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ORAL PHASE
The oral phase of swallowing can be further subdivided
into the oral preparatory and the oral transport phase. In the oral preparatory
phase the lips, tongue, mandible, palate and cheeks act in concert with salivary
flow to grind and manipulate the presented food into a consistency and position
so that the subsequent phases of swallowing can take place safely and appropriately.
The afferent and efferent contributions of the cranial nerves essential for carrying
out the oral phase are listed in Table I. Once the food bolus is prepared, the
oral transport phase occurs as the musculature of the lips and cheeks contract
followed by tongue contraction against the hard palate (1). As tongue-hard palate
contact occurs, the soft palate elevates as the tensor veli palatini, levator
veli palatini and palatophayrngeus muscles contract, drawing the velum superiorly
and posteriorly against the nasopharyngeal mucosa and musculature (2).
Normal
movement of the anterior two thirds of the tongue is essential for carrying out
the tasks of the oral stage of swallowing. Tongue musculature can be broadly divided
into extrinsic and intrinsic muscles. The extrinsic muscles are the genioglossus,
hyoglossus, styloglossus and palatoglossus muscles. These muscles have their origin
along the mental spine, hyoid bone, styloid process and soft palate, respectively,
and insert either into the hyoid bone or into the other extrinsic or intrinsic
tongue muscles. The primary actions of the extrinsic tongue muscles are to pull
the tongue forward, backward, upward and downward (3).
The intrinsic
tongue muscles are bundles of interlacing fibers containing connective tissue
septa. These muscles originate in the tongue submucosa and insert into each other
and into the extrinsic tongue muscles in various locations throughout the tongue.
The primary action of the intrinsic muscles are to produce changes in the shape
of the tongue during articulation and deglutition.
One can see from the
variety of origins and insertions of the tongue muscles that to physiologically
reproduce these intertwining muscular actions is daunting and inefficient, hence
the disparate range of swallowing difficulties necessarily encountered after ablative
cancer surgery of the tongue, no matter how sophisticated the reconstruction (4).
While a functioning anterior two thirds of the tongue is critical to normal
functioning of the oral phase of deglutition, the posterior one third of the tongue,
or tongue base, also plays an important role in the generation of forces that
propel a food bolus posteriorly towards the pharynx. Without a functioning tongue
base, tongue-soft palate contact can not be made. With impaired tongue-soft palate
contact during the oral phase of swallowing, the nasopharynx can not be sealed
from the oral cavity so insufficient negative pressure is generated when the hyomandibular
complex elevates away from the posterior pharyngeal wall during the pharyngeal
phase of swallowing (5). As a result, bolus propulsion becomes significantly impaired.
For normal tongue function to take place both the motor and sensory systems
of the tongue must be intact. To assess tongue motor function the tongue should
first be examined while at rest along the floor of the mouth with the mouth open.
A physical examination demonstrating tongue fasciculation can be the first clue
to impaired neurological function in general and impaired neurological function
in the tongue specifically (6). To further assess tongue motor function one can
assess tongue mobility by having the patient move their tongue superiorly, inferiorly
and laterally on command. Tongue strength can be assessed by having the patient
press their tongue against a tongue blade or against their buccal mucosa.
Assessment of tongue sensation is also critical to the assessment of the
swallow. Using two point discrimination testing, it has been shown that the tongue
tip is the most sensitive area of the tongue surface, followed by the lateral
dorsal tongue, lateral ventral tongue and floor of mouth (7). Impairment of tongue
sensation has been shown to result in major disturbances in oral function, both
in healthy controls and in patients with oral cavity cancer (8, 9).
There
exist age-related changes in sensory discrimination of the tongue, with people
over 60 years of age having a statistically significant less sensitive two point
discrimination level in the anterior two thirds of the tongue than people less
than 40 years old (10). There also exist age-related changes in tongue motor function
with oral transit time in individuals over 60 years of age prolonged when compared
to people less than 60 (11). The coupling of the findings of diminished tongue
sensory and motor function with increasing age might contribute to the increased
prevalence of dysphagia, aspiration and pneumonia seen in the elderly (12, 13).
In healthy individuals, the oral phase of swallowing is generally completed in
approximately 1 second (14).
PHARYNGEAL PHASE
Once
the food bolus encroaches on the palatoglossal folds, or anterior tonsilar pillars,
the pharyngeal phase of swallowing reflexively begins. Factors other than the
food bolus coming in contact with the anterior faucial arches are thought responsible
for the initiation of swallowing, such as posterior tongue movement and stimulation
of the pharynx (15, 16). Furthermore, it has been shown in several studies that
the swallowing reflex can be initiated entirely by peripheral stimulation of the
internal branch of the superior laryngeal nerve (17, 18, 19, 20). The afferent
and efferent contributions of the cranial nerves essential for carrying out the
pharyngeal phase of deglutition are listed in Table II.
What actually
takes place as the swallowing reflex is initiated is as follows:
1. Velopharyngeal
closure to prevent reflux of material into the posterior choana.
2. Closure
of the larynx in a specific sequence to prevent aspiration.
3. Contraction
of the pharyngeal constrictor muscles in a superior to inferior direction.
4. Elevation of the larynx and hyoid bone towards the base of tongue.
5. Relaxation
of the tonically contracted cricopharyngeus to allow passage of the food bolus
into the esophagus.
Velopharyngeal closure is effected by contraction
of the levator veli palatini muscles which elevates the soft palate against the
posterior nasopharyngeal wall. Medial contraction of the lateral pharyngeal wall
musculature in combination with slight anterior movement of the posterior pharyngeal
wall creates Passavant's ridge, which is a ridge of tissue against which the velum
is approximated during the first portion of the pharyngeal phase of swallowing
(21, 22).
Following velopharyngeal closure, the first event in the normal
swallow sequence, preceding even genioglossus electromyography activity which
signals elevation of the hyoid-laryngeal complex, is true vocal fold adduction
(23, 24). It is true vocal fold closure that is the primary laryngopharyngeal
protective mechanism to prevent aspiration during the swallow (24). Subsequently,
false vocal fold adduction, adduction of the aryepiglottic folds and retroversion
of the epiglottis take place (25).
Retroversion of the epiglottis, while
not the primary mechanism of protecting the airway from laryngeal penetration
and aspiration, acts to anatomically direct the food bolus laterally towards the
pyriform sinuses. Since the true vocal folds adduct during the swallow, a finite
period of apnea must necessarily take place with each swallow. When relating deglutition
to respiration, it has been demonstrated that deglutition occurs most often during
expiration and includes a period of apnea ranging from 0.3 sec to 2.5 seconds
(26, 27). The clinical significance of this finding is that patients with a baseline
of compromised lung function will, over a period of time, develop respiratory
distress as a meal progresses. This will lead to fatigue during the meal and the
consequent risks of laryngeal penetration and aspiration (27). This fact underscores
the importance of having available a swallowing evaluation technique that permits
observation of patient fatigue.
Following closure of the larynx, pharyngeal
peristalsis then takes place by sequential contraction of the superior, middle
and inferior pharyngeal constrictor muscles (28). With contraction of the superior
pharyngeal constrictor muscle, the laryngeal elevation takes place. The larynx
elevates because of the hyoid bone and tongue base moving anteriorly secondary
to contraction of the mylohyoid, geniohyoid, stylohyoid and anterior digastric
muscles (5). This anterior movement of the larynx combined with the contraction
of the middle and inferior constrictor muscles strips the food bolus inferiorly,
ushering in the final portion of the pharyngeal phase which is entry of the food
bolus into the cervical esophagus.
The duration of the pharyngeal phase
of swallowing is about 1 sec. Increasing bolus viscosity has been shown to delay
pharyngeal transit, increase the duration of pharyngeal peristaltic waves and
prolong and increase upper esophageal sphincter (UES) opening. Increasing bolus
volume results in earlier onset of tongue base movement, superior palatal movement,
anterior laryngeal movement and UES opening (29). Earlier UES opening results
in increased duration of sphincter opening as well as increasing sphincter diameter.
Pharyngeal transit time also increases slightly with advancing age. The peristaltic
wave sweeping down the pharynx moves along at a rate of approximately 12 cm/sec
(29).
While the oral and pharyngeal phases of swallowing are presented
sequentially, the physiologic reality is that these phases are integrally related.
McConnel described swallowing as a pressure-generation mechanism powered by a
two-pump system. He called these pumps the oropharyngeal propulsion pump (OPP)
and the hypopharyngeal suction pump (HSP) (30). The OPP is the pressure generated
as the anterior two thirds of the tongue propels the food into the oropharynx
accompanied by contraction of the pharyngeal constrictor muscles. The HSP is the
negative pressure generated as the hyoid-laryngeal complex is elevated away from
the posterior pharyngeal wall effectively drawing the food bolus towards the UES.
Underscoring the importance of normal tongue mobility for normal deglutition to
take place is the fact that any condition that affects the anterior two thirds
of the tongue will necessarily affect the OPP and that any problems affecting
the tongue base will alter the HSP.
The UES provides a high pressure
zone between the pharynx and esophagus remaining closed at rest so as to separate
the laryngopharynx from the esophagus. Three muscles contribute to the formation
of the UES, the cricopharyngeus muscle, the most inferior muscle fibers of the
inferior constrictor muscle and the most superior portion of the longitudinal
esophageal muscular fibers (31). These three muscles attach to the posterior lamina
of the cricoid cartilage. Just deep to the UES, also along the posterior lamina
of the cricoid cartilage, is the posterior cricoarytenoid muscle, the primary
abductor of the vocal folds.
At rest, the posterior aspect of the cricoid
cartilage rests along the hypopharyngeal wall. Upon elevation of the larynx away
from the posterior pharyngeal wall, the post cricoid region separates from its
resting position along the posterior hypopharyngeal wall thereby creating a stretching
effect upon the UES (32). The cricopharyngeus has a continual basal tone which
relaxes during the swallow (33, 34). Studies have shown that UES relaxation takes
place during elevation of the hyoid and larynx and reaches its most complete relaxation
at the apex of hyoid and laryngeal elevation (35). What is anatomically taking
place is that the cricoid cartilage is pulled forward by the motion of the hyoid
bone and by contraction of the thyrohyoid muscle. This forward motion of the cricoid
snaps open the UES (36). The UES then closes while the larynx is descending to
its resting position (37). Of note, the UES exhibits a sustained contraction prior
to resuming its basal tone, presumed to assist in preventing immediate regurgitation
once the food bolus enters the esophagus (38).
Regarding motor and sensory
innervation of the cricopharyngeus, the majority of the work in this area had
been on non-human subjects thereby creating significant controversy when applying
animal-subject findings to human physiology. Recent work in humans has led to
a consensus that the cricopharyngeus receives its motor innervation primarily
from the vagus nerve, and to a lesser extent from the glossopharyngeal nerve and
from sympathetic nerves through the cranial nerve ganglia (39, 40). The significant
sensory contributions to the cricopharyngeus are from the ninth nerve with some
contributions from the vagus nerve as well (40, 41, 42).
ESOPHAGEAL
PHASE
Like
the pharyngeal phase of swallowing , the esophageal phase of swallowing is under
involuntary neuromuscular control. However, propagation of the food bolus is significantly
slower than in the pharynx with transit time decreasing to 3-4 cm/sec (29).
The esophagus connects the pharynx to the stomach and can be divided into three
zones (43). The upper zone of the esophagus contains striated muscle beginning
at the UES and continuing inferiorly for approximately 6-8 cm where the striated
muscle of this zone begins to interdigitate with the smooth muscle of the middle
zone, which represents the main portion of the esophagus. The outer fibers of
the upper zone are arranged longitudinally while the inner fibers have a circular
configuration. Subsequent to relaxation of the cricopharyngeus the primary peristaltic
wave of esophageal propagation begins manifested by contraction of the longitudinal
muscles followed immediately by contraction of the circular muscle (43). Recent
work has demonstrated that the primary peristaltic wave is actually two waves
with the first wave dissipating at the end of the upper zone of the esophagus
simultaneous with the generation of a second wave which continues to the distal
portion of the esophagus (44). This physiologic second wave is likely what has
been called secondary esophageal peristalsis which is defined as a reflex response
to esophageal distention alone (45).
The middle zone begins where the
striated and smooth muscle regions join and extends to within 4 cm of the lower
esophageal sphincter (LES). While the upper zone peristaltic wave is under direct
central neural control, in the middle zone the peristaltic wave is primarily controlled
by the nerves of the myenteric plexus which are located between the outer longitudinal
and inner circular muscle layers (46).
The lower zone of the esophagus
contains a short segment of smooth muscle esophagus terminating into the LES.
The LES is an actual anatomic sphincter with localized muscle changes in the circular
muscle (47). Like the UES, the LES is tonically contracted, however, unlike the
UES, there is no constant EMG activity in the LES (43). Anatomically contributing
to the LES are the diaphragmatic crura which have a sphincteric action during
inspiration or straining, which is normally superimposed on the LES (48).
AIRWAY PROTECTIVE MECHANISMS AGAINST ASPIRATION
The airway protective mechanisms that prevent reflux can be divided into two groups,
basal mechanisms and response mechanisms (49). The basal mechanisms operate constantly,
typically without need for stimulation, with the LES and UES being the two best
examples. The response mechanisms are a series of reflexes that generally require
either distension of the esophagus or mechanical stimulation of the pharynx. These
reflexes include the esophago-UES reflex (50), the pharyngo-UES reflex, the esophagoglottal
closure reflex and the pharyngoglottal closure reflex.
The esophago-UES
reflex is a vagally mediated reflex in which distention of the esophagus causes
increased UES pressure or increased cricopharyngeal EMG activity. Distention of
the proximal esophagus is a stronger stimulus for eliciting this reflex than distention
of the distal esophagus (50, 51). The afferent nerve supply to this reflex is
from vagal afferents and slow adapting fibers of the muscular wall of the esophagus.
The pharyngo-UES reflex is an experimentally-induced reflex resulting in
an increase in resting tone of the UES upon water stimulation of the pharynx (42).
The superior laryngeal nerve branch of the vagus is the afferent nerve supply
to this reflex with the efferent source the somato-motor nerves from the vagus.
Abrupt distention of esophagus results in the vocal fold adduction of the
esophagoglottal closure reflex (52). The afferent supply is the vagus nerve carrying
sensory fibers to the brainstem in response to stimulation of stretch receptors
in the body of the esophagus. This reflex has been evoked during spontaneous gastroesophageal
reflux episodes (53).
Finally, the pharyngoglottal closure reflex is
a presumed airway protective reflex which results in brief vocal fold closure
upon stimulation of the pharynx with water (54). The afferent and efferent nerve
supply is similar to that of the laryngeal adductor reflex with afferent innervation
via the internal branch of the superior laryngeal nerve and motor action from
the recurrent laryngeal nerve branch of the vagus.
NEURAL CONTROL
OF SWALLOWING
Swallowing is a centrally mediated phenomenon that
can be divided into supratentorial and infratentorial regions of control. The
supratentorial area of control is located in the frontal cortex anterior to the
sensorimotor cortex (55). The infratentorial or brainstem areas involved in control
of swallowing are located in the dorsal region within and subjacent to the nucleus
of the tractus solitarius as well as in the ventral region around the nucleus
ambiguus (56). In both brainstem sites the neurons surrounding the adjacent medullary
reticular formation are also involved (57).
In general, the cortical
and subcortical regions of the brain are important pathways in the voluntary initiation
of swallowing (58, 59). Studies using transcranial magneto-electric stimulation
to identify corticofugal projections to the muscles of swallowing have demonstrated
that oral muscles, such as the mylohyoid, are represented symmetrically between
the two cortical hemispheres, while laryngopharyngeal and esophageal muscles are
represented asymmetrically, with most people having a dominant swallowing hemisphere
(60). The clinical implication of these findings is that one could expect oropharyngeal
dysphagia to result from a unilateral cortical stroke (61).
The brainstem
is responsible for the involuntary (pharyngeal and esophageal) phases of swallowing.
The dorsal and ventral medullary regions controlling swallowing are represented
on both sides of the brainstem and are interconnected. Either side can coordinate
the pharyngeal and esophageal stages of deglutition, however because they are
interconnected, normal motor and sensory functioning on each side of the laryngopharynx
depends on intactness on both sides of the medulla (62, 63). The clinical implication
is that a unilateral medullary lesion, say after an embolic stroke, can result
in bilateral pharyngeal motor and sensory dysfunction (64, 65). To
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