Download repair of avulsed cervical nerve roots

REPAIR
AN
T.
OF
AVULSED
EXPERIMENTAL
E. J. HEMS,
From
An
STUDY
IN
R. E. CLUTFON,
the University
experimental
CERVICAL
M.
ofEdinburgh
model
A.
GLASBY
School,
established
Scotland
to investigate
the possibility
of repairing
cervical
nerve roots avulsed
from the spinal cord, as occurs
in traction
injuries
of
the brachial
plexus.
In five sheep
the C6 root was
avulsed
and the ventral
root was reattached
using
freeze-thawed
muscle as a short graft (0.5 cm).
Recovery
was assessed
after one year by electrophysiology
and histology.
Stimulation
of the root
produced
muscle contractions
in four out offive sheep.
Action
potentials
were recorded
distal to the grafts in
all five sheep. Histological
examination
showed
regenerated
fibres in the ventral
roots in all cases. These
fibres could be traced distally
to the brachial
plexus.
Our study confirms
that motor fibres can regenerate out of the spinal cord into the ventral
roots and
reinnervate
muscles,
and suggests
that reimplantation
of avulsed
roots is a surgical
option in selected
cases of
traction
injury of the brachial
plexus.
J Bonefoint
Received
Surg
[Br]
25 January
1994;
1994;
76-B:818-23.
Accepted
11 March
ROOTS
SHEEP
Medical
was
NERVE
1994
Traction
injuries
to the brachial
plexus
usually
result from
road-traffic
accidents,
and often
occur
in young
people.
They
have
a devastating
effect
on the function
of the
upper
limb.
In recent
years
surgical
exploration
of the
brachial
plexus
with excision
and grafting
of damaged
areas
has become
more common
(Jamieson
and Bonney
1979;
Birch
1992).
Damage
proximal
to the dorsal
root
ganglion,
however,
is not amenable
to surgical
repair
(Bonney
1991;
Millesi
1991).
Traction
on nerve
roots
usually
results
in avulsion
from the surface
of the spinal
cord
(Sunderland
1974)
and may
be associated
with
damage
to the cord
itself.
Recent
work
has raised
the
possibility
of the repair
of nerve
roots avulsed
from the
spinal
cord (Carlstedt
1991; Hems and Glasby
1992).
There
is considerable
experimental
evidence
to
suggest
cell
that
bodies
axons
in the
ventral
in the
anterior
grey
roots,
horn
which
of the
have
spinal
their
cord,
can regenerate
distally
in a manner
similar
to those which
have been divided
in a peripheral
nerve (Kilvington
1907;
Tower
1943;
Moyer
and Kimmel
1948;
Christophersen
and Wintsch
1977; Carlstedt
Ct al 1986;
Hems and Glasby
1992).
Carlstedt
et a! (1986)
showed
in the rat that axons
can
grow
out of the spinal
cord
into
ventral
roots
reimplanted
after avulsion
and that they make functional
connections.
Cullheim
vation
of muscles
the dorsal
roots
ganglion.
Useful
et a! (1989)
demonstrated
in similar
experiments
have their cell bodies
regeneration
would
reinner-
in cats. Fibres
in
in the dorsal
root
therefore
require
fibres
to grow
into
the spinal
cord
and
make
new
connections
in the CNS.
The classical
view
is that this
cannot
occur;
this was confirmed
by Carlstedt
et a! (1989)
in adult
animals.
Reinnervation
of the cord from dorsal
roots may be possible
in neonates.
We have established
an experimental
model
in the
T. E. J. Hems,
MA, DM, FRCS,
FRCS
Ed, Senior
Orthopaedic
Surgery
John Radcliffe
Hospital,
Headington,
Oxford
OX3
Registrar
9DU,
in Trauma
and
C6 root (the highest
UK.
R. E. Clutton,
BVSc,
DVA, MRCVS,
Lecturer
in Veterinary
Anaesthesia
Royal (Dick)
Veterinary
School,
University
of Edinburgh,
Veterinary
Field
Station,
Easter
Bush, Roslin,
Midlothian
EH2S 9RG, UK.
M. A. Glasby,
MA, MSc, FRCS, FRCS Ed, Reader
Department
of Anatomy,
University
of Edinburgh
Place, Edinburgh
EH8 9AG, UK.
Correspondence
©1994
British
0301-620X/94/S84S
818
should
be sent
Editorial
Society
$2.00
in Anatomy
Medical
School,
to Mr M. A. Glasby.
of Bone
and Joint
Surgery
sheep
for the study
(Hems
and Glasby
simulate
the human
Teviot
plexus)
was
caused
only
was divided
found
of the repair
of cervical
nerve
roots
1992).
A large animal
was selected
to
situation
as closely
as possible.
The
root contributing
to the sheep
to be surgically
minor
proximal
and repaired
accessible
forelimb
proximal
brachial
and division
weakness.
to the root
The root
ganglion.
Evidence
of regeneration
was found
in the ventral
The present
study
extends
this work
to investigate
roots.
the
repair
of roots
avulsed
recovery
of function.
assess
Freeze-thawed
from
muscle
ThE
the
cord
autografts
JOURNAL
OF BONE
and
were
to
used
AND JOINT
in the
SURGERY
REPAIR
repairs
since
method
of
they
have
(Glasby
1991a,b).
et a! 1986a;
Glasby
et a! 1990;
As there appears
to be no possibility
repair
regeneration
of
in the
been
short
shown
defects
dorsal
roots
facilitate
access
to the ventral
possibility
of fibres
crossing
dorsal
roots.
MATERIALS
to be
these
not
Pereira
et a!
of effective
were
removed
was
microscope
to
any
and
divided
give
access
from
Before
the first
water,
was withheld
for 12 to
medication
was xylazine
hydro-
chloride
(Rompun;
Bayer,
Newbury,
UK)
0.2 mg/kg
given
intravenously.
Five minutes
later anaesthesia
was
induced
with
ketamine,
2 to 4 mg/kg
intravenously
(Ketalar;
Parke-Davis,
Eastleigh,
Hampshire,
UK). The
the dura.
Heerbrug
The
lateral
using
Under
M690)
dorsal
edge
to the ventral
the cord
ends
outside
(Wild,
longitudinally.
removed.
The
an operating
the dura
was
opened
rootlets
were
divided
of the dura was retracted
rootlets
which
a Rhoton
nerve
and
to
were
then
avulsed
hook
and
the torn
trimmed.
spinae,
water
for the experiment.
food,
but
Preanaesthetic
of which
nerves
819
ROOTS
NERVE
A piece
sheep
procedure
18 hours.
CERVICAL
effective
roots
and to prevent
between
the ventral
METhODS
five
an
in peripheral
AND
We used
OF AVULSED
of muscle
was
obtained
from
frozen
in liquid
nitrogen,
and
as previously
described
(Glasby
small
piece
(0.5 cm),
was then cut to size,
aspect
of
the
with fibres
longitudinally
inserted
between
the
spinal
cord
and
the
erector
aligned,
anterolateral
ventral
rootlets,
secured
in place
with fibrin
glue (Tisseel:
Sevenoaks,
UK).
The dura was patched
(Ethicon
Ltd, Edinburgh,
UK) which
was
place.
the
thawed
in distilled
et a! 1986a,b).
A
and
Immuno
Ltd,
with
Surgicel
also glued
into
The wound was then closed with Vicryl (Ethicon).
When surgery was almost finished the neuromuscular
trachea
was intubated
with
a cuffed
endotracheal
tube
which
was connected
to a mechanical
ventilator
(CapeWayne;
Cape
Engineering
Ltd,
Warwick,
UK).
The
minute
volume
of ventilation
was 150 ml/kg.
Anaesthesia
was maintained
with
halothane
1.5%
to 2% delivered
from a vaporiser
(Fluotec
Mk III; Ohmeda,
Steeton,
West
blockade
atropine
Yorkshire,
UK)
Carrier
gas-flow
After one year electrophysiological
and histological
examinations
were carried out. The sheep were anaesthe-
in an oxygen/nitrous
rates
were
2 (02)
oxide (1 :2) mixture.
and 4 (N2O) 1/mm.
was reversed
with
(60 .tg/kg)
mixture.
(750 mg)
recovery.
further
and flunixin
Postoperative
doses
offlunixin
doses
an edrophonium
Second
(1.1 mg/kg)
medication
of cefuroxime
1.1 mg/kg
(500
doses
tg/kg)/
of cefuroxime
were
given
consisted
750 mg
12-hourly,
before
of two
8-hourly
and three
both intravenously.
After
induction,
the jugular
vein was catheterised
and an
intravenous
infusion
of Hartmann’s
solution
begun
at a
tised as before
except
withheld.
Induction
rate of 10 ml/kg/hr.
Before
surgery,
intravenous
injections
of buprenorphine
(Temgesic;
Reckitt
and Co!man,
Hull,
UK) 10 rig/kg and flunixin
(Finadyne;
Fisons,
Coalville,
Roche
Products
Ltd, Welwyn
Garden
City, UK) 0.5 mg/
kg mixed with ketamine
2 to 4 mg/kg.
Neurophysiological
investigation
precluded
the use ofneuromuscular
blocking
agents
on this occasion.
A CS to C6 laminectomy
was
UK)
2.2 mg/kg,
were
Ltd,
given.
Greenford,
antibiotic
a non-steroidal
Cefuroxime
UK) 750
a peripheral
Massachussetts).
mental
nerve
doses
for
urinary
measured.
was
1 .0 ml/kg/hr
with
surgery
fully
and
sterile
the
7 rig/kg
Bellerica,
with incre-
(Norcuron;
given
when
the
Vital
signs
first
twitch
were
frusemide
carried
Short
constant-voltage
stimuli
were
applied
if necessary
(Lasix;
in an operating
theatre
conditions.
head
fixed
The animals
securely
in
were
placed
a Mayfield
76-B. No. 5, SEPTEMBER
1994
wire bipolar
C6 root just
from
from
stimulating
proximal
the spinal
for
contractions.
differential
studies
(Fig.
1).
to
A
electrode
was
to the brachial
generator
9200:
girdle
When
low-impedance
EMG recording
into the contracting
muscle
and
NL1O4A
cord
(0. 1 ms, 1OV) square-wave
a signal
source
(Dagan
Omnipulse
Minnesota).
The
shoulder
observed
of
neurosurgical
head holder.
The laminae
of CS and C6 were exposed
on one side
through
an 8 cm longitudinal
midline
incision.
A hemilaminectomy
was performed
at the level of the CS to C6
space
to expose
the dura and the C6 root, the dorsal
part
VOL.
power
tion,
log
out
both C6 roots
plexus.
carried
out electrophysiological
of reinnervation
of muscles
plexus.
UK).
was
to expose
to the brachia!
First, we
find evidence
of the
and urine
production
maintained
in excess
2 mg/kg
bra! muscles
0.3 mm palladium
placed
under
the
monitored
preanaesthetic
medication
was
with
midazolam
(Hypnovel;
performed.
The incision
was then extended
laterally
on
both
sides
to the posterior
triangle
of the neck
with
resection
of the facet joints
and division
of the paraverte-
Orga-
using
a catheter
in the auricular
pressure
and ECG (lead II). The
was catheterised
output
was
Hounslow,
All
(Bard Biomedical,
was maintained
visible.
anaesthesia
arterial
blood
bladder
Urine
Hoechst,
stimulator
Relaxation
UK)
pattern
throughout
artery
for
blockade
was produced
with pancu25 pg/kg
intravenously
(Pavulon;
OrgaLtd, Cambridge,
UK) and monitored
by
of vercuronium
Cambridge,
stimulus
under
prone
drug,
Laboratories
was used
prophylaxis.
Neuromuscular
ronium
bromide
non Laboratories
non,
anti-inflammatory
(Zinacef;
Glaxo
mg intravenously
that
was
a.c.
and
isolated
Dagan
Corporamuscles
were
possible
a
electrode
connected
amplifier
bipolar
was inserted
to a Neuro(Digitimer
Ltd,
Welwyn
Garden City, UK). The output was fed to the Yinput of a digital oscilloscope.
A bipolar
needle electrode
insulated
except
for the
last
1 mm
was
then
in the anterior
were
branch
possible
applied
horn.
from
of the
and
C6
placed
placed
in the
Square-wave
a signal
spinal
cord
stimuli
generator.
root
was
over
a 0.3 mm
The
divided
brachial
as far
palladium
with
its tip
(0.1 ms,
1OV)
plexus
distally
wire
bipolar
as
T. E. J. HEMS,
820
R. E. CLUTFON,
to
M. A. GLASBY
the
recording
averaged
between
time
I
I
EMG (CMAP)
ele:trode
site.
The
signal
16 action
potentials
the stimulating
and
to the first
peak
of the action
to calculate
the conduction
All e!ectrophysiological
on the norma!
and grafted
averaging
in each
recording
facility
case. The
cathodes
potential
distance
and the
were
recorded
velocity.
studies
were performed
sides. The animals
were
under
anaesthesia
on completion
of
(intravenous
pentobarbitone
20 mg/kg).
the
both
killed
investigation
The
C6 root
and the adjacent
spinal
cord
were
removed
and specimens
obtained
for histological
examination
from:
A, the ventral
root above
the dorsal
root
Fig.
Diagram
ventral
to show the apparatus
root repairs.
1
for electrophysiological
assessment
of C6
specimens
were processed
as described
by Gschmeissner,
Gattuso
and Glasby
(1990)
to produce
1 .tm thick resinembedded
transverse
sections
for
light
microscopy.
Sections
were
examined
for overall
appearance.
Morphometric
analysis
was carried
out on sections
of the
ventral
roots using a Vids III computerised
image-analysis
Posterior
primory
ganglion;
B, the complete
root before
the branching
of
the posterior
primary
ramus;
C, the anterior
primary
ramus;
and D, the brachial
plexus
root (Fig.
2). The
romus
system
(Analytical
UK).
Branch
Measuring
A sample
of 200
to
In addition,
Diagram
to show the position
D (see
text)
from
which
examination.
Latency:
cord
2
of the graft
the specimens
in the C6 root and the sites A to
were
taken
for histological
at the
year
Fig.
3
amplifier
and
on a digital
a ground
sections
were
ofthe
fixed
spinal
in formalin,
and cut and stained
with methylene
and eosin,
and luxol
fast blue with
potential.
electrode
after
grafting,
the
sheep
showed
a gradual
procedure
cord
when
over
probably
the root
the first
few
Any functioning
regenerated
from
muscle
on the normal
of avulsed
C6 ventral
repair.
These
occurred
ventral
as
roots.
are some
connected
recordings
repair
each
‘Lotus
and ‘Sta-
as a result
was
avulsed,
Two
after
of trauma
but these
to the
recovered
weeks.
motor
fibres
in the C6 root must
the spinal cord through
the repaired
ventral
root. Stimulation
of the C6 brachial
plexus
root
caused
twitching
of scapular
muscles
on the grafted
side
in four out of five sheep.
The magnitude
of the contraction
was less than that on the normal
side.
Figure
3 shows
recordings
of the EMG
obtained
from the brachiocephalicus muscle
after stimulation
of the C6 root following
Recordings
of the EMG from the brachiocephalicus
side and on the repaired
side one year after grafting
roots (amplifier
gain x2000).
action
transverse
the
the initial
have
compound
from
using
in the proximal
forelimb
weakness.
weakness
and spasticity
of the hindlimbs
rapidly
differential
a.c.
was
displayed
of
Cambridge,
improvement
had some
SV
electrode
Ltd,
measured
RESULTS
8-Oms
spinal
recording
complete
level
embedded
in wax,
blue,
haematoxylin
creosol
violet.
In the
0
was
section.
Statistical
analysis
was carried
out
Symphony’
(Lotus
Corporation,
Massachusetts)
tistica’
(StatSoft
Inc, Tulsa,
Oklahoma).
prevertebrol
muscles
Fig.
Systems
fibres
to
a Neurolog
filter
NL12S.
oscilloscope
In
all
was
electrophysio!ogical
placed
in tissue
close
20 cm from
A compound
NL1O4A
The output
to record
a
confirm
grafted
C6 root
the
reinnervation
the spinal
action
when
spinal
cord indicating
abolished
after the
excluding
that
a result
of regeneration
It is of note that the
effect
potential
stimulating
of muscle
into the
reinnervated
had
repaired
muscles
cord.
was recorded
the
anterior
from
horn
recovery
of motor
fibres.
ventral
roots were divided,
of volume
conductance.
THE JOURNAL
OF BONE
the
of the
This was
therefore
The
AND JOINT
mean
SURGERY
REPAIR
Fig.
OF AVULSED
CERVICAL
NERVE
ROOTS
4a
Cross-sections
of the anterolateral
part of the spinal cord
and repair of the ventral
roots (luxol fast blue and creosol
at the C6 level (a) on the normal
violet stain x28).
Table
I. The axon and fibre diameters
of normal
and repaired
avulsion
are compared
with previous
values
obtained
after root
ventral
division
Roots
Roots
avulsed
Fibre
diameter
Control ventral roots
Median
Mode
Upper quartile
Lower quartile
Mean
(sm)
Axon
diameter
7.70
9.80
9.60
4.70
7.29
SEM
12.50
12.20
14.50
8.60
11.56
4.01
0.13
N
1000
SD
Repaired
ventral
Median
Mode
Upper quartile
Lower quartile
Mean
821
(tm)
Fig.
4b
side
and
(b) one
roots.
Results
and repair
after
avulsion
root
divided
Fibre
diameter
(tm)
Axon
diameter
8.50
9.50
10.50
4.30
0.10
13.70
15.30
15.30
7.50
11.98
4.45
0.16
1000
800
800
5.50
2.90
3.50
7.70
1.30
4.80
1.70
3.45
2.13
0.07
4.70
Multiple
6.70
3.30
5.26
3.28
after
year
(tm)
7.60
3.56
0.13
roots
3.90
5.95
2.55
0.08
SD
SEM
N
1000
2.60
1.80
4.30
1.40
3.11
2.14
0.08
2.44
0.09
1000
800
800
Significance:
Kolmogorov-Smirnov
test
p
<
0.001
p
conduction
velocity
in the grafted
roots was 30.2 ± 3.3 ms
which
was significantly
less than the norma!
value
of
50.35
± 3.7 ms (j
= 0.005)
recorded
at the same temperature.
Cross-sections
VOL
76-B, No. 5, SEPTEMBER
of the
1994
anterolateral
part
of the
spinal
<
0.001
p
<
0.001
p <0.001
cord on the repaired
and normal
sides are shown
in Figure
4. In a!! cases the operated
side ofthe
cord was surrounded
by scar tissue
to which
the dura adhered.
There
was also
a variable
amount
of scar tissue
and demyelination
within
the
cord
itself
on this
side.
The
number
of large
nerve-
T. E. J. HEMS,
822
cell bodies
the avulsion.
the
in the anterior
At the point
surface
of the
horn was
of repair
spinal
cord
reduced
on the side of
of the ventral
roots on
there
containing
regenerated
fibres.
Histological
examination
R. E. CLUYfON,
were
minifascicles
of the ventral
roots
(A)
M. A. GLASBY
(Manthorpe
et a! 1983).
in brain-derived
trophic
rescue’
on
Muscle
is also
neurotrophic
factor
known
and
to be rich
related
neuro-
factors
which
are thought
to be important
‘cellagents
for motor
neurones
(Lindsay
1993).
In this experiment,
surgery
on the ventral
roots was
the grafted
side showed
myelinated
fibres to be present
in
all the sheep.
Table
I is a summary
of the axon and fibre
diameters
obtained
on morphometric
analysis.
The mean
axon and fibre diameter
was reduced
compared
with the
normal
side as is typical
of regenerated
fibres.
Results
were
also compared
with
those
obtained
after
ventral
performed
through
a dorsal
hemilaminectomy.
As mentioned
above
two sheep
had some
temporary
signs
of
damage
to the spinal
cord
probably
as a result
of the
avulsion
trauma
or retraction
of the cord.
Overall,
the
procedure
appears
to have been safe. A similar
surgical
roots
were
motor
More distally
(B, C, and D),
fibres
on the normal
side
can be improved
well as the lamina
divided
and
smaller-diameter
repaired
regenerated
(Hems
and
areas
had
fibres
Glasby
1992).
of large-diameter
been
replaced
on the grafted
by
side.
and
is regeneration
out after avulsion
This builds
on our earlier
ation after repair
of ventral
(Hems
and Glasby
1992).
in the
from
some
that
clearly
ventral
roots
if
the spinal
cord.
in a large
more
likely
animal
to be
to the human
situation.
mean
fibre
diameter
in the ventral
roots
was
greater
(p < 0.001)
than that recorded
after
divided
roots
(Hems
and Glasby
1992).
This
reflects
the longer
time allowed
before
assesscompared
with 8 months)
and strongly
suggests
functional
and Young
connective
regenerating
connections
1946).
tissue
roots
were
being
Normal
ventral
roots
but this
is clearly
as described
made
(1963).
cells
with
production
not occur
in the CNS.
(1990)
that
have
shown
blood-brain
barrier
and locally-produced
there
is a prolonged
after
avulsion
trauma.
trophic
factors
may
of growth
Risling
et a!
defect
in the
Blood-borne
therefore
be
able to act on the CNS neurones
(Kiernan
and Contestabile
1980).
An investigation
of the levels
of growth
factors
associated
with root regeneration
is under way. While
we
have
not compared
freeze-thawed
muscle
grafts
with
other
methods
of repair
in this
study
they
may
be
particularly
beneficial
to the process.
Laminin,
an important constituent
of muscle
basement
membrane,
is a potent
neurite-promoting
factor
which
has
been
shown
to
encourage
sprouting
from
both
CNS
and
PNS
1991).
neck
and
If the
roots
foramena
reattached
late this procedure
conclusion,
subjects.
Exposure
of the facet joint
as
the stability
of the
operation
was
to the
spinal
would
run the risk
cord
artery.
An alternative
would
the spinal cord to important
regeneration
done
could
be passed
back
from
the posterior
of
motor
but
of
be to
motor
fibres
can
follow
repair
of a root avulsion
injury
and functional
connections
can be made.
In addition,
the method
used is
surgically
feasible.
The sheep
is very similar
to man both
in the dimensions
of the structures
involved
and in the
time
course
for
regeneration.
Reimplantation
roots
could
be a surgical
traction
injury
to the brachial
option
plexus.
in
of avulsed
selected
cases
of
The authors
wish to thank Mrs C. M. E. Glasby
and Miss G. Valler
for
nursing
help in the operating
theatre
and Mrs J. S. Wood,
Mr R. Shields
and Mr J. Cable for skilled
technical
assistance
in the laboratory.
This work was supported
by grants from the Sir Jules Thorn Charitable
Trust, the Wellcome
Trust and the Cunningham
Trust.
No benefits
in any form have been received
or will be received
from a
commercial
party related
directly
or indirectly
to the subject
of this article.
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