biceps. Therefore, the rate of
recovery of the biceps after transfer of one or more fascicles from the ulnar
nerve is faster than that after the more classical nerve
transfers10-18.
We now recommend that the Steindler flexorplasty not be performed earlier
than twelve months after nerve transfer if the biceps has grade-0, 1, or 2
strength and not earlier than fifteen months if the biceps has grade-3
strength. Furthermore, in patients who are able to initiate flexion with the
reinnervated biceps, the Steindler flexorplasty does not need to be performed
as has been recommended in the literature. If the patient can initiate elbow
flexion after nerve transfer but lacks the desired power, the Steindler
procedure can be performed in a manner that does not lead to a flexion
contracture19.
Steindler's original idea was to move the insertion of the flexor pronator
mass proximally on the humerus by 6 to 7 cm in order to emphasize its role in
elbow flexion. Doing so had the drawback of aggravating the Steindler effect
(wrist and finger flexion when the elbow flexes) and any elbow flexion
contracture. This is the reason that we move the insertion only 4 cm
proximally. In our opinion, the Steindler flexorplasty is especially useful
for patients who can initiate elbow flexion with the insufficient but
reinnervated biceps (that is, those who have grade-2 or 3 strength) after
nerve transfer.
The technique of transfer of one or more ulnar nerve fascicles to the nerve
to the biceps is easy to perform, does not require multiple or extensive
incisions, and can be performed without special training in brachial plexus
surgery. No nerve graft is required, and a direct end-to-end suture (at only
one site) allows for a quick recovery. As the donor nerve is very near to the
end organ (the end plates of the biceps muscle), the time required for
recovery is relatively short compared with that associated with other
techniques. Furthermore, because the fascicles that are chosen are purely
motor and are directly transferred to the motor fibers of the biceps, no axons
are wasted on the sensory component of the musculocutaneous nerve and there is
little chance of axonal confusion as can occur in the case of cervical root
grafting or intercostal nerve transfer to the musculocutaneous nerve.
This procedure also has the advantage that it can be used for patients in
whom other nerve transfers have led to poor results, such as elderly patients
and those who are seen after a very long delay (as long as one year) after the
injury. Lastly, there is no clinically appreciable nerve deficit after the
transfer, and grip strength is consistently stronger postoperatively.
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