You are on page 1of 9

Received: 13 December 2015

| Accepted: 14 August 2016


DOI 10.1111/vsu.12590

ORIGINAL ARTICLE

C8 cross transfer for the treatment of caudal brachial plexus


avulsion in three dogs

Pierre Moissonnier1 | Claude Carozzo2 | Jean-Laurent Thibaut3 |


Catherine Escriou4 | Antoine Hidalgo1 | Stephane Blot3,5

1
Unites de Chirurgie, Ecole nationale Abstract
veterinaire d’Alfort, Universite
Paris-Est, Maisons-Alfort, France Objective: To evaluate the cervical nerve 8 cross-transfer technique (C8CT) as a
2
Department of Surgery, part of surgical treatment of caudal brachial plexus avulsion (BPA) in the dog.
VetAgroSup, Campus veterinaire de Study Design: Case series.
Lyon, Marcy l’Etoile, France
3
Animals: Client-owned dogs suspected to have caudal BPA based on neurological
Unites de Neurologie, Ecole
examination and electrophysiological testing (n 5 3).
nationale veterinaire d'Alfort,
Universite Paris-Est, Maisons-Alfort, Methods: The distal stump of the surgically transected contralateral C8 ventral
France branch (donor) was bridged to the proximal stump of the avulsed C8 ventral branch
4
Unites de Medecine Interne, (recipient) and secured with 9-0 polypropylene suture under an operating microscope.
VetAgroSup, Campus veterinaire de A carpal panarthrodesis was performed on the injured limb after C8CT.
Lyon, Marcy l’Etoile, France Results: Surgical exploration confirmed avulsion of nerve roots C7, C8, and T1 in
5
Inserm, L’Institut Mondor de all cases. There was no evidence of an iatrogenic effect on the donor forelimb. Grad-
Recherche Biomedicale, University ual improvement in function of the affected forelimb occurred in all dogs, with
Paris Est Creteil, Creteil, France eventual recovery of voluntary elbow extension. Reinnervation was evident in EMG
Correspondence recordings 6 months postoperatively in all three dogs. Stimulation of the donor C8
Pierre Moissonnier, Ecole Nationale ventral branch led to motor evoked potentials in the avulsed side triceps brachialis
Veterinaire, 7 avenue du General de and radial carpus extensor muscles. Variable functional outcome was observed in the
Gaulle, Maisons-Alfort, F-94704, 3 dogs during clinical evaluation 3-4 years after surgery. Digital abrasion wounds,
France. distal interphalangeal infectious arthritis, and self-mutilation necessitated distal pha-
Email: pierre.moissonnier@vet-alfort.fr lanx amputation of digits 3 and 4 in 2 dogs.
Conclusion: C8CT provided partial reconnection of the donor C8 ventral branch to
the avulsed brachial plexus in the 3 dogs of this series. Reinnervation resulted in
active elbow extension and promoted functional recovery in the affected limb.

1 | INTRODUCTION and because of a fundamental lack of axonal regrowth from


damaged neurons in the central nervous system.6 BPA
Brachial plexus avulsion (BPA) is a traumatic condition results in permanent paralysis of affected myotomes and cor-
resulting from traction injury in which nerve roots of the responding dermatomes.
brachial plexus are torn away from the spinal cord.1–4 Fol- Functionally, the canine brachial plexus can be divided
lowing simple nerve transection (neurotmesis), peripheral in 2 parts.4,7–9 The cranial part of the plexus originates from
nerves may regenerate with good functional outcome after the ventral branches of cervical spinal nerves C5, C6, and
surgical repair, depending on the distance between the lesion C7, which control shoulder mobility and elbow flexion. The
and the muscular effector.5 In contrast, rootlet avulsion was caudal part of the plexus originates from the ventral branches
until now considered beyond surgical repair because of the of C7, C8, T1, and sometimes T2, and innervates muscles
size of the gap separating the spinal cord from avulsed roots involved in elbow extension and carpus and digit mobility.

136 | V
C 2017 The American College of Veterinary Surgeons wileyonlinelibrary.com/journal/vsu Veterinary Surgery 2017; 46: 136-144
MOISSONNIER ET AL.
| 137

The caudal part of the plexus is extremely important for 2 | CLINICAL REPORT
locomotion because elbow extension is essential for weight
bearing.8 2.1 | Selection of cases
In the dog2–4,7 and in people,10 the treatment of BPA is
usually palliative. However, recent studies have reported that All dogs included in this study were young adults in which
rootlet reimplantation into the spinal cord in people can right sided caudal BPA was suspected by neurological exam-
promote motor reinnervation of denervated muscles.10,11 In ination and electromyographic testing, and confirmed by sur-
the dog, this potential surgical therapy for brachial plexus gical exploration of the brachial plexus (C7, C8, and T1
injuries has unsatisfactory results because of the large dis- nerve roots found to be avulsed). Case 1 was an 8-month-old
tance of neurotization from the spinal cord to the muscular female Labrador Retriever weighing 19 kg. Case 2 was an 8-
effector, and because of the low number of motor neurons month-old female Rottweiller weighing 28 kg. Case 3 was a
that can regenerate through the reimplanted rootlets.12,13 1-year-old female mongrel weighing 14 kg. All dogs had
Rootlet reimplantation has not been widely used in clinical sustained trauma from being hit by a car 15 days (cases 1
and 3) or 1 month (case 2) before being examined at the
cases by veterinary surgeons for multiple reasons: the need
Centre Hospitalier Universitaire d’Alfort. No spontaneous
for weight bearing in dogs (which is not the case in peo-
recovery could be expected in these cases and we suggested
ple); signs of reinervation take many months during which
to the owners that a C8CT could be performed. The owner
continuous postoperative care is necessary; and the rela-
of each dog signed an informed client consent form before
tively good quality of life after forelimb amputation in
the potential inclusion of their dog in the study.
dogs.3
At the time of examination, all dogs showed typical
We hypothesized that the poor results for surgical treat-
lower motor neuron clinical signs of the affected limb con-
ment of BPA in the dog could be improved by using an
sistent with caudal brachial plexus dysfunction. Partial flex-
anastomosis between the avulsed part of the brachial plexus
ion of shoulder and elbow was observed but neither elbow
and the distal stump of a donor nerve. A technique of cross-
nor carpus extension nor carpus flexion could be detected.
transfer, using the contralateral brachial plexus, has been
Tricipital, extensor carpi radialis, withdrawal and ipsilateral
described and applied in people.14–18 The C7 spinal nerve,
pannicular reflexes were absent. Lack of cutaneous sensation
collected on the healthy side, was anastomosed to the ulnar
(using skin pinch) was observed over radial, ulnar, and
nerve in the affected limb. Three months later, the same
median nerve cutaneous distributions. Dogs 1 and 3 demon-
ulnar nerve could be connected to another injured peripheral
strated a right sided Horner’s syndrome while there were no
nerve, chosen according to the patient’s main functional def- ocular abnormalities in Dog 2. Severe muscular atrophy was
icit (ie, musculocutaneous, median, radial, or thoracodorsal obvious in all muscles of the affected limb at the time of
nerves). examination, but appeared particularly severe in the triceps
We selected the C8 spinal nerve for a similar procedure muscle and the antebrachial muscles.
in dogs. The C8 ventral branch contributes to the radial, Under general anesthesia, EMG recordings20,21 were
median, and ulnar nerves in the dog. However, none of made before surgery with concentric bifilar and monopolar
these nerves originate solely in the C8 ventral branch, per- needle electrodes connected to an EMG device (Viking IVD,
mitting the C8 nerve to be used without loss of radial, Nicolet Instruments Corporation, Madison, Wisconsin). These
median, or ulnar nerve function. In a preliminary experi- studies were conducted in all muscles of the right forelimb.
mental study (unpublished data), we performed C8 ventral EMG recordings were taken in the corresponding muscles of
branch transection in 6 dogs. Over a period of 6 months a the left (unaffected) forelimbs. Spontaneous electrical activity
clinical survey showed no functional consequences of this following denervation was quantified using a subjective
procedure. We experimentally evaluated this new strategy in scale22: 0 5 electrically silent muscle; 1 5 rare spontaneous
the treatment of a caudal brachial plexus lesion and per- activity recorded at few sites; 11 5 diffuse occasional spon-
formed the contralateral transfer of the right, eighth ventral taneous activity or frequent spontaneous activity recorded at
nerve branch (C8) in cats.19 C8 cross-transfer (C8CT) few sites; and 111 5 diffuse abundant spontaneous activity
enabled reinnervation of the contralateral brachial plexus in in the muscle. The level of spontaneous activity was variable.
cats and allowed the establishment of new functional neuro- The most severe spontaneous activity was recorded in the
muscular units.19 Brachial plexus reinnervation can enable muscles innervated by C7, C8, and T1, while muscles inner-
the restoration of function, and could potentially lead to par- vated by C5 and C6 showed no spontaneous activity (Table
tial recovery after caudal BPA in the cat.19 The aim of this 1). The results were consistent with avulsion and/or axonotm-
study was to demonstrate that the C8 ventral branch could esis of the caudal part of the brachial plexus.
be used to neurotize the contralateral avulsed caudal plexus Compound muscle action potentials (CMAP) were
in dogs. recorded (in mV) in the biceps, triceps, and carpus extensor
138 | MOISSONNIER ET AL.

T A B L E 1 Spontaneous electrical activities recorded before tanyl (5 mg/kg IV) and midazolam (0.2 mg/kg IV) for preop-
surgery in forelimb muscles innervated by the avulsed roots erative analgesia. Induction of general anesthesia was
C7, C8, and T1 achieved with thiopental (10 mg/kg IV). General anesthesia
was maintained with isoflurane in oxygen administered
Muscles Dog 1 Dog 2 Dog 3
through a semi-closed circuit. During surgery, dogs received
Interosseous 111 111 111 an IV infusion of 10 mL/kg/h lactated Ringer’s solution.
Analgesia was continued with a constant rate infusion of fen-
Carpal flexor 111 111 11
tanyl (2-5 mg/kg/h as needed), lidocaine (50 mg/kg/min), and
Carpal extensor 111 111 111 ketamine (10 mg/kg/min).
Triceps brachialis 111 111 11 The right brachial plexus was initially examined using
a ventral approach to the cervical spine (Figure 1). The
Biceps brachialis 11 11 11 conventional approach was modified to improve bilateral
Infra/supra spinatus 11 1 1 brachial plexus visualization. A midline incision was made
with a #10 scalpel blade between the sternocephalicus
Deltoid 11 1 11 muscles at the insertion on the manubrium sterni. The ster-
Pectoralis 11 1 1 nohyoidus and sternothyroidius muscles were not separated
to protect the esophagus and the trachea during mobiliza-
Paravertebral 111 11 11
tion. Caspar retractors were used to hold the trachea and
Scale for spontaneous electrical activity following denerva- the surrounding muscles apart, taking care to protect the
tion22: 0 5 electrically silent muscle; 1 5 rare spontaneous carotid sheath, vagus nerve, and the jugular vein from
activity recorded at few sites; 11 5 diffuse occasional spon-
inadvertent damage. The longus colli and the scalenius
taneous activity or frequent spontaneous activity recorded at
few sites; and 111 5 diffuse abundant spontaneous activity muscles were bluntly separated to locate the ventral
in the muscle. branches of spinal nerve C7, C8, and T1. In all dogs, C7,
C8, and T1 nerve roots (the dorsal ganglia could be identi-
fied), spinal nerves, and ventral branches were found under
muscles following supramaximal stimulation of C7 and C8 the scalenus muscles in connection to the brachial plexus,
ventral branches by a 0.45 3 50 mm stimulating anode elec- confirming a caudal BPA (Figure 2). Nerve roots of the
trode introduced percutaneously, caudal to the transverse spinal nerves and their corresponding ventral branches
process of the sixth cervical vertebrae. The stimulating cath- were isolated from a well-established hematoma (Dogs 1
ode electrode was positioned under the skin dorsal and ros- and 3) or from a moderate fibrous scar (Dog 2). The left
tral to the scapulohumeral joint. The recording needle was eighth cervical ventral branch (donor side) was exposed as
positioned in the muscles (active electrode in the belly of the distally as possible and severed before it reached the left
muscle and reference electrode in the tendon distal to the plexus. The proximal extremity of the right (avulsed) C8
active electrode). Both sides were tested with the unaffected was debrided and cut sharply. The distal stump of the left
side being tested first for a frame of reference. No CMAP C8 was bridged to the proximal stump of the avulsed right
were recorded in muscles innervated by the radial, ulnar, or C8, and anastomosed with 6-8 epiperineural simple inter-
median nerves on the right side (side of avulsion). During rupted sutures using 9-0 polypropylene under an operating
this examination, no late potentials (H or F waves) were microscope (Figure 3). The incisions of the surgical site
present in the affected muscles. Sensory nerve conduction were closed routinely. The sternohyoideus muscle and the
was present in the right ulnar and radial nerves (conduction mastoid part of the sternocephalicus muscle were apposed
velocity 5 62-75 m/s; latency 5 2.9-3.5 m/s) for all dogs. along the midline by separate cruciate sutures. The subcu-
The absence of CMAP but presence of a sensory nerve taneous fascia and the skin were closed by continuous pat-
action potential for the same nerve supported a diagnosis of tern sutures.
nerve root avulsion. All electrophysiological testing was con- One (Dog 3), 2 (Dog 2), or 6 months (Dog 1) after
sistent for severe axonotomesis and/or neurotmesis of the C8CT, right side carpal panarthrodesis were performed. A
caudal part of the brachial plexus. dorsal midline approach of the distal part of the radius, the
carpus, and the metacarpus was performed. The radiocarpal,
middle carpal, and carpometacarpal joint surfaces were
2.2 | Surgical procedure
exposed and articular cartilage was removed. A bone plate
Dogs were anesthetized and routinely prepared for aseptic was applied as a compression plate to the dorsal surface of
surgery of the ventral cervical region. Dogs initially received the radius, the carpus, and the metacarpus. The skin was
diazepam (0.2 mg/kg IV) as a preanesthetic medication, fen- sutured with interrupted cruciate sutures.
MOISSONNIER ET AL.
| 139

FIGURE 1 Semischematic perioperative view and cross section describing the C8CT technique. The muscles and vasculature
are not represented to improve visibility. The left C8 ventral branch is dissected as distally as possible before dividing into the left
brachial plexus peripheral branch, then transected and pulled between the trachea and longus coli muscle. This distal stump of left
C8 ventral branch (donor side) is anastomosed to the proximal stump of the right C8 ventral branch (avulsed from the spinal cord;
recipient side). C5-8 5 ventral branchs of cervical spinal nerves 5-8. T1 5 ventral branch of thoracic spinal nerve 1. *Avulsed ven-
tral branches. 1 5 Longus coli muscle. 2 5 First cervical vertebra. 3 5 First rib. 4 5 Trachea. 5 5 Esophagus. X 5 Distal section of
normal C8. O 5 Anastomosis of the distal stump of left C8 ventral branch and the proximal stump of the right C8 ventral branch

2.3 | Postoperative treatment 2.4 | Postoperative evaluation


Following anesthetic recovery, pain was controlled by mor- The effects of C8CT on the left and right limbs were moni-
phine chlorydrate injection (0.2 mg/kg subcutaneously every tored during clinical exam (Dog 1 for 4 years; Dog 2 for 5
6 hours for 24 hours), and by ketoprofen (2 mg/kg IM every years; and Dog 3 for 5 years) and EMG (Dog 1 for 3 years;
once daily) given over 4 days. Postoperative treatment con- Dog 2 for 5 years; and Dog 3 for 5 years) evaluation. Dogs
sisted of passive mobilization of the limb 2 times a day for maintained their ability to walk on the donor forelimb (left)
20 minutes, muscle electrostimulation,23,24 and digit protec- immediately after surgery without any obvious functional
tion using a homemade leather brace covering the entire deficits. There was no evidence of severe pain during the
limb. Isometric electrostimulation (50 Hz; Genesy 600, postoperative period.
Globus, Italy) was applied 30 minutes per day (during the With time, muscle atrophy of the right limb improved
first 6 months) and twice a week (until EMG revealed and the brachial triceps progressively regained muscle mass.
CMAP). The stimulator generated a constant biphasic charge Six months to 1 year after surgery, gradual improvement in
voltage (80 mV) with stimulation currents of 250 mA the function of the right forelimb occurred in all dogs. Vol-
applied by cutaneous electrodes positioned at the level of the untary elbow extension was observed and dogs could bear
brachial and antebrachial muscles. In practice, the stimula- their weight on the repaired limb with the help of external
tion current was progressively increased until the dog exhib- restraint with a modified Robert Jones bandage, but there
ited discomfort and then decreased to a lower intensity. was no carpal extension at this time. After carpal panarthrod-
Stimulation was performed by the surgical staff during the esis, the dogs regained partial use of their limb with external
hospitalization period, and afterwards, by the owner. protection of the toe. At the end of the survey period, the
140 | MOISSONNIER ET AL.

and not in contralateral muscle. These MUAP are consistent


with a reinnervation process.25
Stimulation of the right caudal brachial plexus and direct
stimulation of the left C8 ventral branch led to the recording
of CMAP in the right triceps brachialis 6 months postopera-
tively in Dog 1 and was still observed around 4 years after
surgery in Dogs 2 and 3, showing that a reinnervation process
was occurring and that the muscle was not fibrotic (Table 2).
Progressively the left triceps muscle became free of fibrilla-
tion potentials and of positive sharp waves. There was no
spontaneous activity on the left side 6 months after surgery in
any dogs. Low sensory nerve conduction was recorded in the
FIGURE 2 Perioperative view of the avulsed ventral roots radial and ulnar nerves. The loss of sensation and trophic dys-
and branches during exploration of the right brachial plexus in function led to late complications such as toe abrasion
Dog 2 wounds (3 dogs), distal interphalangeal infectious arthritis (1
dog), and self-mutilation (1 dog). Phalanx amputation of dig-
functional outcome appeared to be variable from 1 dog to its 3 and 4 was necessary in Dogs 1 and 3.
another. Dog 1 showed good functional recovery with walk-
ing, running, and jumping with the right forelimb (Figure 4), 3 | DISCUSSION
while persistent moderate lameness was evident in Dogs 2
(grade 3) and Dog 3 (grade 2). Our case series shows that in dogs with caudal BPA, C8CT
Two to 3 months after surgery, EMG recordings of rein- leads to the reconnection of the donor plexus to the avulsed
nervation appeared in the muscles of the grafted limb. Spon- brachial plexus. This reinnervation promotes a partial func-
taneous activity on the right side in the brachial triceps, tional recovery of the avulsed caudal brachial plexus. Vari-
radial extensor, and interosseous muscles was only observed ability in the functional results seen in the 3 dogs of our
in Dog 2 whereas spontaneous activity was absent in all study could be explained by a fiber misrouting phenomenon
muscles of the right frontlimb of Dogs 1 and 3. These obser- or by the variability in the anatomy of the brachial plexus.
vations could be consistent with reinnervation or the forma- The small sample size is a major limitation of the study,
tion of fibrous tissue in the denervated muscle. In Dog 1, 6 nevertheless, C8CT should be considered as an adjunctive
months after surgery, long duration and polyphasic (5 turns possibility in the treatment of caudal BPA in dogs.
or more) motor unit action potentials (MUAP) were observed The brachial plexus arises from the ventral branches of the
in the right triceps brachialis during voluntary contraction C5 to T2 spinal nerves. These branches contribute in a

FIGURE 3 Perioperative views under operating microscope. A, The left eighth cervical ventral branch (*) has been severed and
is transferred over to the right side by pulling it between the longus colli muscles and the trachea, to the level of the right brachial
plexus. B, Sutures between the distal stump of the left C8 to proximal stump of avulsed right C8
MOISSONNIER ET AL.
| 141

FIGURE 4 Clinical evaluation of locomotion in Dog 1, 2 years after C8CT and carpal panarthrodesis. These sequential pictures,
extracted from a video recording, show that the dog is using its right limb to run with a moderate lameness. Contraction of the
brachial triceps muscle leads to voluntary elbow extension and weight bearing on the limb

variable manner to the formation of the brachial plexus.7,9 The BPA in people. These include avulsed spinal nerve root reim-
brachial plexus is made up of C6, C7, C8, and T1 in 58.62% plantation into the spinal cord,28–31 neurotization of the plexus
of dogs, C5 to T1 in 20.69% of dogs, C6 to T2 in 17.24% of with either the phrenic nerves,32 the intercostal nerves,33–35 or
dogs, and C5 to T2 in 3.4% of dogs. The origins of peripheral the accessory nerves,36–38 cross transfer,39 and, more recently,
nerve roots have also been reported to be variable.7,26,27 The C7-cross-transfer.14–18 The choice among these techniques for
radial nerve usually originates from C7 to T1. The median and human patients remains controversial and depends on the
the ulnar nerves typically originate from C8 and T1. In the sit- exact location and extent of the avulsion.
uation of partial BPA, functional recovery could be the result In dogs with partial BPA, limited treatment can be per-
of collateralization of remaining axons originating from intact formed by various surgical treatments including arthrodesis,
branches or from less severely damaged branches (demonstrat- and the use of various external devices, such as casts. C8CT
ing a neurapaxia or an axonotmesis). offers an alternative to amputation in the case of caudal
The decision to perform C8CT on the dogs in our series BPA. However, the complexity of the surgical procedure, the
was made after avulsion of the C7, C8, and T1 nerve branches length of postoperative care, and potential complications
was confirmed by surgical exploration. Based on the anatomic must be considered when selecting patients as well as the
confirmation of avulsion, postoperative recovery of the triceps owners. Indeed, avoiding amputation in the dogs of this
brachialis muscle function in the dogs of our study could be series necessitated constant postoperative care even after
attributed exclusively to C8CT. Functional recovery of the motor recovery occurred. The axonal regrowth speed after
radial carpal extensor muscle, which is mainly innervated by anastomosis is estimated to be 1-2 mm per day. It may
C7, did not occur. The C7 nerve was not directly involved in require 1 year or more for reinnervation of a large breed
cross transfer and would require axonal regrowth over a long dog’s forelimb. During this time, the distal limb remains
distance for recovery. Thus, in caudal BPA (C7, C8, T1), insensible (dermatome anesthesia), and constant monitoring
functional recovery of the limb muscles depends exclusively of the paw is necessary to avoid formation of secondary
(ulnar nerve) or partially (contribution of C6 to the radial trophic or traumatic injuries (abrasion, infection). Owners
nerve) on the C8CT. were informed of this in the consent form.
The current treatment of complete BPA in dogs is only From the technical point of view, C8CT appears simpler
palliative and limb amputation is often proposed.1–5,21 Various than root reimplantation. Moreover, there is no risk of
surgical techniques have been experimentally designed to treat the dog developing spinal cord trauma secondary to

T A B L E 2 Motor evoked potentials (mV) recorded after supramaximal nerve stimulation preoperatively (preop) and during
the last EMG test

Dog 1 Dog 2 Dog 3


Tested Sites of right
nerve side recording Preop 6 months Preop 4.3 years Preop 3.6 years
Radial Triceps brachialis 0 0 0 3.5 0 30.8

Extensor carpi radialis 0 14.2 0 19.9 0 21.9

Ulnar Interosseus 0 0 0.5 10.4 0 8.3

Left C8 Triceps brachialis – 5.9 – 14.4 – 27.4


The left (donor) C8 ventral branch was stimulated at the left axilla to evaluate reinnervation of the right (avulsed) plexus by the
donor branch. The right peripheral nerves (radial and ulnar) near the right humeral shaft were stimulated to evaluate the reinner-
vation of these nerves after C8CT.
142 | MOISSONNIER ET AL.

reimplantation into the spinal cord.12 The low morbidity we these axons have to follow complex pathways (ventral root-
observed after C8 transection in the donor limb is similar to lets, ventral root, ventral branch, plexus, and peripheral
the low morbidity observed in human patients14 after C7 nerve) to the muscle. In C8CT, regenerating axons are
transection. Furthermore, the distance separating the site of directly injected into the caudal plexus. In a postoperative
anastomosis from the targeted muscle is shorter, reducing the survey of 10 human patients,31 recorded CMAP 9-12 months
time necessary for neurotization and increasing functional after root reimplantation for BPA, and three people showed
recovery.40 Indeed the result of the neurotization procedure satisfactory recovery 2 and 3 years after surgery. We believe
is mainly affected by the regenerative ability of reinnervated that C8CT provides a close viable nerve source, thus ensur-
muscles and the remaining amount of muscular fiber.41,42 ing a more rapid muscle reinnervation. However, it necessi-
Muscle atrophy is transitory if the denervation period is tates a learning phase for the patient, which requires
short.43 In our study, reinnervation was documented in the contralateral spinal neurons to command the avulsed plexus
triceps muscle 6 months after surgery and the function of as has been demonstrated in other neurotization techniques
this muscle was adequate for limb extension and weight in the cat.47
bearing at the end of the survey period. The radial extensor Our study suggests that an active therapeutic approach
muscle showed EMG signs of reinnervation 3 years after for BPA could enhance the functional outcome of this trau-
C8CT; however, this muscle did not recover functionality. matic condition. Therefore, C8CT appears to be an attractive
Carpal panarthrodesis was considered as soon as possible to candidate for caudal BPA treatment. However, before it can
allow dogs to regain weight bearing when reinnervation of be used routinely, many problems have to be addressed such
the triceps brachialis muscle provided functional elbow as better correlation between reinnervation and functional
extension. Our observations were similar to those of clinical recovery, preserving muscle structure during the denervation
trials in human patients after contralateral transfer of C7.14–17 period, attaining more selective neurotization to decrease
The choice of C8 in the dog was made after a comparative axonal misrouting, and stimulating axonal regrowth.
anatomical study demonstrating that C8 plays an important
role in the constitution of all peripheral nerves in the fore- ACKNOW L E DGM E NT
limb and after an experimental study showed that C8 transec-
The authors thank Pr. JA Flanders (Cornell University,
tion did not lead to a severe deficit in the cat.19
Ithaca, NY) for his critical reading and his invaluable help
Fiber misrouting could explain inconstant results after
for rewriting this article, and E Josie for his drawings.
peripheral nerve (or plexus) surgery, and this could be one of
the technique limitations.44 It can be defined as the amount
C O NFL IC T O F IN T E RE S T
of regenerating nervous fibers that reconnect to the wrong
target. Before avulsion, a peripheral nerve is made up of var- The authors declare no conflicts of interest related to this
ious fiber types including autonomic fibers (going, for exam- report.
ple, to an artery), motor fibers connected to flexor muscles,
motor fibers connected to extensor muscles, sensory fibers R EFE RE NC ES
(coming, for example, from a Meissner corpuscule), and sen- [1] Griffiths IR, Duncan ID, Lawson DD. Avulsion of the
sory nociceptive fibers that terminate in the skin. During neu- brachial plexus-2. Clinical aspects. J Small Anim Pract.
rotization, the wrong pathway can be taken by the nerve and 1974;15:177–183.
the new distribution pattern can connect, for example, to a [2] Wheeler SJ, Clayton-Jones DG, Wright JA. The diagno-
vasomotor fiber, or to the end-plate of a flexor muscle, or sis of brachial plexus disorders in dogs: a review of
any other possible combination. Current methods are insuffi- twenty-two cases. J Small Anim Pract. 1896;27:147–157.
cient to demonstrate the extent of misrouting. However, it [3] Rodkey WG, Sharp NJH. Surgery of the peripheral nerv-
could explain the variable results of neurotization. To ous system. In: Slatter D, ed. Textbook of Small Animal
improve the results of C8CT, one of the surgical aims would Surgery. Philadelphia, PA: Saunders; 2003:1218–1219.
be to correctly select the fascicle (motor vs. sensory) used [4] Platt SR, da Costa RC. Brachial plexus trauma. In: Tobias
for neurotization. Another aim would be to increase the KM, Johnston SA, eds. Veterinary Surgery: Small Animal.
speed of axonal regrowth with substances such as nerve St. Louis, MO: Elsevier Saunders; 2012:424–430.
growth factors or stem cells, which have been recently eval- [5] Gibson KL, Daniloff JK. Peripheral nerve repair. Comp
uated in experimental studies in dogs.45,46 Cont Educ Pract Vet. 1989;11:938–945.
The number of axons regenerating in the avulsed plexus [6] Aguayo AJ. Axonal regeneration from injured neurons in
and the small amount of fiber misrouting is decisive in the the adult central nervous system. In: Cotman CW, ed.
functional outcome of the surgical procedure. In root reim- Synaptic Plasticity. New York, NY: Guilford Press;
plantation the number of regenerated axons is low12 and 1985:457–484.
MOISSONNIER ET AL.
| 143

[7] Sharp JW, Bailey CS, Johnson RD, et al. Spinal nerve [23] Kanaya F, Tajima T. Effect of electrostimulation on
root origin of the median, ulna and musculocutaneous denervated muscle. Clin Orthop. 1992;283:296–301.
nerves and their muscle nerve branches to the canine [24] Pshenisnov KP, Pulin AG. The use of preoperative muscle
forelimb. Anat Histol Embryol. 1990;19:359–368. denervation and postoperative electrostimulation to max-
[8] Sharp NJH. Neurological deficits in one limb. In: imalize functional results in microneurovascular muscle
Wheeler SJ, ed. Manual of Small Animal Neurology. transplantation. J Reconstr Microsurg. 1994;10:65–75.
Shurdington, UK: British Small Animal Veterinary Asso- [25] Wijnberg ID, Back W, de Jong M, et al. The role of
ciation; 1995:159–178. electromyography in clinical diagnosis of neuromuscular
[9] Allam MWD, Lee DG, Nulsen FE, et al. The anatomy of locomotor problems in the horse. Equine Vet J. 2004;36:
the brachial plexus in the dog. Anat Rec. 1952;114:173–180. 718–722.
[10] Friedman AH. Neurotization of elements of the brachial [26] Sharp JW, Bailey CS, Johnson RD, et al. Spinal root ori-
plexus. Neurosurg Clin North Am. 1991;2:165–174. gin of the radial nerve and nerves innervating shoulder
[11] Chang KW, Justice D, Chung KC, et al. A systematic muscles of the dog. Anat Histol Embryol. 1991;20:205–
review of evaluation methods for neonatal brachial 214.
plexus palsy. J Neurosurg Pediatr. 2013;12:395–405. [27] Oliver JE, Hoerlein BF, Mayhew IG. Brachial plexus
[12] Moissonnier P, Duchossoy Y, Lavieille S, et al. Evalua- avulsion and compression. Vet Neurol. 1987;366–369.
tion of ventral root reimplantation as a treatment of [28] Carlstedt T, Anand P, Hallin PV, et al. Spinal nerve root
experimental avulsion of the cranial part of the brachial repair and reimplantation of avulsed ventral roots into the
plexus in the dog. Revue Med Vet. 2001;152:587–596. spinal cord after brachial plexus injury. J Neurosurg.
[13] Moissonnier P, Duchossoy Y, Lavieille S, et al. Lateral 2000;93:336–338.
approach of the dog brachial plexus for ventral root reim- [29] Carlstedt T, Hallin RG, Hedstr€om KG, et al. Functional
plantation. Spinal Cord. 1998;36:391–398. recovery in primates with brachial plexus injury after spi-
[14] Gu YD, Zhang GM, Chen DS, et al. Seventh cervical nal cord implantation of avulsed ventral roots. J Neurol
nerve root transfer from the contralateral healthy side for Neurosurg Psychiatry. 1993;56:649–654.
treatment of brachial plexus root avulsion. J Hand Surg. [30] Hems TEJ, Clutton RE, Glasby MA. Repair of avulsed
1992;17:518–521. cervical nerve roots-an experimental study in sheep.
[15] Liu J, Pho RWH, Kour AZ. Neurologic deficit and J Bone Joint Surg (Br). 1994;76-B:818–823.
recovery in the donor limb cross-C7 transfer in brachial- [31] Hoffmann CFE, Thomeer RTWM, Marani E. Reimplan-
plexus injury. J Reconstr Microsurg. 1997;13:237–343. tation of ventral rootlets into cervical spinal cord after
[16] Gu YD, Chen DS, Zhang GM. Long-term functional their avulsion: an anterior surgical approach. Clin Neurol
results of controlateral C7 transfer. J Reconstr Microsurg. Neurosurg. 1993;95:112–118.
1998;14:57–59. [32] Gu Y-D, Wu M-M, Zhen Y-L, et al. Phrenic nerve trans-
[17] Terzis JK, Kokkalis ZT, Kostopoulos E. Contralateral C7 fer for the treatment of root avulsion of the brachial
transfer in adult plexopathies. Hand Clin. 2008;24:389–400. plexus. Chin Med J. 1990;103:267–270.
[18] Lin H, Sheng J, Hou C. The effectiveness of contralateral [33] Isla A, Bejarano B, Morales C, et al. Anatomical and
C7 nerve root transfer for the repair of avulsed C7 nerve functional connectivity of transected ulnar nerve after
root in total brachial plexus injury: an experimental study intercostal neurotization in cats. J Neurosurgery. 1999;
in rats. J Reconstr Microsurg. 2013;29:325–330. 90:1057–1063.
[19] Carozzo C, Cuvilliez V, Escriou C, et al. Cross-neuroti- [34] Malessy MJA, Thomeer RTWM. Evaluation of intercos-
zation of the caudal brachial plexus with the controlateral tals to musculo-cutaneous nerve transfer in reconstructive
C-8 ventral nerve branch in the cat: potential surgical brachial plexus surgery. J Neurosurg. 1998;88:266–271.
applications, effects of graft collection on the healthy [35] Tomita Y, Tsai T-M, Burns JT, et al. Intercostal nerve
donor limb and results. Neurochirurgie. 2005;51:89–105. transfer in brachial plexus injuries; an experimental
[20] Duncan ID. Electromyography and nerve conduction study. Microsurgery. 1983;4:95–104.
studies. In: Wheeler SJ, ed. Manual of Small Animal [36] Allieu Y, Cenac P. Neurotization via the spinal accessory
Neurology. Shurdington, UK: British Small Animal Vet- nerve in complete paralysis due to multiple avulsion inju-
erinary Association; 1995:50–52. ries of the brachial plexus. Clin Orthop Relat Res. 1988;
[21] Sims MH. Electrodiagnostic evaluation. In: Braund KG, 237:67–74.
ed. Clinical Syndromes in Veterinary Neurology. St. [37] Nikkhah G, Carvalho GA, Samii M. Nerve transfer (neu-
Louis, MO: Mosby; 1994:349–362. rotization) for functional reconstruction of arm functions
[22] Le Chevoir M, Thibault JL, Labruyère J, et al. Electro- in cervical root avulsion. Orthopade. 1997;26:606–611.
physiological features in dogs with peripheral nerve [38] Kawai H, Kawabata H, Masada K, et al. Nerve repairs
sheath tumors: 51 cases (1993-2010) J Am Vet Med for traumatic brachial plexus palsy with root avulsion.
Assoc. 2012;241:1194–1201. Clin Orthop Relat Res. 1988;237:75–86.
144 | MOISSONNIER ET AL.

[39] Fisch U. Cross-face grafting in facial paralysis. Arch [44] de Medinaceli L. Functional consequences of experimen-
Otolaryngol. 1976;102:453–464. tal nerve lesions: effects of time, location and extent of
[40] Frykman GK, Mc Millian PJ, Yegges S. A review of damage. Exp Neurol. 1988;100:154–166.
experimental methods measuring peripheral nerve regen- [45] Huang J, Xiang J, Yan Q, et al. Dog tibial nerve regener-
eration in animals. Orthop Clin North Am. 1988;19:209– ation across a 30-mm defect bridged by a PRGD/
219. PDLLA/b-TCP/NGF sustained-release conduit.
[41] Pellegrino C, Franzini C. An electron microscope study J Reconstr Microsurg. 2013;2:77–87.
of denervation atrophy in red and white skeletal muscle [46] Ren Z, Wang Y, Peng J, et al. Role of stem cells in the
fibers. J Cell Biol. 1963;17:327–349. regeneration and repair of peripheral nerves. Rev Neuro-
[42] Anzil AP, Wenig A. Muscle fibre loss and reinnervation sci. 2012;23:135–143.
after long-term denervation. J Neurocytol. 1989;18:833– [47] Liss AG, Af Ekenstam FW, Wiberg M. Re-organisation
845. of primary afferent nerve terminals in the brainstem after
[43] Gulatia K. Restoration of denervated skeletal muscle peripheral nerve injury. An anatomical study in cats.
transplants after reinnervation in rats. Restorative Neurol Scand J Plast Reconstr Surg Hand Surg. 1995;29:185–
Neurosci. 1990;2:23–29. 187.

You might also like