The relationship between neck circumference, ... pharyngeal anatomy, and the obstructive ...

Eur Respir J
1990, 3, 509--514
The relationship between neck circumference, radiographic
pharyngeal anatomy, and the obstructive sleep apneoa
syndrome
R.J.O. Davies, J.R. Stradling
The relationship between neck circumference, radiographic pharyngeal
anatomy, and the obstructive sleep apneoa syndrome. RJ.O. Davies, JR.
Stradling.
ABSTRACT: We have st udied the predictive Importance of neck
circumference, obesity, and several radiographic pharyngeal dimensions
for obstructive sleep apnoea (OSA), In 66 patients. OSA was quantified
as the mean hourly number of >4% dips in arterial oxygen saturation
during sleep. Neck circumference (correlation coefficient (r)=0.63, 95%
confidence Interval (C.I.) 0.4~.76), obesity Index (r=0.54, 95% C.I.
0.39~.69), hyoid position (r=0.40, 95% C.I. 0.17-0.59), soft palate length
(r=0.31, 95% C.I. 0.08-0.51), and hard palate-to-spine angle (r=0.29, 95%
C.I. 0.0~.49), correlated significantly with saturation dips in single
regression analysis. In stepwlse multiple linear regression analysis (saturation dip rate as the dependant variable), only neck size and rctroglossai
space were significant independent correlates (total r 2 =0.42, 95% C.I.
0.22-0.61, p<O.OOOl). We conclude that the relationships between general
obesity, hyoid position, soft palate length, and OSA are probably secondary to variation in neck circumference.
Eur Respir ]., 1990, 3, 509-514.
In man, general obesity has been thought the single
most important risk factor for obstructive sleep apnoea
(OSA) [1). However, OSA patients also have anatomical
cranial and pharyngeal abnormalities. Among these are
bony features such as an elongated lower face [2], and
an acute cranial base flexion [3]; as well as soft tissue
changes which include a narrow retroglossal airway [4-7),
a low set hyoid bone [3, 5-7], and a long sofl palate [2,
3, 5, 8]. Mass loading of the upper airway to simulate
obesity reduces the calibre of the oropharynx, leading to
airway obstruction in an animal model [9], and OSA
patients have more fat deposited around the collapsing
pharyngeal segment than do weight matched controls [10).
In this study we have assessed the predictive value of
neck obesity (assessed by measuring neck circumference),
general obesity, and radiographic pharyngeal dimensions
for OSA in a sleep clinic population. To test the
hypothesis that small changes in head flexion during
pharyngeal radiography can produce large variations in
some of the pharyngeal dimensions mentioned above,
we imaged a group of normals in varying head postures.
The Sleep Clinic, Osier Chest Unit, Churchill
Hospilal, Headington, Oxford OX3 7U, UK.
Correspondence: Dr R.J.O. Davies, The Sleep Clinic,
Osier Chest Unit, Churchill Hospital, Headington,
Oxford OX3 7U, UK.
Keywords: Neck; obesity; obstructive sleep apnoea
syndrome; pharynx; radiology.
Received: September 30, 1989; accepted January 26,
1990.
disorders (snoring, sleepiness, and possible OSA). Each
underwent clinical examination, lateral pharyngeal
radiography, and an eight hour overnight sleep study.
The presence of OSA (quantified as the number of >4%
arterial oxygen saturation dips per hour of sleep) was
then correlated with radiographic pharyngeal
measurements, obesity, and neck size.
Clinical examination
All subjects underwent full general medical
examination including measurement of neck circumference at the level of the cricothyroid membrane, height,
and weight. Obesity was expressed as the index
weight·heighr2 [11]. To compensate for the increase in
neck circumference with height in the normal
population, patient measurements were corrected using a
relationship established in 350 normals by this
department (correlation coefficient (r)==0.18, 95 %
confidence interval (C.I.) 0.08-0.28, p<0.02). The results
were expressed as a percentage of the predicted normal
neck circumference (PPNC) where;
Methods
IOO·neck circumference mm
The study population consisted of 66 patients (52 male,
14 female) referred for the investigation of sleep
PPNC
(0.55·height cm)+ 310
R.J.O. DAVIES, J.R. STRADLING
510
Lateral pharyngeal radiograph
Sleep studies
Each patient underwent lateral pharyngeal radiography
using a variant of the technique described by BEAN et al.
[12]. Subjects stood in a lateral position with the radiograph plate situated at the lateral tip of the acromion
process. The X-ray source to radiograph plate distance
was kept constant at six feet. Subjects were asked not to
chew or swallow, and to occlude the teeth. The head
was held in a comfortable position and a single radiograph taken. One investigator, (RJD), acting blind of the
sleep study findings, measured the following dimensions
directly from each radiograph (fig. 1).
To establish the presence or absence of OSA all 66
patients underwent either full polysomnography (61
cases), or overnight pulse oximetry (BIOX 3700) with
sound and continuous video recording (5 cases). Of the
five subjects studied by video and oximetry alone, none
suffered more than one >4% arterial saturation dip per
hour of sleep. Full polysomnography included recordings of electroencephalogram, electromyogram (EMG),
electroocculogram, pulse oximetry, oro-nasal airflow,
ribcage and abdominal movement.
For statistical analysis OSA was quantified as the
number of >4% dips in arterial oxygen saturation per
hour of sleep (>4% Sao2 dip rate). This is an established
close correlate of the severity of OSA assessed in other
ways [13-15]. Other causes of nocturnal arterial
desaturation, such as hypoxic lung disease, were
excluded by clinical examination and sleep study.
V
Variation of pharyngeal dimensions with head position
in normal subjects
D
D
\'--
Fig. 1. - Tracing of the lateral pharyngeal radiograph of a study
patienL PNS: posterior nasal spine; P: tip of soft palate; HP: line
subtended from hard palate; CS: line subtended from anterior border of
spinal canal at the level of the 2nd and 3rd cervical vertebrae; RS:
retroglossal space; MP: mandibular plane; H: anterior superior point of
hyoid bone.
1) Soft palate length, PNS-P. Posterior tip of the hard
palate to the end of the soft palate.
2) Mandibular plane to hyoid distance, MP-H. The distance from a line parallel to the inferior border of the
mandibular ramus to the most anterior superior point of
the hyoid bone.
3) Retroglossal space at its narrowest point, RS. Defined
anteriorly by the root of the tongue, and posteriorly by
the pharyngeal mucosa.
Head flexion at the time of film exposure was assessed
by measurement of the internal angle between a line
subtending from the hard palate and a line subtending
from the anterior border of the spinal canal at the level
of the second and third cervical vertebrae, HP-CS.
Where any radiographic landmark was insufficiently
well defined to allow accurate measurement, that index
was omitted, and the subject excluded from the multiple
linear regression analysis (7 cases). All the data were
used for the single regression analysis.
To establish the variation of pharyngeal dimensions
with head posture, six normal volunteers underwent
radiography in positions ranging from full head
extension to full flexion, and from full head retraction
to full protraction. In all subjects the range of angle HPCS was at least 85-120°. To minimise the X-ray dose
required these radiographs were taken using fluoroscopic
technique and 100 mm radiograph film (Phillips
Electronics, Diagnost 64, and A.N.C. 6). The images
produced were exactly half the size of the standard
radiographs and a scaling factor of 2 was used to
generate comparable data. PNS-P, MP-H, RS, and
HP-CS, were measured from each image, and HP-CS
was then correlated with the other variables.
80
.:c
•
70
il
,
.e-60
c
••
0
~50
•
•
•
••
•
•
• • •• •
•
~
'
:1
: 40
i
i:
~ 30
•
c
•
••
••
'/.
120
10
•
0
70
80
0
• •
90
100
110
120
130
140
%Predicted normal neck clroomference
Fig. 2. - The relationship between OSA and neck circumference
(n=66). r=0.63, 95% C.l. 0.46--0.76.
NECK SIZE, RADIOLOGY, AND SLEEP APNOEA
Table 1. -The characteristics of the sleep clinic patients
studied
n=66
Median
Age yrs
Weight kg
Obesity index kg·m-2
Neck circumference cm
% Predicted neck circumference
>4% Sao2 dip rate·hr1
Hard palate to spine angle
Mandibular plane to hyoid mm
Soft palate length mm
Retroglossal airway mm
47
90
30
42
102
6
105°
25
45
10
95% Range
24-64
63-156
22-50
35-50
87-123
0.2-59
83-123
15-40
29-60
4.4-20
511
Statistical analysis of patient data
Pearson's correlation coefficient, Speannan's rank
correlation, and stepwise multiple linear regression
analysis (using the stepwise option) were performed using
the SAS statistical analysis software package (SAS
Institute Inc., Cary, North Carolina, USA). A single
regression significance level of p<0.5 was fixed for entry
into the multiple regression analysis, with a significance
level of p<0.15 to remain in the analysis. As the
relationship between PPNC and >4% Sao2 dip rate is
non-linear (fig. 2), Spearman's rank correlation analysis
was used to confirm the correlation between these
variables.
Table 2. - Pearson correlation coefficient matrix for the 66 study patients
>4% Sao2
dip rate
>4% Sao2
dip rate
PPNC
obesity
index
MP-H
PNS-P
RS
0.629.
<0.0001 ..
0.46, 0.76 ...
0.536
<0.0001
0.34, 0.69
0.404
<0.002
0.17, 0.59
0.307
<0.02
0.08, 0.51
NS
0.728
<0.0001
0.305
<0.02
0.572
<0.0001
0.259
<0.04
0.405
<0.001
0.177
0.222
NS
NS
0.296
<0.02
NS
-0.024
-0.2, 0.2
HP-CS
0.285
<0.03
0.04, 0.49
PPNC
0.629
<0.0001
0.46, 0.76
obesity
index
0.536
<0.0001
0.34, 0.69
0.728
<0.0001
MP-H
0.404
<0.002
0.17, 0.59
0.305
<0.02
0.307
<0.02
0.08, 0.51
0.572
<0.0001
0.222
NS
-0.024
0.259
<0.04
0.296
<0.02
-0.144
0.141
0.055
NS
NS
NS
0.405
<0.001
0.476
<0.0001
0.194
0.055
NS
NS
NS
PNS-P
RS
NS
0.224
0.177
0.220
-0.144
NS
NS
NS
0.476
<0.0001
0.220
0.141
0.194
NS
NS
NS
-0.2, 0.2
HP-CS
0.285
<0.03
0.04, 0.49
0.224
": correlation coefficient, r; ••: p value; •••: 95% C.I. for r if applicable; PPNC: % predicted normal neck circumference; MP-H:
mandibular plane to hyoid distance; PNS-P soft palate length; RS: retroglossal space at its narrowest point; HP-CS: head flexion
angle; NS: not significant.
Table 3. -Multiple linear regression analysis of the sleep clinic patient data
(n=59)
r
% predicted neck size
Obesity index
Hyoid distance
Soft palate length
Hard palate to spine angle
Retroglossal airway
0.65
0.02
0.16
0.06
0.02
0.26
95%
C.l.
(r)
%variance
explained
(r2)
p
0.47-0.78
-0.24-0.27
-0.10-0.40
-0.20-0.31
-0.24-0.27
0.00-0.48
42
<1
3
<1
<1
7
<0.0001
NS
NS
NS
NS
<0.01
Total model r 2 = 0.42, 95% C.l. 0.22-0.61 (see text)
r: correlation coefficient; 95% C.l.: 95% confidence interval; NS: not significant.
Dependent variable= >4% Sao2 dip rate.
512
R.J.O. DAVIES, J.R. STRADLING
Results
The study population characteristics are shown in table
1, and the results of the regression analysis in tables 2
and 3, and figure 2. In Pearson's correlation coefficient
analysis neck size, obesity index, PPNC, PNS-P,
l\1P-H, and HP-CS, were all significantly correlated with
>4% Sao2 dip rate. No other variable demonstrated a
significant correlation. Spearman's rank correlation
analysis confirmed the relationship between PPNC and
saturation dip rate, (r=0.69, 95% C.I. 0.53-0.80,
p<O.OOOI).
30
E
E
•
r:0.83, 95% C.l. 0.74-UO,
pc0.0001
25
20
•••
•
•• •
"'
a: 15
10
•
5
0
so
r:0.44, 95% C.l. 0.21-U2,
pc0.001
40
E
~
• ••
••
•
•
30
ci.
:1
20
••
10
70
80
••• • •
•
•
•
100
90
110
Hard paiBtt·to-cervlcal spine angle •
120
130
Fig. 3. - The variation of lateral pharyngeal radiographic dimensions
with head flexion/cxtension in normals (n=6). RS: retroglossal space:
MP-H: mandibular plane to hyoid distance.
Using stepwise multiple linear regression with >4%
Sao2 dip rate as the dependent variable, the model best
describing the variance was:
>4% Sao2 dip rate = 1.46PPNC - 1.17RS - 121.4
The r2 for this model was 0.42, (95% C.l. 0.22--0.61,
p<O.OOOl), thus explaining 42% of the total variance in
>4% Sao2 dip rate. Obesity index, soft palate length ,
mandibular plane to hyoid distance, and hard
palate-to-spine angle, did not contribute significantly to
the model. If a >4% Sao2 dip rate of 10 or more is taken
as evidence of significant OSA, then a PPNC of 105%
(a 42.5 cm (16.75 inch) neck circumference for a 1.78 m
(5 feet lO inch) man) is 77% sensitive and 82% specific
for significant OSA. This is a positive predictive value
of 75%.
Pearson's correlation coefficient analysis (figure 3) of
the normal subject data demonstrated that the retroglossal space, and mandibular plane to hyoid distance,
correlated significantly with hard palate-to-spine angle
(fig. 3); soft palate length did not. A previous study in
six normals (unpublished) has shown neck
circumference does not systematically vary with head
posture.
Djscussioo
For most adult patients with obstructive sleep apnoea,
obesity has been regarded as the most important element
provoking their rusease (1]. This study has shown that
variation in neck size fully explains this relationship. We
have also shown that two radiographic pharyngeal
dimensions which correlate with the presence of sleep
apnoea (l\1P-H, and PNS-P) [2, 3, 5-8), appear to be
secondary effects of neck obesity rather than
independently important aetiological influences.
In this study, we have used a radiological technique
which differs from those used elsewhere. All previous
studies have attempted to generate a reproducible image
by ensuring the head lies with the pituitary sella to nasion
line within seven degrees of the horizontal [3, 7, 8, 16].
To achieve this, subjects have either been fixed in a
cephalostat, or asked to maintain a horizontal gaze by
fixing vision on their reflection in a mirror. In our
technique we have removed these constraints, and
allowed the subject to adopt a comfortable unrestrained
posture. Our nonnal subject analysis has shown that small
changes in angle HP-CS produce large variations in
pharyngeal dimensions. Therefore, in order to establish
whether conclusions drawn from our technique are
comparable with those of others, we have measured
angle HP-CS in 16 randomly selected adult orthodontic
cephalostats drawn from a large library. The range of
HP-CS was substantial, (median 91°,95% range 80-107),
presumably due to movement of the body under the fixed
head. Varying HP-CS across this 95% range generates at
least a three fold variation in retroglossal space, and
significant variation in hyoid position (fig. 3) [17).
Cephalometry demands that the head be fixed in a
selected posture. However, we have preferred to image
the pharynx in a physiological position chosen by the
patient. This avoids unnatural changes in pharyngeal
dimensions induced by forcing an arbitrary head
position. Although an unrestrained head position varies
between subjects, it has been shown to be reproducible
in an individual [18], and allows any compensatory
responses for airway abnormalities to occur and be
recorded in the final image.
We have found obesity index, l\1P-H, PNS-P, and
HP-CS, to be correlated with >4% Sao2 dip rate in single
regression analysis. Other groups have reported similar
findings [3-8], and the increase in neck size among
patients with OSA has been reported by this unit and
others [19, 20]. However, this is the first work to relate
neck size to radiographic pharyngeal dimensions in the
sleep apnoea syndrome. In our multiple linear
regression analysis obesity index, MP-H, PNS-P, and HPCS, do not explain significantly more variation in >4%
Sao2 dip rate than does neck size alone. Thus the single
regression correlations of these indices with OSA are
NECK SIZE, RADIOLOGY, AND SI..EEP APNOEA
secondary phenomena consequent on variation in neck
size. We consider there may be several explanations for
each of these secondary relationships. Soft palate size
may simply be an indirect marker of neck obesity, since
sleep apnoea patients have fat deposits in the uvula which
are absent from weight matched controls [10]. Furthermore, since neck size is a powerful predictor of complete
pharyngeal obstruction (OSA), it is likely to be a powerful predictor of partial obstruction: partial pharyngeal
obstruction leads to snoring which is, itself, suggested
to provoke oedema and elongation of the uvula [21].
The increase in MP-H may also be explained in several
ways. T AILGREN and Soww have shown that MP-H varies
with head flexion [17], as is seen in both our normal and
patient data (fig. 3, table 2). We have shown variation
in head flexion can occur even during cephalostatic
radiography. Since angle HP-CS is positively correlated
with >4% Sao2 dip rate (table 2), some of the increase
in MP-H in OSA patients compared to controls may be
explained by systematic head extension during imaging,
even in the cephalostatic series. Since our normal subject
data shows that head extension markedly widens the
retroglossal airway (fig. 3), we hypothesise that the
increase in angle HP-CS is a response learned by OSA
patients to reduce the increased upper airway resistance
caused by a small pharynx [4, 22, 23].
After surgical mandibular shortening (when the airway
is narrowed by repositioning of the tongue), WICKWIRE
et al. have shown that the hyoid descends, drawing the
root of the tongue down and out of the overcrowded
pharynx [24]. We suggest a similar response may occur
when it is neck obesity which results in narrowing of the
pharyngeal airway. If this is so, some of the increase in
MP-H seen in OSA patients would represent a
compensatory response to airway narrowing. In OSA
patients with an increased mandibular plane to hyoid
distance, the hyoid bone has been surgically elevated as
part of treatment [25, 26]. If a low set hyoid is a
secondary phenomena consequent on neck obesity, such
an approach may be inappropriate if weight loss and thus
reduction in neck size can be achieved.
Other groups have reported observations which
support a significant role for neck fat deposition in OSA.
In a rabbit model, simulating obesity by mass loading
the pharynx leads to concentric airway narrowing and
pharyngeal obstruction [9]. in man, sleep apnoea has
been provoked by a superficial neck lipoma loading the
airway, and cured by its resection [27]. There is also
supportive evidence for compensatory pharyngeal
responses protecting the airway from collapse. SURATT
et al. [28] have shown that the genioglossus musculature
exhibits more phasic EMG activity in OSA patients than
controls during both wakefulness and sleep, and that
this correlates with the resistance of the nasopharyngeal
airway. Similar increases in genioglossus activity have
been reported in children with OSA due to structural
upper airway abnormalities [29]. If pharyngeal patency
has to be maintained by extra muscular activity,
collapse of the airway with sleep onset might be anticipated since there are other examples of respiratory compensations which fail on falling asleep. For example ,
513
subjects breathing against added positive end-expiratory
pressure accommodate to maintain a constant functional
residual capacity (FRC) when awake. However, with the
onset of sleep this adjustment fails and FRC rises [30].
The retroglossal space is not significantly correlated
with >4% Sao2 dip rate in our single regression analysis,
but is significant in the multiple linear regression, and
thus is acting as a suppressor variable [31]. Therefore,
its contribution to the multiple linear regression analysis
cannot be interpreted reliably and it is not discussed
further.
In conclusion, we have shown variation in neck
circumference to be a close correlate of sleep apnoea,
and thus a powerful physical sign when considering OSA
in the sleepy patient who snores. We have also
demonstrated that the widely recognised relationship
between general obesity and sleep apnoea is fully
explained by variation in neck size, implying that obesity
mediates its effect through fat deposition in the neck.
Finally, the relationships of soft palate length and
mandibular plane to hyoid distance with the severity of
OSA, both appear to be secondary to variation in neck
circumference. In 1988, LuoAREsi et al. suggested that
the anatomical upper airway changes seen in OSA
patients may be secondary effects of the disease process
[32]. We now present some evidence suggesting that for
mandibular plane to hyoid distance and soft palate length
this is likely to be true.
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26. Guilleminault C, Riley RW, Powell NB. - Surgical
treatment of obsttuctive sleep apnoea. In: Principles and
Relation entre la circonference du cou, /'anatomie pharyngee
radiologique, et le syndrome d'apnie obstructive du sommeil.
R. Davies, J. Stradling.
RESUME: Nous avons etudie, chez 66 patients, la valeur
predictive de la circonference du cou, de l'obesite, et de
ccrtaines dimensions du pharynx obtenues par etude
radiologique, en ce qui conceme le syndrome d'apnee
obstructive du sommeil (OSA). OSA a ete quantifie comme le
nombre moyen horaire de chutes de la saturation oxygenee du
sang arteriel > 4% pendent le sommeil. La circonference du
cou (r=0.63, 95% C.I. 0.46-0.76), l'index d'obesite (r=0.54,
95% C.I. 0.39-0.69), la position de l'hyoi'de (r=0.40, 95% C.I.
0.19-0.59), la longueur du voile du palais (r=Q.31, 95% C.l.
0.08-0.51), et I'angulation de palais osseux a la colonne (r=0.29,
95% C.J. 0.04-0.49). sont en correlation significative avec Ies
creux de saturation dans une analyse de regression simple. Dans
une analyse de regression lineaire multiple par echelons (ou le
taux de creux de saturation est la variable dependante), seuls la
dimension du cou e t l'espace retro-lingual sont en correlation
independante significative (total rl=0.42, 95% C.I. 0.22 a 0.61,
p<0.0001). Nous concluons que les relations enlre l'obesite
generale, la position de l'os hyoide, la longueur du voile du
palais, et le syndrome d'apnee du sommeil, sont probablement
secondaires aux modifications de la circonference du cou.
Eur Respir J., 1990, 3, 509- 514.