Oral Preparatory Stage

The oral preparatory aspect of deglutition, which prepares food for the swallow, involves the coordination of (1) lip closure to hold food in the mouth anteriorly, (2) tension in the labial and buccal musculature to close the anterior and lateral sulci, (3) rotary motion of the jaw for chewing, (4) lateral rolling motion of the tongue to position food on the teeth during mastication, and (5) bulging forward of the soft palate to seal the oral cavity posteriorly and widen the nasal airway.⁴ The forward position of the soft palate is not present during active chewing, and premature spillage while chewing is common and normal in people of all ages. Much of this coordination requires cerebellar input.⁸ The oral phase of deglutition is mechanical in that it involves the reduction of solid food to a pulverized consistency that may be easily swallowed. The most important neuromuscular function involved in the oral preparatory phase is the lateral rolling motion of the tongue.⁹ Without normal range-of-tongue motion, the manipulation and mastication of food during the oral preparatory phase would be impossible. At the termination of the oral preparatory phase, the tongue pulls the food together into a ball or bolus and holds it in a cohesive fashion on the floor of the mouth or against the hard palate (Fig. 90-1) in preparation for the beginning of the oral phase of the swallow.^4,7,10–13

Figure 90-1. The anterior and lateral views of tongue position in holding bolus immediately before initiating oral stage of swallow.

Oral Stage

The oral stage of the swallow is also a mechanical, voluntary stage and is designed to move food from the front of the oral cavity to the pharynx, wherein the pharyngeal stage of swallow is initiated. Again, tongue motion is the most critical element in this phase of the swallow because the tongue shapes, lifts, and squeezes the bolus upward and backward along the hard palate until the food reaches the pharynx.^14–17 During this posterior propulsion by the midline of the tongue, the lateral margins of the tongue are sealed against the alveolar ridge, providing resistance against which the midline of the tongue propels the bolus.¹⁵ Tension in the buccal musculature is also thought to contribute to propelling the bolus backward, but to a much lesser degree than tongue movements.¹⁸ When the head or leading edge of the mandible crosses the tongue base, the pharyngeal swallow should be triggered in healthy people of all ages (Fig. 90-2). The pharyngeal swallow is usually triggered by the glossopharyngeal nerve (C9). In healthy people, the oral stage lasts no more than 1 to 1.5 seconds and is slightly prolonged with increasing age and with increasing viscosity of the bolus swallowed.^5,19

Figure 90-2. The lateral view of the head and neck illustrating the normal point at which swallowing reflex triggers.

In animal studies and in healthy humans, the pharyngeal swallow has been found to be triggered not only from C9 but also from the superior laryngeal nerve at the inlet of the larynx.^20–25 Normal swallowing does not use this secondary mechanism for triggering the pharyngeal swallow because food would have almost entered the airway by the time the pharyngeal swallow was triggered. Thus when videofluoroscopic examination of a patient shows that the pharyngeal swallow triggers late, as food is about to enter the airway or after the bolus has come to rest in the valleculae or pyriform sinuses, the patient is said to have a disorder of swallowing called a delayed triggering of the pharyngeal swallow.

Pharyngeal Stage

The pharyngeal stage of the swallow is the more physiologically important one because airway protection occurs during this stage in healthy people. The oral preparatory and oral stages of the swallow may be bypassed by reducing the consistency of food to liquid, by syringing food into the back of the mouth, or by positioning the head back so that gravity carries the food into the pharynx. The pharyngeal stage of the swallow cannot be bypassed.

The pharyngeal swallow is mediated in the lower brainstem (the medulla) in the reticular formation immediately adjacent to the respiratory center. Coordination exists between these two centers because respiration ceases for a fraction of a second when the airway closes during the pharyngeal swallow. There is also cortical input to the triggering of the pharyngeal swallow through the tongue movement patterns in the oral phase of the swallow.²⁰ The exact neurologic substrate for this cortical input is not clearly understood.²⁶

Neuromuscular Activities Characteristic of the Pharyngeal Swallow

When the swallowing reflex is triggered, the brainstem swallowing center programs five neuromuscular activities to occur (Fig. 90-3). If triggering of the pharyngeal swallow is delayed, none of these neuromuscular activities occurs until pharyngeal swallow triggers (1) velopharyngeal closure to prevent backflow of material up the nose; (2) tongue base retraction to propel the bolus through the pharynx; (3) pharyngeal contraction to clear residue through the pharynx; (4) airway protection, which involves both elevation and closure of the larynx; and (5) cricopharyngeal or upper esophageal sphincter (UES) opening to allow the bolus to pass into the esophagus.^1,2,27–33

Figure 90-3. The lateral view of the head and neck, showing four neuromuscular components triggered by swallowing reflex: (1) closure of soft palate, (2) peristaltic action, (3) elevation and closure of larynx, and (4) relaxation of cricopharyngeal muscle.

Velopharyngeal closure and hyoid and laryngeal elevation occur as the first response to triggering the pharyngeal swallow. Then laryngeal closure occurs, followed closely by opening of the cricopharyngeal sphincter. These neuromuscular functions also overlap but do not all last for the entire pharyngeal stage of the swallow. Instead, each lasts only as long as the bolus is passing that part of the pharynx. When the bolus has reached the middle to lower pharynx, the soft palate lowers. At that time, the larynx is closed and elevated and the upper esophageal sphincter is open, preventing the passing bolus from entering the airway and allowing it to enter the esophagus. The duration of the pharyngeal stage of the swallow normally lasts a maximum of 1 second and does not vary dramatically with the consistency of food or age or gender of the patient.^5,19

Airway Protection

Airway protection, as noted previously, involves two dimensions: elevation and closure. Elevation is created by contraction of strap musculature, which positions the larynx upward and forward under the tongue base as it is retracted at the end of the oral phase of the swallow. The larynx is pulled up and out of the way of the passage of the food bolus over the base of the tongue. Closure of the larynx involves three sphincters: the epiglottis and aryepiglottic folds, the false vocal folds and airway entrance, and the true vocal folds.^{27,28,34–36} The relative importance of each of the three sphincters has been debated in the literature.^35,37,38 Most authors agree that the epiglottis and aryepiglottic folds play a relatively minor role in protecting the airway; their purpose is to divert food around the airway. The most important level of closure, airway entrance closure, is maintained only for the fraction of a second that the bolus is passing the airway.

Cricopharyngeal (Upper Esophageal Sphincter) Opening

The cricopharyngeus muscle acts in opposition to the function of the constrictor mechanism of the pharynx. At rest the constrictors are relaxed, and the cricopharyngeus muscle or upper esophageal sphincter is in tonic contraction to prevent air intake into the esophagus concurrent with inhalation into the lungs. Also, the contracted cricopharyngeus muscle prevents backflow from the esophagus into the pharynx.¹ During the swallow, as the constrictor mechanism is contracting, the cricopharyngeus muscle relaxes at the appropriate moment. The anterior superior movement of the larynx opens the UES, and the bolus passes into the esophagus. The duration of UES opening and airway closure increases as bolus volume increases.³⁹

Pharyngeal Pressure Generation: Tongue Base Retraction and Pharyngeal Contraction

When the tail of the bolus reaches the tongue base, the tongue base moves rapidly backward like a piston, increasing pressure in the pharynx. As the tongue base moves backward, the lateral and posterior pharyngeal walls at the tongue base level move inward. The tongue base and pharyngeal walls should make complete contact. Electromyographic and radiographic studies have shown that pharyngeal contraction, or the squeezing action of the constrictor mechanism to move the bolus through the pharynx, occurs sequentially, beginning in the superior constrictor muscle and moving through the medial to the inferior constrictor muscle.^29,40

Pharyngeal contraction is responsible for clearing material from the pharyngeal walls and pyriform sinuses. When residue or material remains in the valleculae after the swallow, it is interpreted as a symptom of reduced tongue base movement.⁴¹ Tongue base movement occurs later as bolus volume increases.

Esophageal Stage

When the bolus has passed through the UES, the esophageal phase of swallow begins. The esophageal stage has greater variability in duration than the other stages of the swallow. Normal esophageal transit may vary from 8 to 20 seconds.⁴ The upper third of the esophagus is composed of mixed voluntary and involuntary muscle, and the lower two thirds is composed entirely of involuntary muscle. The lower esophageal sphincter acts as a valve to the stomach, which must open in time to allow the bolus to pass from the esophagus into the stomach.

In summary, the pharyngeal stage of the swallow is responsible for transit of material into the esophagus and for airway protection, probably the most important aspect of deglutition.

Figure 90-4 illustrates the progression of the bolus through the pharynx. If an anatomic or neuromuscular disorder affects the pharyngeal stage of the swallow, aspiration may result.

Figure 90-4. A through E, Lateral views of the head and neck illustrating progression of bolus through the pharynx.

Aspiration (Coughing, Choking)

Aspiration is the entry of material into the airway below the true vocal folds. The effect of chronic aspiration in adults is not well understood, but in the long term it may result in pneumonia or pulmonary changes. Patients who are observed to aspirate on a radiographic study of swallowing are at significantly greater risk of pneumonia developing than patients who do not show aspiration on such a study. Many patients with head and neck cancer who have chronic aspiration do not survive long enough to experience the long-term effects of their aspiration. Aspiration may occur before, during, or after the pharyngeal swallow.⁴ Aspiration that occurs before the pharyngeal swallow may result from one of two disorders: reduced tongue control or a delayed or absent pharyngeal swallow. When tongue control is reduced during the oral preparatory or oral stages of the swallow, bits and pieces of food may fall into the pharynx and the open airway as the patient chews. Importantly, the airway is normally open during the oral preparatory and oral stages of the swallow. The airway is closed only for a fraction of a second during the pharyngeal swallow. Aspiration before the swallow can also occur because of a delayed or absent pharyngeal swallow. In these patients, the food is propelled out of the oral cavity by the tongue and falls into the pharynx, wherein it may come to rest in the valleculae, the pyriform sinus, or the airway before the pharyngeal swallow is triggered. The entry of food into the airway does not always trigger a cough, particularly in neurologically impaired patients and some patients with head and neck cancer in whom sensory input is damaged.^41,42

Aspiration during the swallow takes place when airway closure is inadequate to prevent material from entering the airway during the pharyngeal swallow. Aspiration after the swallow occurs for a number of reasons including reduced laryngeal elevation, reduced tongue base retraction, reduced pharyngeal contraction, unilateral pharyngeal damage, or cricopharyngeal dysfunction. In all of these instances, residue remains in the pharynx after the swallow. When the patient opens the larynx to inhale as is normal after a swallow, some of this residue is sucked or falls into the airway. Determination of the cause of aspiration is critical for efficient treatment. Aspiration is only a symptom of a disorder. Evaluation of swallow is designed to identify the anatomic or physiologic cause of the aspiration. Treatment is designed to eliminate the reason for the aspiration. Each of the disorders noted previously as potential causes of aspiration is treated differently.

Inefficient Swallowing

Inefficient swallowing (i.e., inability to propel food or liquid into the stomach) at each meal can cause malnutrition, dehydration, and/or weight loss. Many different anatomic or physiologic swallowing disorders may cause these complications. As with aspiration, treatment is directed at the anatomic or physiologic disorder causing these complications.

Bedside Evaluation

Bedside evaluation is the next step after screening a patient and includes assessment of facial, lip, tongue, pharyngeal, laryngeal, and respiratory control, as well as the patient’s ability to follow directions. The bedside evaluation also includes an oropharyngeal structural examination. It ends with a recommendation as to whether the patient needs an instrumental assessment such as fluoroscopy or endoscopy. An instrumental assessment is necessary if the clinician suspects that the patient may have a pharyngeal stage abnormality that is invisible on bedside evaluation.

Videofluoroscopy

Videofluoroscopy is the only available procedure that allows direct observation of the upper aerodigestive tract during all four stages of deglutition, beginning with the oral preparatory phase and terminating with the esophageal phase. The standard barium swallow or “upper gastrointestinal (GI)” procedure is inappropriate for head and neck surgical patients or neurologic patients who have severe problems swallowing because of severe risk for aspiration.

In the usual barium swallow procedure, the patient is given a cup of barium and asked to swallow repeatedly. This procedure is designed to examine anatomy and motility in the esophagus, which is a collapsed tube that must be filled with barium to be viewed. For accurate evaluation of esophageal peristalsis without the effect of gravity, the patient lies in a supine position and usually viewed in the anteroposterior plane.

The modified barium swallow (MBS) technique is used to examine the oral cavity and pharynx radiographically, which presents different problems from those encountered when examining the esophagus. By definition, the oral cavity and pharynx are cavities. When they are filled with large amounts of material, visualization of their structure and function is obliterated rather than enhanced. In addition, the patient with an oral or pharyngeal swallowing disorder has greater difficulty handling a large bolus and is at much higher risk of aspiration. Thus modification of the barium swallow technique is necessary when assessing patients with oral and pharyngeal swallowing disorders. Only measured amounts of material are used because patients may exhibit difficulty in swallowing liquids as volume increases but not in swallowing heavier foods or vice versa.

During the MBS, the patient is seated upright in a normal eating position. In dysphagic patients, the physiology of the oral cavity and pharynx in the normal eating position must be established first. Then, if desired, the patient’s position can be changed to note the postural effects on food flow during swallowing. In the modified barium swallow procedure, the patient is initially viewed in the lateral plane with the fluoroscopy tube focused on the lips anteriorly and the seventh cervical vertebra inferiorly as shown in Figure 90-5. This allows complete assessment of oral and pharyngeal motility and of aspiration during the pharyngeal aspect of the swallow. In the anteroposterior view, the trachea overlies the esophagus, making assessment of aspiration difficult.

Figure 90-5. Positioning of patient during modified barium swallow. The structures to be examined in this lateral view are shown in lower right corner.

The major purposes of the modified barium swallow are to (1) define the immediate oral and pharyngeal motility disorders during the swallow; (2) identify the presence of aspiration during swallow of any food consistency; (3) assess the speed of the swallow (compared with normal); and (4) assess the effects of therapy strategies such as postural changes, heightened sensory input, and therapy procedures including swallowing maneuvers.^{16,36,41,43–50} If the patient aspirates or has a highly inefficient swallow, treatment procedures are introduced during the videofluoroscopic study to improve the swallow and allow the patient to continue to eat orally or return to oral intake as quickly as possible. The purpose of the test is to restore oral intake—not to stop the patient from eating.

Endoscopy

Endoscopy by way of transnasal placement of a flexible fiberoptic scope has been used to evaluate some selected aspects of the swallow.^50–53 The oral stages cannot be viewed, and during the swallow the image disappears as the pharynx contracts and closes against the scope. Any residual food in the pharynx after the swallow may be identified, as may any aspiration of the residue after the swallow.

Manometry

Manometry is usually used to examine esophageal peristalsis and the adequacy of functioning of the upper and lower esophageal sphincters.^3,54,55 The patient swallows a soft tube containing pressure sensors. These sensors are positioned so that one registers the pressure in the UES, the second registers pressure changes in the body of the esophagus, and the third registers pressure in the lower esophageal sphincter. The gauges also may be positioned to register pressure in the pharynx, cricopharyngeal sphincter, and the body of the esophagus, thus permitting observation of the temporal relationship between pharyngeal contraction and opening of the cricopharyngeal sphincter.

Ultrasonography

Ultrasonography is used to assess the anatomy and physiology of the tongue during swallowing, but it currently cannot be used to examine the pharynx or larynx because of skeletal interference.¹² Thus it is limited to the study of the oral stage of deglutition.

Radiotherapy

Radiotherapy for the oral cavity and pharynx, in addition to reducing salivary flow and causing short-term oral or pharyngeal edema, may lead to difficulties with triggering of the pharyngeal swallow, laryngeal elevation, and pharyngeal contraction that may begin immediately or months after the therapy is completed.^4,56 Presumably, the problem with laryngeal elevation and pharyngeal contraction relates to increased fibrosis after radiation. The symptoms vary in duration and severity and may appear 6 months or more after completion of a full course of radiotherapy. The long-term effects of radiotherapy on swallowing deserve greater attention and more thorough study.

Chemoradiation

In recent years, treatment protocols that use high-dose concurrent chemoradiation have been increasingly used. Some of the patients undergoing these protocols develop severe swallowing problems, generally including a delayed triggering of the pharyngeal swallow, reduced laryngeal elevation, and reduced pharyngeal contraction, and must take nutrition nonorally. Over time (3 to 12 months), these disorders may reduce in severity so that some of these patients can return to oral intake. A great deal more research is necessary on measurement and treatment of these swallowing disorders after chemoradiation.

Surgical Treatment

The effects of surgical treatment for patients with head and neck cancer on swallowing depend on the site and extent of the resection and the nature of reconstruction.^4,57,58 Some data indicate that the reconstruction determines the swallowing pattern of the patient postoperatively, particularly when smaller amounts of tissue are resected.

Tongue

Within the oral cavity, the tongue is the most important organ for maintaining normal food intake. The tongue is responsible for oral manipulation and chewing to prepare food for the swallow and is responsible for the oral initiation of the swallow. Every effort should be made to permit as much range and coordination of tongue motion as possible. Use of the tongue in surgical closure may dramatically reduce the patient’s ability to handle a normal diet.¹⁶

Posterior Oral Cavity

When a tumor invades the posterior oral cavity, a number of swallowing actions may be affected⁵⁹ including tongue mobility during oral preparation and the oral initiation of the swallow, triggering of the pharyngeal swallow, velopharyngeal closure, tongue base retraction, and pharyngeal contraction. Surgery at the tonsil and base of the tongue directly invades the sensory area where the pharyngeal swallow is usually triggered and also damages the attachments of the pharyngeal constrictors into the base of the tongue, thus reducing tongue base retraction and pharyngeal contraction. Reconstruction of this area with a thick and bulky flap interferes with functioning of the pharynx, tongue, and remaining healthy tissues.⁶⁰

Pharynx

Surgical involvement of the pharyngeal wall itself may dramatically impair pharyngeal contraction. If the surgical resection involves only one side of the pharynx, the patient may turn his or her head to the operated side to assist swallowing on the unoperated and less damaged side, thus directing food down the more normal side.⁴³ Alternately, the patient may tilt his or her head toward the more normal side to assist gravitational drainage of food down the stronger side. As in the oral cavity, the nature of the reconstruction may interfere with function on the unoperated side so that even with a change in head position the patient is permanently unable to handle food thicker than liquid and may even have difficulty with liquid. Greater pharyngeal peristalsis is required to move heavier and thicker food than is required for liquid.

Larynx

Resection of a part of the larynx, as occurs in hemilaryngectomy or supraglottic laryngectomy, may interfere with three aspects of the swallow: laryngeal elevation, laryngeal closure, and tongue base retraction.

After hemilaryngectomy, laryngeal closure is the greatest problem.⁴ Depending again on the nature of the reconstruction and on the nature and amount of tissue positioned on the resected side, many patients regain normal swallowing in a relatively short time (1 month) after hemilaryngectomy with swallowing retraining, which usually involves laryngeal adduction exercises.⁶¹

Patients who have undergone supraglottic laryngectomy often have multiple problems with swallowing, which may include reduction in laryngeal elevation, laryngeal entrance closure, and tongue base retraction.⁶² During the supraglottic laryngectomy procedure, portions or all of the hyoid bone are removed, and thus laryngeal suspension from the hyoid is disturbed.^63,64 Resultant residue at the top of the larynx may be aspirated after the swallow when the patients open the larynx and inhale. Airway protection in these patients is achieved by retraction of the tongue base to contact the anteriorly tilting arytenoid cartilages.⁶⁵ Any damage to the tongue base or the arytenoid cartilages or their function in adduction and anterior tilting results in inability to protect the airway and aspiration after the swallow.