John C Rosenbek and Neila J Donovan

Thyroid Factor

The Natural Thyroid Diet

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Department of Communicative Disorders, VA RR&D Brain Rehabilitation Research Center, University of Florida, Gainesville, FL, USA

Dysphagia is defined as difficulty moving food and liquid from the mouth into the stomach. Traditionally this condition is divided into oropharyngeal and esophageal dysphagia to identify the locus of involvement. Oropharyngeal dysphagia is the focus of this chapter. It results when the structures or functions of the face, mouth, palate, pharynx, rostral esophagus, or larynx are altered by disease. For decades a feeding tube was the treatment of choice. Beginning in the 1960s and 1970s an array of clinical and instrumental evaluative techniques and medical, surgical, and behavioral approaches to its rehabilitation began appearing (Carrau and Murray, 1999; Huckabee and Pelletier, 1999). The evaluative approaches, including videofluoroscopy of the swallowing structures in action (Logemann, 1997) and endoscopic visualization during swallowing (Langmore, 2000), have increased understanding of the disturbed biomechan-ics responsible for impaired swallowing. Similarly the treatments for these biomechanical abnormalities have become increasingly powerful influences on the swallowing mechanism and on its neural controls in the nervous system.

This chapter's main purpose is to discuss the notion of neural plasticity in relation to dysphagia rehabilitation. The relative infancy of dysphagia science and the relatively short modern duration of excitement about the nervous system's plastic response to systematic stimulation mean that the data on changes in brain in response to swallowing treatment are in very short supply. They are, however, emerging, and the extant data will be reviewed. That review requires a context comprising brief discussion of the:

1 structures and neural controls on which swallowing depends,

2 causes of dysphagia,

3 approaches to evaluation, including measurement of treatment effect,

4 classification and description of the most frequently employed treatment approaches.

These brief reviews will acquaint the reader with the clinical science of dysphagia and make the subsequent discussion of the plasticity data easier to evaluate.

23.1 Anatomy

Multiple structures of the head and neck are critical to normal oropharyngeal swallowing which traditionally is divided into oral and pharyngeal stages. During the oral stage the jaw contributes to mouth closure and stabilizes and helps raise the tongue toward the hard and soft palates as the swallow is triggered. The lips and teeth form a cavity with the tongue to contain the bolus of food or liquid in the mouth. The tongue moves the bolus around to mix it with saliva and then propels it posteriorly through the anterior and posterior faucial pillars and into the pharynx. This posterior movement triggers what has come to be called the swallow's pharyngeal stage. Simultaneously, or somewhat ahead of this

Figure 23.1. Head and neck structures that contribute to swallowing (Bosma et al., 1986, reprinted with permission).

Oral palate

Pharyngeal palate Uvula

Genioglossal membrane

Vallecula Geniohyoid membrane Mylohyoid membrane

Figure 23.1. Head and neck structures that contribute to swallowing (Bosma et al., 1986, reprinted with permission).

Hyoid bone

Orifice of eustachian tube Torus tubarius Salpingopharyngeal fold Superior constrictor membrane

Middle constrictor membrane Laryngeal aditus

Hyoid bone


Ventricular fold (false cord) Laryngeal ventricule Vocal fold (True cord) Thyroid cartilage Cricoid cartilage Trachea Thyroid gland

Laryngeal vestibule

- Eminence of cuneiform cartilage

Eminence of corniculate cartilage

Interarytenoid membrane



Esophagus posterior movement, the soft palate elevates toward the posterior pharyngeal wall thereby preventing passage of bolus into the nose. Simultaneously as well, the larynx squeezes shut so material cannot fall into the airway and begins - along with the hyoid bone to which it is connected - to move anteriorly and superiorly in the neck. It is this elevation that both contributes to airway protection and to the opening of the rostral esophagus, called the upper esophageal sphincter (UES). UES opening occurs prior to the bolus's arrival at the rostral esophagus and is made possible by the muscle and tendon connections of the hyoid bone, larynx, and UES. This elevation also causes the epiglottis to tilt down over the opening into the larynx, thereby offering further protection to the airway. These structures are shown in Fig. 23.1.

23.2 Neurophysiology

Predictably this complex set of activities requires complex neural controls. Motor fibers of cranial nerves V, VII, IX, X, XI, and XII innervate jaw, face, palate, pharynx, larynx, and tongue, respectively. As the motor system depends on sensory information if swallowing is to occur normally, sensory fibers from these same cranial nerves, with the exception of XI and XII, which are motor only, are also critical. These sensory components transport taste, temperature,

Vestibular nucleus (VIII)

Cochlear nucleus (VIII)

Nucleus solitarius (X) (gustatory rostral portion - VII, IX caudal portion - IX, X)

Nucleus of the spinal tract of the trigeminal

Accessory (spinal) nucleus (XI)

Figure 23.2. Brainstem structures involved in the central pattern generator for swallowing Crary and Groher, 2003, p. 29, reprinted with permission.

Trigeminal motor nucleus (V)

Abducens nucleus (VI) Facial motor nucleus (VII) Superior (VII) and inferior (IX) salivatory nuclei

Nucleus ambiguous (IX, X) Dorsal vagal nucleus (X)

Hypoglossal nucleus (XII)

Accessory (spinal) nucleus (XI)

Figure 23.2. Brainstem structures involved in the central pattern generator for swallowing Crary and Groher, 2003, p. 29, reprinted with permission.

touch, and pressure from critical structures in the mouth, pharynx, and larynx.

Central pattern generator

Miller (1986, 1999) has written the most thorough description of the central pattern generator in the medulla where this sensory and motor information is mixed and controlled. Central pattern generator structures are displayed in Fig. 23.2.

The dorsal region of the central pattern generator contains the sensory components comprising nucleus tractus solitarius and the surrounding reticular activating system with additional input from the sensory nucleus of the Vth cranial nerve and from more rostral cortical and subcortical structures. Taste, temperature, touch, and pressure are integrated in this sensory portion of the pattern generator. The resulting cascade of sensations has a twofold effect. First, the cascade facilitates the initiation and repeated activation of the muscles involved in the pharyngeal phase of swallowing. Second, it activates the interneurons that modify the motor output to the swallowing musculature.

The ventral region comprises the nucleus ambiguous and surrounding reticular activating system with additional motor influences from the Vth and XlIth cranial nerves. The ventral motor complex contributes to swallowing by coordinating the complex movements needed to complete the swallow. In addition, according to Miller, this area contains neurons with special properties. Specifically, the neurons in this area produce cyclic bust patterns that allow for timed and sequential discharges, thereby supporting the complex coordinations essential to normal swallowing.

Subcortical and cortical influences

The oropharyngeal swallow is more profitably viewed as a highly patterned response than as a reflex. However, the unfolding swallowing response is increasingly more automatic as one moves from the mouth's chewing, bolus formation, and posterior bolus movement functions to the functions of the pharyngeal stage. Nonetheless, some control can be extended even over the pharyngeal component of the swallow. This control is possible because of interactions of subcortical and cortical centers with the central pattern generator. Relevant subcortical and cortical areas include left and right basal ganglia, insula, sensorimotor cortex, and the supplementary and premotor areas of both frontal lobes. Martin and Sessle (1993) suggest that the cerebral cortex is important to initiation and modulation of the stages of swallowing, as well as to integration of swallowing with other sensorimotor functions, including alimentation and respiration.

23.3 Causes of dysphagia

Any abnormality of critical swallowing structures or neural controls can disrupt swallowing with the nature of the deficit being at least in part the result of the locus and type of involvement. Major structural abnormalities are, of course, head and neck tumors such as a cancer invading the floor of the mouth. Surgical and radiation for these tumors can also contribute to the swallowing dysfunction. In the latter case a major cause is fibrotic change to otherwise healthy tissue. Reduced saliva from surgery, radiation, or medications is another negative influence on swallowing. The full panoply of neurologic diseases can also make swallowing difficult or impossible depending on the site of neurologic involvement. These include stroke, tumor, trauma, infectious disease, movement disorders, and other degenerative diseases. In addition muscle and connective disease such as polymyositis can cause dysphagia. Finally deconditioning as when a geriatric person fractures a hip and is immobilized and nourished via tube during the period before and after surgery can cause swallowing to deteriorate.

23.4 Evaluation

The purposes of evaluation in dysphagia are to:

1 determine the presence of a dysphagia by identifying signs of abnormality,

Figure 23.3. Videofluoroscopic image of the swallowing structures Crary and Groher, 2003, p. 190A, reprinted with permission.

2 support hypotheses about the underlying pathophysiology, whether it is weakness, abnormal tone, or discoordination for example,

3 provide guidance to an appropriate treatment,

4 measure change with time, disease, or treatment.

A clinical examination such as the MASA (Mann assessment of swallowing ability; Mann, 2000) is the usual first step and because sensitivity and specificity of signs from this examination are known, especially for stroke patients, it may be the only examination administered. Frequently, however, an instrumented examination follows. The two most frequently employed are the videofluoroscopic swallowing examination (VFSE) and the endoscopic swallowing examination. A videofluoroscopic image of the swallowing structures appears in Fig. 23.3.

23.5 Treatment

Surgical, medical, and behavioral treatments for dysphagia are now available (Carrau and Murray, 1999; Huckabee and Pelletier, 1999). Surgical and medical treatments may be curative, palliative, or result in improvements that are nonetheless inadequate to adequate, safe nutrition. The behavioral treatments, which may precede, follow, or be administered concurrently with medical and surgical ones are traditionally divided into compensatory and rehabilitative. Only the rehabilitative treatments will be discussed, because their influence on the person with dysphagia provides the greatest contribution to what is known about plasticity in dysphagia.

Rehabilitative treatments

Treatments to improve tongue function, pharyngeal muscle activity, laryngeal closure, and anterior and superior movement, UES opening, to heighten sensory input, and to improve the coordination of movements among all these structures have been developed. Data documenting their effects on swallowing movements and functional status including improved rate of eating and drinking have also begun to appear. Table 23.1 comprises a listing of the most commonly used methods, brief descriptions of how they are to be performed, indications for use, references, and levels of evidence in support of application.

23.6 Treatment effects

The two principle classes of outcome measurement in the majority of treatment studies are:

1 biomechanical measures of durational relationships between test boluses (material swallowed whether liquid, semi-solid, or solid) and structural movements,

2 measures of bolus flow abnormality.

An example of a traditional durational measure is duration of swallow initiation defined as the time from the bolus' arrival at the posterior mouth to the beginning of pharyngeal stage activity. A traditional and critical bolus flow measure is aspiration defined as bolus passing through the larynx and into the trachea either before, during, or after the swallow. These and other biomechanical measures are usually influenced in positive ways by the treatments previously described. Delays are reduced or eliminated and bolus flow is improved so that aspiration is eliminated or reduced in amount and frequency. These findings are consistent with the hypothesis that the nervous system's potential plasticity can be activated by treatment.

23.7 Evidence for plasticity

Filipek (2000) defines plasticity as "the brain's ability to recover function that was lost as a result of a defined insult that produced a discrete lesion" (p. 265). The effort to establish the central or plastic effects of treatment for dysphagia is in its infancy. The seminal data are arriving primarily from a single laboratory in Manchester, England (Hamdy et al., 1998, 1999; Fraser et al., 2002; Power et al., 2004). Transcranial magnetic stimulation (TMS) has been the primary method of determining changes in brain (see Volume I, Chapter 15), although positron emission tomography (PET) data are also available (see Volume II, Chapter 5). The only treatment studied in any detail is electrical stimulation applied either to the faucial pillars or pharynx. The population has been limited to stroke, usually unilateral hemispheric stroke in particular. Despite these limitations, the data are informative and are kindling a worldwide effort at replication and expansion of the findings.

Cortical swallowing control

Using TMS and PET, Hamdy and colleagues (1996) were the first to demonstrate the bilateral asymmetric cortical modulation of the oropharyngeal swallow, asymmetric modulation that is independent of handedness. They identified relatively distinct, but overlapping regions of control for oral, pharyngeal, and esophageal stages of swallowing. The oral stage region, as determined by the mylohyoid muscle which shares responsibility for the lingual triggering of the swallow, was more anterolateral than the pharyngeal stage region, which in turn was more anterolateral than the region for the esophagus. More specifically the region for the mylohyoid was located in lateral precentral and inferior frontal gyri. For the pharynx the area was in the anterolateral precentral and middle frontal gyri, and for the esophagus the locus was similar except it involved the superior frontal gyri. As they say in summary: "the mylohyoid locus, therefore,

Table 23.1. Rehabilitative treatments, methodology, indications, and *levels of evidence.





*Levels of evidence

Improved tongue function

Improved posterior pharyngeal wall movement

Increased laryngeal closure

Improved UES opening

Heightened sensory input

Showa maneuver (Hirano et al., 1999)

Lee Silverman voice treatment (Sharkawi et al., 2002)

Masako maneuver (Fujiu et al., 1995; Fujiu and Logemann, 1996)

Supraglottic swallow (Logemann et al., 1997)

Mendelsohn maneuver (Mendelsohn and Martin, 1993)

Shaker head raise (Shaker et al.,


Tactile thermal stimulation (Rosenbek et al., 1996,1998)

Electrical stimulation of pharynx (Hamdyetal., 1998)

Electrical stimulation of faucial pillars (Power et al., 2004)

Subject instructed to take a deep breath and hold it while pressing the tongue to the roof of the mouth and performing an effortful swallow Valsalva maneuver with vowel prolongation at maximum performance level Subject protrudes tongue maximally and holds it comfortably between central incisors while performing an effortful swallow

Subject takes a breath and holds it before and during the swallow, and coughs immediately after the swallow but before inhaling Subject is asked to swallow normally and when the larynx reaches the highest point, to hold it there for a short time

Subject lies supine on a firm surface and lifts head keeping shoulders down.

Therapist rubs both of the patient's faucial pillars three to four times with an ice stick with firm strokes and asks the subject to swallow hard (300-450 trials)

Electrical stimulation of the pharynx at midline is administered via a swallowed electrode. Stimulation occurs for lOmin at 5 Hz Electrical stimulation of the faucial pillars may inhibit the swallow and do more harm than good

For individuals with decreased Level 3 (n = posterior tongue movement design

0: Case-control

For individuals with dysphagia Level 4 (n = 8): observational secondary to Parkinson's disease

For individuals with reduced or restricted posterior pharyngeal wall movement

For individuals with inadequate laryngeal closure

For individuals with inadequate UES opening

For individuals with inadequate UES opening

For individuals with delayed swallow response secondary to decreased sensation

For individuals with delayed swallow response and general pharyngeal dysphagia

For individuals with delayed swallow response and general pharyngeal dysphagia studies without controls

Level 4 (n = 10): observational studies without controls

Level 4 (n = 9): observational studies without controls

Level4 (n = 10): observational studies without controls

Level 2 (n = 27): nonrandomized controlled trial

Level 2 (n = 45): nonrandomized controlled trial

Level 3 (n = 10): observational studies without controls

Level 3 (n = 10): observational studies with controls

* Agency for Healthcare Research and Quality, 2001.



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