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The human larynx is a neuromuscularly complex organ responsible for three primary and often opposing functions: respiration, swallowing, and speech. The most primitive responsibilities include functioning as a conduit to bring air to the lungs and protecting the respiratory tract during swallowing. These duties are physiologically opposite; the larynx must form a wide caliber during respiration but also be capable of forming a tight sphincter during swallowing. Speech functions are fine-tuned permutations of laryngeal opening and closure against pulmonary airflow. Innervation of this organ is complex, and its design is still being elucidated. Efferent fibers to the larynx from the brainstem motor nuclei travel by way of the vagus nerve to the superior laryngeal nerve (SLN) and the recurrent laryngeal nerves (RLNs). Afferent fibers emanate from intramucosal and intramuscular receptors and travel along pathways that include the SLN (supraglottic larynx) and the RLN (subglottic larynx). Autonomic fibers also innervate the larynx, but these are poorly understood (see also anatomy of the human larynx).
Reinnervation of the larynx was first reported 1909 by Horsley, who described reanastomosis of a severed RLN. Reports of laryngeal reinnervation spotted the literature over the next several decades, but it was not until the last 30 years that reinnervation techniques were refined and became performed with relative frequency. Surely this is associated with advances in surgical optics as well as microsurgical instrumentation and technique. Indications for laryngeal reinnervation include functional reanimation of the paralyzed larynx, prevention of denervation atrophy, restoration of laryngeal sensation, and modification of pathological innervation (Crumley, 1991; Aviv et al., 1997; Berke et al., 1999).
Anatomy and Technique of Reinnervation
The technique of reinnervation is similar for both sensory and motor systems. The nerve in question is identified through a transcervical approach. Usually a horizontal skin incision is placed into a neck skin crease at about the level of the cricoid cartilage. Subplatysmal flaps are elevated and retracted. The larynx is further exposed after splitting the strap muscles in the midline. Sensation to the supraglottic mucosal is supplied via the internal branch of the SLN. This structure is easily identified as it pierces the thyrohyoid membrane on either side (Fig. 1). The motor innervation of the larynx is somewhat more complicated. All of the intralaryngeal muscles are innervated by the RLN. This nerve approaches the larynx from below in the tracheoesophageal groove. The nerve enters the larynx from deep to the cricothyroid joint and immediately splits into an anterior and a posterior division (Fig. 2). The anterior division supplies all of the laryngeal adductors except the cricothyroid muscle; the posterior division supplies the only abductor of the larynx, the posterior cricoarytenoid muscle. The anterior division further arborizes to innervate each of the intrinsic adductors in a well-defined order: the interarytenoid followed by the lateral cricoarytenoid, and lastly the thyroarytenoid muscles. The interarytenoid muscle is thought to receive bilateral innervation, while the other muscles all receive unilateral innervation. The external branch of the SLN innervates the only external adductor of the larynx—the cricothyroid muscle. Although the SLN and the main trunk of the RLN can be approached without opening the larynx, the adductor branches of the RLN can only be successfully approached after opening the thyroid cartilage. A large inferiorly based window is made in the thyroid lamina and centered over the inferior tubercle. Once the cartilage is opened the anterior branch can be seen coursing obliquely toward the terminus in the midportion of the thyroarytenoid muscle. The posterior division is approached by rotation of the larynx, similar to an external approach to the arytenoid. Identification and dissection of the fine distal nerve branches is usually carried out under louposcopic or microscopic magnification using precision instruments.
Figure 1..
Stylized left lateral view of the left SLN. The internal (sensory) branch pierces the thyrohyoid membrane and terminates in the supraglottic submucosal receptors. The external (motor) branch terminates in the cricothyroid muscle. Branching of the SLN occurs proximally as it exits the carotid sheath.
Figure 2..
Stylized left lateral view of the left RLN. The branching pattern is quite consistent from patient to patient. The RLN divides into an anterior and a posterior division just deep to the cricothyroid joint. The posterior division travels to the posterior cricoarytenoid (PCA) muscle. The anterior division gives off branches at the interarytenoid (IA) and lateral cricoarytenoid (LCA) muscles and then terminates in the midportion of the thyroarytenoid (TA) muscle. The branches to the TA and LCA are easily seen through a large inferiorly based cartilage window reminiscent of those done for thyroplasty. If preserved during an anterior approach, the inferior cornu of the thyroid cartilage protects the RLN's posterior division and the IA branch during further dissection.
Once the damaged nerve is identified, it is severed sharply with a single cut of a sharp instrument. This is important to avoid crushing trauma to the nerve stump. The new motor or sensory nerve is brought into the field under zero tension and then anastomosed with several epineural sutures of fine microsurgical material (9-0 or 10-0 nylon or silk). The anastomosis must be tension-free. The donor nerve is still connected to its proximal (motor) or distal (sensory) cell bodies. Selection of the appropriate donor nerve is discussed subsequently.
Over the next 3–9 months healing occurs, with neurontization of the motor end-plates or the sensory receptors. Although physiological reinnervation is the goal, relatively few reports have demonstrated true volitional movement. Typically, one can hope to prevent muscle atrophy and help restore muscle bulk. Sensory reinnervation is less clear.
Prior to the microsurgical age, most reinnervation procedures of the larynx were carried out with nerve-muscle pedicle implantation into the affected muscle. With modern techniques, end-to-end nerve-nerve anastomosis with epineural suture fixation is a superior and far more reliable technique of reinnervation.
Reinnervation for Laryngeal Paralysis
Paralysis of the larynx is described as unilateral or bilateral. The diagnosis is made on the basis of history and physical examination including laryngoscopic findings, and sometimes on the basis of laryngeal electromyography or radiographic imaging. The unilaterally paralyzed larynx is more common and is characterized by a lateralized vocal cord that prevents complete glottic closure during laryngeal tasks. The patient seeks care for dysphonia and aspiration or cough during swallowing. The etiology is commonly idiopathic, but the condition may be due to inflammatory neuropathy, iatrogenic trauma, or neoplastic invasion of the recurrent nerve. Although many patients are successfully treated with various static procedures, one can argue that, theoretically, the best results would restore the organ to its preexisting physiological state. Over the past 20 years there has been increased interest in physiological restoration, a concept championed by Crumley (Crumley, 1983, 1984, 1991; Crumley, Izdebski, and McMicken, 1988). A series of patients with unilateral vocal cord paralysis were treated with anastomosis of the distal RLN trunk to the ansa cervicalis. The ansa cervicalis is a good example of an acceptable motor donor nerve (Crumley, 1991; Berke et al., 1999). This nerve normally supplies motor neurons to the strap muscles (extrinsic accessory muscles of the larynx), whose function is to elevate and lower the larynx during swallowing. Fortunately, when the ansa cervicalis is sacrificed, the patient does not have noticeable disability. The size match to the RLN is excellent when using either the whole nerve bundle for main trunk anastomosis or an easily identifiable fascicle for connection to the anterior branch.
Hemilaryngeal reinnervation with the ansa cervicalis has been shown to improve voicing in those patients undergoing the procedure (Crumley and Izdebski, 1986; Chhetri et al., 1999). Evaluation of these patients, however, does not demonstrate restoration of normal muscular physiology. The affected vocal cord has good bulk, but volitional movement typically is not restored. Proponents of other techniques have argued that the ansa cervicalis may not have enough axons to properly regenerate the RLN, or that synkinesis has occurred (Paniello, Lee, and Dahm, 1999). Synkinesis refers to mass firing of a motor nerve that can occur after reinnervation. In the facial nerve, for example, one may see mass movement of the face with volitional movement because all the braches are essentially acting as one. The RLN contains both abductor and adductor (as well as a small amount of sensory and autonomic) fibers. With reinnervation, one may hypothesize that mass firing of all fibers cancels the firings of individual fibers out and thus produces a static vocal cord. With this concept in mind, some have recommended combining reinnervation with another static procedure to augment results (combination with arytenoid adduction) or to avoid the potential for synkinesis by performing the anastomosis of the donor nerve to the anterior branch of the recurrent nerve (Green et al., 1992; Nasri et al., 1994; Chhetri et al., 1999).
Paniello has proposed that the ansa cervicalis is not the best donor nerve to the larynx (Paniello, Lee, and Dahm, 1999). He suggests that the hypoglossal nerve would be more appropriate because of increased axon bulk and little donor morbidity. Animal experiments with this technique have demonstrated volitional and reflexive movement of the reinnervated vocal cord.
Neurological bilateral vocal cord paralysis is often post-traumatic or iatrogenic. These patients are troubled by a fixed small airway and often find themselves tracheotomy dependent. Therapy is directed at restoring airway caliber while avoiding aspiration. Voicing issues are usually considered secondary to the airway concerns. Although most practitioners currently treat with static techniques, physiological restoration would be preferred. In the 1970s, Tucker advocated reinnervation of the posterior cricoarytenoid with a nerve muscle pedicle of the sternohyoid muscle and ansa cervicalis (Tucker, 1978). Although his results were supportive of his hypothesis, many have had trouble repeating them. More recently, European groups have studied phrenic nerve to posterior branch of the RLN transfers (van Lith-Bijl et al., 1997, 1998). The phrenic nerve innervates the diaphragm and normally fires with inspiration; it has been shown that one of its nerve roots can be sacrificed without paralysis of the diaphragm. Others have suggested use of the SLN as a motor source for the posterior cricoarytenoid muscle (Maniglia et al., 1989). Most techniques of reinnervation for bilateral vocal cord paralysis still have not enjoyed the success of unilateral reinnervation and are only performed by a few practitioners. The majority of patients with bilateral vocal cord paralysis undergo a static procedure such as cordotomy, arytenoidectomy, or tracheotomy to improve their airway.
Sensory Palsy
Recent work has highlighted the importance of laryngeal sensation. After development of an air-pulse quantification system to measure sensation, it was shown that patients with stroke and dysphagia have a high incidence of laryngosensory deficit. Studies performed in the laboratory demonstrated that reanastomosis of the internal branch of the SLN restored protective laryngeal reflexes (Blumin, Berke, and Blackwell, 1999). Clinically, anastomosis of the greater auricular nerve to the internal branch of the SLN has been successfully used to restore sensation to the larynx (Aviv et al., 1997).
Modification of Dystonia
Spasmodic dysphonia is an idiopathic focal dystonia of the larynx. The majority of patients have the adductor variety, characterized by intermittent and paroxysmal spasms of the vocal cords during connected speech. The mainstay of treatment for this disorder is botulinum toxin (Botox) injections into the affected laryngeal adductor muscles. Unfortunately, the effect of Botox is temporary, and repeated injections are needed indefinitely. A laryngeal denervation and reinnervation procedure has been designed to provide a permanent alternative to Botox treatment (Berke et al., 1999). In this procedure, the distalmost branches of the laryngeal adductors are severed from their muscle insertion. These “bad” nerve stumps are then sutured outside the larynx to avoid spontaneous reinnervation. A fascicle of the ansa cervicalis is then suture-anastomosed to the distal thyroarytenoid branch for reinnervation. Reinnervation maintains tone of the thyroarytenoid, thus preventing atrophy and theoretically protecting that muscle by occupying the motor end-plates with neurons unaffected by the dystonia. This approach has had great success, with about 95% of patients achieving freedom from further therapy.
Laryngeal Transplantation
Transplantation of a physiologically functional larynx is the sought-after grail of reinnervation. For a fully functional larynx, eight nerves would be anastomosed—bilateral anterior and posterior branches of the RLN and bilateral external and internal branches of the SLN. To date, success has been reliably achieved in the canine model (Berke et al., 1993) and partially achieved in one human (Strome et al., 2001). Current research has been aimed at preventing transplant rejection. The technique of microneural, microvascular, and mucosal anastomosis has been well worked out in the animal model.
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