Summary

Avulsion of nerve roots from the spinal cord is widely regarded as an
untreatable injury. However, a series of experiments in animals has shown
that, if continuity is restored between spinal cord and ventral roots,
axons from spinal motor neurons can regrow into the peripheral nerves with
recovery of motor function. These observations were applied in the
treatment of a man with avulsion of the 6th cervical (C6) to 1st thoracic
roots due to brachial plexus injury. Two ventral roots were implanted into
the spinal cord through slits in the pia mater, C6 directly and C7 via
sural nerve grafts.

Voluntary activity in proximal arm muscles was detected
electromyographically after nine months and clinically after one year.
After three years the patient had voluntary activity (with some
co-contraction) in the deltoid, biceps, and triceps muscles. To determine
whether the improvement was due to spontaneous recovery from C5, the C5
root was blocked pharmacologically, and the results indicated that the
repaired roots were contributing substantially to motor function.

Repair of spinal nerve roots deserves further exploration in management of
brachial plexus injury.

Lancet 1995; 346: 1323-25

Introduction

Avulsion of nerve roots from the spinal cord is a devastating injury with a
bleak prognosis.[1] Unfortunately it is common after severe traction on the
brachial plexus.' Reimplantation has been tried experimentally[3] but
surgical repair has been judged futile.[4] Theoretical reasons for
pessimism are that injury close to the perikarya is likely to kill many of
the motor neurons; that motor neurites will not regenerate within central
nervous tissue; and that, even if the nerve defect is bridged, functional
synapses with appropriate muscles will not be achieved.

These matters have been addressed in long series of animal experiments
prompted by the original observation that, after separation within the
spinal cord, axons from spinal cord motor neurons can grow into ventral
roots and peripheral nerves.[5] Half of the motor neuron population
survived the injury and their axons regrew into the ventral roots within a
month after the injury.[6] Implantation of avulsed ventral roots was shown
to promote motor recovery in rats,[7] cats,[8] and non-human primates;[9]
and functional integration of regenerated neurons in spinal cord circuits
was demonstrated by intracellular techniques and by staining.[8] Initial
growth of axons within the spinal cord was associated with tissue
components specific for regeneration within the peripheral nervous
system--for example, laminin and the low-affinity neurotrophin
receptor.[10] In primate experiments whereby the avulsed roots were
implanted immediately after avulsion, there was no loss of neurons. Because
muscle reinnervation derived from various populations of spinal neurons[9]
one might have expected functional chaos, with attempts at voluntary
contraction producing wholesale and uncoordinated activation.
Electromyographic recordings did indeed demonstrate simultaneous
contractions in agonist and antagonist muscle groups, and isolated
voluntary activation of either group proved impossible. However, with
maturation of the re-established neuromuscular network, gross arm movement
became more dextrous. These encouraging results led us to attempt
reimplantation of avulsed ventral roots in a patient with brachial plexus
injury.

Case-report

In a motor-cycle accident a man aged 25 sustained blunt trauma to the left
shoulder which resulted in fracture of the clavicle and a flail arm and
hand. He had a Horner syndrome and there was total absence of motor
function in the shoulder, arm, and hand. The anterior part of the shoulder
was dysaesthesic but sensation was normal over the lateral and dorsal areas
and in the proximal arm. The rest of the arm was without sensation.
Electromyography one month after the trauma showed slight voluntary
activity only in the supraspinatus muscle; biceps was totally denervated
(figure 1).

The proximal part of the brachial plexus was explored one month after the
accident by a posterior subscapular approach.[11] The 5th, 6th, and 7th
cervical (C5-7) spinal nerves were in continuity as far as the
intervertebral foramina, whereas C8 and the 1st thoracic (T1) had been torn
out of the spinal canal. A left-sided laminectomy was performed from C5 to
C7, including partial facetectomy of C6 and C7. Incision of the dura
revealed that the C5 ventral and dorsal roots were in continuity with the
spinal cord but the C6 to T1 roots were avulsed (figure 2). The ventral
roots were implanted into the ventrolateral spinal cord, C6 directly and C7
via three 7-8 cm sural nerve grafts. The nerve rootlets or grafts were
pushed into the cord through small slits in the pia mater. So as not to
interfere with fibre tracts and other elements, they were placed just below
the surface of the cord and secured with tissue glue (Tisseal);[12]
experimentally we had found that grafts were quickly fixed in position by
pial scarring?

Results

Voluntary activity in proximal arm muscles was first detected
electromyographically nine months after surgery (figure 1) and clinically
in the deltoid, biceps, and triceps muscles at one year. At 3 years power
in the biceps was M4 on the Medical Research Council scale of 1-5, and the
patient had voluntary activity also in the deltoid (M2), triceps (M1- 2),
and brachioradialis (M1-2). When the elbow was flexed, co-contractions in
the deltoid and extensors were clinically detectable; he was unable to
activate the deltoid in isolation.

To assess how much of the improvement was due to spontaneous recovery from
the remaining C5 root, we selectively blocked conduction in the C5 spinal
nerve with 3 mL 2% lignocaine (figure 3). Soon after injection the power of
the deltoid muscle was greatly reduced, with corresponding
electromyographic changes (figure 4). At the time of maximum reduction the
patient noticed pronounced anaesthesia of overlying skin. In biceps, by
contrast, the changes were small and transient, with full recovery at 60
min--a time when recovery of the deltoid was still incomplete.

Discussion

Might the functional recovery in this patient be attributable to something
other than the nerve reimplantations? The results of the nerve-block test
indicated that the implanted roots contributed substantially. A further
consideration is plasticity of motor centres, with reorganisation of the
motor cortex after the avulsion trauma. However, when an area is deprived
of its peripheral effectors this is usually compensated by enlargement of
neighbouring motor representations supplying other effectors.[13] Therefore
in this patient the recovery was unlikely to be due to neuroplasticity.

The observations in this case suggest that an active surgical approach to
ventral root avulsions, if applied early, may lead to recovery of useful
function in proximal muscles. This method deserves further exploration in
the management of brachial plexus injuries.

This work was supported by the Swedish Medical Research Council (project
7127), the Karolinska Institute, the International Research Institute for
Paraplegia, the International Spinal Research Trust, Claes Groschinky' s
Minnesfond, Harald Jeanssons Stiftelse and Harald and Greta Jeanssons
Stiftelse, Ake Wibergs Stiftelse, and the Independent Order of Oddfellows
in Stockholm. We thank Dr Staffan Cullheim for reviewing the paper.

GRAPH: Figure 1: Preoperative and postoperative electromyograms; EMGs made
with concentric needle electrode (Judex Datasystem) and four- channel
recorder (Dantec Counterpoint). Upper overview windows display 2 s of
continuous EMG; vertical cursors in these windows delimit the part of the
record shown in expanded time scale (5 ms/division) in lower left window.;
(A) Needle movement in biceps elicits insertion activity; no denervation
activity and no activity during attempts at voluntary contraction. B, 5 mo
postoperative. Needle insertion provokes long bursts of denervation
activity; no activity during attempts at voluntary contraction. (C, D) 9 mo
postoperative. Denervation activity persists; however, occasional
polypbasic motor unit potentials in response to attempted muscle
contraction (D).

DIAGRAM: Figure 2: Operative appearances; (A) Avulsion of C6-8 and T1
roots. (B) Root reimplantations.

PHOTO (BLACK & WHITE): Figure 3: Radiograph showing Localisation of
blocking agent to C5 spinal nerve; Needle was positioned under radiological
control, then blocking agent (labelled with Omnipaque), shown by arrow, was
injected through a catheter.

DIAGRAM: Figure 4: Electromyograms at 3 years, with C5 block EMGs recorded
on Medelec MS91 machine: A-D, biceps; E-H, deltoid.; EMG activity at
maximum voluntary effort before (A and E) and 20 min (B and F) and 60 min
(D and H) after injection of lignocaine.

References

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4 Seddon HJ. Surgical disorders of the peripheral nerves. Baltimore:
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5 Risling M, Cullheim S, Hildebrand C. Reinnervation of the ventral root L7
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12 Carlstedt T Le futur. Reparation de lesions supraganglionaires du plexus
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~~~~~~~~

By Departments of Orthopaedics (T Carlstedt MD), Neuroradiology (P Grane
MD), and Neurosurgery (R G Hallin MD), Karolinska Hospital; and Department
of Neuroscience (G Noren MD, T Carlstedt), Karolinska Institute, Stockholm,
Sweden

By T Carlstedt, P Grane, R G Hallin, G Noren Correspondence to: Dr T
Carlstedt, Department of Orthopaedics, Karolinska Hospital, S-17176
Stockholm, Sweden

Copyright 1995 by Lancet. Text may not be copied without the express
written permission of Lancet.

Carlstedt, et, Return of function after spinal cord implantation of....,
Vol. 346, Lancet, 11-18-1995, pp 1323.
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