Otolaryngol Clin N Am 40 (2007) 971–989

Neurolaryngologic Evaluation of the Performer
Adam D. Rubin, MDa,b,*
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 Valsalva, 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 involves 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]. Numerous 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 complete 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




production, however, with the left primary motor cortex playing a more dominant 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 interconnections 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, dysdiadokinesia, 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 vagus 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



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 cricothyroid. These include the thyroarytenoid (TA), posterior cricoarytenoid (PCA), lateral cricoarytenoid (LCA), and interarytenoid (IA) muscles. Muscle 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 ganglion, 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. Unopposed 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



oropharyngeal musculature may affect resonance. A palatal paralysis results in a more hypernasal voice. Impairment of cranial nerve V, VII, or XII function 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 pseudobulbar 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 pseudobulbar palsy often have inappropriate emotional outbursts. A pseudobulbar 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 autosomal-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 Upper motor neuron General findings Spasticity, hyperreflexia, rigidity, positive Babinski sign, myoclonus Weakness, flaccidity, fasciculations Laryngeal/speech findings Spastic vocal fold paralysis/ paresis, spastic dysarthria, laryngeal myoclonus Flaccid vocal fold paralysis/ paresis, glottic insufficiency, hypernasal speech, flaccid dysarthria Vocal fold bowing, mid-fold insufficiency, tremor, laryngeal dystonia, dysdiadochokinesia Hypomobility, immobility, ?atrophy (tone depends on degree of reinnervation) Hypomobility, flaccidity

Lower motor neuron


Peripheral nerve

Tremor (pill-rolling in Parkinson’s disease), dystonia, dyskinesia, dysdiadochokinesia Weakness, atrophy, sensory deficits Weakness, flaccidity




Physical findings differ between upper and lower motor neuron processes. Upper motor neuron findings include spasticity of musculature and hyperreflexia. 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 neuron findings depending on the size and location of the stroke. Strokes may result from ischemia (secondary to thrombosis or hypotension) or hemorrhage. 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 temperature, 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, spasmodic 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 movement. Classic findings include tremor, rigidity, bradykinesia, and postural instability.



(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 often perceive their voice as normal. Affect is often flat (‘‘masked’’). In addition, 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 characteristic 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 dysfunction 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.



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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 symptoms 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 cerebellar 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 laryngeal 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 different 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. Typically, 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 neuromuscular junction. Although ocular involvement is most common, laryngeal myasthenia may present independently or in conjunction with other muscles [4,11,28]. Laryngeal finding are best appreciated with fiberoptic laryngeal examinations. Vocal fold fatigability with repetitive phonatory tasks is characteristic. Fluctuating movement asymmetry may be observed (one side appears



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 register [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 intermittent choking symptoms. Hypoesthesia in addition to pharyngeal dysfunction 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. Injury 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. Denervation 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



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 suggested 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



instability, air hunger, or fatigability? Given the close interrelationship of voice, swallowing, and airway function, questions should address these issues 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 process. 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 spasmodic dysphonia. Patients who have adductor SD have spasms intermittently 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 disorders. 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 particular attention to cranial nerve function. Flaccidity of oral motor musculature is a sign of lower motor neuron disease. Spasm of facial musculature may indicate upper motor neuron disease, a focal dystonia or other extrapyramidal process. A detached or flat affect manifested as limited facial expression 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 symmetry 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.



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 videostroboscopy 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 paresis may be subtle. Rapid repetitive phonatory tasks are useful for eliciting 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 phonation 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 neurologic examination. It is useful for identifying dysdiadochokinesia, rigidity, and cogwheeling.
Table 2 Dynamic voice evaluation Vocal task Count 1–10 in comfortable pitch range Count 1–10 in high pitch range Whistle ‘‘Yankee Doodle’’ Glissando 5 rapid sniffs Sniff-/i/-sniff-/i/-. i/-/hi/-/i/-/hi/-/i/-/hi/. /pa/-/ta/-/ka/-/pa/-/ta/ka/-pa/ta/ka Singing, performing sample Sustained /i/ under stroboscopic light Findings Symmetry, hyperfunction, aberrant motion Symmetry, hyperfunction, aberrant motion Symmetry Symmetry in longitudinal tension, rotation of posterior larynx, vocal process levels Symmetry in PCA (abductor) function Symmetry, fatigability, abductor and adductor function Symmetry, fatigability, adductor function Dysdiadochokinesia, rigidity, cogwheeling Manifestations and compensatory technique in professional voice Vocal process height, amplitude of wave, muscle tonicity, presence of mass lesions



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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 discrepancy 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, differentiation 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



for identifying muscles most affected by laryngeal tremor to target Botox therapy [25]. LEMG can confirm or refute clinical suspicions obtained from the physical examination. Asymmetric vocal fold motion seen on flexible examination 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] demonstrated 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 neuropathy in more than 85% of suspected cases. LEMG is also useful in determining 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 laryngoplasty 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, intracranial 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



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, antistriatal muscle, and anti– muscle-specific tyrosine kinase (MuSK) antibodies. 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, planning swallowing therapy, and providing strategies to enable patients to eat the least restrictive diet possible. Flexible endoscopic evaluation of swallowing (FEES) and modified barium swallow (MBS) are useful tools for evaluating 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 significant 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 neurologic processes and is a useful tool for analyzing effectiveness of treatment [22]. In addition, a recent study in our voice laboratory demonstrated that



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 laryngologist before presenting to the neurologist. The laryngologist therefore has to be aware of the vocal manifestations of neurologic disease. Unfortunately, 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 optimization. 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 contemplating thyroid or cervical spine surgery in cases without absolute indications 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 hemithyroidectomy. 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 complex, particularly if the performer is able to obtain glottic closure. Voice complaints 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 paresis has been there for years and another insult (eg, reflux) has caused the patient to become symptomatic. The same is true for a small mass on the vocal fold of a performer. Performers seldom have baseline examinations (when



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 contributing factors, (eg, reflux, allergies) should always be attempted before considering 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 neurodegenerative 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. References
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