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1019
Occlusion and Narrowing of the Pharyngeal Airway in Obstructive Sleep Apnea: Evaluation by Ultrafast Spoiled
Frank
Morphologic
G. SheIlock13
Charles Fred
Julien1’2
be detected clinically
Steinberg2
Tom K. F. Foo4 Martin L. Hopp5 Philip R. Westbrook2
sition
sleep
the presence scans
state
sleep
and/or
airway
structural apnea MR
had
ultrafast
imaging
narrowings.
at the
rate
of one
techniques.
in patients airway
can
Ten patients
with
gradient-recalled
pharyngeal
Twelve
found
in the pharyngeal spoiled
of the
plane and at eight transverse obtained
are frequently
alterations
by using rapid imaging
(GRASS)
of occlusions were
These
patients
obstructive
steady
at one midsagittal The
of the pharyngeal
apnea.
in awake
proved in the
MR Imaging
abnormalities
with obstructive
J. Schatz1’2
Peter
GRASS
airway
sequential
images
acquito determine
were
obtained
planes through the pharyngeal
image
per
1.04
sec
while
the
airway.
patient
was
breathing quietly. Occlusions or narrowings of the pharyngeal airways were detected on MR images in all patients. The site(s) of the occlusions and the site(s) and extent of the narrowings varied. Six patients had occlusions and four had narrowings of one or more sites. This study shows that ultrafast spoiled GRASS MR imaging can be used to evaluate patients with obstructive sleep apnea during tidal breathing and is useful for determining the presence of occlusions and narrowings of the pharyngeal airway. 158:1019-1024,
AJR
Sleep apnea
May
1992
is a condition
characterized
by episodic
cessation
of breathing
during sleep [1 -3]. Total collapse and occlusion of the upper airway combined with respiratory efforts is a form of sleep apnea referred to as obstructive sleep apnea. Previous investigations [4-i 2] have shown that the pharyngeal airways are frequently occluded and the cross-sectional areas are significantly narrowed in sleeping and awake patients who have this disorder. These morphologic alterations have been studied objectively by various imaging techniques including plain film cephalometrics, fluoroscopy, conventional CT, and cine CT [2, 4, 6, 8, 9, i ii. Received November 6, 1991 ; accepted December 23, 1991.
after re-
1 Tower Magnetic Imaging, 90048. 2 Department of Radiology,
Los
,
Angeles,
Cedars-Sinai
CA Medi-
cal Center, 8700 Beverly Blvd., Los Angeles, CA 90048. Address reprint requests to F. G. Shellock, 1 2245 San Vicente Blvd., Los Angeles, CA 90049. Department of Radiological Sciences, University of California, Los Angeles, Medical Center, Los Angeles, CA 90024. 3
General WI 5320i.
Electric
Medical
Systems,
Because
the cross-sectional
9, 1 1 1 3], total
vision
Milwaukee,
occlusion
area of the upper airway varies with respiration
and significant
narrowing
(which
are frequently if the imaging
[8,
transient technique
processes) may be overlooked or not fully appreciated used to assess these abnormalities lacks sufficient temporal resolution to show the dynamic changes in the dimensions of the upper airway [8, 9, i 1 ]. Cine CT is particularly useful for detecting occlusion and narrowing of the pharyngeal airways of patients with obstructive sleep apnea because this technique in the size of the airway during respiration, even in tachypneic
can show changes patients [8, 9, 1 i].
Previously, MR imaging has not been used to study dynamic alterations of the pharyngeal airway because of the poor temporal resolution of this imaging tech-
les, CA 90048.
nique. However, the recent advent of rapid MR imaging techniques has provided a means of obtaining multiple images at multiple locations with sufficient image quality and temporal resolution to allow a dynamic evaluation of the pharyngeal airway [14].
0361 -803x/92/1 585-1019 © American Roentgen Ray Society
sition
Division of Otolaryngology, Surgery, Cedars-Sinai Medical
Head Center,
and Neck Los Ange-
This report describes in the steady
state
the application (GRASS)
of ultrafast
MR imaging
spoiled
gradient-recalled
for evaluation
acqui-
of the pharyngeal
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1020
SHELLOCK
ET
AL.
AJR:i58,
airway of awake patients with known obstructive sleep apnea in order to identify occlusion and narrowing during tidal breath-
proceeding
ing.
As the receiver phase is advanced in synchrony with the RF pulse, no additional postprocessing is required. The phase angle for optimal contrast between various anatomic structures varies with TA and tissue Ti and T2. In the study of the pharyngeal airway, the initial spoiling or phase angle was 109.9#{176}. A rapidly obtained image free from significant blurring or other
Subjects
and Methods
Subjects
The subjects included nine men (average age, 47 years; range, 40-53 years) and one woman (age, 34 years) with proved obstructive
sleep apnea as determined by strict clinical criteria, including a history of habitual snoring, restless sleep, morning headaches, daytime hypersomnolence, and intellectual deterioration [1-3]. Each subject had two or more of these signs and symptoms, and each had an overnight sleep study to determine the presence of unequivocal episodes of obstructive sleep apnea. Sleep studies were performed with
standardized
polysomnographic
techniques
that
included
contin-
uous monitoring of the electroencephalogram, electrooculogram, submental electromyogram, body position, body movement, ECG, oxygen saturation, oronasal air flow, sonogram, cross-sectional area
changes in the chest and abdominal wall(inductive
plethysmography),
and anterior tibial electromyogram [1 -3]. The patient was observed via closed-circuit television. For a diagnosis of obstructive sleep apnea, a cessation of air flow had to persist for a period of 20 sec or longer and occur at least 30 times during a 6-hr nocturnal sleep period, or a rate exceeding 10 episodes per hour. The mean apnea/ hypopnea index for these patients was 61 episodes per hour and ranged from 48 to 72 episodes per hour. The patients examined in this study were selected because of their severe apnea/hypopnea.
spoiling
to
May 1992
offset
increment
the
phase
distortion was reconstructed partial k-space reconstruction tion
[14-17].
higher
angle
for the nth RF pulse
This
resolution
such
that
receive-only,
wraparound
anterior
neck
local
of a 1 .5-T, 64-MHz Milwaukee, WI) and a
coil
coil (General
Electric
Medical Systems). This local coil was positioned over the nose, mouth, chin, and hyoid bone of the patient to optimize the signal-tonoise ratio of the images obtained of the pharyngeal airway. An ultrafast RF phase spoiled GRASS pulse sequence [1 4] was used to image the pharyngeal airway during tidal breathing, as follows (General Electric 4X Advantage hardware and software upgrades are required for the implementation of this pulse sequence): In the first series, transverse images (used as a localizer), 8.4/2.9/20#{176}(TA/TEl flip angle), were obtained with one excitation, 160 x 1 28 matrix, 20cm field of view, 5-mm section thickness, and approximate imaging time of 10 sec for 1 0 section locations. In the second series, sagittal images (midline slice obtained in reference to the axial plane localizer), 8.4/2.9/200, were obtained with one excitation, 1 60 x 1 28 matrix, 20-cm
field
of view,
5-mm
section
thickness,
and
acquisition
time
of
approximately 1 2 sec for 12 images at a single section location. In the third series, transverse images (section locations obtained from the nasopharynx to the hyoid referenced to the previously obtained sagittal
plane
image),
8.4/2.9/200,
were
obtained
with
one
allowed
a reduction
images
could
in the minimum
be recovered
TE and
from
receiver
filter
bandwidth
and
acquires
a partial
echo
[14].
A
image is obtained by spoiling the residual transverse magnetization of the steady-state free precession signal [14I 6]. In the pulse sequence used for this study, RF phase spoiling was used. This involved applying the RF pulses at varying phase offsets in the rotating frame, starting with an initial angle, 0, and more
Ti-weighted
TR,
reduced
as
partial-
using 67% of the echo), the minimum TE and TA were 2.9 and 8.4 msec, respectively. The very short TE used for this pulse sequence should minimize air
and
bone
susceptibility
artifacts
and
spurious
narrowings
of the
soft tissue-air interface. To assess the relative accuracy of the ultrafast spoiled GRASS pulse sequence for measuring cross-sectional areas, a phantom study was conducted. The phantom contamed cylinders of various sizes (cross-sectional areas ranging from 0.25 to 5.0 cmi), filled separately with either peanut oil, copper sulfate, or air. Cross-sectional areas were determined for these cylinders by using a cursor and the software incorporated with the MR scanner.
study
of
the
pharyngeal
airway
during
active
sequence
respiration
for were
acquired at the rate of one image per 1 .04 sec. This temporal resolution permitted 1 2 images to be obtained during tidal breathing of approximately two to four respiratory cycles. The patient was supine, with the head placed in a neutral position to ensure a consistent positioning technique for the study. Any narrowing of the pharyngeal airway seen with the head in a neutral position would be worsened by the slight flexion of the neck that normally
occurs
imaging,
the
with the typical
patient
was
instructed
the mouth
closed
and to refrain
acquisition
of the
images.
The
sleeping
posture
to breathe
[5, 1 3]. During
through
from
coughing
patient
was
the
nose
or swallowing
awake
during
MR with
during the
entire
procedure. Immediately after completion of each series, images were viewed as a cine-loop display and inspected to determine if the patient coughed or swallowed during the examination. If necessary, any images that were technically inadequate were redone. The average total examination time (including setting up equipment, positioning of the patient, and explaining the study) was approximately 17 mm.
Display
and
Evaluation
of Images
excitation,
160 x 128 matrix, 20-cm field of view, 7-mm section thickness, 2mm interslice gap, and approximate acquisition time of 2 mm 55 sec for 12 images obtained at 12 section locations. The ultrafast spoiled GRASS pulse sequence uses a ±32-kHz digital
or
echo data sets. For a 1 60 x 128 acquisition matrix (frequency samples x views), an image with an effective resolution of 256 x 128 was generated. If 256 frequency samples in a full echo were to be acquired, a minimum TE of 4.7 msec and a minimum TA of 9.0 msec could be achieved for an image with the other aforementioned imaging parameters. By using partial-echo acquisition with 160 frequency samples (i.e., by
the
MR imaging was performed with the body MR imager (General Electric Medical Systems,
phase
+ nO [14-17].
from a partial echo data set by using a algorithm based on homodyne detec-
The accuracy of this measurement was ±1 0%. Images obtained with this ultrafast spoiled GRASS
MR Imaging
the
...
was 0 + 20 +
The 12 images obtained sagittal
and
multilevel
at each section
transverse
plane
location
sections
were
for the midline viewed
as cine-
loop displays in order to optimally show the alterations of the airway dimensions associated with respiration. Although the sagittal images often showed potential sites of occlusion or narrowing of the pharyngeal airway (Fig. 1), they were considered to be potentially unreliable for showing morphologic abnormalities because of the possible presence of asymmetric narrowing of the airway (i.e. narrowing may have occurred off axis). Therefore, only transverse images were used for ,
the
assessment
of occlusion
and
narrowing.
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AJR:158,
GRASS
May 1992
MR
IN OBSTRUCTIVE
SLEEP
APNEA
1021
Fig. 1.-Patient with obstructive sleep apnea. A-D, Sagittal ultrafast spoiled GRASS MR images (8.4/2.9) obtained during respiration (four images selected from 12 images obtained at same section location during respiration) show apparent occlusions of pharyngeal airway in regions of high oropharynx, mid oropharynx, low oropharynx (arrowbeads), and high hypopharynx (arrow) (D).
Evaluation
of Images
The following
eight
transverse
section
locations
obtained
through
the pharyngeal airway were evaluated, as previously described [9]: (1) nasopharynx, (2) hard palate, (3) soft palate, (4) high oropharynx, (5) mid oropharynx, (6) low oropharynx, (7) high hypopharynx, and (8) hyoid bone (1 2 transverse section locations were normally acquired in order to obtain section locations through these areas of interest,
and
the
section
locations
that
best
depicted
these
anatomic
locations were used for analysis) [18]. Criteria of abnormalities included (1) any occlusion of the airway seen during tidal breathing at any section location imaged and/or (2) airway cross-sectional areas less than those reported for control subjects studied by CT [4, 5, 8, 9, 1 1]. Determination of abnormal narrowing
of the airway
was based
on measurement
of the minimum obtained at a single the one with the minimal
cross-sectional
area of the airway (i.e. all images
section
were inspected
location
,
to determine
cross-sectional area, and measurement of cross-sectional area was performed on this image) [4, 5, 8, 9, 1 1 1 8]. As mentioned, the measurement of cross-sectional area was done by determining the area with a cursor and the software incorporated with the MR ,
scanner.
The accuracy
of this measurement
is ±10%.
Results Technically in each scan
acceptable plane and
results section
were obtained in all patients locations evaluated despite
the dental materials and devices present in nine of the 10 patients (i.e., only localized artifacts were produced by the presence of metallic dental objects, and these did not affect the imaging area of interest). In each of the patients with obstructive sleep apnea, occlusion (Fig. 2) and/or narrowing (Figs. 3 and 4) of the pharyngeal airways was seen during tidal breathing. The occlusion or narrowing of the pharyngeal airway usually was seen on only two or three of the 12 images (depending on the patient’s respiratory rate) obtained during tidal breathing. The site(s) of the occlusions and the site(s) and extent of the narrowings varied (Table 1). Six of the patients had occlusions present in one or more pharyngeal airway sites: (1) high oropharynx and mid oropharynx, (2) soft palate and high oropharynx, (3) soft palate and high oropharynx, (4) high oropharynx, (5) low oropharynx, and (6) nasopharynx and high oropharynx. Of these six patients, five also had abnormal narrowing of the cross-sectional areas of the pharyngeal airways at the following sites: (1) soft palate (0.37 cm2), (2) mid oropharynx (0.1 6 cm2), (3) soft palate (0.27 cm2), (4) soft palate (0.28 cm2), and (5) soft palate (0.54 cm2). The remaining four patients had one or more abnormal narrowings of the cross-sectional areas of the pharyngeal airways at the following sites: (1) high hypopharynx (0.32
1022
SHELLOCK
ET AL.
AJR:158,
May 1992
Fig. 2.-Patient with obstructive sleep apnea. A-D, Transverse ultrafast spoiled GRASS MR images (8.4/2.9) obtained during respiration (four images selected from 12 images obtained at same section location during respiration) show occlusion of pharyngeal airway at level of mid oropharynx (images are magnified to show detail of airway).
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Pharyngeal tongue
airway
was
occluded
by base
of
(A).
Fig. 3.-Patient with obstructive sleep apnea. A and B, Transverse ultrafast spoiled GRASS MR images (8.4/2.9) obtained during respiration (two images showing largest [A] and smallest [B] cross-sectional areas selected from 12 images obtained at same section location during respiration) show narrowing (arrow) of pharyngeal airway at level of soft palate. (Images are magnified to show detail of airway.)
cm2); (2) soft palate (0.79 cm2), high oropharynx and high hypopharynx (0.51 cm2); (3) soft palate high oropharynx (0.2 cm2), and mid oropharynx and (4) soft palate (0.21 cm2), high oropharynx and mid oropharynx (0.80 cm2).
(0.44 (0.12 (0.51 (0.86
cm2), cm2), cm2); cm2),
Discussion Using a variety of assessment techniques (e.g., convenCT, cine CT, acoustic-reflection), previous investigators established that patients with obstructive sleep apnea typitional
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AJA:158,
GRASS
May 1992
MR
IN OBSTRUCTIVE
SLEEP
APNEA
1023
Fig. 4.-Patient with obstructive sleep apnea. A and B, Transverse ultrafast spoiled GRASS MR images (8.4/2.9) obtained during respiration (two Images showing smallest IA] and largest [B] cross-sectional areas selected from 12 images obtained at same section location during respiretion) show severe vertical narrowing (A) of pharyngeal airway. (Images are magnified to show detail of airway.)
cally have abnormal changes in pharyngeal airway dimensions, namely, occlusions and narrowings, compared with the pharyngeal airways of the different control groups studied (e.g., age- and weight-matched subjects; snorers vs nonsnorers) [4-9, 1 1 1 9-21 ]. These abnormalities can be seen in awake patients with obstructive sleep apnea by using conventional CT [4, 5]. Occlusions and narrowings are most apparent during tidal breathing because of the dynamic alterations in the pharyngeal airway associated with changes in lung volume [8, 9, 1 1 1 3]. Therefore, rapid imaging techniques are crucial for a thorough and accurate assessment of the pharyngeal airways of patients with obstructive sleep apnea in order to detect morphologic abnormalities, which are often transient processes [8, 9, 1 1 1 8, 1 9, 21]. Otherwise, occlusions and narrowings of the pharyngeal airway may not be detected. In addition, rapid imaging techniques are espedaIly needed for assessing the pharyngeal airways of patients with tachypneic obstructive sleep apnea [8]. Although an occlusion of the pharyngeal airway is an Undeniably significant finding in the awake patient with obstructive sleep apnea, it is also important to determine if abnormal cross-sectional narrowing of the pharyngeal airway is present [4-i 2, 21 22]. An abnormally narrowed pharyngeal airway ,
,
,
,
observed in an awake patient with obstructive sleep apnea is thought to be a precursor to airway occlusion that may occur during sleep [9] and is an important contributing factor to the pathology of this disorder [6, 1 2]. This abnormal anatomic predisposition to occlusion of the pharyngeal airway is usually undetectable by clinical examination methods [5, 7]. In this study, we found abnormally narrowed pharyngeal airways in the patients with obstructive sleep apnea that were comparable in size to those reported in other studies in which cine CT and conventional CT were used [4, 5, 8, 9, 1 1]. The sites of occlusion and narrowings of the pharyngeal airways of patients with obstructive sleep apnea are variable; the oropharynx is the area most often affected [5, 7, 1 0]. In addition, multiple sites of occlusions and narrowings are common [8, 1 1 1 8-21], similar to the findings in the obstructive sleep apnea patients we studied. The actual sites and extent of the occlusions and narrowings are important to determine in order to understand the pathologic aspects of this sleep disorder [2, 10]. Detection and characterization of the sites of occlusion and narrowing of the pharyngeal airway are of particular clinical importance insofar as the planning of therapy, especially surgical intervention, is typically based on this information [1, 2, 21 22]. Multiple surgical procedures have been developed in an attempt to treat obstructive sleep apnea patients found to have associated structural abnormalities of the pharyngeal airways [1 2, 21-23]. These include uvulopalatopharyngoplasty, in which the uvula and a portion of the soft palate is removed, or tracheostomy, for patients with obstruction in the hypopharyngeal area. An ultrafast spoiled GRASS MR imaging study of the pharyngeal airway may be useful for evaluating the efficacy of the selected surgical treatment of patients with obstructive sleep apnea. The advantages of ultrafast spoiled GRASS MR imaging of the pharyngeal airway compared with cine CT include no exposure to ionizing radiation and fewer artifacts associated with metallic dental objects. Metallic dental objects can significantly obscure cine CT scans, making it difficult to interpret the findings at a particular level of the pharyngeal airway (which is usually the level of the soft palate or high oropharynx where many occlusions and narrowings tend to occur) [5, ,
,
TABLE 1: Transverse Sections Evaluated in Obstructive Apnea Patients During Dynamic Study of the Pharyngeal
Sleep
Airways
Location
Cross-Sectional Area (cm2)
of Section
Airway
Nasopharynx Hard palate Soft palate High oropharynx Mid oropharynx
Note-The
Mean
Range
1 .81 1 .03 0.34 0.37
0-3.79 0.36-2.38 0-0.79 0-1 .31
1 0 2 5
0-1 .39
1
0-4.1 2 0.32-4.51 0.49-4.60
1 0 0
0.84
Low oropharynx High hypopharynx Hyoid bone
a
minimum
No. of Pharyngeal
1 .66 1 .77 2.09
Occlusionsa
cross-sectional area in each subject was used. with occlusions had them at two sites.
Four of the six patients
,
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1024
SHELLOCK
1 1]. By comparison, on the ultrafast spoiled GRASS MR images, artifacts caused by metallic dental objects were localized to the immediate area of the objects and did not affect the evaluation of the dimensions of the pharyngeal airway. In addition, ultrafast spoiled GRASS MR imaging can be used to obtain a view of the pharyngeal airway in the sagittal plane, without reformatting, at an orientation that shows the entire motion of the airway, providing a different perspective of potential sites of occlusions or abnormal narrowings. Finally, the ultrafast spoiled GRASS pulse sequence is readily available on conventional MR imagers and does not require a specialized imaging device for accomplishing a dynamic study of the pharyngeal airway, such as that required for cine CT. The expense of using ultrafast spoiled GRASS MR imaging to examine the pharyngeal airway has yet to be established. However, the time required to accomplish this study makes it a relatively efficient MR procedure that should allow a high patient throughput. One potential limitation of our work is that we did not study the pharyngeal airways in a group of control subjects. Instead, we compared our measurements of cross-sectional area of the pharyngeal airways with previously reported values obtamed in patients with obstructive sleep apnea and in different control groups assessed by other imaging techniques [4, 5, 8, 9, 1 1 ]. Nevertheless, the cross-sectional areas measured for the abnormally narrowed pharyngeal airways of our obstructive sleep apnea patients were comparable to the smallest minimum areas reported for other patients [4, 5, 8, 9, 1 1]. Another possible limitation is that we did not compare the ultrafast spoiled GRASS MR imaging technique with cine CT. However, we did determine the relative accuracy of using the ultrafast MR technique to determine cross-sectional areas by conducting a phantom study that yielded acceptable resuIts. The primary intent of this study was to show that ultrafast spoiled GRASS MR imaging can be used for dynamic study of the pharyngeal airway in patients with obstructive sleep apnea in order to detect the presence of occlusions and significant narrowings so that the potential of this imaging procedure could be determined. We acknowledge that refinement of this imaging technique and additional studies of the pharyngeal airways of obstructive sleep apnea patients and control subjects are necessary. Because of the experimental design of this investigation, it is unknown whether dynamic study of the pharyngeal airway with ultrafast spoiled GRASS MR imaging is also useful for screening patients with suspected obstructive sleep apnea. However, this rapid imaging technique does appear to serve as a useful test that supplements the information currently obtained by physiologic testing of patients with obstructive sleep apnea.
ET AL.
AJR:158,
May 1992
REFERENCES 1 . Kales 2. 3.
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8. 9. 1 0. 1 1. 1 2. 1 3. 14.
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21
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A, Kales
JD.
Sleep
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1019
Occlusion and Narrowing of the Pharyngeal Airway in Obstructive Sleep Apnea: Evaluation by Ultrafast Spoiled
Frank
Morphologic
G. SheIlock13
Charles Fred
Julien1’2
be detected clinically
Steinberg2
Tom K. F. Foo4 Martin L. Hopp5 Philip R. Westbrook2
sition
sleep
the presence scans
state
sleep
and/or
airway
structural apnea MR
had
ultrafast
imaging
narrowings.
at the
rate
of one
techniques.
in patients airway
can
Ten patients
with
gradient-recalled
pharyngeal
Twelve
found
in the pharyngeal spoiled
of the
plane and at eight transverse obtained
are frequently
alterations
by using rapid imaging
(GRASS)
of occlusions were
These
patients
obstructive
steady
at one midsagittal The
of the pharyngeal
apnea.
in awake
proved in the
MR Imaging
abnormalities
with obstructive
J. Schatz1’2
Peter
GRASS
airway
sequential
images
acquito determine
were
obtained
planes through the pharyngeal
image
per
1.04
sec
while
the
airway.
patient
was
breathing quietly. Occlusions or narrowings of the pharyngeal airways were detected on MR images in all patients. The site(s) of the occlusions and the site(s) and extent of the narrowings varied. Six patients had occlusions and four had narrowings of one or more sites. This study shows that ultrafast spoiled GRASS MR imaging can be used to evaluate patients with obstructive sleep apnea during tidal breathing and is useful for determining the presence of occlusions and narrowings of the pharyngeal airway. 158:1019-1024,
AJR
Sleep apnea
May
1992
is a condition
characterized
by episodic
cessation
of breathing
during sleep [1 -3]. Total collapse and occlusion of the upper airway combined with respiratory efforts is a form of sleep apnea referred to as obstructive sleep apnea. Previous investigations [4-i 2] have shown that the pharyngeal airways are frequently occluded and the cross-sectional areas are significantly narrowed in sleeping and awake patients who have this disorder. These morphologic alterations have been studied objectively by various imaging techniques including plain film cephalometrics, fluoroscopy, conventional CT, and cine CT [2, 4, 6, 8, 9, i ii. Received November 6, 1991 ; accepted December 23, 1991.
after re-
1 Tower Magnetic Imaging, 90048. 2 Department of Radiology,
Los
,
Angeles,
Cedars-Sinai
CA Medi-
cal Center, 8700 Beverly Blvd., Los Angeles, CA 90048. Address reprint requests to F. G. Shellock, 1 2245 San Vicente Blvd., Los Angeles, CA 90049. Department of Radiological Sciences, University of California, Los Angeles, Medical Center, Los Angeles, CA 90024. 3
General WI 5320i.
Electric
Medical
Systems,
Because
the cross-sectional
9, 1 1 1 3], total
vision
Milwaukee,
occlusion
area of the upper airway varies with respiration
and significant
narrowing
(which
are frequently if the imaging
[8,
transient technique
processes) may be overlooked or not fully appreciated used to assess these abnormalities lacks sufficient temporal resolution to show the dynamic changes in the dimensions of the upper airway [8, 9, i 1 ]. Cine CT is particularly useful for detecting occlusion and narrowing of the pharyngeal airways of patients with obstructive sleep apnea because this technique in the size of the airway during respiration, even in tachypneic
can show changes patients [8, 9, 1 i].
Previously, MR imaging has not been used to study dynamic alterations of the pharyngeal airway because of the poor temporal resolution of this imaging tech-
les, CA 90048.
nique. However, the recent advent of rapid MR imaging techniques has provided a means of obtaining multiple images at multiple locations with sufficient image quality and temporal resolution to allow a dynamic evaluation of the pharyngeal airway [14].
0361 -803x/92/1 585-1019 © American Roentgen Ray Society
sition
Division of Otolaryngology, Surgery, Cedars-Sinai Medical
Head Center,
and Neck Los Ange-
This report describes in the steady
state
the application (GRASS)
of ultrafast
MR imaging
spoiled
gradient-recalled
for evaluation
acqui-
of the pharyngeal
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1020
SHELLOCK
ET
AL.
AJR:i58,
airway of awake patients with known obstructive sleep apnea in order to identify occlusion and narrowing during tidal breath-
proceeding
ing.
As the receiver phase is advanced in synchrony with the RF pulse, no additional postprocessing is required. The phase angle for optimal contrast between various anatomic structures varies with TA and tissue Ti and T2. In the study of the pharyngeal airway, the initial spoiling or phase angle was 109.9#{176}. A rapidly obtained image free from significant blurring or other
Subjects
and Methods
Subjects
The subjects included nine men (average age, 47 years; range, 40-53 years) and one woman (age, 34 years) with proved obstructive
sleep apnea as determined by strict clinical criteria, including a history of habitual snoring, restless sleep, morning headaches, daytime hypersomnolence, and intellectual deterioration [1-3]. Each subject had two or more of these signs and symptoms, and each had an overnight sleep study to determine the presence of unequivocal episodes of obstructive sleep apnea. Sleep studies were performed with
standardized
polysomnographic
techniques
that
included
contin-
uous monitoring of the electroencephalogram, electrooculogram, submental electromyogram, body position, body movement, ECG, oxygen saturation, oronasal air flow, sonogram, cross-sectional area
changes in the chest and abdominal wall(inductive
plethysmography),
and anterior tibial electromyogram [1 -3]. The patient was observed via closed-circuit television. For a diagnosis of obstructive sleep apnea, a cessation of air flow had to persist for a period of 20 sec or longer and occur at least 30 times during a 6-hr nocturnal sleep period, or a rate exceeding 10 episodes per hour. The mean apnea/ hypopnea index for these patients was 61 episodes per hour and ranged from 48 to 72 episodes per hour. The patients examined in this study were selected because of their severe apnea/hypopnea.
spoiling
to
May 1992
offset
increment
the
phase
distortion was reconstructed partial k-space reconstruction tion
[14-17].
higher
angle
for the nth RF pulse
This
resolution
such
that
receive-only,
wraparound
anterior
neck
local
of a 1 .5-T, 64-MHz Milwaukee, WI) and a
coil
coil (General
Electric
Medical Systems). This local coil was positioned over the nose, mouth, chin, and hyoid bone of the patient to optimize the signal-tonoise ratio of the images obtained of the pharyngeal airway. An ultrafast RF phase spoiled GRASS pulse sequence [1 4] was used to image the pharyngeal airway during tidal breathing, as follows (General Electric 4X Advantage hardware and software upgrades are required for the implementation of this pulse sequence): In the first series, transverse images (used as a localizer), 8.4/2.9/20#{176}(TA/TEl flip angle), were obtained with one excitation, 160 x 1 28 matrix, 20cm field of view, 5-mm section thickness, and approximate imaging time of 10 sec for 1 0 section locations. In the second series, sagittal images (midline slice obtained in reference to the axial plane localizer), 8.4/2.9/200, were obtained with one excitation, 1 60 x 1 28 matrix, 20-cm
field
of view,
5-mm
section
thickness,
and
acquisition
time
of
approximately 1 2 sec for 12 images at a single section location. In the third series, transverse images (section locations obtained from the nasopharynx to the hyoid referenced to the previously obtained sagittal
plane
image),
8.4/2.9/200,
were
obtained
with
one
allowed
a reduction
images
could
in the minimum
be recovered
TE and
from
receiver
filter
bandwidth
and
acquires
a partial
echo
[14].
A
image is obtained by spoiling the residual transverse magnetization of the steady-state free precession signal [14I 6]. In the pulse sequence used for this study, RF phase spoiling was used. This involved applying the RF pulses at varying phase offsets in the rotating frame, starting with an initial angle, 0, and more
Ti-weighted
TR,
reduced
as
partial-
using 67% of the echo), the minimum TE and TA were 2.9 and 8.4 msec, respectively. The very short TE used for this pulse sequence should minimize air
and
bone
susceptibility
artifacts
and
spurious
narrowings
of the
soft tissue-air interface. To assess the relative accuracy of the ultrafast spoiled GRASS pulse sequence for measuring cross-sectional areas, a phantom study was conducted. The phantom contamed cylinders of various sizes (cross-sectional areas ranging from 0.25 to 5.0 cmi), filled separately with either peanut oil, copper sulfate, or air. Cross-sectional areas were determined for these cylinders by using a cursor and the software incorporated with the MR scanner.
study
of
the
pharyngeal
airway
during
active
sequence
respiration
for were
acquired at the rate of one image per 1 .04 sec. This temporal resolution permitted 1 2 images to be obtained during tidal breathing of approximately two to four respiratory cycles. The patient was supine, with the head placed in a neutral position to ensure a consistent positioning technique for the study. Any narrowing of the pharyngeal airway seen with the head in a neutral position would be worsened by the slight flexion of the neck that normally
occurs
imaging,
the
with the typical
patient
was
instructed
the mouth
closed
and to refrain
acquisition
of the
images.
The
sleeping
posture
to breathe
[5, 1 3]. During
through
from
coughing
patient
was
the
nose
or swallowing
awake
during
MR with
during the
entire
procedure. Immediately after completion of each series, images were viewed as a cine-loop display and inspected to determine if the patient coughed or swallowed during the examination. If necessary, any images that were technically inadequate were redone. The average total examination time (including setting up equipment, positioning of the patient, and explaining the study) was approximately 17 mm.
Display
and
Evaluation
of Images
excitation,
160 x 128 matrix, 20-cm field of view, 7-mm section thickness, 2mm interslice gap, and approximate acquisition time of 2 mm 55 sec for 12 images obtained at 12 section locations. The ultrafast spoiled GRASS pulse sequence uses a ±32-kHz digital
or
echo data sets. For a 1 60 x 128 acquisition matrix (frequency samples x views), an image with an effective resolution of 256 x 128 was generated. If 256 frequency samples in a full echo were to be acquired, a minimum TE of 4.7 msec and a minimum TA of 9.0 msec could be achieved for an image with the other aforementioned imaging parameters. By using partial-echo acquisition with 160 frequency samples (i.e., by
the
MR imaging was performed with the body MR imager (General Electric Medical Systems,
phase
+ nO [14-17].
from a partial echo data set by using a algorithm based on homodyne detec-
The accuracy of this measurement was ±1 0%. Images obtained with this ultrafast spoiled GRASS
MR Imaging
the
...
was 0 + 20 +
The 12 images obtained sagittal
and
multilevel
at each section
transverse
plane
location
sections
were
for the midline viewed
as cine-
loop displays in order to optimally show the alterations of the airway dimensions associated with respiration. Although the sagittal images often showed potential sites of occlusion or narrowing of the pharyngeal airway (Fig. 1), they were considered to be potentially unreliable for showing morphologic abnormalities because of the possible presence of asymmetric narrowing of the airway (i.e. narrowing may have occurred off axis). Therefore, only transverse images were used for ,
the
assessment
of occlusion
and
narrowing.
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AJR:158,
GRASS
May 1992
MR
IN OBSTRUCTIVE
SLEEP
APNEA
1021
Fig. 1.-Patient with obstructive sleep apnea. A-D, Sagittal ultrafast spoiled GRASS MR images (8.4/2.9) obtained during respiration (four images selected from 12 images obtained at same section location during respiration) show apparent occlusions of pharyngeal airway in regions of high oropharynx, mid oropharynx, low oropharynx (arrowbeads), and high hypopharynx (arrow) (D).
Evaluation
of Images
The following
eight
transverse
section
locations
obtained
through
the pharyngeal airway were evaluated, as previously described [9]: (1) nasopharynx, (2) hard palate, (3) soft palate, (4) high oropharynx, (5) mid oropharynx, (6) low oropharynx, (7) high hypopharynx, and (8) hyoid bone (1 2 transverse section locations were normally acquired in order to obtain section locations through these areas of interest,
and
the
section
locations
that
best
depicted
these
anatomic
locations were used for analysis) [18]. Criteria of abnormalities included (1) any occlusion of the airway seen during tidal breathing at any section location imaged and/or (2) airway cross-sectional areas less than those reported for control subjects studied by CT [4, 5, 8, 9, 1 1]. Determination of abnormal narrowing
of the airway
was based
on measurement
of the minimum obtained at a single the one with the minimal
cross-sectional
area of the airway (i.e. all images
section
were inspected
location
,
to determine
cross-sectional area, and measurement of cross-sectional area was performed on this image) [4, 5, 8, 9, 1 1 1 8]. As mentioned, the measurement of cross-sectional area was done by determining the area with a cursor and the software incorporated with the MR ,
scanner.
The accuracy
of this measurement
is ±10%.
Results Technically in each scan
acceptable plane and
results section
were obtained in all patients locations evaluated despite
the dental materials and devices present in nine of the 10 patients (i.e., only localized artifacts were produced by the presence of metallic dental objects, and these did not affect the imaging area of interest). In each of the patients with obstructive sleep apnea, occlusion (Fig. 2) and/or narrowing (Figs. 3 and 4) of the pharyngeal airways was seen during tidal breathing. The occlusion or narrowing of the pharyngeal airway usually was seen on only two or three of the 12 images (depending on the patient’s respiratory rate) obtained during tidal breathing. The site(s) of the occlusions and the site(s) and extent of the narrowings varied (Table 1). Six of the patients had occlusions present in one or more pharyngeal airway sites: (1) high oropharynx and mid oropharynx, (2) soft palate and high oropharynx, (3) soft palate and high oropharynx, (4) high oropharynx, (5) low oropharynx, and (6) nasopharynx and high oropharynx. Of these six patients, five also had abnormal narrowing of the cross-sectional areas of the pharyngeal airways at the following sites: (1) soft palate (0.37 cm2), (2) mid oropharynx (0.1 6 cm2), (3) soft palate (0.27 cm2), (4) soft palate (0.28 cm2), and (5) soft palate (0.54 cm2). The remaining four patients had one or more abnormal narrowings of the cross-sectional areas of the pharyngeal airways at the following sites: (1) high hypopharynx (0.32
1022
SHELLOCK
ET AL.
AJR:158,
May 1992
Fig. 2.-Patient with obstructive sleep apnea. A-D, Transverse ultrafast spoiled GRASS MR images (8.4/2.9) obtained during respiration (four images selected from 12 images obtained at same section location during respiration) show occlusion of pharyngeal airway at level of mid oropharynx (images are magnified to show detail of airway).
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Pharyngeal tongue
airway
was
occluded
by base
of
(A).
Fig. 3.-Patient with obstructive sleep apnea. A and B, Transverse ultrafast spoiled GRASS MR images (8.4/2.9) obtained during respiration (two images showing largest [A] and smallest [B] cross-sectional areas selected from 12 images obtained at same section location during respiration) show narrowing (arrow) of pharyngeal airway at level of soft palate. (Images are magnified to show detail of airway.)
cm2); (2) soft palate (0.79 cm2), high oropharynx and high hypopharynx (0.51 cm2); (3) soft palate high oropharynx (0.2 cm2), and mid oropharynx and (4) soft palate (0.21 cm2), high oropharynx and mid oropharynx (0.80 cm2).
(0.44 (0.12 (0.51 (0.86
cm2), cm2), cm2); cm2),
Discussion Using a variety of assessment techniques (e.g., convenCT, cine CT, acoustic-reflection), previous investigators established that patients with obstructive sleep apnea typitional
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AJA:158,
GRASS
May 1992
MR
IN OBSTRUCTIVE
SLEEP
APNEA
1023
Fig. 4.-Patient with obstructive sleep apnea. A and B, Transverse ultrafast spoiled GRASS MR images (8.4/2.9) obtained during respiration (two Images showing smallest IA] and largest [B] cross-sectional areas selected from 12 images obtained at same section location during respiretion) show severe vertical narrowing (A) of pharyngeal airway. (Images are magnified to show detail of airway.)
cally have abnormal changes in pharyngeal airway dimensions, namely, occlusions and narrowings, compared with the pharyngeal airways of the different control groups studied (e.g., age- and weight-matched subjects; snorers vs nonsnorers) [4-9, 1 1 1 9-21 ]. These abnormalities can be seen in awake patients with obstructive sleep apnea by using conventional CT [4, 5]. Occlusions and narrowings are most apparent during tidal breathing because of the dynamic alterations in the pharyngeal airway associated with changes in lung volume [8, 9, 1 1 1 3]. Therefore, rapid imaging techniques are crucial for a thorough and accurate assessment of the pharyngeal airways of patients with obstructive sleep apnea in order to detect morphologic abnormalities, which are often transient processes [8, 9, 1 1 1 8, 1 9, 21]. Otherwise, occlusions and narrowings of the pharyngeal airway may not be detected. In addition, rapid imaging techniques are espedaIly needed for assessing the pharyngeal airways of patients with tachypneic obstructive sleep apnea [8]. Although an occlusion of the pharyngeal airway is an Undeniably significant finding in the awake patient with obstructive sleep apnea, it is also important to determine if abnormal cross-sectional narrowing of the pharyngeal airway is present [4-i 2, 21 22]. An abnormally narrowed pharyngeal airway ,
,
,
,
observed in an awake patient with obstructive sleep apnea is thought to be a precursor to airway occlusion that may occur during sleep [9] and is an important contributing factor to the pathology of this disorder [6, 1 2]. This abnormal anatomic predisposition to occlusion of the pharyngeal airway is usually undetectable by clinical examination methods [5, 7]. In this study, we found abnormally narrowed pharyngeal airways in the patients with obstructive sleep apnea that were comparable in size to those reported in other studies in which cine CT and conventional CT were used [4, 5, 8, 9, 1 1]. The sites of occlusion and narrowings of the pharyngeal airways of patients with obstructive sleep apnea are variable; the oropharynx is the area most often affected [5, 7, 1 0]. In addition, multiple sites of occlusions and narrowings are common [8, 1 1 1 8-21], similar to the findings in the obstructive sleep apnea patients we studied. The actual sites and extent of the occlusions and narrowings are important to determine in order to understand the pathologic aspects of this sleep disorder [2, 10]. Detection and characterization of the sites of occlusion and narrowing of the pharyngeal airway are of particular clinical importance insofar as the planning of therapy, especially surgical intervention, is typically based on this information [1, 2, 21 22]. Multiple surgical procedures have been developed in an attempt to treat obstructive sleep apnea patients found to have associated structural abnormalities of the pharyngeal airways [1 2, 21-23]. These include uvulopalatopharyngoplasty, in which the uvula and a portion of the soft palate is removed, or tracheostomy, for patients with obstruction in the hypopharyngeal area. An ultrafast spoiled GRASS MR imaging study of the pharyngeal airway may be useful for evaluating the efficacy of the selected surgical treatment of patients with obstructive sleep apnea. The advantages of ultrafast spoiled GRASS MR imaging of the pharyngeal airway compared with cine CT include no exposure to ionizing radiation and fewer artifacts associated with metallic dental objects. Metallic dental objects can significantly obscure cine CT scans, making it difficult to interpret the findings at a particular level of the pharyngeal airway (which is usually the level of the soft palate or high oropharynx where many occlusions and narrowings tend to occur) [5, ,
,
TABLE 1: Transverse Sections Evaluated in Obstructive Apnea Patients During Dynamic Study of the Pharyngeal
Sleep
Airways
Location
Cross-Sectional Area (cm2)
of Section
Airway
Nasopharynx Hard palate Soft palate High oropharynx Mid oropharynx
Note-The
Mean
Range
1 .81 1 .03 0.34 0.37
0-3.79 0.36-2.38 0-0.79 0-1 .31
1 0 2 5
0-1 .39
1
0-4.1 2 0.32-4.51 0.49-4.60
1 0 0
0.84
Low oropharynx High hypopharynx Hyoid bone
a
minimum
No. of Pharyngeal
1 .66 1 .77 2.09
Occlusionsa
cross-sectional area in each subject was used. with occlusions had them at two sites.
Four of the six patients
,
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1024
SHELLOCK
1 1]. By comparison, on the ultrafast spoiled GRASS MR images, artifacts caused by metallic dental objects were localized to the immediate area of the objects and did not affect the evaluation of the dimensions of the pharyngeal airway. In addition, ultrafast spoiled GRASS MR imaging can be used to obtain a view of the pharyngeal airway in the sagittal plane, without reformatting, at an orientation that shows the entire motion of the airway, providing a different perspective of potential sites of occlusions or abnormal narrowings. Finally, the ultrafast spoiled GRASS pulse sequence is readily available on conventional MR imagers and does not require a specialized imaging device for accomplishing a dynamic study of the pharyngeal airway, such as that required for cine CT. The expense of using ultrafast spoiled GRASS MR imaging to examine the pharyngeal airway has yet to be established. However, the time required to accomplish this study makes it a relatively efficient MR procedure that should allow a high patient throughput. One potential limitation of our work is that we did not study the pharyngeal airways in a group of control subjects. Instead, we compared our measurements of cross-sectional area of the pharyngeal airways with previously reported values obtamed in patients with obstructive sleep apnea and in different control groups assessed by other imaging techniques [4, 5, 8, 9, 1 1 ]. Nevertheless, the cross-sectional areas measured for the abnormally narrowed pharyngeal airways of our obstructive sleep apnea patients were comparable to the smallest minimum areas reported for other patients [4, 5, 8, 9, 1 1]. Another possible limitation is that we did not compare the ultrafast spoiled GRASS MR imaging technique with cine CT. However, we did determine the relative accuracy of using the ultrafast MR technique to determine cross-sectional areas by conducting a phantom study that yielded acceptable resuIts. The primary intent of this study was to show that ultrafast spoiled GRASS MR imaging can be used for dynamic study of the pharyngeal airway in patients with obstructive sleep apnea in order to detect the presence of occlusions and significant narrowings so that the potential of this imaging procedure could be determined. We acknowledge that refinement of this imaging technique and additional studies of the pharyngeal airways of obstructive sleep apnea patients and control subjects are necessary. Because of the experimental design of this investigation, it is unknown whether dynamic study of the pharyngeal airway with ultrafast spoiled GRASS MR imaging is also useful for screening patients with suspected obstructive sleep apnea. However, this rapid imaging technique does appear to serve as a useful test that supplements the information currently obtained by physiologic testing of patients with obstructive sleep apnea.
ET AL.
AJR:158,
May 1992
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