Keywords brachial plexus - nerve graft - vascularized ulnar nerve - allograft
Introduction
Restoring elbow flexion is a priority in adults with complete brachial plexus palsy.
If the upper nerve roots are not avulsed, a graft can be used to restore flexion.[1 ] Currently, the preferred technique uses the sural nerve.[2 ] This long graft, however, does not have a feeder artery to ensure its survival with
a high risk of central necrosis.[3 ] For this reason, vascularized nerve grafts have been introduced in 1976, by Taylor
and Ham. They were the first to describe using vascularized grafts to improve the
outcomes of long nerve grafts, aiming to reduce the likelihood of necrosis of the
interposed nerve graft.[1 ] The aim of this study was to evaluate the outcomes of using pedicled vascularized
ulnar nerve grafts to restore active elbow flexion in adults with complete brachial
plexus palsy.
Materials and Methods
This retrospective case series consisted of 20 men who had complete brachial plexus
palsy secondary to a motorcycle accident. The mean patient age was 31 years (15–60).
The patients were operated a mean of 5 months (2–7) after the accident. All patients
underwent a magnetic resonance imaging beforehand to confirm the upper cervical nerve
roots were not avulsed.
With the patient under general anesthesia, the cervical area was explored to confirm
the C5 or C6 nerve root was available for grafting. When a root was available, a vascularized
ulnar nerve harvested from the ipsilateral arm was used a graft on the motor portion
of the musculocutaneous nerve. The vascularized graft was 19 cm long, on average (14–20).
In two patients, since another root was available for grafting, a nonvascularized
graft (the remaining ulnar nerve) was added between C6 and the median nerve trunk
([Fig. 1 ]).
Fig. 1 Intraoperative photos (right upper limb). —of distal suturing of a vascularized ulnar
nerve graft (UNG) on the musculocutaneous nerve (MC) to restore elbow flexion. —of
the transfer of 3 intercostal nerves (ICN) on the long head of triceps nerve (LHTN)
to restore elbow extension. —of a nonvascularized ulnar nerve graft remnant (NVUN)
being transferred on the median nerve (MN) to restore finger flexion.
The vascularized graft was turned around its vascular pedicle and slipped into a subcutaneous
tunnel until the cervical region, where it is sutured to the target nerve root ([Fig. 2 ]). Using a microscope, epiperineural suturing was done and supplemented by fibrin
glue. The patient's arm was immobilized for 6 weeks; rehabilitation was initiated
to mobilize the joints and reduce the risk of stiffness.
Fig. 2 Schema of the vascularized ulnar nerve graft technique. The ulnar nerve is severed
at the wrist and then turned around its pedicle, the distal part becomes proximal
and is sutured to the root, and the proximal part becomes distal and is sutured to
the musculocutaneous nerve.
Results
The mean follow-up was 38 months (16–120). Six patients recovered M4 elbow flexion
strength on the Medical Research Council scale ([Fig. 3 ]). Five patients had M2 strength, 4 had M1, and 5 had M0. None of the patients had
M3 strength. On average, recovery of elbow strength took 17 months (10–22). None of
the patients had persistent pain due to pseudo-Tinel sign sensations during percussion
of the cervical area ([Table 1 ]).
Fig. 3 Graph of motor recovery after ulnar vascularized graft for elbow flexion (according
the classification of British Medical Council: M0: No muscle activation; M1: Trace
muscle activation, such as a twitch, without achieving full range of motion; M2: Muscle
activation with gravity eliminated, achieving full range of motion; M3: Muscle activation
against gravity, full range of motion; M4: Muscle activation against some resistance,
full range of motion; M5: Muscle activation against examiner's full resistance, full
range of motion.
Table 1
Patient data summary
Age (y)
Sex
Time before surgery (mo)
Ruptured
roots
Avulsed roots
Grafted root to MCN nerve
Vascularized ulnar nerve length (cm)
Elbow flexion (BMC scale)
Other procedures
Patient 1
27
M
4
C5C6
C7T1
C5
20
M4
SAN to SSN/ICN to LHTN
Patient 2
29
M
2
C5T1
C5
20
M4
Shoulder fusion/ICN to LHTN/ FL Transfer
Patient 3
16
M
4
C5C6
C7T1
C5
20
M4
SAN to SSN/ICN to LHTN
Patient 4
30
M
4
C5C6
C7T1
C6
19
M4
SAN to SSN/ICN to LHTN
Patient 5
23
M
7
C5C6
C7T1
C5
14
M2
SAN to SSN/ICN to LHTN
Patient 6
35
M
6
C5T1
C5
16
M2
C6 median (NVUN) (shoulder fusion refused)
Patient 7
54
F
2
C5C6
C7T1
C6
20
M1
SAN to SSN/ICN to LHTN
Patient 8
17
M
6
C5C6
C7T1
C5
19
M2
C6 median (SG)/SSN grafting/ICN to LHTN
Patient 9
38
M
2
C5C6
C7T1
C5
20
M0
Trapezius transfer/ICN to LHTN
Patient 10
60
M
6
C5
C6T1
C5
17
M0
SAN to SSN
Patient 11
15
M
5
C5C6C7
C8T1
C6
20
M4
C7 median/shoulder fusion/ICN to LHTN
Patient 12
35
M
3
C5C6
C7T1
C5
19
M1
SAN to SSN/ICN to LHTN
Patient 13
18
F
3
C5C6
C7T1
C5
20
M2
C6 median (SG)/shoulder fusion
Patient 14
35
M
5
C5C6C7
C8T1
C5
19
M4
C6 median (SG)/shoulder fusion
Patient 15
32
F
5
C5C6C7
C8T1
C5
20
M1
C6 median (SG)/shoulder fusion refused
Patient 16
27
M
6
C5T1
C5
19
M0
C6 median (SG)/shoulder fusion
Patient 17
18
M
6
C5C6C7
C8T1
C5
18
M0
C6 median (NVUN)/SSN recovery/ICN to LHTN
Patient 18
31
M
5
C5T1
C5
20
M1
Shoulder fusion
Patient 19
19
M
5
C5T1
C5
19
M2
Shoulder fusion
Patient 20
27
M
6
C5C6
C7T1
C5
20
M0
SSN to SAN
Abbreviations: F, female; FL, fascia lata; ICN intercostal nerve; LHTN, long head
of the triceps nerve; M, male; MCN, musculocutaneous nerve; NVUN, nonvascularized
ulnar nerve; SAN, spinal accessory nerve; SG, sural graft; SSN, suprascapular nerve.
Discussion
The results in terms of muscle strength are poor in our series, with only 30% of M4
results. These results are comparable with those reported in the literature. As a
matter of fact, in a case series of eight patients with complete brachial plexus palsy,
Bertelli et al. did a C5 root graft onto the musculocutaneous nerve using a vascularized
ulnar graft. At more than 2 years' follow-up, six patients had achieved M2 strength
only in their biceps.[4 ] The results reported by Birch et al.[5 ] appear better, likely because their grafts were shorter (14 cm) than ours since
they were sutured onto secondary trunks (given that patients had a retroclavicular
injury), which led to faster muscle reinnervation and therefore, better motor recovery.
After placing a vascularized ulnar nerve graft between the C5 root and the median
nerve, Chang et al. reported that 75% of their 25 patients had M3 finger flexion strength,[6 ] which is a poor functional result.
It is difficult to explain why the results with this technique are inadequate. The
vascularization provided by the accompanying artery may not be sufficient to vascularize
the entire nerve after its distal end is cut. Thrombosis after pedicle or artery manipulation
is another potential explanation, as is spontaneous thrombosis of the extended artery
after its distal end is cut. Questions about the suturing's effectiveness are natural
when nerve surgery fails. However, the diameter of the ulnar nerve corresponds exactly
to that of the torn nerve roots, making the graft and root anatomically compatible.
Also, microsurgical suturing is done in a comfortable and reproducible anatomical
environment. Lastly, the repairs are sufficiently permeable, since 13 of our patients
had achieved M1 to M4 strength and nerve regrowth was occurring based on the Tinel
sign, although it did not reach the motor end-plates for sufficient recovery to M3.
Our conclusion that the nerve root was graftable from a macro- and microscopic perspective
can be brought into question and may be another reason for failure. Here again, several
studies that did not confirm the nerve root was available for grafting based on trimmed
nerve specimens examined by histopathology still reported satisfactory results with
shorter grafts. Lastly, none of the well-known patient-specific factors that limit
nerve regrowth, such as smoking were present in our case series.[7 ]
The lack of a control group with conventional sural grafts is a limitation of our
study. However, there are many published studies describing acceptable, but sometimes
inconsistent results with this type of graft with no more than 55% of M3 to M4 active
elbow flexion,[8 ] even though the use of a sural nerve remains the most commonly used technique for
brachial plexus reconstruction in most international teams.[2 ]
The 3-year follow-up period appears to be sufficient. In fact, motor recovery can
take up to 2 years after this type of surgery.[5 ] The time elapsed between the accident, and the surgery impacts recovery. All the
patients in our case series were operated within 5 months on average, a time frame
in which the prognosis is best.[9 ] Chronic denervation of the ulnar nerve due to an initially complex brachial plexus
injury can also explain the lower effectiveness of the denervated graft,[10 ] we believe this is the primary reason for these results.
Excessive regrowth related to graft vascularization and the magnitude of intraneural
connections in the ulnar nerve may explain the worse results for this type of graft,
as shown by Bertelli et al.[11 ] While the radial or sural nerve has been used as vascularized grafts they are currently
not used for brachial plexus injuries.[12 ]
[13 ] Using a nonvascularized allograft has not yet been evaluated in adult brachial plexus
injuries, although some authors have published encouraging results for the repair
of injuries to the large peripheral nerve trunks.[14 ]
Conclusion
While the principle is attractive from an intellectual point of view, the outcomes
of using long vascularized ulnar nerve grafts do not yield consistently satisfactory
results when used to restore elbow flexion in adults with complete brachial plexus
palsy. We now use these graft only when a nerve transfer cannot be done, or the sural
nerve cannot be used as a free graft. The use of a vascularized sural nerve for long
grafts in the management of long grafts in brachial plexus palsy could be a suitable
solution involving the use of a healthy nerve with sufficient vascularization to avoid
graft necrosis. A clinical study should be proposed to confirm this hypothesis.
