Tongue Base Ultrasound: A Diagnostic Tool For Predicting Obstructive Sleep Apnea

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Annals of Otology, Rhinology & Laryngology 118(3):179-184.

© 2009 Annals Publishing Company. All rights reserved.

Tongue Base Ultrasound: A Diagnostic Tool for Predicting


Obstructive Sleep Apnea
Yonatan Lahav, MD; Eyal Rosenzweig, MD, PhD; Zehava Heyman, MD;
Julia Doljansky, MA; Amit Green, MA; Yaron Dagan, MD, DSc

Objectives: We assessed the value of an ultrasound (US) examination in the diagnostic workup of patients with sleep-
related breathing disorders by correlating US measurements with known parameters for the presence and severity of ob-
structive sleep apnea.
Methods: Forty-one male patients who complained of snoring and/or daytime somnolence participated. The diagnos-
tic protocol included history-taking, physical examination, polysomnography, and transcervical US examination of the
tongue. The US results were compared with all of the other parameters.
Results: The US imaging was reliable for demonstrating anatomic structures of the tongue base, discriminating between
muscle, mucosa, and blood vessels. The lingual arteries were clearly visualized entering the tongue base at its lower lat-
eral borders. There was a significant relationship between the severity of sleep-related breathing disorders (measured by
polysomnography) and the width of the lower tongue base (measured as the distance between the lingual arteries). The
distance between the lingual arteries also correlated with physical examination findings and patient complaints of day-
time somnolence and the sensation of choking during the night.
Conclusions: Tongue base width, measured by US, may influence the severity of obstructive sleep apnea. This is the first
demonstration of the possible role of US examination, an inexpensive, noninvasive, and non-irradiating office procedure,
in the diagnostic workup for sleep-related breathing disorders.
Key Words: obstruction, sleep apnea, tongue, ultrasound.

Introduction hand and speech production on the other.3 The evo-


Obstructive sleep apnea (OSA) is a prevalent dis- lutionary changes in the shape and location of the
order among adults (4% to 8%). It is well known tongue that enabled speech and language develop-
to decrease the individual’s quality of life and in- ment were also responsible for the development of
crease the risk for hypertension, ischemic heart dis- OSA. The shortening of the nose and jaws and the
ease, vascular diseases, cerebrovascular accidents, change in the cranial base angle caused the descent
brain damage, and general deterioration of cognitive of the tongue base into the pharynx and a consid-
function. It also increases the likelihood of traffic erable narrowing of the pharyngeal airway. These
accidents.1 The major anatomic site in which air- changes significantly increase the likelihood of air-
way obstruction occurs is the pharynx, being the way obstruction during sleep.4
only segment of the upper airway that is not bound- Polysomnography is the gold standard for diag-
ed by bony structures. Obstruction can occur sepa- nosing OSA. The Apnea-Hypopnea Index (AHI),
rately or simultaneously in any part of the pharynx, which is the sum of obstructive events (apneas and
from concentric narrowing of the soft palate, to me- hypopneas) divided by total hours of sleep, is the
dian attachment of the tonsils or lateral pharyngeal core polysomnographic output. It is used to diag-
walls, to prolapse of the tongue base upon the la- nose normal and/or primary snoring (AHI of 0 to
ryngeal aperture.2 The tongue is a unique organ that 5) and mild, moderate, and severe OSA, with AHI
possesses multiple muscle groups intermixed with ranges of 6 to 15, 16 to 30, and 31 or more, respec-
each other, enabling exact and rapid movements in tively. Several imaging modalities have been offered
almost any direction. The rich neuromuscular sup- for the estimation of risk, severity, and treatment op-
ply enables chewing and swallowing on the one tions of OSA.5 Cephalometry enables measurements
From the Department of Otolaryngology, Kaplan Medical Center, Rehovot, affiliated with Hebrew University (Jerusalem) (Lahav); the
Institute for Fatigue and Sleep Medicine (Rosenzweig, Doljansky) and the Division of Diagnostic and Interventional Imaging, Ultra-
sound Unit (Heyman), Sheba Medical Center, Tel Hashomer, affiliated with Tel Aviv University (Tel Aviv), the Department of Medical
Education, Tel Aviv University, Tel Aviv (Dagan); and the Institute for Sleep Medicine, Assuta Medical Center, Petach Tikva (Green,
Dagan); Israel.
Correspondence: Yonatan Lahav, MD, Kaplan Medical Center, PO Box 1, Rehovot, Israel.

179
180 Lahav et al, Tongue Ultrasound for Obstructive Sleep Apnea 180

of the dimensions of soft and bony structures and ported by spouse, daytime somnolence, mouth dry-
the angles of the upper airway. It is, however, lim- ness, and subjective sensation of nasal obstruction.
ited to a lateral reflection and cannot help in assess- All parameters were graded on a scale from 0 to
ing the lateral walls or the tongue base width. Com- 3 (none, mild, moderate, and severe). Additional-
puted tomography (CT) gives a more accurate view ly, every patient completed an Epworth Sleepiness
in axial, coronal, and sagittal sections, but it expos- Scale questionnaire in order to quantify the risk for
es the patient to irradiation and cannot discriminate daytime sleepiness.7
well between adjacent soft tissues. In addition, the
Physical Examination. The pharyngeal airway
CT image of the pharynx is often distorted by den-
was evaluated with direct inspection of the orophar-
tal material artifacts. Magnetic resonance imaging
ynx, considering tongue size, the tongue’s relative
(MRI) is excellent in discriminating between soft
hiding of the free edge of the soft palate, and ton-
tissue components in all dimensions, but it is usu-
sil size. Friedman’s stage8 was calculated to esti-
ally not available in ordinary clinical practice be-
mate the relative risk for OSA and the major site
cause of its high cost. Fluorography can show real-
of obstruction. A flexible endoscopic examination
time narrowing of the airway during sleep, but it,
was then performed in order to estimate the degree
too, exposes the patient to irradiation, and the ana­
of narrowing in the retropalatal and retrolingual re-
tomic correlation of the image is suboptimal. Ultra-
gions. Specifically, the contribution of the tonsils,
sonography (US) differs from all other modalities in
the position and size of the tongue base, and the
some important respects. It is a dynamic examina-
influence of the tongue base on epiglottis position
tion modality in which the operator decides when
were documented. The Muller maneuver9 was then
and where to freeze the image. It can show soft tis-
performed. The pharynx and larynx were inspect-
sue accurately, especially blood vessels, by use of
ed with the endoscope, and the patient was asked
the Doppler effect mode. It is not expensive relative
to inspire air while the examiner lightly pushed the
to other imaging techniques, and it is not associated
alae nasi medially in order to increase airway resis-
with risks such as exposure to irradiation or a mag-
tance. The negative pressure created by the maneu-
netic field. However, not all of the anatomic areas of
ver caused narrowing in the segment most suscep-
the pharynx can be imaged with US, because of the
tible to collapse during apnea. Finally, the anatomic
acoustic shadows caused by the jaws. The tongue is
level of obstruction was determined based on all the
an ideal organ for US evaluation, especially its base,
findings. Each patient was classified into 1 of 5 lev-
as this area can be imaged directly by applying the
els: 1) retropalatal obstruction only, 2) mostly retro-
transducer on the examinee’s submental skin. Our
palatal obstruction, 3) equal obstruction along the
literature search failed to find any prior investiga-
pharyngeal airway, 4) mostly retrolingual obstruc-
tions on the possible quantitative relationship be-
tion, and 5) retrolingual obstruction only. The nasal
tween US measurements of the tongue base and the
airway was assessed for septal deviation, turbinate
risk for OSA. We hypothesized that there would be a
hypertrophy, adenoids, and polyps. Body mass in-
significant association between US tongue base di-
dex (BMI) was calculated, as well.
mensions and the polysomnographic, patient histo-
ry, and physical examination findings. Polysomnography. The examination channels in-
cluded electroencephalography, electro-oculogra-
Materials and Methods phy, elec­tromyography, electrocardiography, a snor-
Population. The study group was derived from a ing microphone, a flowmeter, chest and abdominal
list of patients who underwent polysomnography in belts for respiratory effort and body position moni-
the Institute for Fatigue and Sleep Medicine, Sheba toring, the oxygen saturation level, and heart rate.
Medical Center, Tel Hashomer, Israel, during 2005. The equipment and analyzing software in the sleep
Only men were included, in order to avoid gender- laboratory were by Embla — the Somnologica 3.2
related anatomic craniofacial variation as described (Embla, Denver, Colorado). The AHI was the crite-
in cephalometric studies.6 Adult male patients with rion for categorization of patients as having primary
a broad sleep disturbance severity range (ie, primary snoring (5 or less) or mild (6 to 15), moderate (16 to
snoring or mild, moderate, or severe OSA) were in- 30), or severe (31 or more) OSA.
vited to participate in the study, of whom 41 agreed Ultrasound Examination. The device used was
to take part. All of them underwent a diagnostic the Acuson Super Sequoia 512 (Siemens Medical
workup that included history-taking and physical Solutions, Malvern, Pennsylvania) with a convex
examination before the US examination. transducer in the frequencies 4 and 6 MHz. With the
Questionnaire. The patients were asked about patient in a seated position, the transducer was in-
snoring intensity, sensation of apnea or apnea re- troduced to the skin of the neck in the submental re-
181 Lahav et al, Tongue Ultrasound for Obstructive Sleep Apnea 181

A B

C D

Fig 1. Ultrasound images. A) Lingual arteries are seen with Doppler mode (dotted circles) on both sides of lower
lateral borders of tongue base. Also seen are mucosal covering of tongue (1) and genioglossus (2), geniohyoid (3),
and mylohyoid (4) muscles. B) Areas 1-4 in A. Also seen are two acoustic shadows, reflecting body of mandible
(5) and hyoid bone (6). C) Distance between lingual arteries (DLA) as they enter tongue base inferiorly (1), maxi-
mal width of tongue base (2), and tongue base height (3). D) Maximal height of mid-tongue (4), height in area of
hyoid bone (5), and geniohyoid distance (6).

gion coronally, immediately cephalad to the body of measures and quantitative parameters, such as the
the hyoid bone, and midsagittally, ie, in the area be- AHI, was calculated with Pearson’s test. Linear cor-
tween the hyoid bone and the symphysis of the man- relation with qualitative variables, such as sleepi-
dible. The examinees were instructed to remain still ness level or level of obstruction, was calculated
and silent and to avoid tongue movements, swallow- with Spearman’s rho. The relationships between the
ing, or talking. All examinations were conducted by BMI, the AHI, and the US measurements were ana-
trained US technicians under the supervision of the lyzed by partial correlation coefficient. A regression
first author. model was established for the prediction of the exis-
tence and the severity of OSA as determined by US
Study Approval. The study was approved by the
measurements.
ethics (Helsinki) committee of Sheba Medical Cen-
ter, Tel Hashomer, Israel. Results
Statistics. The dependent variables were the di- A total of 41 men (age range, 20 to 71 years; av-
mensions of the tongue base as measured by US. erage, 49 years) who were evaluated for sleep dis-
The independent variables were obtained from poly- turbance at the sleep institute of the Sheba Medical
somnography (AHI), the questionnaire, and physi- Center were included in the study. The US images of
cal examination. The linear correlation between US the tongue gave a satisfactory resolution of the soft
182 Lahav et al, Tongue Ultrasound for Obstructive Sleep Apnea 182

Table 1. ultrasound measurements of tongue measurements and age, history of snoring, nasal ob-
Reference Average struction, mouth dryness, or score on the Epworth
  Figure Parameter ± SD (mm) Sleepiness Scale. A linear regression model yielded
Figure 1C Distance between lingual arteries 31 ± 5.1 a correlation of 0.557 between the DLA and the AHI
Maximal width of tongue base 48 ± 7.3 (p < 0.001). The DLA had a higher correlation with
Tongue base height 36 ± 6.4 the AHI than did the other variables in this study
Figure 1D Maximal height of mid-tongue 45 ± 4.1 population, and it explained 31% percent of the AHI
Tongue height in area of hyoid bone 19 ± 5.7 variability (Fig 2).
Geniohyoid distance 52 ± 5.4
Further analysis of the data using a 2 × 2 frequen-
tissues of the tongue such as muscles, connective cy table revealed that distances of 30 mm between
tissue, mucosa, and blood vessels. The lingual arter- the lingual arteries can be considered as a point
ies were visualized in the Doppler mode as they en- above which patients have a higher risk for moder-
tered the tongue base in a coronal section (Fig 1A). ate to severe OSA (AHI of more than 15) and below
The anatomic details of nearly all of the tongue were which they have a greater likelihood of having mild
seen in the sagittal section, except for the most ante- or no OSA (AHI of 15 or less; Table 3). Eighteen
rior part, which was hidden by the acoustic shadow patients (43.9%) had a DLA of 30 mm or less, and
caused by the body of the mandible (Fig 1B). Six 23 (56.1%) had a DLA of more than 30 mm. There
longitudinal and transverse measurements were per- was no difference in variability within the 2 groups
formed and reviewed in the current study. They are (Levene’s test for equality of variances). The aver-
illustrated in Fig 1C,D, and Table 1 summarizes the age AHI in the group with a DLA of more than 30
numerical results. The distance between the lingual mm was 36, and the average AHI in the group with
arteries (DLA) was the single measurement that was a DLA of 30 mm or less was 13 (p = 0.003, indepen-
shown to be strongly correlated to the studied vari- dent sample t-test). When the DLA was more than
ables (Table 2). The other US measurements failed 30 mm, the relative risk for moderate to severe OSA
to demonstrate any similarly significant relationship. was 2.78 to 1. The sensitivity and specificity of this
Additionally, no correlation was found between US indicator were found to be 80% and 67%, respec-
Table 2. Summary of parameters correlated with DLA
No. of Average
Patients DLA
Finding (n = 41) (mm) p
Daytime somnolence 0.044
None 7 30
Mild 4 26
Moderate 16 31
Severe 14 34
Sensation of apnea 0.011
None 17 29
Mild 7 30
Moderate 9 34
Severe 8 32
Site of obstruction 0.002
Retropalatal only 6 29
Mostly retropalatal 15 29
Both retropalatal and retrolingual 9 33
Mostly retrolingual 9 34
Retrolingual only 2 37
Apnea-Hypopnea Index <0.001
Normal and/or primary snoring (0-5) 11 27
Mild OSA (6-15) 10 31
Moderate OSA (16-30) 4 32
Severe OSA (≥31) 16 34
DLA — distance between lingual arteries; OSA — obstructive sleep apnea.
183 Lahav et al, Tongue Ultrasound for Obstructive Sleep Apnea 183

Table 3. 2 × 2 frequency table for AHI above


and below 15 episodes per hour versus DLA
above and below 30 millimeters
AHI ≤15 AHI >15
DLA ≤30 mm 14   4 18
DLA >30 mm   7 16 23
21 20 41
AHI — Apnea-Hypopnea Index.

ies in support of our hypothesis that US can be uti-


lized in the evaluation and treatment of patients
with OSA. Siegel et al11 performed simultaneous
US examination of the pharynx synchronized with
polysomnography in 5 patients during sleep. Dur-
Fig 2. Linear regression line of distance between lingual ing the episodes of apnea that were documented by
arteries (DLA) against Apnea-Hypopnea Index (AHI).
the sleep study, transcervical US demonstrated re-
tively. laxation of the muscles of the floor of the mouth
and a dropping back of the tongue base. Robinson
A high BMI is a known risk factor for OSA. One et al12 performed transcervical US-guided radiofre-
of the generally accepted reasons is diffuse enlarge- quency reduction of the tongue base in 15 patients.
ment of the tongue. The average BMI in our study The US image enabled them to direct the radiofre-
group was 28 (range, 23 to 41). Partial correlation quency probe into the tongue base musculature at
coefficients were calculated while controlling for a safe distance from the neurovascular bundles, ie,
BMI in order to check whether the correlation be- the hypoglossal nerves and the lingual arteries. Blu-
tween the DLA and the AHI had been influenced by men et al13 also performed the same procedure in 10
the BMI; it remained significant (p < 0.05). Further- more patients. Maturo and Mair14 carried out cobla-
more, the lack of a correlation between the BMI and tion reduction of the tongue mass in patients with
the AHI in this study (p = 0.094) made the DLA a macroglossia by a transoral approach, guided by US
more significant factor than the BMI in predicting to avoid damage to the lingual arteries. These stud-
the presence and severity of OSA in this group of ies reflect the increasing awareness of physicians of
patients. the unique contribution of US imaging of the tongue
Discussion in patients with OSA.
This study revealed a significant relationship be- One limitation of the current study is that all of
tween US measurements of the tongue base and pa- the patients had already presented with some lev-
tient complaints, physical findings, and OSA severi- el of sleep disturbance. In order to further validate
ty measured by polysomnography. The absolute size our results, US examination should be carried out
of the tongue base, and not its dimensions relative on a randomly selected group. A control group of
to other structures in the pharynx, may play a ma- subjects free of any sleep disturbance will enable a
jor role in the pathogenesis of OSA, as the risk for calculation of specificity and sensitivity that reflects
moderate to severe OSA rises significantly when the the actual power of this examination in the general
DLA exceeds 30 mm. population.

The range of DLA measurements was comparable Conclusions


to the findings in the anatomic study of Lauretano et
al.10 They dissected the pharynges of 10 fresh ca- This study demonstrated the possible contribution
davers and calculated the distance between the mid- of US examination to the diagnostic evaluation of
line of the tongue and the lingual artery in the area patients with OSA. The width of the lower tongue
it enters the tongue base. The precise distance was base, measured as the DLA, was found to be associ-
16.6 mm on average, ranging from 12 to 21 mm. ated with the existence of and severity of OSA. Our
Since the tongue is a symmetric organ, the product results highlighted the principal role of the absolute
of this distance would be equivalent to the DLA. In size of the tongue base as an important factor af-
our study, the DLA was 31 mm on average, ranging fecting the severity of sleep disturbance. More stud-
from 22 to 42 mm — values almost identical to the ies are warranted to optimize the ability of this tool
results of their anatomic study. to predict and diagnose OSA. Ultrasonography of
the tongue base may emerge as a screening tool for
Our review of the literature yielded several stud- practicing physicians in the clinical setting.
184 Lahav et al, Tongue Ultrasound for Obstructive Sleep Apnea 184

Acknowledgment: We thank Esther Eshkol for editorial assistance.

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