Recurrent laryngeal nerve

Anatomy of the larynx and related structures is discussed in detail elsewhere . This article reviews only a few of the relationships that are most important when evaluating vocal fold mobility disorders.

The nuclei of the recurrent laryngeal nerve (RLN) axons lie within the nucleus ambiguus in the medulla of the brainstem. The RLN axons travel with the vagus nerve down the neck until they branch off at the level of the aortic arch on the left and the subclavian artery on the right. On the left, the nerve passes inferior and posterior to the aortic arch and reverses its course to continue ly into the visceral compartment of the neck. The right RLN loops behind the right subclavian artery and ascends superomedially toward the tracheoesophageal groove. Both RLNs travel just lateral to or within the tracheoesophageal groove and enter the larynx posterior to the cricothyroid joint. The positions of the nerves in the neck make them susceptible to iatrogenic injury during surgery. Low in the neck, the course of the right recurrent nerve is more oblique, lateral, and probably more prone to injury than the left RLN .

Approximately 5 out of 1000 people have a nonrecurrent laryngeal nerve on the right. A nonrecurrent laryngeal nerve occurs only on the right, except in the rare case of situs inversus. It branches from the vagus nerve at the level of the cricoid cartilage and enters the larynx directly, without looping around the subclavian artery. This anomaly occurs in conjunction with a retroesophageal right subclavian artery .

The RLN innervates four of the intrinsic muscles of the larynx: 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 . 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.

The PCA is the main vocal fold abductor. Paralysis of this muscle results in an inability to abduct during inspiration. Denervation of the PCA usually causes the arytenoid cartilage to subluxate anteromedially in unilateral vocal fold paralysis. The denervatedPCAno longer counters the anterior pull on the arytenoid cartilage by the vocal ligament . If both PCA muscles are denervated, as in the case of bilateralRLNparalysis, airway obstruction may occur.

The IA muscle is actually three muscles: the transverse arytenoideus muscle and two oblique arytenoideus muscles. The function of the IA muscle is not completely understood; however, it may assist in vocal fold adduction and provide medial compression to close the posterior glottis .

Superior laryngeal nerve

The laryngeal nerve (SLN) branches from the vagus nerve just inferior to the nodose ganglion, which contains the sensory cell bodies of the SLN. The nerve 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 laryngeal artery and supplies sensory innervation to the larynx. The external division of the SLN provides motor innervation to the cricothyroid (CT) muscle. The CT muscle changes vocal fold tension by elongating the fold. It is responsible for increasing the fundamental frequency of the voice. The external division of the SLN lies close to the thyroid artery, although its exact relationship to the artery is variable .

Recurrent laryngeal nerve paresis/paralysis

The RLN may be injured by several means, including iatrogenic or noniatrogenic trauma, neurologic disease, tumor infiltration or compression, infection, collagen-vascular disease, or idiopathic disease. This event may occur with or without concomitant SLN injury, depending on the cause and site of the lesion. The RLN is at risk for injury during many surgical procedures, such as thyroid, anterior cervical spine, and thoracic surgery. The true incidence of vocal fold paralysis remains unknown. The incidence of injury to the recurrent laryngeal nerve from thyroid surgery has been reported as between 0.3% and 13.2%, and from anterior cervical spine surgery as between 2% and 21.6% . Mechanisms of iatrogenic injury include intubation, transection, crush, traction, inadvertent ligature placement, and thermal injury.

The laryngologist must always consider unusual causes. Several neurologic diseases may affect vocal fold movement, including multiple sclerosis, amyotrophic lateral sclerosis, syringomyelia, myasthenia gravis, Guillain-Barré, and Parkinson disease . Cerebrovascular accidents may result in injury to RLN neurons, but typically other neurons are affected also. Central nervous system (CNS) tumors, such as gliomas, can cause RLN paralysis, and diabetics may develop RLN neuropathy . More unusual cases include disorders such as Gerhard syndrome, laryngeal abductor paralysis that may be familial (autosomal dominant, autosomal recessive or X-linked inheritance and with adult onset) or acquired secondary to bulbar lesions or neurodegenerative disease .

Aggressive thyroid malignancies may invade and injure the RLN. Compression by large thyroid goiters, benign neoplasms, and nonthyroid malignancies, such as the classic Pancoast tumor of the left upper lung, may also injure the nerve .

Idiopathic vocal fold paralysis is not well understood. Some suspect a viral cause, because many patients report an upper respiratory infection before the onset of vocal symptoms. There are several infectious causes that have been reported to cause RLN paralysis, such as Lyme disease, tertiary syphilis, Epstein-Barr virus, and herpes . Other causes of RLN injury reported include systemic lupus erythematosus, patent ductus arteriosus, mediastinal radiation, I-131 therapy, amyloidosis, Charcot-Marie-Tooth, mitochondrial disorders, porphyria, polyarteritis nodosa, silicosis, and familial hypokalemic periodic paralysis .

The natural history of vocal fold paralysis depends on the mechanism and degree of injury to the nerve. The Sunderland classification system describes different degrees of nerve injury. First-degree injury means neurapraxia. Nerve function should recover completely. Second-degree injury means that Wallerian degeneration has occurred distal to an injured site (axonotmesis). Second-degree injury usually occurs after a crush injury and also results in complete recovery. Because the endoneural sheaths remain intact in a second-degree injury, synkinesis does not occur. Third-degree injury includes endoneural scarring, which can cause misdirected regeneration. Fourth-degree injury involves scarring that may block regenerating axons. Fifth-degree injury signifies complete transection of the nerve .

Clinically, unilateral RLN injury presents as a breathy voice. Diplophonia, aspiration, and dysphagia symptoms may also occur. After a few weeks, the contralateral vocal fold may compensate by adducting further to improve vocal quality and aspiration. Should reinnervation occur, typically it may not be detectable initially . The clinical course following reinnervation is determined by the degree of reinnervation and synkinesis.

Synkinesis

Reinnervation prevents muscle atrophy. Shindo and colleagues demonstrated in a canine model that during the first 3 months after transection of the RLN there is atrophy of the TA and PCA muscles. After 3 months, however, the muscle fiber diameters of the denervated muscle begin to increase. By 9 months, the fiber diameters of the denervated muscles approach those of normal muscle. Spontaneous reinnervation may occur after nerve transection and prevent muscle atrophy. 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 .

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 innervation of adductor and abductor muscles. As a result, muscles that perform opposite 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.

Crumley describes a classification system for laryngeal synkinesis. In Type I synkinesis, or “favorable synkinesis,” there is little or no vocal fold movement. The patient’s airway and voice are fairly normal, however. Types II, III, and IV are considered “unfavorable synkinesis.” A spastic vocal fold that may twitch without control characterizes type II. Voice quality is poor. In type III synkinesis there is tonic adduction of the vocal fold. This adduction results in a reasonable voice, but the airway may be compromised. Type IV synkinesis involves tonic abduction of the vocal fold resulting in a breathy voice and greater risk for aspiration. Type III synkinesis probably results from greater reinnervation of the LCA in comparison with the PCA fibers, whereas in Type IV the opposite likely occurs.

Superior laryngeal nerve paresis/paralysis

Superior laryngeal nerve paresis or paralysis may be caused by various conditions. Iatrogenic trauma during thyroidectomy has been historically accepted as the most frequent cause of SLN paralysis . In 1980, Adour and colleagues reported that SLN palsy was part of a combined cranial polyneuropathy attributable to viral infections. Similarly, Dursun and colleagues suggested that viral infections, such as herpetic cold sores and upper respiratory infections, are commonly associated with this condition. A likely explanation is that infections lead to viral neuritis, resulting in SLN damage. To the best of our knowledge, this retrospective review included the largest population of confirmed SLN paresis and paralysis in the medical literature. Of the total sample (n = 126), 118 patients (93.6%) reported a viral infection immediately before the sudden onset of vocal impairment. Some of the patients used aspirin to relieve pain or fever accompanying acute infection. In some patients aspirin ingestion probably contributed to vocal fold hemorrhage, which resulted in further voice dysfunction. Often, several months elapsed after the causative infection before the patients sought medical attention. Before the diagnostic examination, these patients attributed the symptoms of SLN damage to upper respiratory infections. The development of compensatory mechanisms, such as muscle tension dysphonia (MTD), which subjectively improved voice quality, sometimes resulted in further delays in seeking treatment. As expected, singers were more aware of their symptoms than nonsingers, and delay in seeking attention tended to be shorter in this population. This observation was confirmed in a study by Eckley and colleagues that demonstrated that voice range measurement is a useful parameter for analyzing the effects of SLN paresis or paralysis on voice and may also be used for measuring outcome following voice therapy. The effects of SLN paresis on vocal range help explain the sensitivity of professional voice users (especially singers) to the effects of the condition. Laboratory investigations performed during selected patient evaluations often demonstrated increased serum titers indicating herpesvirus types I and II and antibodies to influenza type A and other common viruses. This evidence suggested infection at some undetermined time in the past.

There were 8 patients in Dursun’s study who had iatrogenic causes, such as thyroid surgery or external trauma. Such findings suggest that iatrogenic trauma can also cause isolated SLN paresis. Extreme care must be taken, particularly during thyroid surgery, to protect the external branch of the SLN in the pole of the thyroid, where it descends close to the thyroid vessels. Jansson and colleagues performed pre- and postoperative electromyography (EMG) on 20 patients undergoing thyroid surgery. Nine patients had postoperative SLN paresis by EMG. Additionally, 3 patients who had goiters had preoperative SLN paresis, which worsened postoperatively. Some 58% of the SLN pareses were present at 1 year follow-up, although most cases had some nerve recovery. To avoid harming the SLN during thyroid surgery, some authors recommend ligating distal branches of the thyroid artery as close to the thyroid capsule as possible, whereas others suggest identification of the external branch of the SLN to prevent injury . Less common causes have also been reported, including neurologic disorders, anterior approach to the cervical vertebrae during surgery, carotid endarterectomy, nonsurgical trauma, and Reye syndrome .

The clinical manifestations of SLN paresis and paralysis are variable. The variability relates to different degrees of impairment, other associated pathologies, and the voice needs and awareness of each patient. Normally, the CT muscle contracts briskly in falsetto, vocal inflection, and modal phonation to increase tension in the vocal fold . In SLN paresis and paralysis, the loss of this function may lead to lowered pitch, a more monotone voice, and poor vocal performance, especially at higher pitches . SLN paresis and paralysis may cause 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 to project, by hyperfunctional compensatory gestures, or by pathologic neuromuscular fatigue in cases of marked paresis. The clinical manifestations of SLN paresis or paralysis, particularly loss of upper range, are more troublesome in singers and professional speakers. These patients often develop MTD to generate a stronger voice. In Dursun’s series, 23.8% of the patients had MTD that seemed to be compensatory. It must be remembered that SLN paresis may be the underlying cause of voice misuse and consequent structural lesions.

Although not a commonly described finding, choking with or without regurgitation and throat clearing may also occur especially if there is associated neuralgia, hypoesthesia, or paresthesia. Anesthesia of the upper laryngeal space suggests injury to the internal branch of the SLN. The absence of anesthesia does not always rule out SLN paresis or paralysis, however, because the external branch may be the only affected portion. Although anesthesia usually is not seen even with complete paralysis of the SLN, subtle decreased ipsilateral gag (hypesthesia) is fairly common.

Indirect laryngoscopy or mirror examination may or may not reveal vocal fold abnormalities. A strong activation of the normal CT muscle must occur to cause laryngeal tilt toward the weak side, another sign of unilateral SLN paresis . Flaccidity of the affected vocal fold may cause irregular vertical movements during respiration, which in turn causes various configurations of the glottis. A bowed vocal fold may be evident in SLN paresis or paralysis. These vocal folds are slightly concave, and glottic closure is usually incomplete. This finding may be associated with other coexisting conditions, however, such as recurrent laryngeal nerve paresis or paralysis, advanced age, or other neurologic disorders .

Several authors have discussed the position of the vocal folds and glottic configuration in SLN paresis and paralysis. The studies reflect different opinions . Contraction of a normal CT muscle rotates the posterior commissure toward the inactive side, which causes the paralyzed vocal fold to shorten and form an obliquely shaped glottis . A thinned, shortened, and bowed vocal fold and an oblique glottis deviating to the paralyzed side are most consistent signs described in previous reports . These are evident only in some cases of unilateral paralysis, however, and in the authors’ experience the lack of these signs does not rule out paralysis or paresis. Moreover, these findings may be observed if CT contractions are weak or if the patients have MTD, which involves not only the hyperadduction of the normal vocal fold but also anterior–posterior compression of the glottis . Vocal fold lag (sluggish motion) during phonation requiring rapidly repeated adduction is the most consistent and easily observed sign of SLN paresis or paralysis.

Recurrent laryngeal nerve paresis/paralysis

The RLN may be injured by several means, including iatrogenic or noniatrogenic trauma, neurologic disease, tumor infiltration or compression, infection, collagen-vascular disease, or idiopathic disease. This event may occur with or without concomitant SLN injury, depending on the cause and site of the lesion. The RLN is at risk for injury during many surgical procedures, such as thyroid, anterior cervical spine, and thoracic surgery. The true incidence of vocal fold paralysis remains unknown. The incidence of injury to the recurrent laryngeal nerve from thyroid surgery has been reported as between 0.3% and 13.2%, and from anterior cervical spine surgery as between 2% and 21.6% . Mechanisms of iatrogenic injury include intubation, transection, crush, traction, inadvertent ligature placement, and thermal injury.

The laryngologist must always consider unusual causes. Several neurologic diseases may affect vocal fold movement, including multiple sclerosis, amyotrophic lateral sclerosis, syringomyelia, myasthenia gravis, Guillain-Barré, and Parkinson disease . Cerebrovascular accidents may result in injury to RLN neurons, but typically other neurons are affected also. Central nervous system (CNS) tumors, such as gliomas, can cause RLN paralysis, and diabetics may develop RLN neuropathy . More unusual cases include disorders such as Gerhard syndrome, laryngeal abductor paralysis that may be familial (autosomal dominant, autosomal recessive or X-linked inheritance and with adult onset) or acquired secondary to bulbar lesions or neurodegenerative disease .

Aggressive thyroid malignancies may invade and injure the RLN. Compression by large thyroid goiters, benign neoplasms, and nonthyroid malignancies, such as the classic Pancoast tumor of the left upper lung, may also injure the nerve .

Idiopathic vocal fold paralysis is not well understood. Some suspect a viral cause, because many patients report an upper respiratory infection before the onset of vocal symptoms. There are several infectious causes that have been reported to cause RLN paralysis, such as Lyme disease, tertiary syphilis, Epstein-Barr virus, and herpes . Other causes of RLN injury reported include systemic lupus erythematosus, patent ductus arteriosus, mediastinal radiation, I-131 therapy, amyloidosis, Charcot-Marie-Tooth, mitochondrial disorders, porphyria, polyarteritis nodosa, silicosis, and familial hypokalemic periodic paralysis .

The natural history of vocal fold paralysis depends on the mechanism and degree of injury to the nerve. The Sunderland classification system describes different degrees of nerve injury. First-degree injury means neurapraxia. Nerve function should recover completely. Second-degree injury means that Wallerian degeneration has occurred distal to an injured site (axonotmesis). Second-degree injury usually occurs after a crush injury and also results in complete recovery. Because the endoneural sheaths remain intact in a second-degree injury, synkinesis does not occur. Third-degree injury includes endoneural scarring, which can cause misdirected regeneration. Fourth-degree injury involves scarring that may block regenerating axons. Fifth-degree injury signifies complete transection of the nerve .

Clinically, unilateral RLN injury presents as a breathy voice. Diplophonia, aspiration, and dysphagia symptoms may also occur. After a few weeks, the contralateral vocal fold may compensate by adducting further to improve vocal quality and aspiration. Should reinnervation occur, typically it may not be detectable initially . The clinical course following reinnervation is determined by the degree of reinnervation and synkinesis.

Synkinesis

Reinnervation prevents muscle atrophy. Shindo and colleagues demonstrated in a canine model that during the first 3 months after transection of the RLN there is atrophy of the TA and PCA muscles. After 3 months, however, the muscle fiber diameters of the denervated muscle begin to increase. By 9 months, the fiber diameters of the denervated muscles approach those of normal muscle. Spontaneous reinnervation may occur after nerve transection and prevent muscle atrophy. 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 .

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 innervation of adductor and abductor muscles. As a result, muscles that perform opposite 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.

Crumley describes a classification system for laryngeal synkinesis. In Type I synkinesis, or “favorable synkinesis,” there is little or no vocal fold movement. The patient’s airway and voice are fairly normal, however. Types II, III, and IV are considered “unfavorable synkinesis.” A spastic vocal fold that may twitch without control characterizes type II. Voice quality is poor. In type III synkinesis there is tonic adduction of the vocal fold. This adduction results in a reasonable voice, but the airway may be compromised. Type IV synkinesis involves tonic abduction of the vocal fold resulting in a breathy voice and greater risk for aspiration. Type III synkinesis probably results from greater reinnervation of the LCA in comparison with the PCA fibers, whereas in Type IV the opposite likely occurs.

Superior laryngeal nerve paresis/paralysis

Superior laryngeal nerve paresis or paralysis may be caused by various conditions. Iatrogenic trauma during thyroidectomy has been historically accepted as the most frequent cause of SLN paralysis . In 1980, Adour and colleagues reported that SLN palsy was part of a combined cranial polyneuropathy attributable to viral infections. Similarly, Dursun and colleagues suggested that viral infections, such as herpetic cold sores and upper respiratory infections, are commonly associated with this condition. A likely explanation is that infections lead to viral neuritis, resulting in SLN damage. To the best of our knowledge, this retrospective review included the largest population of confirmed SLN paresis and paralysis in the medical literature. Of the total sample (n = 126), 118 patients (93.6%) reported a viral infection immediately before the sudden onset of vocal impairment. Some of the patients used aspirin to relieve pain or fever accompanying acute infection. In some patients aspirin ingestion probably contributed to vocal fold hemorrhage, which resulted in further voice dysfunction. Often, several months elapsed after the causative infection before the patients sought medical attention. Before the diagnostic examination, these patients attributed the symptoms of SLN damage to upper respiratory infections. The development of compensatory mechanisms, such as muscle tension dysphonia (MTD), which subjectively improved voice quality, sometimes resulted in further delays in seeking treatment. As expected, singers were more aware of their symptoms than nonsingers, and delay in seeking attention tended to be shorter in this population. This observation was confirmed in a study by Eckley and colleagues that demonstrated that voice range measurement is a useful parameter for analyzing the effects of SLN paresis or paralysis on voice and may also be used for measuring outcome following voice therapy. The effects of SLN paresis on vocal range help explain the sensitivity of professional voice users (especially singers) to the effects of the condition. Laboratory investigations performed during selected patient evaluations often demonstrated increased serum titers indicating herpesvirus types I and II and antibodies to influenza type A and other common viruses. This evidence suggested infection at some undetermined time in the past.

There were 8 patients in Dursun’s study who had iatrogenic causes, such as thyroid surgery or external trauma. Such findings suggest that iatrogenic trauma can also cause isolated SLN paresis. Extreme care must be taken, particularly during thyroid surgery, to protect the external branch of the SLN in the pole of the thyroid, where it descends close to the thyroid vessels. Jansson and colleagues performed pre- and postoperative electromyography (EMG) on 20 patients undergoing thyroid surgery. Nine patients had postoperative SLN paresis by EMG. Additionally, 3 patients who had goiters had preoperative SLN paresis, which worsened postoperatively. Some 58% of the SLN pareses were present at 1 year follow-up, although most cases had some nerve recovery. To avoid harming the SLN during thyroid surgery, some authors recommend ligating distal branches of the thyroid artery as close to the thyroid capsule as possible, whereas others suggest identification of the external branch of the SLN to prevent injury . Less common causes have also been reported, including neurologic disorders, anterior approach to the cervical vertebrae during surgery, carotid endarterectomy, nonsurgical trauma, and Reye syndrome .

The clinical manifestations of SLN paresis and paralysis are variable. The variability relates to different degrees of impairment, other associated pathologies, and the voice needs and awareness of each patient. Normally, the CT muscle contracts briskly in falsetto, vocal inflection, and modal phonation to increase tension in the vocal fold . In SLN paresis and paralysis, the loss of this function may lead to lowered pitch, a more monotone voice, and poor vocal performance, especially at higher pitches . SLN paresis and paralysis may cause 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 to project, by hyperfunctional compensatory gestures, or by pathologic neuromuscular fatigue in cases of marked paresis. The clinical manifestations of SLN paresis or paralysis, particularly loss of upper range, are more troublesome in singers and professional speakers. These patients often develop MTD to generate a stronger voice. In Dursun’s series, 23.8% of the patients had MTD that seemed to be compensatory. It must be remembered that SLN paresis may be the underlying cause of voice misuse and consequent structural lesions.

Although not a commonly described finding, choking with or without regurgitation and throat clearing may also occur especially if there is associated neuralgia, hypoesthesia, or paresthesia. Anesthesia of the upper laryngeal space suggests injury to the internal branch of the SLN. The absence of anesthesia does not always rule out SLN paresis or paralysis, however, because the external branch may be the only affected portion. Although anesthesia usually is not seen even with complete paralysis of the SLN, subtle decreased ipsilateral gag (hypesthesia) is fairly common.

Indirect laryngoscopy or mirror examination may or may not reveal vocal fold abnormalities. A strong activation of the normal CT muscle must occur to cause laryngeal tilt toward the weak side, another sign of unilateral SLN paresis . Flaccidity of the affected vocal fold may cause irregular vertical movements during respiration, which in turn causes various configurations of the glottis. A bowed vocal fold may be evident in SLN paresis or paralysis. These vocal folds are slightly concave, and glottic closure is usually incomplete. This finding may be associated with other coexisting conditions, however, such as recurrent laryngeal nerve paresis or paralysis, advanced age, or other neurologic disorders .

Several authors have discussed the position of the vocal folds and glottic configuration in SLN paresis and paralysis. The studies reflect different opinions . Contraction of a normal CT muscle rotates the posterior commissure toward the inactive side, which causes the paralyzed vocal fold to shorten and form an obliquely shaped glottis . A thinned, shortened, and bowed vocal fold and an oblique glottis deviating to the paralyzed side are most consistent signs described in previous reports . These are evident only in some cases of unilateral paralysis, however, and in the authors’ experience the lack of these signs does not rule out paralysis or paresis. Moreover, these findings may be observed if CT contractions are weak or if the patients have MTD, which involves not only the hyperadduction of the normal vocal fold but also anterior–posterior compression of the glottis . Vocal fold lag (sluggish motion) during phonation requiring rapidly repeated adduction is the most consistent and easily observed sign of SLN paresis or paralysis.