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Sleep, 19(10):SI70-S 174
© 1996 American Sleep Disorders Association and Sleep Research Society
Functional Properties of the Pharyngeal Airway
Properties of Tissues Surrounding the Upper Airway
Richard J. Schwab
Pulmonary and Critical Care Division in the Department of Medicine, and
Center for Sleep and Respiratory Neurobiology, University of Pennsylvania Medical Center,
Philadelphia, Pennsylvania, U.S.A.
Summary: The pathogenesis of obstructive sleep apnea (OSA) remains unknown. However, we are beginning to
understand the mechanisms leading to sleep apnea by evaluating the structure and function of the upper airway
(UA) and the surrounding soft-tissue structures using sophisticated magnetic-resonance-imaging techniques. Knowledge of the morphology and mechanical behavior of the soft-tissue structures is essential for a complete understanding of the physiology of the UA. Although the tongue and soft palate have been considered the most important UA
soft-tissue structures, our data have highlighted the importance of the lateral pharyngeal walls in the mediating UA
caliber. We have demonstrated that: (I) during wakefulness, the predominant anatomic abnormality underlying UA
narrowing in patients with OSA is thickening of the lateral pharyngeal walls; (2) during respiration, there are
significant changes in lateral airway dimensions as well as in the thickness of the lateral walls; and (3) incremental
levels of continuous positive airway pressure (CPAP) result in progressive thinning of the lateral pharyngeal walls.
The dynamic biomechanical behavior of the lateral pharyngeal walls during wakefulness, sleep, and during apneas
needs to be investigated. Key Words: Upper airway-Magnetic resonance imaging (MRI)-Iateral pharyngeal
walls-CPAP-Tongue-Soft palate.
The upper airway (UA) is an extremely complicated
structure, and we presently possess only fragmentary
knowledge about the properties of the UA soft-tissue
structures or about the basic abnormalities that lead to
UA closure during apnea. Modem imaging techniques
(1-4), however, have allowed us to begin to understand the mechanisms leading to sleep apnea by evaluating the structure and function of the VA and surrounding soft-tissue structures. These imaging techniques provide high-resolution anatomical data on the
changes in UA soft-tissue structures (tongue, soft palate, lateral pharyngeal walls, parapharyngeal fat pads)
that are necessary to understand the biomechanics of
the airway (examination of the "donut" rather than
the "hole in the center of the donut"). We believe that
structures lateral to the airway (lateral pharyngeal
walls, parapharyngeal fat pads), in addition to the
tongue and soft palate, are critical to understanding the
pathogenesis of obstructive sleep apnea (OSA) (Fig.
1).
Accepted for publication October, 1996.
Address correspondence and reprint requests to Richard J.
Schwab, M.D., Center for Sleep and Respiratory Neurobiology, 893
Maloney Building, University of Pennsylvania Medical Center, 3600
Spruce Street, Philadelphia, Pennsylvania 19104-4283, U.S.A.
The upper airway may be subdivided into three
regions: (1) nasopharynx (region between the nasal
turbinates and hard palate), (2) oropharynx, which can
be subdivided into the retropalatal (also called the velopharynx) and retroglossal regions, and (3) hypopharynx (region from the base of the tongue to the
larynx) (1,5,6). Figure 2 displays a volumetric magnetic-resonance (MR) image in a normal subject demonstrating the retropalatal and retroglossal regions of
the oropharynx. During wakefulness, VA caliber is
usually smallest in the oropharynx (retropalatal region)
in both normals and apneics (1,2,7). There are a number of structures that make up the anterior, posterior,
and lateral walls of the oropharynx. The anterior wall
is composed primarily of the soft palate, tongue, and
lingual tonsils; the posterior wall is bounded by a muscular wall made up of primarily the superior, middle,
and inferior constrictor muscles (these muscles also
form a portion of the lateral wall) in front of the cervical spine (5,8). The lateral pharyngeal walls as defined using MR imaging (see Fig. 1) are a complex
structure made up of a number of muscles [hypoglossus, styloglossus, stylohyoid, stylopharyngeus, palatoglossus, palatopharyngeus, the pharyngeal constric-
S170
S171
PROPERTIES OF UPPER AIRWAY TISSUES
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FIG. 1. An axial MR image of a normal subject at the retropalatal
region highlighting the important anatomical structures (tongue, lateral pharyngeal walls, lateral parapharyngeal fat pads, mandibles).
tors (superior, middle, and inferior)], lymphoid tissue,
(palatine tonsils) and pharyngeal mucosa. The styloglossus, stylohyoid, and stylopharyngeus muscles arise
from the styloid process while the hypoglossus, middle
constrictor, and stylohyoid muscles insert on the hyoid
bone. The biomechanical relationships between these
muscles and the way they interact with the soft palate
and tongue are not well understood. At the present
time, MR imaging does not have sufficient resolution
to allow differentiation of the specific muscles that
make up the lateral walls. Thus, the lateral walls are
a complex structure made up of a number of muscles,
and further investigation is needed to determine the
factors that control these muscles.
During wakefulness, UA caliber is, in general,
smaller in patients with sleep apnea compared to normal subjects (1,2,9). Moreover, imaging studies
(1,2,10) have demonstrated that the shape of the UA
is different in apneics than normals (see Fig. 3). The
major axis of the apneic airway is oriented in the anterior-posterior dimension (lateral narrowing); in contrast, the major axis of the normal airway is oriented
in the horizontal dimension (2,10). This airway configuration in apneics has been hypothesized to adversely affect UA muscle activity and, therefore, predispose
the apneic to airway closure during sleep (11). These
configurational changes suggest the apneic UA is narrowed laterally. The two primary structures lateral to
the UA are the lateral pharyngeal walls and lateral
parapharyngeal fat pads. Obesity, or more specifically
increased neck size, is a known risk factor for sleep
apnea (12). Weight loss has been shown in multiple
studies to decrease the severity of OSA (13,14) and
result in decreased collapsibility of the airway (measured by increased Pcrit) (15). Therefore, it has been
hypothesized (3,16) that increased adipose tissue, specifically deposited in the lateral parapharyngeal fat
FIG. 2. Volume-rendered head with extracted UA and 3-d centerline (black dots within the white airway) superimposed on image.
Two oblique images locally perpendicular to airway are depicted at
the retropalatal (RP) and retroglossal (RG) regions. The centerline
program allows computation of a series of oblique slices locally
perpendicular to the 3-d curvilinear centerline traversing the entire
length of the airway. from which geometric measurements can be
automatically calculated and displayed.
pads, leads to airway narrowing and subsequent apneas. However, our own recent studies have demonstrated that increased thickness of the lateral pharyngeal walls in apneics is the primary basis for the lateral
airway narrowing (1). Figure 4 demonstrates the comparison of an axial image at the minimum airway area
(retropalatal region) of a normal subject and a patient
with sleep apnea. Airway size and airway width are
smaller in the patient with sleep apnea. In addition, the
thickness of the lateral pharyngeal wall is larger in the
apneic. Our results demonstrated that the lateral pharyngeal walls were larger in apneics than normals and
that the lateral pharyngeal walls were the soft-tissue
structure most closely associated with small airway
size in all subject groups (normals, snorers, and apneics). We found that the parapharyngeal fat pads were
not closer together, and the area and width of the fat
pads were not larger in apneics at the level of the minimum airway. Our study (1) indicated that the thickness of the lateral pharyngeal walls, not the size of the
soft palate, tongue, or parapharyngeal fat pads, was
the predominant anatomic factor causing airway narrowing in apneics.
Normal
Snorer
Apneic
FIG. 3. Schematic diagram of the differences in UA configuration
in a normal, snorer, and apneic.
Sleep, Vol. 19, No. 10, 1996
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R. J. SCHWAB
FIG. 4. Volumetric rendering of head with segmented airway.
Oblique sections are displayed in a normal and an apneic at the
retropalatal level. The mandibular distance is similar between subjects, however, airway size is smaller in the apneic. The majority of
this airway narrowing is in the lateral direction and secondary to
enlargement of the lateral pharyngeal wall.
The basis for the increased thickness of the lateral
pharyngeal walls in apneics is unknown. We hypothesized that fat or water (edema) could be the cause of
the increased thickness of the lateral pharyngeal walls.
We have used a proton-spectroscopic technique called
HUPSPEC (Hydrogen Ultrathin Phase-Encoded Spectroscopy) in conjunction with MR imaging to study
this hypothesis (17,18). This spectroscopic technique
yields measurements of relative intensities of fat and
water along a selected linear volume of tissue by separating them along the spectral axis (17). HUPSPEC
allows determination of the percentage of fat and water
in the lateral pharyngeal walls, tongue and soft palate.
We studied 10 normals and 10 apneics with HUPSPEC
and found the following results: (1) no significant fat
infiltration in the lateral pharyngeal muscles in normals or apneics, (2) no significant differences in fat
infiltration in the lateral walls, tongue, and soft palate
between apneics and normals, and (3) no significant
differences in water content in the lateral pharyngeal
muscles, soft palate, or tongue between apneics and
normals (18). These data indicate that the increased
thickness of lateral pharyngeal walls in patients with
sleep apnea is not secondary to increased fat infiltration or edema.
Another plausible, albeit unproven hypothesis, is
that weight gain results in increased muscle mass and
an increase in the size of the lateral pharyngeal walls
as well as the tongue and soft palate. Weight loss is
known to decrease fat and muscle mass (19,20). Fatfree tissue comprises 25-30% of the increased weight
in obese patients (19,21). The percentage of muscle in
the uvula of patients with sleep apnea compared to
Sleep, Vol. 19. No. 10. 1996
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FIG. 5. Dynamic airway soft-tissue changes from end inspiration
(first image, top row) to end expiration (last image, bottom row) at
the retropalatal region during exaggerated nasal breathing in normal
subject using the fast gradient echo MR sequence (350 msecondsl
image). The airway is largest and lateral walls maximally narrowed
at mid expiration (last image, top row). Note the significant lateraldimensional changes in the airway. At the end of expiration, the
airway narrows substantially and the lateral walls thicken.
normals is also increased (22). Therefore, obesity may
predispose to sleep apnea by increasing the size of the
UA soft-tissue structures rather than by the direct deposition of fat in the parapharyngeal fat pads or by
compressing the lateral airway walls by these fat pads.
Further studies are necessary to: (1) clarify the mechanism whereby obesity predisposes to sleep apnea, (2)
assess the entire three-dimensional configuration of fat
deposition around the airway, (3) examine the anatomic changes in UA soft-tissue structures (fat and muscle) with weight loss, (4) evaluate the biomechanical
interrelationships between the tongue, soft palate, and
lateral pharyngeal walls, and (5) determine UA softtissue changes that correlate with the degree of sleep
apnea.
Not only are the lateral pharyngeal walls thicker in
apneics than normals under static conditions but, during dynamic conditions (i.e. respiration), there is an
inverse relationship between airway caliber and the
size of the lateral pharyngeal walls as measured by our
cine-computed tomography studies (2,23) and in preliminary studies with a fast-gradient echo MR sequence (Fig. 5). Our own recent studies (2,23) provide
an extensive analysis of the changes that take place
during respiration in wakefulness in normals and apneics. We have demonstrated four distinct phases of
the respiratory cycle with respect to UA dimensions
(Fig. 6). In the first phase (labeled 1, Fig. 6), at the
onset of inspiration, there is an increase in UA area.
This presumably reflects increased action of UA dilator muscles. In the second phase of inspiration (labeled
2, Fig. 6), UA area is maintained relatively constant.
PROPERTIES OF UPPER AIRWAY TISSUES
S173
FIG. 6. Diagram of changes in UA area as a function of tidal
volume in patients with sleep apnea. Four distinct phases are recognized as discussed in the text.
This suggests that there is a balance between the action
of negative intraluminal pressure tending to collapse
the airway and that of airway-dilator muscles tending
to enlarge the airway. Phase 3 delimits the beginning
of expiration. At this time, the airway widens, presumably secondary to positive intraluminal pressure. In
Phase 4, there is a rapid reduction in airway dimensions toward the end of expiration. The airway appears
headed toward its resting position when it is no longer
maintained open either by the positive intraluminal
pressure (at the onset of expiration, phase 3) or the
phasic action of airway dilator muscles (during inspiration, phases 1 and 2). This suggests that the airway
is particularly vulnerable to collapse at the end of expiration. The respiratory-related UA changes demonstrated in these studies (2,23) were predominantly in
the lateral dimension. It has been suggested that the
changes in the lateral walls with respiration may be
related to lung traction effects. Lung volume has been
shown to effect UA size (24). If increases in lung volume resulted in traction and thinning of the lateral pharyngeal walls, then these walls should be thinnest at
the end of inspiration with full-lung expansion. However, as shown in Fig. 4, the lateral walls are thinnest
at mid expiration, not at end inspiration. This indicates
that lung volume has little effect on lateral pharyngeal
wall dimensional changes.
If the lateral pharyngeal walls are the critical structures controlling the UA, then treatment of patients
with sleep apnea should be directed at these lateral
walls. In fact, the effects of continuous positive airway
pressure (CPAP), the treatment of choice in patients
with sleep apnea, are mediated through the lateral pharyngeal walls. We studied changes in UA and surrounding soft-tissue structures with CPAP in 10 normal subjects with MR imaging (25). Incremental levels
FIG. 7. Axial images at the retropalatal region in a normal subject.
Airway enlargement (predominantly laterally) and thinning of the
lateral walls are demonstrated with progressive increases in CPAP.
of CPAP (5, 10, and 15 cm H 20) resulted in: (1) increases in airway volume and airway area within the
retropalatal and retroglossal regions, (2) greater lateral
than anterior-posterior airway dimensional changes
(Fig. 7), and (3) decreases in lateral pharyngeal-wall
thickness and increases in the distance between the
lateral parapharyngeal fat pads (Figure 6). An inverse
relationship was demonstrated between CPAP level
and pharyngeal wall thickness. Our study demonstrated that CPAP predominantly effects structures lateral
to the UA rather than anterior-posterior structures
(tongue and soft palate). This investigation (25) provided further evidence that the lateral pharyngeal walls
play an important role in mediating UA caliber.
In order to understand the pathogenesis of OS A, we
need to understand the biomechanical properties of the
UA soft-tissue structures. We believe that the key
structures mediating changes in airway size in patients
with sleep apnea are the lateral pharyngeal walls. Although the lateral pharyngeal walls are important
structures, we do not understand the dynamic biomechanical behavior of these walls during wakefulness or
sleep or the factors that control the dimensions of these
walls. How do they move during respiration or during
apnea to modulate airway size? The motion of the lateral walls may not be simple. Soft-tissue structures in
the pharynx of patients with apnea may be "redundant". Therefore, motion of the walls may be related
to folding and unfolding. Further investigation is needed to determine the factors that control the thickness
and motion of the lateral pharyngeal walls during
Sleep. Vol. 19. No. 10. 1996
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R.I. SCHWAB
wakefulness and sleep and how these walls interact
with other structures in the UA.
Acknowledgements:
This investigation was supported
by the National Institutes of Health grants HL-03124, MOl
RR00040, Whitaker Research Grant.
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