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Otolaryngol Clin N Am

40 (2007) 971–989

Neurolaryngologic Evaluation
of the Performer
Adam D. Rubin, MDa,b,*
a
Lakeshore Professional Voice Center, Lakeshore Ear, Nose and Throat Center,
21000 E. Twelve Mile Road, Suite 111, Saint Clair Shores, MI 48081, USA
b
Department of Otolaryngology-Head and Neck Surgery, University of Michigan Medical
Center, 1904 Taubman Center, 1500 E. Medical Center Drive, Ann Arbor,
MI 48109-0312, USA

Innervation of voice and speech


The neuroanatomy of voice and speech is complex. An intricate neural
network is responsible for ensuring that the larynx performs its main
functions: providing and protecting the airway, producing cough and Val-
salva, and producing voice. The complexity is greater considering all of
the other muscles of support and articulation that need to be coordinated
during voice and speech production. Human beings have more voluntary
control over the laryngeal and articulating muscles than other animal
species. Although more primitive visceromotor pathways are involved,
particularly with more cathartic vocal functions, human voice production
is marked by greater cortical control [1]. As with other voluntary motor
systems, the neuromuscular pathway of voice and speech production in-
volves upper and lower motor neurons, the basal ganglia and cerebellum,
neuromuscular junctions, and the target muscle.

Central innervation
Upper motor neurons relay signals from the cortex to lower motor neurons
in the brainstem and spinal cord to initiate voluntary movement [2]. Numer-
ous cortical areas contribute to vocalization. Some areas are excitatory,
whereas others are inhibitory. Cortical input affecting vocal fold movement
is bilateral, which is why a unilateral cortical injury seldom results in a com-
plete vocal fold paralysis. There is hemispheric specialization with speech

* Corresponding author. Lakeshore ENT, Lakeshore Professional Voice Center, 21000 E.


Twelve Mile Road, Suite 111, Saint Clair Shores, MI 48081.
E-mail address: rubinad@sbcglobal.net

0030-6665/07/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.otc.2007.05.005 oto.theclinics.com
972 RUBIN

production, however, with the left primary motor cortex playing a more dom-
inant role [3,4]. The right motor cortex likely plays an important role in the
prosody, or melody, of speech [5].
The cell bodies of the laryngeal nerves lie within the nucleus ambiguus in
the medulla. In addition to upper motor neuron input, these lower motor
neurons receive input from other brainstem nuclei, including the nucleus
tractus solitarius and nucleus parabrachialis. This complex network of inter-
connections integrates afferent input and modifies reflexes. Other synapses
occur from neurons in the periaqueductal gray matter, the final pathway
of the visceromotor system, and are likely involved in the cathartic functions
of voice, such as during crying or screaming [1,4]. The lower motor neuron is
the final common pathway to the target muscle [1].

Extrapyramidal system
Upper and lower motor neurons are part of the pyramidal system and
control voluntary movement. The basal ganglia and cerebellum are part
of the extrapyramidal system. The extrapyramidal system is important in
controlling gross motor function. It inhibits erratic movements and helps
maintain muscle tone. The basal ganglia inhibit the rapid firing of motor
neurons (the ‘‘release phenomenon’’). They receive input from most cortical
areas and send output to areas of the frontal cortex involved with planning
movement. The cerebellum improves accuracy of movement by comparing
central motor commands with sensory input from the periphery [2]. It is
likely involved in vocal self-monitoring and fine-tune adjustments in pitch
and airflow [1]. Neurodegenerative processes involving the extrapyramidal
system may result in abnormal movement, such as tremor, dystonia, dysdia-
dokinesia, as well as, abnormal muscle tone [2].

Peripheral innervation
The motor nerves (cranial and spinal) synapse at the motor endplate of
the target muscle. This synapse is called the neuromuscular junction. The
neurotransmitter acetylcholine is released from the nerve terminal and
triggers an action potential, which results in muscle contraction.
The intrinsic muscles of the larynx are supplied by the recurrent (RLN)
and superior (SLN) laryngeal nerves. The nerve fibers travel within the va-
gus nerve through the jugular foramen of the skull base. The RLN branches
from the vagus within the superior mediastinum and loops around the aortic
arch on the left and subclavian artery on the right. It travels back superiorly
within or just lateral to the tracheoesophageal groove until it enters the
larynx posterior to the cricothyroid joint. The SLN branches off the vagus
nerve just inferior to the nodose ganglion. The nodose ganglion contains
the sensory cell bodies of the SLN. The SLN travels inferiorly along the
side of the pharynx, medial to the carotid artery, and splits into two
branches at about the level of the hyoid bone. The internal division of the
NEUROLARYNGOLOGIC EVALUATION OF THE PERFORMER 973

SLN penetrates the thyrohyoid membrane with the superior laryngeal artery
and supplies sensory innervation to the larynx. The external division of the
SLN provides motor innervation to the cricothyroid (CT) muscle.
The RLN innervates all of the intrinsic muscles of the larynx except the cri-
cothyroid. These include the thyroarytenoid (TA), posterior cricoarytenoid
(PCA), lateral cricoarytenoid (LCA), and interarytenoid (IA) muscles. Mus-
cle innervation is unilateral except for the IA muscle, which receives
contributions from both RLNs [6]. The TA and LCA muscles are vocal fold
adductors. Unilateral denervation of these muscles results in an inability to
close the glottis, with resulting breathy voice and possible aspiration [7].
The PCA is the main vocal fold abductor. Paralysis of this muscle results
in an inability to abduct during inspiration. When both PCA muscles are
denervated, airway obstruction may occur. Denervation of the PCA may
cause the arytenoid cartilage to subluxate anteromedially in unilateral vocal
fold paralysis. The denervated PCA no longer counters the anterior pull on
the arytenoid cartilage by the vocal ligament [6,7].
The SLN branches from the vagus nerve just inferior to the nodose gan-
glion, which contains the sensory cell bodies of the SLN. The SLN branches
into an internal and external division. The internal division of the SLN
penetrates the thyrohyoid membrane with the superior laryngeal artery
and supplies sensory innervation to the larynx. The external division of
the SLN provides motor innervation to the cricothyroid (CT) muscle. Un-
opposed CT muscle contraction lengthens the vocal fold, increasing tension
and thus the fundamental frequency of the voice [7].
Although the intrinsic laryngeal muscles are classically described as
abductors and adductors, their functions are more complex. Antagonistic
muscles contract simultaneously during normal vocal function. For example,
unopposed TA contraction results in shortening of the vocal fold. It acts
synergistically with the CT muscle to affect vocal fold tension [8]. CT muscle
function may also depend on the position of the vocal fold at the time of
contraction. It may be active with some voice production regardless of pitch
variation. Different patterns of intrinsic muscle activation are seen depending
on the purpose of motion. For example, different muscles may be activated or
deactivated during adduction or abduction depending on whether the motion
occurs during cough, respiration, or voice production. The CT muscle is active
during abduction with sniff, but not respiration [1,8].

Manifestations of neurologic disease


Neurologic disorders may affect voice and speech production in several
ways. Central injury may affect initiation, coordination, and quality of voice
and speech. Direct effects on the larynx can affect glottic closure patterns
and efficiency along with laryngeal muscle tone. Denervation of muscles
involved in the support mechanism of the voice, such as the diaphragm or
chest wall musculature, affects voice strength and quality. Dysfunction of
974 RUBIN

oropharyngeal musculature may affect resonance. A palatal paralysis results


in a more hypernasal voice. Impairment of cranial nerve V, VII, or XII func-
tion can affect articulation. Findings on general neurologic and laryngeal
examination depend on which nerves are involved and where the disorder
affects the neuromuscular pathway (Table 1).

Motor neuron diseases


Motor neuron diseases may result from degeneration of upper motor
neurons, lower motor neurons, or both. When both upper and lower motor
neurons are involved, the diagnosis of amyotrophic lateral sclerosis (ALS)
or Lou Gherig’s Disease is made [9]. ALS is fatal, usually from respiratory
failure, but the clinical course is variable. Other examples of upper motor
neuron disease processes include progressive lateral sclerosis and pseudobul-
bar palsy. Primary lateral sclerosis typically involves destruction of upper
motor neurons only. The diagnosis is typically made after 4 years of
predominantly upper motor neuron involvement [10]. Pseudobulbar palsy
results from interruption of bilateral corticospinal tract axons from other
disease processes, such as stroke, multiple sclerosis, or tumor, as opposed
to destruction of the neuronal cell body itself [11]. Patients who have pseu-
dobulbar palsy often have inappropriate emotional outbursts. A pseudobul-
bar palsy affect is often seen in patients who have ALS [12].
Lower motor neuron diseases include ALS, progressive bulbar palsy, and
spinal muscle atrophy. Progressive bulbar palsy is essentially ALS affecting
only the cranial nerves. Progressive spinal atrophy includes several autoso-
mal-recessive disorders that involve degeneration of the anterior horn cells
of the spinal cord. Although some forms present in adulthood, many present
in younger patients [9].

Table 1
Laryngeal and general findings of neurologic disease
Site of lesion General findings Laryngeal/speech findings
Upper motor neuron Spasticity, hyperreflexia, Spastic vocal fold paralysis/
rigidity, positive Babinski paresis, spastic dysarthria,
sign, myoclonus laryngeal myoclonus
Lower motor neuron Weakness, flaccidity, Flaccid vocal fold paralysis/
fasciculations paresis, glottic insufficiency,
hypernasal speech, flaccid
dysarthria
Extrapyramidal Tremor (pill-rolling in Vocal fold bowing, mid-fold
Parkinson’s disease), insufficiency, tremor,
dystonia, dyskinesia, laryngeal dystonia,
dysdiadochokinesia dysdiadochokinesia
Peripheral nerve Weakness, atrophy, sensory Hypomobility, immobility,
deficits ?atrophy (tone depends on
degree of reinnervation)
Myopathy Weakness, flaccidity Hypomobility, flaccidity
NEUROLARYNGOLOGIC EVALUATION OF THE PERFORMER 975

Physical findings differ between upper and lower motor neuron processes.
Upper motor neuron findings include spasticity of musculature and hyper-
reflexia. Spasticity of laryngeal musculature often results in a strained voice
that might be misconstrued as spasmodic dysphonia. Patients may suffer
from intermittent laryngospasm. Spasticity of oral musculature results in
strained, effortful dysarthria. Myoclonus may occur. Extremity involvement
may be noted. A positive Babinski reflex is a classic finding of upper motor
neuron disease [9,11].
Lower motor neuron processes result in flaccid paralysis, muscle atrophy,
and fasciculations. Patients may develop weak, breathy voices, bowing of
the vocal folds, and poor cough. Palatal involvement may lead to nasal
regurgitation and hypernasal speech. Pharyngeal musculature involvement
leads to oropharyngeal dysphagia. Tongue and facial muscle involvement
leads to slurred speech and oral dysphagia. With poor oral motor function,
pharyngeal squeeze, and glottic incompetence, these patients are often at
significant risk for aspiration [9,11,13,14].

Cerebrovascular accident
Cerebrovascular accidents may present with upper and lower motor neu-
ron findings depending on the size and location of the stroke. Strokes may
result from ischemia (secondary to thrombosis or hypotension) or hemor-
rhage. Unilateral cortical strokes are unlikely to result in complete vocal
fold paralysis because of bilateral cerebral innervation of the laryngeal
nerves. Brainstem stroke may cause vocal fold paralysis if disruption of
the nucleus ambiguus or corticobulbar fibers synapsing with the nucleus
ambiguus occurs. Isolated vocal fold paralysis secondary to stroke is rare.
Wallenberg syndrome or lateral medullary syndrome results from occlusion
of the posterior inferior cerebellar artery. It may result in some combination
of vocal fold paresis or paralysis, decrease in ipsilateral facial pain and tem-
perature, decrease in contralateral body pain and temperature, dysphagia,
dysarthria, vertigo, Horner syndrome, ataxia, and hiccoughs [15]. Stroke
patients often are debilitated, which also contributes to poor voice quality.
Abnormal body positioning and strength contribute to vocal problems. In
addition, these patients often have significant dysphagia and are at high
risk for aspiration pneumonia.

Extrapyramidal diseases
Diseases of the extrapyramidal system include Parkinson’s disease, spas-
modic dysphonia, and laryngeal tremor. Parkinson’s disease is a movement
disorder resulting from degeneration of dopamine-secreting cells within the
substantia nigra of the brainstem. This process results in loss of the neural
pathways through the basal ganglia that are involved in control of move-
ment. Classic findings include tremor, rigidity, bradykinesia, and postural
instability.
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(Access Video on Parkinsonian Cogwheeling in online version of this article at: http://
www.oto.theclinics.com/.)

More than 70% of patients who have Parkinson’s disease have voice and
speech manifestations. Patients who have Parkinson’s disease often have
soft, breathy, monotonal voices. Laryngeal tremor is common. Patients of-
ten perceive their voice as normal. Affect is often flat (‘‘masked’’). In addi-
tion, patients who have Parkinson’s disease may have significant dysarthria
and dysphagia. Characteristic laryngeal signs include vocal fold bowing,
glottic insufficiency, and slow vibration. The glottic insufficiency and poor
breath support attributable to debilitation and chest wall rigidity result in
a soft, breathy voice quality [5,11,16–18].
Vocal fold paralysis should raise suspicion of a Parkinson plus syndrome,
such as progressive supranuclear palsy, Shy-Drager syndrome, and multisystem
atrophy. These disease processes are usually more rapidly progressing and less
responsive to medication. In addition, patients who have multisystem atrophy
are at risk for bilateral vocal fold paralysis and airway obstruction [11,18,19].

Spasmodic dysphonia
Spasmodic dysphonia (SD) is a focal dystonia the larynx. As with other
dystonias, it is characterized by involuntary muscle contractions or spasms.
These spasms are task-specific. Adductory spasmodic dysphonia (AdSD)
accounts for 80% of the cases of SD, with abductory (AbSD) and mixed
dysphonias occurring less frequently. Patients who have AdSD have a char-
acteristic strained/pressed quality to their voices.
(Access Video on Adductor Spasms in online version of this article at: http://www.oto.
theclinics.com/.)

They suffer voice breaks with voiced consonants. Patients who have
AbSD have spasms of the PCA muscle with voiceless consonants, resulting
in intermittent breathiness [5,20].
(Access Video on Mixed adductor/abductor Spasms in online version of this article at:
http://www.oto.theclinics.com/.)

The pathophysiology of SD is uncertain. It may be attributable to dys-


function of the laryngeal feedback systems resulting in disinhibition of
laryngeal muscle action [5,21]. Laryngeal tremor may be present in addition
to the dystonia. The combination of tremor and dystonia is referred to as
dystonic tremor. These entities can be difficult to distinguish at times [22].
Spasmodic dysphonia might also be difficult to distinguish from muscle
tension dysphonia or other functional dysphonias.

Laryngeal tremor
Vocal tremor presents as nearly regular oscillations of the laryngeal and
pharyngeal musculature.
NEUROLARYNGOLOGIC EVALUATION OF THE PERFORMER 977

(Access Video on Laryngeal Tremor in online version of this article at: http://www.oto.
theclinics.com/.)

The voice is unstable with frequent breaks. Tremor may be seen as


a manifestation of several neurologic diseases, including Parkinson’s,
ALS, and cerebellar diseases [23]. Usually other neurologic signs and symp-
toms are present when a more severe neurologic disease is present. Tremor
may also be seen with and is often difficult to distinguish from spasmodic
dysphonia [22]. When laryngeal tremor is present, a thorough neurologic
evaluation is required, with assessment of cranial nerve, extremity, and cer-
ebellar function and gait.
When no other signs or symptoms are present, vocal tremor is usually
a manifestation of essential tremor, one of the most common causes of voice
tremor. It may be the only manifestation, but typically the extremities are
involved also. The voice is affected in approximately 20% of cases of essential
tremor [24]. In addition to the intrinsic laryngeal muscles, the extrinsic laryn-
geal muscles, pharyngeal muscles, and muscles of respiration may be involved.
The pathophysiology of tremor is incompletely understood. Electromyograph
studies have demonstrated that various laryngeal muscles may oscillate at dif-
ferent frequencies, suggesting multiple foci of central stimulus, or peripheral
contribution to the oscillatory pattern by a reflex arc. In addition, there may
be different degrees of severity amongst each of the laryngeal muscles [25].

Myoclonus
Segmental myoclonus may occur within the pharynx and larynx. Typi-
cally, involuntary, arrhythmic, jerk-like movements are seen. Usually it is
bilateral, although it may occur unilaterally. Palatopharyngeal myoclonus
may produce slow, regular voice arrests that may be missed in running
speech. It may also be triggered by speech and result in more rapid, dramatic
voice arrests [26]. Myoclonus is believed most commonly to arise from
dysfunction or lesions within the dentate, red, and inferior olivary nuclei.
Unlike tremor, it typically does not involve opposing muscle groups.
Myoclonus may be seen in neurodegenerative diseases [4,5,15,26,27].

Neuromuscular junction
Myasthenia gravis is an autoimmune disease characterized by muscle
weakness exacerbated by repetitive use and improved with rest. Antibodies
are produced to the postsynaptic acetylcholine receptor at the neuromuscu-
lar junction. Although ocular involvement is most common, laryngeal my-
asthenia may present independently or in conjunction with other muscles
[4,11,28].
Laryngeal finding are best appreciated with fiberoptic laryngeal examina-
tions. Vocal fold fatigability with repetitive phonatory tasks is characteris-
tic. Fluctuating movement asymmetry may be observed (one side appears
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to move more briskly and then appears more sluggish in comparison with
the contralateral side) [5,11,28]. Patients may also suffer from dysphagia
and dysarthria.

Peripheral nerve
Peripheral nerve injury, specifically to the vagus nerve or the recurrent or
superior laryngeal nerve branches, typically presents with absent or sluggish
vocal fold movement. Proximal vagal injuries may also present with palatal
and pharyngeal paralysis. Clinically, unilateral RLN paralysis typically
presents as a breathy voice. Diplophonia and aspiration may occur [7].
Classically, paralysis of the SLN results in loss of a patient’s upper reg-
ister [29,30]. Normally, the CT muscle contracts briskly in falsetto or modal
phonation to increase tension in the vocal fold [31]. The inability to increase
vocal tension results in poor vocal performance, especially at higher pitches
[29,30]. The clinical manifestations specific to SLN paralysis are likely more
troublesome for singers and professional speakers [5,7]. Moreover, the
internal division of the SLN carries afferent fibers from the larynx to the
central nervous system. This afferent input likely plays a role in vocal
control and modulation [8].
More subtle paresis of the SLN or RLN may cause numerous voice
complaints, including vocal fatigue, hoarseness, impairment of volume,
loss of upper range, loss of projection, and breathiness. Vocal fatigue may
be caused by the additional effort required to raise vocal pitch and project,
and by hyperfunctional compensatory gestures. Patients who have either
RLN or SLN paresis often develop a compensatory, hyperfunctional
MTD to generate a ‘‘stronger’’ voice [32].
Other symptoms may occur with injury to the vagus or the laryngeal
nerve branches. Hypoesthesia of the supraglottic larynx suggests injury to
the internal division of the superior laryngeal nerve and may cause intermit-
tent choking symptoms. Hypoesthesia in addition to pharyngeal dysfunc-
tion can place the patient at significant risk for aspiration [33,34].
Neuralgia or paresthesia of the laryngeal nerves may also manifest as or
contribute to chronic cough, globus, or laryngeal pain syndromes [35,36].
Dysphagia often occurs with vocal fold paralysis and paresis. Patients
may aspirate, particularly if there is significant pharyngeal involvement. In-
jury to the SLN may result in dysphagia by several mechanisms. Injury to
the internal division results in loss of afferent input to the swallowing center
in the brainstem. In addition, recent evidence has suggested that the external
division of the SLN may supply innervation to the cricopharyngeus. Dener-
vation may result in cricopharyngeal dysfunction and subsequent dysphagia
[37].
Laryngeal findings usually depend on which nerves are involved and the
severity of injury. A vocal fold paralysis results in absent motion on the
affected side. Vocal fold paresis may be more subtle. Vocal fold lag, or
NEUROLARYNGOLOGIC EVALUATION OF THE PERFORMER 979

sluggishness, is the most common sign. This lag may only become apparent
with repetitive tasks that cause the patient to fatigue. Asymmetry in motion
should raise suspicion of a paresis, but does not always indicate which
nerves in particular are involved [38–40]. Supraglottic hyperfunction is often
present in patients who have paresis and may make the examination more
difficult to interpret. Efforts to try to relax or ‘‘unload’’ the hyperfunction
may help in determining which muscles are affected. Asymmetry may be
present in patients who have muscle tension dysphonia without paresis.
Vocal fold tone is variable after injury to the recurrent laryngeal nerve
and depends on the degree of reinnervation. Reinnervation prevents muscle
atrophy. Spontaneous reinnervation may occur after nerve transection. The
source of the reinnervation is not known, but may include regenerating
fibers from the transected RLN, the SLN, cervical autonomic nerves, and
nerve branches innervating pharyngeal constrictors [41].
Should reinnervation occur after nerve transection, it is usually not
detectable for about 4 months [41,42]. The clinical course after 4 months
is determined by the degree of reinnervation and synkinesis. Although
reinnervation after a complete RLN transection prevents muscle wasting,
typically it does not restore useful movement to the vocal fold because of
synkinesis. Synkinesis results from nonselective reinnervation of adductor
and abductor muscles. As a result, muscles that perform opposing functions
contract simultaneously, resulting in immobility or hypomobility of the
vocal fold. The clinical picture depends on the proportion of adductor
and abductor fibers reinnervated and the ability of the contralateral vocal
fold to compensate by crossing the midline of the glottis [6,7].

Myopathy
Myopathies may be inherited or result from metabolic or inflammatory
processes [43]. Isolated laryngeal myopathy is rarely reported, although
chronic steroid inhaler use has been insinuated as a cause [44]. Laryngeal
findings include loss of muscle tone and hypomobility. These findings are
similar to those that may be seen with motor neuropathy. Some have sug-
gested that myopathy is underdiagnosed as a laryngeal disorder, because
we tend to think more about nerve injuries when we see weak, flaccid vocal
folds [44].

Neurolaryngologic evaluation
A thorough neurologic evaluation should be routine for any patient
presenting with voice complaints. A thorough history should be performed,
including presenting symptoms, rapidity of onset, progressive nature, and
inciting or precipitating factors, such as a URI or neck surgery. Specifics
about the patient’s voice complaints should be elicited. For example, does
the patient complain of raspiness, breathiness, loss of range, vocal
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instability, air hunger, or fatigability? Given the close interrelationship of


voice, swallowing, and airway function, questions should address these is-
sues also. Laryngospasm, although often caused by reflux, may also occur
with neurologic disease [45]. Patients should be asked about dysphagia,
choking, cough, and airway obstruction. A complete neurologic review of
systems and family history should be obtained.
The general appearance of the patient can give clues as to underlying
neurologic disease. Abnormal posturing, muscle tone, gait, and extremity
or head tremor should be noted. Listening to voice and speech patterns is
critical. Dysarthria, or poor articulation, is an ominous sign of a central pro-
cess. Abnormalities in voice quality should be noted, including voice breaks,
spasms, spastic quality, breathiness, tremor, and pitch range. Attention
should be paid to speech prosody.
Specific voice tasks may help distinguish pathology. For example,
counting from 80 to 89 and 60 to 69 are good tasks for assessing for spas-
modic dysphonia. Patients who have adductor SD have spasms inter-
mittently during the voiced consonants of the 80 to 89 tasks, whereas
abductory SD presents as breathy breaks during voiceless consonants of
the 60 to 69 tasks. Mixed SD has intermittent spasms during both, whereas
functional disorders are usually pressed through the entirety of each of the
vocal tasks.
(Access Videos on Adductor Spasms, Mixed Adductor/Abductor Spasms, Supraglottic
Hyperfunction in online version of this article at: http://www.oto.theclinics.com/.)

These tasks should be attempted when no endoscopy is being performed,


because distractions, such as endoscopy, often can suppress the spasms.
Moreover, patients should be asked to sing and speak in a high-pitched
‘‘Minnie Mouse’’ voice, which may help distinguish SD from functional dis-
orders. Patients who have SD tend to have fewer spasms with caricature
voicing and singing tasks [5,40].
A thorough head and neck examination should be obtained with partic-
ular attention to cranial nerve function. Flaccidity of oral motor muscula-
ture is a sign of lower motor neuron disease. Spasm of facial musculature
may indicate upper motor neuron disease, a focal dystonia or other extrapy-
ramidal process. A detached or flat affect manifested as limited facial expres-
sion may also suggest an extrapyramidal process, such as Parkinson’s
disease [5,8,16,17].
Oral motor function should be assessed closely. The tongue should be
inspected for atrophy, strength, ‘‘bag of worm’’ fasciculations, and symme-
try in motion. Symmetry in palatal elevation and gag reflex should be
tested. Unilateral palatal paralysis suggests a high vagal lesion, whereas
asymmetry in gag may suggest a glossopharyngeal nerve paresis. Palatal
myoclonus may be observed. Systemic neurologic examination should be
performed when there is suspicion of a more diffuse neurodegenerative
process.
NEUROLARYNGOLOGIC EVALUATION OF THE PERFORMER 981

Endoscopic visualization of the larynx is a critical part of the evaluation


of any patient who has a voice complaint. A dynamic voice assessment is
best performed with a flexible rhinolaryngoscope to allow the patient to
be in as physiologic positioning as possible to evaluate the movements of
the larynx and vocal tract during unaltered vocal posturing. Rigid videostro-
boscopy is essential to look for vibratory abnormalities and to assess
discrepancies in vocal process height. Protrusion of the tongue during rigid
videostroboscopy creates a nonphysiologic position for vocalization and
therefore is less useful at assessing for fine movement abnormalities of the
larynx than is the flexible rhinolaryngoscope.
The patient should be asked to perform various vocal tasks (Table 2) to
observe the movement of the vocal folds [8,38–40,46].
(Access Video on Normal Neurolaryngeal Examination in online version of this article at:
http://www.Oto.TheClinics.com.)

One should inspect for asymmetry in motion, hyperfunction, tremor,


spasms, dysdiadochokinesia, and other irregular motions. Vocal fold pa-
resis may be subtle. Rapid repetitive phonatory tasks are useful for elic-
iting subtle vocal fold lag, which can be a sign of vocal fold paresis
[7,38–40]. Repeated maneuvers alternating a sniff with the sound /i/ are
particularly helpful in unmasking mild PCA paresis. Repeated rapid pho-
nation on /i/ with a complete stop between each phonation during the
task /i/-/hi/-/i/-/hi/-/i/-/hi/ frequently causes increased vocal fold lag,
because the pathologic side fatigues more rapidly than the normal side.
Having the patient repeat /pa/-/ta/-/ka/-/pa/-/ta/ka/-pa/ta/ka is
analogous to rapid alternating maneuvers performed in a general neuro-
logic examination. It is useful for identifying dysdiadochokinesia, rigidity,
and cogwheeling.

Table 2
Dynamic voice evaluation
Vocal task Findings
Count 1–10 in comfortable pitch range Symmetry, hyperfunction, aberrant motion
Count 1–10 in high pitch range Symmetry, hyperfunction, aberrant motion
Whistle ‘‘Yankee Doodle’’ Symmetry
Glissando Symmetry in longitudinal tension, rotation of
posterior larynx, vocal process levels
5 rapid sniffs Symmetry in PCA (abductor) function
Sniff-/i/-sniff-/i/-. Symmetry, fatigability, abductor and adductor
function
i/-/hi/-/i/-/hi/-/i/-/hi/. Symmetry, fatigability, adductor function
/pa/-/ta/-/ka/-/pa/-/ta/ka/-pa/ta/ka Dysdiadochokinesia, rigidity, cogwheeling
Singing, performing sample Manifestations and compensatory technique in
professional voice
Sustained /i/ under stroboscopic light Vocal process height, amplitude of wave, muscle
tonicity, presence of mass lesions
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(Access Video on Dysdiadokinesia and Parkinsonian Cogwheeling in online version of


this article at: http://www.oto.theclinics.com/.)

Vocal fold lag is sometimes easier to see during whistling, which may help
distinguish lag resulting from a true paresis from asymmetry created from
supraglottic muscle tension. The open laryngeal posture during whistling
provides particularly good visibility of rapid vocal fold motions for easier
assessment of asymmetries in vocal fold mobility [7].
A glissando maneuver, asking the patient to slide slowly from his or her
lowest to highest note and then slide back down is invaluable for assessing
SLN function. If a superior laryngeal nerve is injured, longitudinal tension
does not increase as effectively on the abnormal side, disparities in vocal fold
length are apparent at higher pitches, and the vocal folds may actually
‘‘scissor’’ slightly, with the normal fold being higher. This height discrep-
ancy is easier to observe with rigid videostroboscopy. The classic finding
of rotation of the posterior larynx to the side of SLN injury is likely to occur
only with complete and isolated unilateral SLN paralysis [7,47].
The patient should also be asked to use the voice as he or she would in the
work environment. Singers should be asked to demonstrate their vocal
range, whereas professional speakers or teachers should give a sample of
their day-to-day vocal demands. This gives more insight to the patient’s
capability of performing in the workplace and reveals how much he or
she is compensating to meet these vocal demands.

Other studies
Laryngeal electromyography
Laryngeal electromyography (LEMG) evaluates the integrity of the
nerves and muscles of the larynx. Although its usefulness remains unproven
by evidence-based data, it remains the most objective means of evaluating
neuromuscular function of the larynx. In addition to identifying RLN or
SLN paresis, it is useful for evaluating lower and upper motor neuron
disorders, neuromuscular junction disorders, prognosis for recovery of vocal
fold paralysis, differentiation of paralysis and arytenoid fixation, differenti-
ation of malingering and psychogenic dysphonia, basal ganglia disorders,
laryngeal dystonias and tremors, and myopathic disorders. Edrophonium
chloride may be administered to test for myasthenia. Repetitive nerve
stimulation and single-fiber EMG may also be useful [7,18]. For many of
the neurodegenerative processes, EMG of other muscle groups (eg, tongue)
may be helpful in establishing the diagnosis.
LEMG is useful for localization of specific muscles for injection of Botox
in the treatment of spasmodic dysphonia [43,48–54]. Diagnostic LEMG may
be useful in helping to confirm the presence of dystonia and in identifying
which muscles are most involved [39]. Some have suggested its usefulness
NEUROLARYNGOLOGIC EVALUATION OF THE PERFORMER 983

for identifying muscles most affected by laryngeal tremor to target Botox


therapy [25].
LEMG can confirm or refute clinical suspicions obtained from the phys-
ical examination. Asymmetric vocal fold motion seen on flexible examina-
tion may suggest the presence of a mild vocal fold paresis [38–40]. Even if
a paresis is present, however, the examiner might predict the nerve or side
involved incorrectly. A recent study by Rubin and colleagues [38] demon-
strated that 25% of the time a unilateral mild paresis was suspected in
patients who had mobile vocal folds on endoscopic examination, laryngeal
EMG disagreed with the side of paresis predicted. In addition, in some cases
in which the laryngeal examination was believed to be normal, LEMG
demonstrated bilateral paresis. The failure to predict paresis on examination
in these cases was likely because movement was fairly symmetrical because
both sides were affected [38]. Heman-Ackah and Barr found that LEMG
agreed with the nerve predicted to be involved in only 64% of cases [39].
In both of these studies, however, LEMG confirmed the presence of neurop-
athy in more than 85% of suspected cases. LEMG is also useful in determin-
ing site of lesion. Koufman and colleagues [51] reported on 50 patients
who had vocal fold paresis. They found 40% had both RLN and SLN
involvement, whereas 60% had involvement of either the RLN or SLN.
LEMG can be helpful for management of patients who have movement
abnormalities on examination. Voice therapy routines can be created to
focus on strengthening muscles specifically affected by the paresis. For
example, for isolated SLN injury, exercises such as a glissando in thirds
or fifths can be performed to strengthen the cricothyroid muscles, taking
care to avoid compensatory hyperfunction in other muscles. Moreover,
the information obtained can give clinical insight for surgical planning.
For example, a patient who seems on examination to have a unilateral
paresis may benefit from bilateral thyroplasty if a bilateral paresis is noted
on LEMG. Also, one might choose to medialize a patient with injection lar-
yngoplasty at the time of mass excision should the patient have significant
paresis. By revealing an underlying neurologic problem, the LEMG may
bring insight and comfort to a patient who eventually requires a surgical
procedure for glottic insufficiency and to the voice team that has been
unable to remedy the problem with behavioral intervention alone [7,38].

Imaging studies
In a patient who has RLN injury, a CT scan with contrast from the skull
base through the mediastinum is essential. If the paralysis involves recurrent
and superior laryngeal nerves or if there are other neurologic findings, intra-
cranial studies should be considered as well. Because of the seriousness of
missing intracranial lesions, many physicians obtain MRI with and without
gadolinium of the brain and the path of the 10th cranial nerve in all cases.
This practice certainly is not unreasonable. MRI of the brain may be useful
984 RUBIN

if motor neuron disease or other central nervous system processes are


suspected.

Serology
Serologic testing may be appropriate in some cases. For example, if
myasthenia is suspected one should order antiacetylcholine receptor, anti-
striatal muscle, and anti– muscle-specific tyrosine kinase (MuSK) anti-
bodies. Anti-MuSK antibodies are found in 40% of seronegative patients
who have myasthenia gravis. In these patients, weakness typically affects
neck and respiratory muscles [55]. Myasthenia symptoms may be isolated
to the larynx, but serologic tests are often negative.
Although the usefulness of serologic testing in patients who have vocal
fold paralysis is controversial, certain tests may be useful, particularly
when the history is suggestive. Some serologic tests to consider include:
thyroid function tests, thyroid antibodies, autoimmune labs (eg, anti-nuclear
antibodies, rheumatoid factor, erythrocyte sedimentation rate), tests for
tertiary syphilis and Lyme disease, fasting blood glucose, cholesterol, and
triglycerides.

Flexible endoscopic evaluation of swallowing with sensory testing


Flexible endoscopic evaluation of swallowing with sensory testing
(FEESST) is a useful tool for patients who have dysphagia in identifying
the presence of laryngeal sensory deficits, evaluating aspiration risk, plan-
ning swallowing therapy, and providing strategies to enable patients to eat
the least restrictive diet possible. Flexible endoscopic evaluation of swallow-
ing (FEES) and modified barium swallow (MBS) are useful tools for evalu-
ating swallowing physiology. Sensory testing, however, provides additional
information concerning sensory deficits that can contribute to dysphagia
and aspiration risk. Air pulses are delivered by way of a port in a flexible
laryngoscope (or sheath over a flexible laryngoscope) to mucosa innervated
by the internal division of the superior laryngeal nerve. Sensory capacity is
measured by thresholds required to elicit the laryngeal adductor reflex
[33,34]. A randomized prospective study failed to demonstrate any signifi-
cant difference in outcomes of dysphagia patients managed with FEESST
or MBS. In stroke patients managed by FEESST, however, the incidence
of aspiration pneumonia was significantly lower than in those managed by
MBS [56].

Voice laboratory
Computerized voice analysis can help distinguish between some neuro-
logic processes and is a useful tool for analyzing effectiveness of treatment
[22]. In addition, a recent study in our voice laboratory demonstrated that
NEUROLARYNGOLOGIC EVALUATION OF THE PERFORMER 985

electroglottography (EGG) can help in the evaluation of suspected paresis


to determine if LEMG is warranted in patients who have asymmetric but
mobile vocal folds. More than 90% of patients who had a normal EGG
waveform despite asymmetry in vocal fold motion had a normal LEMG.
A normal EGG waveform thus had a negative predictive value of greater
than 90%, suggesting LEMG would be low yield in such patients [57].

Considerations for the performer who has neurolaryngologic issues


The performer likely is more sensitive to vocal changes than others whose
livelihood is not so dependent on their voices. As a result, the performer
who has early underlying neurologic disease may present to the laryngolo-
gist before presenting to the neurologist. The laryngologist therefore has
to be aware of the vocal manifestations of neurologic disease. Unfortu-
nately, other manifestations of the disease may become of higher priority
for the patient’s well-being, but vocal problems are still likely to weigh
heavily on the performer’s mind and quality of life.
Performers who have vocal fold paralysis may need urgent intervention
to help them return to work. Early voice therapy is important to avoid
the development of hyperfunctional compensatory habits that could be
difficult to break if nerve function returns. In some cases, voice therapy
can provide enough improvement in the voice that surgery can be avoided.
Injection laryngoplasty is an excellent option when it is unclear if nerve
function will return. Extra care must be taken to avoid superficial injection
into Reinke space, which impedes mucosal wave and delays vocal optimiza-
tion. Laryngeal framework surgery is appropriate after 1 year from time of
injury or if nerve recovery is not expected (eg, after nerve transection).
Expectations should be tempered depending on the vocal demands of
each individual patient.
The best treatment of vocal fold paralysis is prevention. Performers con-
templating thyroid or cervical spine surgery in cases without absolute indi-
cations need to be clear about the risk for voice change after surgery (even if
the nerve is not transected). For instance, the soprano who has a thyroid
nodule of borderline size and indeterminate fine needle aspiration (FNA)
might want to follow the nodule clinically before proceeding to hemithyroi-
dectomy. Obviously, one should not risk missing a malignancy, but all the
potential risks need to be weighed and presented to the patient so that he
or she can make the best informed decision possible.
Treatment of the performer who has a subtle vocal fold paresis is more com-
plex, particularly if the performer is able to obtain glottic closure. Voice com-
plaints are often multifactorial and nonspecific. It is often difficult to be certain
that even if a paresis is present, it is the cause of the problem. Perhaps the pa-
resis has been there for years and another insult (eg, reflux) has caused the pa-
tient to become symptomatic. The same is true for a small mass on the vocal
fold of a performer. Performers seldom have baseline examinations (when
986 RUBIN

they are not having problems) for comparison. If one excises a mass before
treating all other potential contributing factors, one risks making the voice
worse. The same is true when approaching a suspected paresis.
History is helpful, but still not always completely enlightening. For
instance, voice change after thyroid or neck surgery without any evidence
of mucosal or vibratory abnormality is likely caused by nerve injury. The
same could be said for symptoms starting after an upper respiratory
infection [32]. Unfortunately, evaluation often reveals other pathology,
such as edema or a mass. Conservative management, particularly in subtle
cases, is always wise. Voice therapy and treatment of all possible contribut-
ing factors, (eg, reflux, allergies) should always be attempted before consid-
ering surgical intervention. Some performers want earlier intervention and
more immediate effects, however, to meet their obligations.

The future
Current treatment options for vocal fold paresis, paralysis, and other
neurologic disorders are suboptimal. We still are unable to restore
movement to the paralyzed vocal fold. Ideal treatment of many neurodegen-
erative disorders needs to address neuronal preservation and regeneration.
Techniques such as stem cell implantation and gene therapy are promising
[58–60]. The issue of synkinesis offers additional challenges for restoring
useful vocal fold motion after paralysis. Innovative techniques have been
suggested, but most have not been proven effective in clinical practice
[61]. Laryngeal pacing holds some promise [62–64].

Summary
A thorough neurolaryngologic evaluation is important for the assessment
of any patient who has voice complaints. Voice changes may be the initial
presentation of neurologic disease. The otolaryngologist must be familiar
with laryngeal neuroanatomy and laryngologic manifestations of neurologic
disorders. Collaboration with a neurologist is essential when systemic or
central neuromuscular disease is suspected. The otolaryngologist can play
an important role in the care of patients who have voice, swallowing, and
airway issues resulting from neurodegenerative disease.

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