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Selective Cricothyroid Muscle Reinnervation by Muscle-Nerve-Muscle Neurotization
Hussam K. El-Kashlan, MD;
William R. Carroll, MD;
Norman D. Hogikyan, MD;
Douglas B. Chepeha, MD;
Paul R. Kileny, PhD;
Ramon M. Esclamado, MD
Arch Otolaryngol Head Neck Surg. 2001;127:1211-1215.
ABSTRACT
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Objective To determine if selective reinnervation of the cricothyroid muscle could
be achieved with muscle-nerve-muscle neurotization.
Design Case series.
Setting Tertiary referral center.
Patients Three consecutive patients with high vagal lesions that resulted in
unilateral laryngeal paralysis.
Interventions Patients underwent laryngeal reinnervation with ansa hypoglossi to recurrent
laryngeal nerve anastomosis. In addition, patients underwent selective cricothyroid
muscle reinnervation by muscle-nerve-muscle neurotization technique.
Main Outcome Measures Objective and subjective improvement in voice quality and electromyographic
evidence of selective reinnervation of the cricothyroid muscle.
Results All patients recovered normal or near-normal speaking voice and had
normal objective measures of voice quality. They also showed electromyographic
evidence of cricothyroid muscle reinnervation.
Conclusion The muscle-nerve-muscle neurotization technique was successful in providing
selective reinnervation of the cricothyroid muscle in our 3 patients.
INTRODUCTION
IT IS UNIVERSALLY accepted that expedient movement- and temporal-specific
reinnervation is the treatment of choice following denervation of skeletal
muscle in the head and neck. This goal has been elusive in our efforts to
provide optimal rehabilitation for patients with laryngeal paralysis.
When skeletal muscles are denervated, the method of reinnervation has
a major impact on the structure and function of the target skeletal muscle.
Several types of reinnervation exist. Direct reinnervation results in superior
recovery of contractile function and is the preferred option when available.
Examples include primary nerve repair and nerve grafting. Neural neurotization
is a second type of reinnervation and involves implantation of the transected
motor nerve directly into the target muscle belly. Direct nerve implant and
nerve-muscle pedicles are examples of neural neurotization. Muscle-to-muscle
neurotization is a third type and occurs when axons sprout from an adjacent,
innervated skeletal muscle to innervate a target denervated muscle. The latter
types of reinnervation typically result in diminished recovery of contractile
function when compared with direct reinnervation.
Muscle-to-muscle neurotization was first used in facial reanimation
in the early 1970s. Small muscles were transplanted without vascular anastomosis
and positioned adjacent to the muscle bellies of innervated, functional facial
muscles. Thompson1-2 demonstrated,
first in dogs and later in humans, a degree of functional recovery in these
muscle grafts. Carlson and Faulkner3 demonstrated
that the force of contraction of such grafts may only be 20% of the original
muscle. Hakelius4 described 28 patients with
facial paralysis treated by this technique. Twenty-three of these patients
developed marked improvement in facial symmetry and motion.
Muscle-nerve-muscle neurotization builds on the principles demonstrated
by these investigators. One end of an autogenous nerve graft is placed into
the belly of a donor (innervated) muscle, and the other end into a target
(denervated) muscle. Axons sprouting from the donor muscle are channeled into
the target muscle via the nerve graft. The minor injury at the site of nerve
implantation is functionally inconsequential and serves to stimulate axonal
sprouting.5 Muscle-nerve-muscle neurotization
was first used clinically for selective facial reanimation. Millesi, an expert
in the field of nerve repair, and colleagues6
reported successful reinnervation of the orbicularis oris muscle in 6 patients
by performing a muscle-nerve-muscle graft from the innervated orbicularis
oris to the contralateral denervated orbicularis oris muscle.
The purpose of this article is to report our clinical experience with
the successful reinnervation of the cricothyroid muscle via muscle-nerve-muscle
grafts.
MATERIALS AND METHODS
Three patients with high vagal lesions are the subjects of this report.
The procedures were performed after detailed discussion and informed consent
was obtained. Patients were candidates for and underwent a contralateral ansa
hypoglossi–to–recurrent laryngeal nerve (RLN) anastomosis. In
addition, selective cricothyroid reinnervation was attempted using the muscle-nerve-muscle
neurotization technique. A segment of peripheral nerve long enough to span
between the cricothyroid muscles was harvested from the ansa hypoglossi. One
end of the graft was buried in the belly of the innervated cricothyroid muscle
and the other end was buried in the denervated side. The graft was secured
at the point of entry into each muscle using fine suture from epineurium to
muscular fascia. Patient 1 had 2 such grafts placed. Patients underwent videostroboscopic
examination of the larynx and perceptual and acoustic analysis of voice preoperatively
and at multiple postoperative intervals.
RESULTS
CASE 1
A 45-year-old woman was referred with the chief complaint of a persistent
right-sided oropharyngeal mass noted following an upper respiratory tract
infection. She also complained of right-sided otalgia and mild neck stiffness,
but had no voice or swallowing complaints. Physical examination was remarkable
for an approximately 2.5 x 3-cm right oropharyngeal mass covered by
mucosa and centered in the tonsillar fossa. Cranial nerve examination was
grossly normal except for mild incidental right lip weakness. A computed tomographic
(CT) scan of the neck and angiography demonstrated a vascular mass in the
right prestyloid parapharyngeal space consistent with a glomus tumor and a
right-sided thyroid nodule. A multiple endocrine neoplasia syndrome was ruled
out. The patient subsequently underwent embolization of feeding vessels followed
by transcervical resection of the tumor.
Surgical findings included a 4 x 2-cm vascular mass surrounding
the vagus nerve and close association of the mass with cranial nerve XII.
The vagus nerve was cut to remove the tumor, and the findings of the pathologic
examination were consistent with a vagal paraganglioma. The patient's voice
was severely breathy postoperatively, consisting essentially of only audible
air escape, and she required enteral nutrition via a nasogastric tube for
3 months. Four months postoperatively, a laryngeal electromyogram (EMG) demonstrated
electrical silence in the atrophic right thyroarytenoid muscle, and her voice
remained severely breathy. The results of acoustic voice assessment were grossly
abnormal, with jitter of 20.50% and shimmer of 1.85 dB. One month later, she
underwent laryngeal reinnervation with a contralateral ansa hypoglossi–to–ipsilateral
RLN anastomosis and a muscle-nerve-muscle reinnervation of the ipsilateral
cricothyroid muscle using 2 cable grafts spanning from the contralateral cricothyroid
muscle (Figure 1A). An injection
of the right vocal fold with an absorbable gelatin sponge (Gelfoam) and a
right hemithyroidectomy were also performed at the same time.
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Figure 1. A, Photograph showing the muscle-nerve-muscle
technique. Two cable grafts are seen (arrows), extending from one cricothyroid
muscle (CM) to the other. The cricoid cartilage (C) is also seen. B, Evoked
electromyogram (EMG) (M-wave potential) elicited by stimulating the normal,
left CM and recording from the reinnervated, right CM. Several evoked compound
muscle action potential responses (Responses) are demonstrated. C, EMG tracing
from reinnervated, right CM during phonation showing recruitment of motor
unit potentials.
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Postoperatively, the patient's voice was initially much improved, but
was breathy again by 6 weeks after the injection with the absorbable sponge
and reinnervation. At approximately 2 months after reinnervation, she felt
that her voice strength again began to improve, and by 4 months it was only
mildly breathy. Laryngeal videostroboscopy at that time showed good glottic
closure in mid- and lower-pitch ranges and incomplete closure in her upper
range. A laryngeal EMG was performed at 7 months after reinnervation. The
intact, donor cricothyroid muscle was stimulated transcutaneously using a
bipolar needle electrode. Recording from the reinnervated cricothyroid muscle
was accomplished using a concentric needle electrode. This demonstrated compound
potentials (M-wave potentials) in the reinnervated cricothyroid muscle with
stimulation of the contralateral donor muscle (Figure 1B) and confirmed reinnervation of the right thyroarytenoid
muscle. Activity in the reinnervated cricothyroid muscle was also demonstrated
with high-pitched vocal tasks (Figure 1C).
The results of acoustic analysis 7 months postoperatively were within normal
limits, with jitter of 0.88% and shimmer of 0.17 dB. The patient's maximum
phonation time for a sustained vowel was 12 seconds, and perceptual speaking
voice quality was normal except for hypernasal resonance.
CASE 2
A 41-year-old woman presented with a 2-year history of a slow-growing,
right-sided neck mass and hoarseness. The results of physical examination
were remarkable for a 4 x 3-cm, right-sided neck mass behind the angle
of the mandible. There was a medial bulge of the right lateral oropharyngeal
wall, which extended superiorly into the nasopharynx. Right true vocal fold
(TVF) movement was sluggish. Both CT and magnetic resonance imaging scans
were obtained and showed a large vascular right parapharyngeal space mass
consistent with a paraganglioma. Carotid angiography demonstrated a large,
extremely vascular mass with significant anterior displacement of the internal
carotid artery compatible with a glomus vagale tumor. The identifiable blood
supply to the tumor was embolized. The patient was taken to the operating
room the next day and underwent excision of the tumor through a mandibular
swing approach. Tumor extirpation required interruption of cranial nerves
IX, X, XI, and XII. Postoperatively, the patient had dysphagia and an immobile
right TVF, resulting in extreme breathiness and poor projection, which did
not improve for 6 months. Acoustic voice analysis showed a jitter of 0.75%
and shimmer of 0.19 dB.
Six months following resection, the patient was taken to the operating
room, where she underwent direct laryngoscopy and laryngeal EMG. These procedures
demonstrated an absence of motor unit potential activity in the right thyroarytenoid
muscle, whereas the left thyroarytenoid muscle had normal motor unit potential
recruitment synchronized with the patient's spontaneous respiration. The cricothyroid
muscle showed no motor unit potentials on the right side, whereas the left
side was normal. The patient underwent laryngeal reinnervation by left ansa
hypoglossi–to–right RLN anastomosis. A muscle-nerve-muscle graft
was performed from her functional left cricothyroid muscle to the nonfunctional
right cricothyroid muscle. An injection with an absorbable gelatin sponge
(Gelfoam) was also given.
Approximately 3 months after surgery, the patient noticed gradual improvement
of her vocal quality. There was a significant improvement in terms of voice
strength and projection between 4 and 5 months after surgery. Initial stroboscopic
examination before laryngeal reinnervation showed the paralyzed right TVF
to be in the intermediate position with incomplete closure of the glottis
during phonation. The TVFs were at a slightly different vertical level, which
contributed to the inadequacy of glottic closure. Postreinnervation stroboscopy
at 6 months showed the right TVF to be in the midline with adequate glottic
closure, except for a very small posterior gap, which was clinically insignificant.
The right TVF had good bulk and tone and was at the same vertical level of
the normal left fold. The patient considered her voice to be normal with an
almost normal frequency range. The results of acoustic analysis 8 months postoperatively
were within normal limits, with jitter of 0.39% and shimmer of 0.14 dB. Her
perceptual speaking voice quality was normal, except for hypernasal resonance. Figure 2 shows the prereinnervation and postreinnervation
EMG tracings from cricothyroid muscles, confirming reinnervation of the right
cricothyroid muscle.
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Figure 2. A, Electromyographic (EMG) tracings
from the right (upper) and left (lower) cricothyroid muscles during spontaneous
respiration before reinnervation. Please note absence of motor potentials
in the denervated right cricothyroid muscle, whereas the left cricothyroid
muscle showed normal motor unit potentials (arrows). B, EMG tracings from
right cricothyroid muscle 6 months after reinnervation procedure. Upper tracing
during normal respiration showing polyphasic, reinnervation potentials (arrows).
Lower tracing during vocal recruitment showing more prominent motor unit potentials.
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CASE 3
A 26-year-old man presented with a high, left-sided neck mass. Appropriate
workup was performed, and the mass was consistent with a large glomus vagale
extending from the jugular foramen to C3. Carotid angiography was performed.
Carotid occlusion studies and tumor embolization were performed. The patient
then underwent excision of the tumor with division of cranial nerve X. Because
of anticipated dysphagia from the interruption of cranial nerve X, type I
thyroplasty was performed to facilitate glottic closure and postoperative
swallowing. He also underwent primary laryngeal reinnervation with a contralateral
ansa hypoglossi–to–ipsilateral RLN anastomosis and muscle-nerve-muscle
reinnervation of the ipsilateral denervated cricothyroid muscle using a nerve
cable graft from the normal innervated contralateral cricothyroid muscle.
Postoperatively, the patient's voice was rough and raspy with significant
problems with projection and pitch control. He was only able to speak 1 to
3 words per breath. Videolaryngoscopy showed the paralyzed left TVF to be
in the paramedian position with incomplete closure of the glottis during phonation.
Approximately 4 months postoperatively, the patient reported gradual improvement
of his voice, with increase in phonation time and increased projection. The
patient also noted significant increase of his pitch range, and he described
his voice as being completely normal approximately 6 month postoperatively.
Videolaryngoscopic examination at that time showed the paralyzed left TVF
to be in the midline with complete glottic closure during phonation. Both
vocal folds were at the same vertical level and had similar bulk. The EMG
recordings showed reinnervation of the left cricothyroid muscle with some
normal configuration motor unit potentials at rest and recruitment with phonation
(Figure 3). The results of acoustic
analysis 6 months postoperatively were within normal limits, with jitter of
0.74% and shimmer of 0.29 dB. His maximum phonation time was 12 seconds for
a sustained vowel, and his perceptual speaking voice quality was normal.
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Figure 3. A, Postreinnervation electromyographic
(EMG) tracing from left cricothyroid muscle during rest showing some spontaneous
activity (arrows). B, Postreinnervation EMG tracing from left cricothyroid
muscle during vocal tasks demonstrating recruitment.
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COMMENT
This report verifies the successful reinnervation of a denervated laryngeal
muscle using the muscle-nerve-muscle neurotization technique. The EMG recordings
from the reinnervated cricothyroid muscles demonstrated resting motor unit
potentials. There was a significant recruitment of motor units on EMG with
higher-pitched phonation. Selective reinnervation was further confirmed for
patient 1 by recording a response from the reinnervated muscle with stimulation
of the contralateral donor muscle. Although the EMG evidence confirms reinnervation,
it does not measure contractile function of the reinnervated muscle, and we
are unable to objectively compare contractile function of the normal vs reinnervated
side. However, indirect evidence suggests that the reinnervated cricothyroid
muscle was functional. In all patients, the speaking voice was perceptually
normal, and jitter and shimmer were within normal limits. All patients had
a wide frequency range of their voices and were able to perform high-pitch
tasks without significant pitch breaks. We speculate that their better voice
quality and their enhanced ability to control voice pitch without significant
breaks are related to the reinnervation and functional recovery of the previously
denervated cricothyroid muscle. This allows the patients to symmetrically
increase the tension in both TVFs, resulting in better control over voice
pitch. Crumley and Izdebski7 described a patient
with a high vagal lesion who had good voice quality after laryngeal innervation
with ansa hypoglossi–to–RLN anastomosis. The patient was a singer
and wanted a better voice quality and pitch control. The patient underwent
a cricothyroid muscle reinnervation by direct suturing of the contralateral
ansa hypoglossi to the denervated muscle. Postoperatively, an improvement
in pitch control and production of the higher voice fundamental frequencies
was noted within 4 months. Thus, with a nerve transfer operation that would
primarily provide tone to the cricothyroid muscle, the vocal capabilities
were believed to have been improved. We would expect that motion-specific
reinnervation achieved through muscle-nerve-muscle neurotization would give
even better voice quality due to active muscle control.
Muscle-nerve-muscle neurotization represents a novel but largely unsubstantiated
method for the reinnervation of skeletal muscle. As previously described,
muscle-nerve-muscle neurotization is a surgical procedure whereby one end
of an autogenous nerve graft is placed in the belly of an innervated muscle,
and the distal end of the nerve graft is placed in the belly of a target,
denervated muscle. By selecting an appropriate muscle, this technique has
the potential to provide motion-specific innervation. The only report of this
method has been by Millesi et al.6 Their work
describes a series of 6 patients with long-standing, unilateral orbicularis
oris paralysis. Sural nerve grafts were harvested and one end was implanted
in the innervated orbicularis oris muscle. The nerve grafts were then tunneled
across the midline and the other end implanted in the denervated orbicularis
oris. Sufficient reinnervation to restore oral competence and spontaneous,
bilateral animation was obtained in all patients. Stimulation of the normal
muscle elicited an evoked EMG response in the contralateral muscle, and a
nerve biopsy specimen from one patient demonstrated multiple, myelinated axons
within the nerve graft.
Theoretically, this technique for laryngeal reinnervation has many advantages.
First, it can provide motion-specific reinnervation. There is considerable
evidence demonstrating that reinnervated muscle takes on the characteristics
of the donor nerve.8-9 Reinnervation
of a muscle through nerve fibers routed from its contralateral equivalent
should maintain the muscle's fiber composition and its response and biochemical
characteristics, which should result in optimal functional recovery. In addition,
the reinnervated muscle should respond almost synchronously with the normally
innervated contralateral muscle, resulting in near-normal coordination of
laryngeal muscular functions. Second, the paired nature and proximity of laryngeal
muscles make them ideal candidates for muscle-nerve-muscle reinnervation,
and their relatively small size makes it likely that functional contractility
can be achieved. The functional properties of laryngeal muscles reinnervated
using this technique are currently being evaluated in an animal model.
In conclusion, the muscle-nerve-muscle neurotization technique was successful
in providing selective reinnervation of the cricothyroid muscle in our 3 patients.
This method has great potential for clinical application in cases of unilateral
laryngeal paralysis.
AUTHOR INFORMATION
Accepted for publication June 11, 2001.
Presented as a poster at the Annual Meeting of the American Academy
of Otolaryngology–Head and Neck Surgery, New Orleans, La, September
26-29, 1999.
Corresponding author and reprints: Hussam K. El-Kashlan, MD, Department
of Otolaryngology, University of Michigan, 1500 E Medical Center Dr, Ann Arbor,
MI 48109-0312 (e-mail: hussam{at}umich.edu).
From the Departments of Otolaryngology, University of Michigan, Ann
Arbor (Drs El-Kashlan, Hogikyan, Chepeha, and Kileny), University of Alabama
at Birmingham (Dr Carroll), and Cleveland Clinic Foundation, Cleveland, Ohio
(Dr Esclamado).
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