11.2.1 Swallowing Neurophysiology

Swallowing is a complex interaction of biomechanical, neurophysiological, and behavioral events that occur in strict hierarchical sequence and that depend on intact sensory awareness and basic recognition of the act of eating. Historically, swallowing was considered solely a brainstem function of sensory and motor integration coordinated by the reticular nuclei within the pons and medulla.12 ^,​ 13 However, ongoing research using functional magnetic resonance imaging (fMRI) has shown broad cortical involvement during swallowing, with the most prominent centers of activity located within the lateral precentral and postcentral gyri and the right insula.

Sensory innervation to the mouth, pharynx, and larynx is generally provided by the trigeminal (cranial nerve V), glossopharyngeal (cranial nerve IX), and vagus (cranial nerve X) nerves. Each of these nerves provides important sensory information that helps initiate and control the act of swallowing. Although the sequence of muscle activity in swallowing generally occurs once the pharyngeal swallow has been triggered, sensory feedback may alter the precise occurrences of muscle contractions. Motor innervation in swallowing is mediated primarily via cranial nerves V, IX, X, and XII.14

Table 11.1 summarizes the impact to physiology and speech and swallowing symptoms associated with cranial nerve injury. Many of the techniques used for swallowing rehabilitation rely on this sensorimotor interrelationship, using sensory pathways to stimulate motor function.15

Swallowing generally occurs in four phases or stages: oral preparatory, oral, pharyngeal, and esophageal. The sequence of these stages is generally predictable, although the relative timing varies depending on the size and texture of the food being swallowed. Swallowing has been recognized as largely reflexive, because only the oral preparatory and oral phases are purely voluntary. The oral preparatory phase initiates the process of swallowing. During this phase, smooth coordination and transition between mastication and manipulation prepares and forms the food into a cohesive, manageable bolus that is ultimately propelled posteriorly to the oropharynx.

The next phase of swallowing, the pharyngeal phase, combines both voluntary and involuntary control and occurs with the initiation or “trigger” of the swallowing reflex. Generally, the area between the anterior faucial arches and the point at which the tongue base crosses the rim of the mandible is considered to be the key location for initiation of the pharyngeal swallow. The swallow trigger primarily depends on cranial nerve IX. In synchrony with the onset of the swallow reflex, the soft palate elevates and retracts to close the velopharyngeal port, thereby preventing nasal regurgitation of swallowed material. The base of tongue makes contact with the bulging posterior pharyngeal wall to help propel the food through the pharynx, while the hyoid and larynx bone move superiorly and anteriorly to prevent food from entering the airway, thereby directing the bolus posteriorly into the cervical esophagus. The elevation and anterior movements of the hyolaryngeal complex are essential to the opening of the upper esophageal sphincter, or cricopharyngeus muscle, which allows the bolus to enter the cervical esophagus without aspiration.

11.2.2 Communication Neurophysiology

It is important to remember that communication is more than simply the articulation of sounds and syllables into meaningful utterances, or speech. Communication begins within the cerebral cortex and subcortex as a thought that is then organized and converted into language within the perisylvian region of the dominant hemisphere, specifically Broca’s area and the insula. The motor program or plan is transferred from the premotor cortex to the lower portion of the motor cortex through tracts to the cranial nerves that activate the muscles of the respiratory tract, larynx, and oral cavity for speech production.16 As a result, any disruption or injury to these regions or tracts will result in communication problems.

11.3.1 Anterior Skull Base

Swallowing disorders associated with anterior skull base tumors occur as a result of anatomical alterations rather than cranial nerve dysfunction. The surgical exposure of anterior skull base tumors may require resection of structures such as the maxilla or mandible that provide important structural support during swallowing. As a result, functional deficits most commonly occur in the oral preparatory and/or oral phases of swallowing. In general, anterior skull base tumors do not affect the pharyngeal stage of swallowing.

Labial sensory and motor loss resulting from splitting of the maxilla often renders patients unable to maintain a labial seal, leading to drooling and food loss from the mouth. More extensive surgical approaches such as total maxillectomy cause palatal defects that hinder oral transit, lingual movements and contacts, often resulting in velopharyngeal incompetency and nasal regurgitation. Current advances in endoscopic surgical approaches to anterior skull base tumors have shown improved speech and swallowing outcomes, because they are less invasive and thus result in fewer injuries to the structures critical for swallowing. Fewer lower cranial nerve injuries are thus associated with this approach than are associated with open anterior craniotomy (0% vs. 23.5%, p = 0.04, respectively).18

11.3.2 Middle Skull Base

Like tumors of the anterior skull base, tumors of the middle base of skull are more apt to affect the oral preparatory and oral phases of swallowing than they are the pharyngeal phase. Damage to the middle skull base can result in unilateral or bilateral impairment of cranial nerves V and/or VII, which control the ability to open the mouth and masticate as well as the ability to maintain facial tone and symmetry. Data have shown a 41% incidence of facial nerve palsy in patients after cerebellopontine angle (CPA) surgery.19 Generally patients are able to compensate for unilateral damage, but when the patient experiences facial nerve involvement, patient surveys report lower quality of life measures, including by describing eating as challenging, especially in social settings.19

11.3.3 Posterior Skull Base

Although anterior and middle skull base tumors can cause significant swallowing difficulties and impede the speed, adequacy, and efficiency of oral intake, patients can usually compensate for these deficits. However, tumors that affect the posterior skull base generally result in far more severe deficits and present greater challenges for rehabilitation of swallowing function because of the effect on the involuntary pharyngeal phase of swallowing. Dysphagia has been reported in 29% of patients after posterior fossa surgery, 41.1% of whom aspirate.6

In most cases, injuries to cranial nerves IX and X occur together, because both nerves exit the base of skull through the jugular foramen. Researchers found that nearly half of a population of 181 patients who experienced unilateral vagal palsy after CPA surgery also experienced pharyngeal palsy.8 When injury occurs to cranial nerve IX, the pharyngeal swallowing reflex, pharyngeal contraction, and velopharyngeal competency are generally affected. Subsequently, patients may present with delayed or even absent swallow reflex, resulting in aspiration, pharyngeal stasis of food, and nasal regurgitation.5 Injury to the vagus nerve often results in more severe swallowing impairment, as this nerve is responsible for several physiologic activities that work in concert with the pharyngeal trigger of swallowing. High vagal injuries, especially those associated with skull base surgeries, result in the most serious problems, because they affect all three branches of the nerve—the pharyngeal, superior laryngeal, and recurrent laryngeal nerves20—and can thus significantly affect both voice and swallowing. Patients may require a tracheostomy tube8 ^,​ 17 because of airway compromise, and vocal fold medialization in cases of vocal fold paralysis (10–29%),8 ^,​ 19 to restore phonation and an efficient cough. In the most severe cases, placement of an enteral feeding tube has been reported in 5 to 66% of patients.5 ^,​ 8 ^,​ 17 In addition, because of the significant morbidity associated with skull base surgeries, patients often require longer hospital stays, which reduce emotional well-being and quality of life.5 ^,​ 8 ^,​ 21

Insult at any level of the vagus nerve may result in aspiration because of decreased laryngeal sensation, impaired pharyngeal contraction, or reduced airway closure.22 Clinically, the superior and recurrent laryngeal branches of the vagus nerve are most important for glottic airway protection, whereas the pharyngeal branch ensures adequate pharyngeal contraction via innervation to the pharyngeal constrictor musculature. Injury to the superior laryngeal nerve can leave patients insensate to aspirate, causing them to silently, without coughing or any indication of awareness, aspirate food or liquid into the trachea. Damage to the recurrent laryngeal nerve usually results in paresis or paralysis of one or both of the true vocal cords, depending on the level of injury, impairing glottic valving in response to the aspirate. Clinicians should be advised that patients who have vagal injuries are at high risk for aspiration, with up to a 67% incidence rate reported.5 ^,​ 8 It is important to remember that a lack of patient reaction should not be equated with safe swallowing in this population, whose members are at high risk for silent aspiration.

One of the most important cranial nerves involved in the oropharyngeal swallow is cranial nerve XII, the hypoglossal nerve, which innervates the tongue muscles. Any damage to the hypoglossal nerve, whether unilateral or bilateral, affects the lingual movements critical to the manipulation and transport of food from the anterior portion of the oral cavity to the pharynx. Patients who have hypoglossal nerve injuries will have difficulty maintaining a cohesive food bolus during the oral stage of swallowing, resulting in oral residue after the swallow.22 More important, base of tongue retraction to the posterior pharyngeal wall helps propel the food through the pharynx. If this movement is impaired, then a significant amount of food collects within the valleculae, making swallowing laborious and inefficient, so that patients may expend inordinate effort for little nutritional gain. In addition, these patients remain at risk for aspiration, because food left in the pharynx after the swallow may easily fall into an airway at test.

Aspiration and dysphagia resulting from surgical damage to lower cranial nerves has been found to be the most dangerous complication related to resection of skull base tumors.4 Alternatively, patients who have gradual tumor progression generally demonstrate the best potential for compensation of swallowing deficits, whereas patients who experience acute insults often have more severe problems, because they have not had the benefit of time to adjust to their swallowing problems.2 ^,​ 21 It is critical that patients who have cranial nerve dysfunction be referred to a speech-language pathologist for baseline evaluation of dysphagia to maintain oral nutrition and reduce complications.