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Departments of 1 Internal Medicine, 2 Plastic Surgery, and 3 Radiology, University of Virginia Medical Center, Charlottesville, Virginia 22908
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Winter, W. Christopher, Tom Gampper, Spencer B. Gay, and
Paul M. Suratt. Lateral pharyngeal fat pad pressure during breathing in anesthetized pigs. J. Appl.
Physiol. 83(3): 688-694, 1997.
It has been
hypothesized that the pressure in tissues surrounding the upper airway
is one of the determinants of the size and shape of the upper airway.
To our knowledge, this pressure has not been measured. The purpose of
this study was to test whether the pressure in a tissue lateral to the
upper airway, the lateral pharyngeal fat pad pressure (Pfp), differs
from atmospheric and pharyngeal pressures and whether it changes with
breathing. We studied six male lightly sedated pigs by inserting a
transducer tipped catheter into their fat pad space by using
computerized tomographic scan guidance. We measured airflow with a
pneumotachograph attached to a face mask and pharyngeal pressure with a
balloon catheter. Pfp differed from atmospheric pressure, generally
exceeding it, and from pharyngeal pressure. Pfp correlated positively
with airflow and with pharyngeal pressure, decreasing during
inspiration and increasing during expiration. Changes in Pfp with
ventilation were eliminated by oropharyngeal intubation. We conclude
that Pfp differs from atmospheric and pharyngeal pressures and that it
changes with breathing.
pharyngeal airway; upper airway; fat; sleep apnea
syndromes
INTRODUCTION THE SIZE AND SHAPE of the pharyngeal airway are thought
to depend on the balance of forces (1, 6) developed by muscles that
contract to expand the airway (9), on the pressure within the airway,
and on the pressure in tissues surrounding the airway (3). The pressure
in tissues surrounding the airway, however, has never been measured to
our knowledge. Isono and Remmers (3) postulated, however, that this
pressure would not always be equal to atmospheric pressure and that it
would be determined by a number of influences, some of which operate at
a considerable distance from the pharyngeal lumen.
The purpose of this study was to attempt to measure the pressure in
tissue surrounding the pharyngeal airway. We specifically wished to
determine whether the pressure in the tissue differed from atmospheric
and pharyngeal pressures. If it did differ from these pressures, did it
change with breathing and, if so, how did it change with breathing? We
chose to measure tissue pressure in one location, the lateral
pharyngeal fat pad. The lateral pharyngeal fat pad is immediately
lateral to the muscles that form the lateral wall of the retropalateal
and pharyngeal airways.
METHODS
Table 1.
Age and weight of pigs
Pig
no.
Age, mo
Weight,
kg
1
40
140.4
2
38
130.9
3
5
68.2
4
7
96.8
5
3
25.0
6
3
27.4
in. long, thin wall) was inserted into the
lateral pharyngeal fat pad, and its position within the fat pad was
verified by CT scans. Axial images were periodically repeated during
the procedure to verify instrument position. A guide wire (0.038 in.
diameter, 100 cm long, 3-mm curve radius; Cook, Bloomington, IN) was
inserted through the needle; the needle was then removed, leaving the
tip of the guide wire in place in the lateral pharyngeal fat pad. Dilator catheters, 8- and then 10-Fr, were placed in succession over
the guide wire followed by a peel-away sheath (11-Fr, 15 cm long,
Medi-Tech, Watertown, MA). A Millar catheter with a transducer on its
tip (model SPC-350, Millar Instruments, Houston, TX) was then inserted
through the sheath into the lateral pharyngeal fat pad. The peel-away
sheath was then removed, and the position of the transducer tip
catheter was confirmed by using CT scans.
To determine how catheter position influenced results, in
pig 6, after studies were completed on
the right fat pad, the catheter was forcibly pushed into the fat pad
and the studies were repeated. Then the catheter was withdrawn from the
right fat pad and placed in the left fat pad. Measurements were made,
the catheter was then withdrawn incrementally, and measurements were
repeated at each location.
Pressure and flow measurements.
Tissue pressure was recorded from the transducer-tipped catheter.
Pharyngeal pressure was measured with a 1-cm-long Hyatt-type balloon
(A&E Medical, Farmingdale, NJ) and with no. 100 polyethylene tubing
that had multiple holes in the distal portion, which was covered by the
balloon. The balloon was inserted through the mouth, placed caudal to
the soft palate, and inflated with 0.25 ml of air. The tubing was
attached to a differential pressure transducer (model MP 45-28-871, Validyne Engineering, Northridge, CA). The other port of the transducer
was attached to a face mask with a rubber seal that was placed over the
nose and mouth.
A Fleisch pneumotachograph was attached to the face mask to measure
airflow. The ports of the pneumotachograph were attached to a pressure
transducer (2 cmH2O; model MP
45-14-871, Validyne Engineering), and flow was calibrated to 1 l/s by
using a rotometer. The face mask was a large clear lexan conical canine
mask (Webster, Sterling, MA). It was 4 3/4 in.
long and was covered at the large end of the cone with a highly
flexible rubber diaphragm with an outer diameter of 5 
in. and a 2 1/2-in. hole in the middle. The
pig's nose and mouth were place in the hole of the diaphragm, and the
mask was advanced over the snout until there was no apparent air leak.
The diaphragm restricted but did not prevent the pig from opening its
mouth. We did not control or monitor whether the pig breathed through
its nose or mouth.
Signal processing.
Data were recorded on a portable computer (Dolch V-P.A.C 386, San Jose,
CA) utilizing AT/MCA-CODAS hardware and software (DATAQ Instruments,
Akron, OH) at 40 Hz. Signals were displayed during the study for
calibration and for reference.
Protocol.
After the transducer-tipped catheter was inserted, the pig was allowed
to breathe spontaneously while we measured tissue pressure, pharyngeal
pressure, and flow. In four pigs
(1-3 and
5), after measurements were
obtained, an endotracheal tube was inserted through the mouth into the
trachea, the cuff was inflated, and the pneumotachometer was attached
to endotracheal tube. Measurements of tissue pressure, pharyngeal
pressure, and flow were repeated. In two animals, a fixed inspiratory
resistance (42 cmH2O · l
1 · s)
was added to the endotracheal tube to simulate and exceed the higher
resistance that occurred when the animals breathed through their nose
and mouth.
Data analysis.
All signals were imported into a spreadsheet (Excel, Microsoft,
Redmond, WA) for comparisons and for statistical analysis.
Transmural pressure (Ptm) was calculated by subtracting fat pad
pressure (Pfp) from pharyngeal pressure (Pph) (Ptm = Pph 
Pfp). Transmural pressure was plotted against flow, and linear regression analysis was performed on the entire curve, on the inspiratory limb and then on the expiratory limb of the curve. To look
for hysteresis in the transmural pressure-flow relationship, we
selected data points from both late expiration and early inspiration and then from both late inspiration and early expiration.
We then calculated the slopes of the lines formed by each set of data points and the intercepts of transmural pressure at zero flow by using
linear regression analysis. Transmural pressure at end inspiration was
taken as the zero-flow intercept of the curve consisting of data points
from late inspiration and early expiration. Transmural pressure at end
expiration was taken as the zero-flow intercept of the curve consisting
of data points from late expiration and early inspiration. Transmural
pressures at end inspiration were compared with transmural pressures at
end expiration with a paired t-test.
We also examined separately the transmural pressure-flow relationship
for early inspiration, for late inspiration, for early expiration, and
for late expiration by using linear regression analysis. Other data
were also analyzed with univariate regression analysis.
RESULTS
Pressure was measured in the fat pad at a distance of 1.1-2.0 cm
lateral to the airway (Fig. 1).
In all animals pressure in the fat pad was higher during expiration
than during inspiration. There was a significant positive linear
correlation between airflow and pressure in the fat pad in each animal
(Fig.
2A). The
slopes of the linear regression equations for the pressure-flow curves
(pressure on x-axis, flow on
y-axis) were always positive and
ranged from 0.081 to 0.18 l · s1 · cmH2O1
[mean 0.12 ± 0.044 (SD)
l · s1 · cmH2O1].
Pressure in the fat pad exceeded atmospheric pressure at all times in
three pigs (1,
2, and
4) and most of the time in three pigs (3,
5, and
6) (Fig.
2A). The maximal pressure recorded
was 24 cmH2O, and the minimal was
3 cmH2O. Pressure in the
fat pad was independent of the age and weight of the pigs.
Pressure in the fat pad also correlated linearly with pharyngeal pressure in all animals (Fig. 2B). Increases in fat pad pressure were associated with increases in pharyngeal pressure while decreases in fat pad pressure were associated with decreases in pharyngeal pressure. The slope of the curve (fat pad pressure on the x-axis, pharyngeal pressure on the y-axis) was >1 in all pigs except pig 4 (slope in pig 4 = 0.85).
Orotracheal intubation markedly decreased the changes in fat pad
pressure during breathing (Fig. 3). This
was reflected by a significant increase in the slope of the
pressure-flow curve in three of the four animals that were intubated
and by the absence of any significant relationship between flow and fat
pad pressure in the fourth. The addition of an inspiratory resistance
to the orotracheal tube did not significantly change fat pad pressure from the values during intubation without the inspiratory resistance.
The variability of fat pad pressure when the catheter was forced in,
placed in the contralateral fat pad, and then incrementally withdrawn
is shown in Fig. 4. Forcing the catheter in
the fat pad increased the pressure at all flows and decreased the slope (Fig. 4A,
bottom). Fat pad pressure measured
in the contralateral left fat pad (Fig.
4B) continued to increase with
expiration and decrease with inspiration, but the slope and intercept
of the curves were lower than on the right side. When the
catheter was withdrawn 2.8 cm from the lateral edge of the
retropalateal airway, the catheter detected smaller changes in tissue
pressure than when it was closer to the airway.
Transmural pressure and flow during breathing are shown in Fig.
5. The slopes of the line derived from both
inspiration and expiration were positive in all pigs except that in
pig 4 the relationship was not
significant because the line was vertical. Separation of inspiration
from expiration revealed that the slope of the line derived from
inspiration alone was positive in all pigs except pig
4. The slope of the line derived from expiration alone
was also positive in all pigs except pig
5. The slope of the expiration portion of the curve was
greater than the inspiration portion in all pigs except
pig 6.
Further analysis of the transmural pressure-flow relationship was performed by combining late inspiration with early expiration and then combining late expiration with early inspiration. The slopes of these lines were always positive and not significantly different from one another in each pig. In pig 4, however, the slope of late expiration and early inspiration was not significant so that in this pig no comparison could be made between the two phases of ventilation. The zero-flow intercept of these lines revealed that transmural pressure at end expiration (calculated from the late expiration-early inspiration curve) was higher than transmural pressure at end inspiration (calculated from the late inspiration-early expiration curve) in all five pigs in which significant zero-flow intercepts could be calculated (P < 0.02; Table 2).
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Transmural pressures relative to flow in early inspiration, late
inspiration, early expiration, and late expiration are shown in Fig.
6. The slopes of the regression lines for
each of these ventilatory phases are shown in Table
3. Many slopes were not significant, and no consistent differences among the different ventilatory phases were apparent.
), late inspiration (
), early expiration (
), and late expiration (
). Points for late inspiration and early expiration were
combined to calculate transmural pressure at zero flow for end
inspiration. Similarly, points for late expiration and early inspiration were combined to calculate transmural pressure at zero flow
for end expiration. See Tables 2 and 3 for statistical analysis.
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DISCUSSION
This study has shown that pressure in the lateral pharyngeal fad pad is different from both atmospheric and pharyngeal pressures. Fat pad pressure generally exceeded atmospheric pressure. Fat pad pressure was positively correlated with pharyngeal pressure and varied with breathing. During expiration, fat pad pressure increased, and during inspiration it decreased. Orotracheal intubation eliminated most of these changes in fat pad pressure during breathing.
This study thus confirms the predictions of Isono and Remmers (3) that the pressure in tissues surrounding the upper airway differs from atmospheric pressure. This study also reveals that the pressure in the lateral pharyngeal fat pad is closely linked to breathing. This initial study of tissue pressure does not, however, reveal what influences fat pad pressure and how it is linked to breathing. Also, because we did not measure the force of muscles acting on the upper airway, this study is not able to confirm the balance of forces theory.
The close linkage between fat pad and pharyngeal pressures may be simply due to transmission of pharyngeal pressure through the lateral pharyngeal wall into the fat pad. This mechanism is suggested by elimination of changes in fat pad pressure with intubation.
Another possible mechanism linking changes in fat pad pressure to breathing is via tracheal tug. Caudal movement of the trachea in dogs has been shown to decrease upper airway resistance (8); this occurs through caudal traction on cervical structures mechanically linking the thorax and the upper airway. The precise mechanism of how and where tracheal tug expands the upper airway is unknown. Caudal traction on these structures could also tug on the fat pad and decrease its pressure. In the present study we anchored the trachea by intubating it and preventing it from moving caudally during inspiration. Thus we cannot exclude tracheal tug as a mechanism of changing fat pad pressure during breathing. Studies with isolated laryngeal and thoracic tracheae will be necessary to test whether tracheal tug influences fat pad pressure. These studies could also determine whether changes in pharyngeal pressure are transmitted directly to the fat pad.
Fat pad pressure might also be altered by contraction of upper airway muscles. These muscles could be either adjacent to the fat pad or attached to other structures that are adjacent to the fat pad. We know of no muscles, however, with respiratory activity that are adjacent to the fat pad that might increase fat pad pressure during expiration and decrease it during inspiration.
Because the density of fat (~0.9 gm/cm3) is less than that of water, the major component of most tissues, fat is more compressible than most tissues. When fat is surrounded by more rigid tissues, it could act as a hydraulic to transfer pressures generated in one location to another location. For example, caudal traction on the inferior portion of the fat pad would lower the pressure throughout the entire fat pad just as lowering pressure at the valve stem of a tire lowers pressure throughout the tire. If there were a very compliant structure adjacent to the fat pad such as the lateral pharyngeal wall, the lateral pharyngeal wall would be pulled into the fat pad space and enlarge the upper airway. This mechanism can be tested in future studies. Because the physical characteristics of fat in the lateral pharyngeal fat pad are unknown, it would also be important in future studies to determine the density and connective tissue structure of fat in this location.
The close correlation between fat pad and pharyngeal pressures suggests that the fat pad could act as a spring to absorb and return forces created by changes in pharyngeal pressure. When pharyngeal pressure increases during early expiration, the lateral pharyngeal wall moves laterally (7). This would be expected to compress and increase the pressure in the fat pad. When pharyngeal pressure returns to atmospheric pressure such as at the end of expiration, the fat pad would return the pressure to the lateral airway wall and narrow the airway. During inspiration, when pharyngeal pressure decreased, the higher pressure in the fat pad would be expected to press the lateral pharyngeal airway wall into the pharynx unless fat pad pressure fell more than pharyngeal pressure or unless the lateral pharyngeal wall stiffened because of muscle contraction or passive lengthening. During sleep when muscle tone decreases, the airway would be more susceptible to narrowing caused by fat pad pressure on the lateral pharyngeal wall.
As mentioned above, during inspiration when pharyngeal pressure decreases, the fat pad would be expected to press on the lateral pharyngeal wall and narrow the airway unless fat pad pressure fell more than pharyngeal pressure or the lateral pharyngeal wall stiffened. In our anesthetized pigs, pharyngeal pressure changes exceeded the changes in fat pad pressure in five of six animals. This suggests that in these animals during inspiration, pharyngeal pressure would fall more than fat pad pressure and the upper airway would be vulnerable to compression from the fat pad unless the lateral pharyngeal wall stiffened.
The muscles that comprise most of the lateral pharyngeal wall are the superior and possibly the middle pharyngeal constrictors. Contraction of these muscles would probably stiffen the muscles and diminish transmission of pressure to the fat pad. In normal humans, Kuna (4) found that phasic activation of these muscles with breathing occurred only occasionally in awake subjects, sporadically in rapid-eye-movememt sleep, and not at all during non-rapid-eye-movement sleep (4). In decerebrate tracheotomized cats, however, these muscles contracted when the airway was small, tending to enlarge it (5). It is possible that the anesthesia in our pigs decreased contraction of the lateral constrictors more than occurs during sleep and thus augmented the transmission of pressure from the pharynx to the fat pad.
If the fat content of fat pad cells increases with weight gain, either the pressure within the fat pad would increase or the fat pad would increase in size and displace more compliant adjacent structures. This could displace the lateral pharyngeal wall into the upper air- way if the lateral pharyngeal wall muscles are not con- tracting or are not stiffened by being stretched. We re- cently demonstrated that increasing the volume of the fat pad space did narrow the upper airway of anesthetized pigs (10). This suggests that an increase in the fat content of fat cells could narrow the upper airway.
Measurment of fat pad pressure allowed us to calculate airway
transmural pressure. Transmural pressure (Ptm = Pph Pfp)
represents the dilating and compressing forces on the airway. An
increase in transmural pressure implies airway dilatation, whereas a
decrease in transmural pressure suggests airway compression (3). During inspiration, transmural pressure decreased in the five of six pigs, as
reflected by a positive slope indicating that both transmural pressure
and flow were decreasing together. During expiration both transmural
pressure and flow increased in five of six pigs, as again reflected by
a positive slope. These data suggest that the airway was compressed
during inspiration in five pigs and dilated in expiration in five pigs.
Although we found the slopes to be greater in expiration than in
inspiration in five of six pigs, the low correlation coefficients of
some of the curves make comparison of small differences in slopes
questionable.
Our data suggest there may be hysteresis in the transmural-flow pressure relationship. Transmural pressure at end expiration was higher than at end inspiration in five pigs in which it could be detected. When intraluminal pressure is zero, any differences in transmural pressure can be attributed to differences in fat pad pressure. Thus the lower transmural pressure at end inspiration suggests more airway compression due to fat pad pressure than at end expiration.
There are several inherent technical difficulties in measuring tissue pressure that may influence measurements of fat pad pressure. First, introduction of a catheter into a previously intact tissue may compress the tissue lateral to the transducer and thus increase pressure measured by the transducer. We did observe that forcing an already placed catheter in further did increase measured pressure. Second, local surface forces between tissue-sensor contract points may induce artifacts in the measurements. Both of these reasons may explain the difference we observed between catheter pressure observed in the left and right fat pads of the same pig. Despite these problems and limitations, however, we did observe consistent changes in fat pad pressure during breathing.
CT scans show that both pigs and humans (2) have fat pads lateral and adjacent to their upper airway muscles. This suggests that our data obtained by using the fat pad and upper airway of pigs may be applicable to humans.
ACKNOWLEDGEMENTS
This work was supported by the American Lung Association of Virginia and the University of Virginia Research and Development Committee.
FOOTNOTES
Address for reprint requests: P. M. Suratt, Univ. of Virginia Medical Center, Box 546, Charlottesville, VA 22908.
Received 15 August 1996; accepted in final form 8 April 1997.
REFERENCES
| 1. |
Brouillette, R. T.,
and
B. T. Thatch.
A neuromuscular mechanism maintaining extrathoracic airway patency.
J. Appl. Physiol.
46:
772-779,
1979 |
| 2. | Eller, K., H. Woodson, S. Gay, and P. M. Suratt. Pharyngeal adipose tissue in obstructive sleep apnea. Am. Rev. Respir. Dis. 148: 462-466, 1992. |
| 3. | Isono, S., and J. E. Remmers. Anatomy and physiology of upper airway obstruction. In: Principles and Practice of Sleep Medicine, edited by M. H. Kryger, T. Roth, and W. C. Dement. Philadelphia, PA: Saunders, 1994, p. 642-656. |
| 4. | Kuna, S. T. Respiratory-related activity of the pharyngeal constrictor muscles during wakefulness and sleep in normal adult humans (Abstract). Am. J. Respir. Crit. Care Med. 151: A556, 1995. |
| 5. | Kuna, S. T. Effect of pharyngeal constrictor activation on the pharyngeal airway (Abstract). Am. J. Respir. Crit. Care Med. 153: A688, 1996. |
| 6. |
Remmers, J. E.,
W. J. deGroot,
and
E. K. Sauerland.
Pathogenesis of upper airway occlusion during sleep.
J. Appl. Physiol.
44:
931-938,
1978 |
| 7. | Schwab, R. J., W. B. Gefter, E. A. Hoffman, K. B. Gupta, and A. I. Pack. Dynamic upper airway imaging during awake respiration in normal subjects and patients with sleep disordered breathing. Am. Rev. Respir. Dis. 148: 1385-1400, 1993[Medline]. |
| 8. |
Van de Graaff, W.
Thoracic influences on upper airway patency.
J. Appl. Physiol.
65:
2124-2131,
1988 |
| 9. | Van Lunteren, E., and K. P. Strohl. Striated respiratory muscles of the upper airways. In: Respiratory Function of the Upper Airway, edited by O. O. Mathew, and G. Sant'Ambrogio. New York: Dekker, 1988, vol. 35, p. 87-123. (Lung Biol. Health Dis. Ser.) |
| 10. |
Winter, W. C.,
T. Gampper,
S. B. Gay,
and
P. M. Suratt.
Enlargement of the lateral pharyngeal fat pad space in pigs increases upper airway resistance.
J. Appl. Physiol.
79:
726-731,
1995 |
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