Keywords
Cephalometry - Sleep Apnea - Obstructive - Anthropometry - Body Mass Index - Abdominal
Circumference - Waist Circumference
Introduction
Obstructive sleep apnea-hypopnea syndrome (OSAHS) is a disorder characterized by recurrent
episodes of partial or total upper airway obstruction during sleep. The apnea-hypopnea
index (AHI) refers to the number of episodes of apnea and hypopnea that occur per
hour of sleep[1].
OSAHS affects 4–7% of the general adult population[2]. Owing to its current prevalence, it is considered a major public health concern,
which can manifest serious physical and social consequences if not managed properly[2]
[3]. This disorder mainly affects middle-aged economically active patients, resulting
in high costs and lost workdays[4]. Medical costs can be significantly reduced when effective diagnosis and treatment
are performed early[5]. The diagnosis of OSAHS is based on a combination of the laboratory findings of
apnea and hypopnea with clinical symptoms[6].
Radiographic imaging of the upper airways allows for the study of bone and soft tissue
anatomy, in addition to the determination of the site of obstruction and the choice
of appropriate treatment for OSAHS patients[7]. Cephalometry has been used since 1983 and was initially applied in patients with
sleep-related breathing disorders. It consists of cephalometric tracings obtained
by teleradiography of the facial profile. The aim of the test is to study the facial,
maxillary, and mandibular skeleton and any relationships with the soft tissues that
may cause pharyngeal obstruction[8]. Cephalometry is an easy, low-cost, non-invasive, and widely available modality
in the majority of hospitals. Radiation use is minimal, readily accessible to clinicians,
and not uncomfortable for the patient. It has proved to be useful for the evaluation
of the upper airways and bone structure in normal subjects and OSAHS patients[9]
[10]
[11].
A complete cephalometric analysis should be performed in patients with OSAHS to identify
associated maxillofacial abnormalities[12]. From this perspective, it has been used in several sleep disorder centers, with
the purpose of diagnosing the site of obstruction in patients with obstructive sleep
apnea. In some centers, this test is part of a service protocol that is important
for the decision as to which type of surgery should be performed. Therefore, it is
recommended in all patients with OSAHS undergoing surgery[8]
[9]
[12]
[13]
[14]
[15]. It is also used with mandibular advancement devices to assess therapeutic efficacy
in patients with mild to moderate OSAHS[15]
[16].
Obesity, in particular the presence of visceral fat, is considered a predictive factor
for OSAHS[17]. Several studies have been performed using anthropometric measurements of obesity
in patients with OSAHS, e.g., body mass index (BMI), neck circumference (NC), waist
circumference (WC), and hip circumference (HC)[18]
[19]
[20]
[21]. These measurements may be used both to assess the need for patient referral to
polysomnographic evaluation and to anticipate treatment in high-risk patients, since
this disorder may cause severe consequences in untreated patients[2]
[21]. Polysomnography is not an accessible test for most individuals. It is expensive
and easier, more affordable tests with less technological density, such as cephalometry[9]
[10]
[11], are required[17]
[19]
[22]
[23] to screen for OSAHS. Anthropometric measurements are easily obtained and fundamental
for the preparatory study of a patient with suspected OSAHS. Therefore, the number
of patients referred for polysomnography could be greatly reduced, lowering healthcare
expenses, with simple measurement of cervical, waist, and hip circumferences. The
use of these measurements in patients with snoring and those clinically suspected
of having OSAHS would thus prioritize complementary polysomnography testing in patients
with higher suspicion of disease[24].
The aim of this study was to correlate cephalometric and anthropometric measurements
with the AHI, in order to assess if these measurements can be used as predictors of
OSAHS severity.
Method
Data obtained from the medical charts of 93 male and female patients with OSAHS, ranging
in age from 19 to 80 years, were studied. These patients had been examined from July
2010 to July 2012 in a specialist private clinic in Teresina. The medical charts of
patients who had undergone previous surgical treatment for OSAHS, including use of
continuous positive airway pressure devices or intraoral devices, in addition to patients
with craniofacial deformities and upper airway tumors, were excluded from the study.
Overnight polysomnography was analyzed by a single professional, who specialized in
sleep disorders. Patients were considered to have OSAHS if, in addition to clinical
complaints, they had an AHI ≥ 5 upon overnight polysomnography testing[1]. Severity was measured by the AHI. Cephalometry was also performed by a single radiologist,
who specialized in orthodontic radiographs. Each examiner was blinded to the test
results obtained by the other examiner.
The following cephalometric traces were considered, since they are the most commonly
used cephalometric measures: retroglossal posterior airway space (PAS), defined as
the space between the base of the tongue and the posterior pharyngeal wall; the distance
between the mandibular plane and the hyoid bone (MP-H); the SNA angle, formed by the
junction between the sellar point (S, midpoint of the sella turcica), nasion (N, junction
between the frontal and nasal bones), and point A (deepest concavity on the anterior
profile of the maxilla); the SNB angle, formed by the junction between the sellar
point (S), nasion (N), and point B (deepest concavity on the anterior profile of the
mandibular symphysis); the distance between the posterior nasal spine and the tip
of the soft palate (PNS-P); and the difference between SNA and SNB (ANB) ([Figure 1])[8]
[9]
[12]
[15].
Figure 1. Description of cephalometric parameters (Source: the author).
Concerning anthropometric measurements, BMI, NC, WC, and HC were evaluated. BMI was
calculated as the weight of the subject (in kilograms) divided by their height (in
meters) squared. Obesity is defined as a BMI ≥ 30 kg/m2
[25]. NC was measured at the level of the crycothyroid cartilage. WC was measured between
the last rib and the iliac crest and HC was measured as the maximum circumference
at the level of the border of the trochanter. Anthropometric measurements were based
on the World Health Organization manual [26].
Data was entered into the Statistical Package for the Social Sciences (SPSS) version
16.0 program for calculation of simple descriptive statistics, e.g., percentage distribution,
mean, and standard deviation. A normality test (Kolmogorov-Smirnov) was applied and
the adequate statistical test was chosen for each type of variable (parametric or
nonparametric). Pearson's correlation coefficients were examined between AHI and the
following variables: age, BMI, NC, WC, HC, and cephalometric measurements (SNA, SNB,
ANB, MP-H, PAS, and PNS-P). Sex differences were compared by the Student's t test.
Statistical significance was set at p < 0.05.
The project was approved by the Research Ethics Committee of the Universidade Federal do Piauí, under CAAE number 0047.0.045.000-10.
Results
Of the 93 patients studied, 54 (58.1%) were male. The mean BMI was 27.68 ± 3.83 kg/m2 (women, 27.41 ± 4.50 kg/m2; men, 27.88 ± 3.30 kg/m2). There were 69 (74.19%) nonobese (BMI, 25.90 ± 2.29 kg/m2) and 24 (25.81%) obese (BMI, 32.81 ± 2.50 kg/m2) patients ([Table 1]).
Table 1.
Sample distribution according to gender and obesity.
|
|
n
|
%
|
BMI, kg/m2
|
|
|
|
|
(mean ± SD)
|
Gender
|
Male
|
54
|
58.06
|
27.88 ± 3.30
|
|
Female
|
39
|
41.94
|
27.41 ± 4.50
|
|
Total
|
93
|
100.00
|
27.68 ± 3.83
|
Obesity
|
Nonobese
|
69
|
74.19
|
25.90 ± 2.29
|
|
Obese
|
24
|
25.81
|
32.81 ± 2.50
|
|
Total
|
93
|
100.00
|
27.68 ± 3.83
|
Note: BMI = body mass index.
The mean age of the patients was 46.70 ± 15.46 years (range, 19 to 80 years). [Table 2] describes the sample characteristics and variables studied, including their variations
and means.
Table 2.
Characteristics of the sample including age, anthropometric parameters, cephalometric
parameters, and AHI (n = 93).
Variable
|
Minimum
|
Maximum
|
Mean
|
Standard deviation
|
Age, years
|
19.0
|
80.0
|
46.70
|
15.46
|
BMI, kg/m2
|
19.72
|
40.18
|
27.68
|
3.83
|
NC, cm
|
30.0
|
47.0
|
38.56
|
3.92
|
WC, cm
|
73.0
|
125.0
|
97.59
|
10.10
|
HC, cm
|
87.0
|
131.0
|
104.09
|
7.39
|
SNA°
|
72.0
|
92.0
|
82.77
|
4.08
|
SNB°
|
69.0
|
92.0
|
80.96
|
4.41
|
ANB°
|
−13.0
|
10.0
|
1.82
|
3.90
|
MP-H, mm
|
4.0
|
45.0
|
19.21
|
8.22
|
PAS, mm
|
3.0
|
20.0
|
10.04
|
3.80
|
PNS-P, mm
|
20.0
|
52.0
|
39.84
|
5.37
|
AHI, events/h
|
5.00
|
83.40
|
34.67
|
17.41
|
Note: AHI = apnea-hypopnea index; BMI = body mass index; NC = neck circumference; WC = waist
circumference; HC = hip circumference; SNA = angle formed by the junction of the sella
(S), nasion (N), and point A; SNB = angle formed by the junction of the sella (S),
nasion (N), and point B; ANB = difference between SNA and SNB; MP–H = distance between
the mandibular plane and the hyoid bone; PAS = space between the base of the tongue
and the posterior pharyngeal wall; PNS–P = distance between the posterior nasal spine
and the tip of the soft palate.
[Table 3] shows an analysis of the Pearson correlation coefficients used to evaluate the relationship
between AHI, age, and anthropometric/cephalometric measurements. Analyzing the relationship
between age and OSAHS severity by AHI showed a positive correlation between these
2 data series, indicating that OSAHS was more severe in older patients. Similarly,
there was also a positive correlation between BMI and AHI, which allowed us to infer
that the higher the BMI, the greater the AHI. Regarding body circumference measurements,
both NC and WC showed a statistically significant positive correlation with OSAHS
severity. Concerning the relationship between cephalometric data and AHI, a statistically
significant positive correlation for MP-H and PNS-P was observed ([Table 3]).
Table 3.
Correlation of age and anthropometric/cephalometric data with AHI (n = 93).
|
Age
|
BMI
|
NC
|
WC
|
HC
|
SNA
|
SNB
|
ANB
|
MP-H
|
PAS
|
PNS-P
|
Pearson correlation
|
0.241
|
0.207
|
0.365
|
0.337
|
0.201
|
−0.044
|
0.031
|
−0.081
|
0.235
|
−0.102
|
0.282
|
p-value (two-tailed)
|
0.020
|
0.047
|
0.000
|
0.001
|
0.053
|
0.676
|
0.769
|
0.441
|
0.023
|
0.329
|
0.006
|
Note: AHI = apnea-hypopnea index; BMI = body mass index; NC = neck circumference; WC =
waist circumference; HC = hip circumference; SNA = angle formed by the junction of
the sella (S), nasion (N), and point A; SNB = angle formed by the junction of the
sella (S), nasion (N), and point B; ANB = difference between SNA and SNB; MP–H = distance
between the mandibular plane and the hyoid bone; PAS = space between the base of the
tongue and the posterior pharyngeal wall; PNS–P = distance between the posterior nasal
spine and the tip of the soft palate
Comparing anthropometric parameters between men and women indicated a statistically
significant difference for NC and WC, but not for HC. Regarding cephalometry, MP-H
and PNS-P were significantly different between men and women ([Table 4]).
Table 4.
Comparison between males and females for anthropometric/cephalometric data and AHI.
|
Females (n = 39)
|
Males (n = 54)
|
p-value
|
Age, years
|
49.77 ± 14.32
|
44.48 ± 15.99
|
p > 0.05
|
BMI, kg/m2
|
27.41 ± 4.50
|
27.88 ± 3.30
|
p > 0.05
|
NC, cm
|
35.31 ± 2.27
|
40.91 ± 3.09
|
**p < 0.01
|
WC, cm
|
94.41 ± 10.79
|
99.89 ± 8.99
|
**p < 0.01
|
HC, cm
|
102.56 ± 8.65
|
105.19 ± 6.18
|
p > 0.05
|
SNA°
|
82.74 ± 3.38
|
82.80 ± 4.56
|
p > 0.05
|
SNB°
|
80.41 ± 4.35
|
81.35 ± 4.44
|
p > 0.05
|
ANB°
|
2.33 ± 3.98
|
1.44 ± 3.83
|
p > 0.05
|
MP-H, mm
|
15.04 ± 6.62
|
22.22 ± 8.00
|
**p < 0.01
|
PAS, mm
|
9.28 ± 3.44
|
10.59 ± 3.98
|
p > 0.05
|
PNS-P, mm
|
37.82 ± 5.10
|
41.30 ± 5.12
|
**p < 0.01
|
AHI, events/h
|
31.02 ± 15.20
|
37.30 ± 18.53
|
p > 0.05
|
Note: AHI = apnea-hypopnea index; BMI = body mass index; NC = neck circumference; WC = waist
circumference; HC = hip circumference; SNA = angle formed by the junction of the sella
(S), nasion (N), and point A; SNB = angle formed by the junction of the sella (S),
nasion (N), and point B; ANB = difference between SNA and SNB; MP–H = distance between
the mandibular plane and the hyoid bone; PAS = space between the base of the tongue
and the posterior pharyngeal wall; PNS–P = distance between the posterior nasal spine
and the tip of the soft palate
[Tables 5] and [6] show an analysis of the Pearson correlation coefficients used to assess the relationship
between AHI and age as well as anthropometric/cephalometric measurements for males
and females.
Table 5.
Pearson correlation of AHI with age and anthropometric data for males and females.
|
|
Age
|
BMI
|
NC
|
WC
|
HC
|
M
|
Pearson correlation
|
0.358
|
0.273
|
0.349
|
0.395
|
0.156
|
|
p-value (two-tailed)
|
0.008**
|
0.046*
|
0.010**
|
0.003**
|
0.259
|
|
n
|
54
|
54
|
54
|
54
|
54
|
F
|
Pearson correlation
|
0.131
|
0.123
|
0.329
|
0.192
|
0.212
|
|
p-value (two-tailed)
|
0.426
|
0.457
|
0.041*
|
0.242
|
0.195
|
|
n
|
39
|
39
|
39
|
39
|
39
|
Note: AHI = apnea-hypopnea index; M = males; F = females; BMI = body mass index; NC = neck
circumference; WC = waist circumference; HC = hip circumference; ** p < 0.01; * p < 0.05.
Table 6.
Pearson correlation between AHI and cephalometric data for males and females.
|
|
SNA
|
SNB
|
ANB
|
MP-H
|
PAS
|
PNS-P
|
M
|
Pearson correlation
|
−0.075
|
0.031
|
−0.125
|
0.229
|
−0.212
|
0.305
|
|
p-value (two-tailed)
|
0.592
|
0.822
|
0.368
|
0.096
|
0.124
|
0.025*
|
|
n
|
54
|
54
|
54
|
54
|
54
|
54
|
F
|
Pearson correlation
|
0.020
|
−0.021
|
0.040
|
0.073
|
0.010
|
0.135
|
|
p-value (two-tailed)
|
0.904
|
0.898
|
0.809
|
0.660
|
0.951
|
0.412
|
|
n
|
39
|
39
|
39
|
39
|
39
|
39
|
Note: AHI = apnea-hypopnea index; M = males; F = females; SNA = angle formed by the junction
of the sella (S), nasion (N), and point A; SNB = angle formed by the junction of the
sella (S), nasion (N), and point B; ANB = difference between SNA and SNB; MP–H = distance
between the mandibular plane and the hyoid bone; PAS = space between the base of the
tongue and the posterior pharyngeal wall; PNS–P = distance between the posterior nasal
spine and the tip of the soft palate; * p < 0.05.
For anthropometric measurements, AHI showed a statistically significant correlation
with age, BMI, NC, and WC in males. Only NC showed a significant correlation in females.
In both genders, the most significant correlation was with NC ([Table 5]). Regarding cephalometric measurements, the only correlation found was that of AHI
with PNS-P measurement in males ([Table 6]).
Discussion
Obesity may increase susceptibility to OSAHS by causing fat deposition in the upper
airway tissues, narrowing the nasopharyngeal caliber and/or leading to hypoventilation
in association with reduced wall complacency[27]. Assessment of craniofacial morphology in OSAHS patients not only aids specialists
concerned with recognizing morphologic changes induced by altered sleep patterns,
but also provides the patient with adequate treatment[11].
There is a vast amount of scientific literature on cephalometric and anthropometric
measures, which compares control groups and snorers to OSAHS patients and aims at
using these measurements as predictors of this condition[7]
[9]
[10]
[11]
[13]
[15]
[18]
[20]
[22]
[28]
[29]
[30]
[31]
[32]. Some studies have been performed to assess appropriate treatments, surgical treatment
plans, and the indications of intraoral devices[11]
[16]
[27]
[33]
[34]
[35]
[36]
[37]
[38]
[39]
[40], while others were performed to evaluate the relationship between these measurements
and OSAHS severity[17]
[18]
[19]
[20]
[22]
[23]
[24]
[32]
[40]
[41]
[42]
[43]
[44]
[45].
In the current study, there was a significant correlation between age and AHI ([Table 3]), indicating that OSAHS is more severe in older patients. This is in agreement with
the majority of previous studies[17]
[22]
[23]
[24]
[45]
[46], with the exception of those by Mayer et al42 and Schellenberg, Maisline, and Schwab[37].
It was observed that BMI was correlated with AHI, allowing us to infer that more severe
OSAHS occurs in subjects with a higher BMI, which is concordant with most published
studies[17]
[19]
[21]
[22]
[23]
[31]
[32]
[37]
[39]
[42]
[45]
[46]
[47]. Nevertheless, this fact was not observed by Yucel et al[41] and Martinez-Rivera et al[24].
NC is a simple measurement that is easily performed. Findings in the present study
point to a positive correlation between NC and AHI, which is in agreement with other
studies[19]
[20]
[22]
[24]
[31]
[32]
[37]
[38]
[39]
[41]
[46]. A correlation with BMI was also observed previously[17]
[18]
[19]
[23]
[32]
[44], suggesting that obesity affects patients with OSAHS through fat deposition in the
neck[20]
[23]
[30]. In contrast to the majority of studies, Ogretmenoglu et al[17] stated that NC was more weakly correlated with AHI than BMI.
WC also showed a positive correlation with AHI, in agreement with other studies[19]
[23]
[24]
[32]
[38]
[39]
[46].This correlation was weaker than that observed with NC, supporting the existing
literature[19]
[23]
[39]. The present study is also consistent with others [19]
[32] showing that the correlation of AHI with WC is greater than that with BMI. However,
Davidson and Patel[32] observed that WC was more predictive than BMI as well as NC.
Analyzing the relationship between cephalometric data and AHI showed a statistically
significant correlation for MP-H and PNS-P, indicating an increased palatal length
and an increased distance between the hyoid bone and the mandibular plane, which was
consistent with other studies[29]
[42]
[43]
[46]
[48]. According to Yucel et al[41], only MP-H measurement is related to AHI. The position of the hyoid bone, which
has an impact on the shape and position of the tongue, affects hypopharyngeal airway
patency[41].
A study by Bharadwaj, Ravikumar, and Krishnaswamy conducted in India compared 10 OSAHS
patients to a control group of 10 healthy subjects (mean age, 34.9 years). These authors
concluded that upright cephalometry demonstrated mandibular retrognathism, increased
ANB angle, increased PNS-P length and increased soft palate thickness, increased tongue
length, and decreased PAS in the group of OSAHS patients when compared to the control
group[11]. Other studies have shown that PNS-P and MP-H measurements are increased, while
PAS is decreased, in patients with OSAHS, and these measurements were considered predictive
of OSAHS[7]
[9]
[15]. PAS measurement was correlated with severity of OSAHS assessed using the AHI[7]
[9]. A study conducted in Strasbourg (France) in 1990, comparing 43 OSAHS patients to
a control group of 40 asymptomatic individuals, showed that PNS-P measurement was
increased in patients with OSAHS, while SNA, SNB, and ANB measurements did not demonstrate
any alterations in either group[28]. Other studies have shown increased MP-H measurement and decreased PAS measurement
in comparisons between OSAHS groups and control groups[13]
[40]. However, Mayer et al[42] found no correlation between PAS measurement and AHI.
In a comparison between male and female patients in the present study, BMI and HC
were similar. NC and WC were significantly higher in males than in females. These
results are partially in agreement with findings by Millman et al[49], who described a higher NC for males, but no difference between the genders for
BMI and WC. Another study demonstrated a significantly increased BMI in females[41]. This fact reflects well-known characteristics concerning body fat distribution
in men and women[49].
In the current study, NC was more closely correlated with AHI than WC and BMI, both
in the overall population and in male and female subjects, indicating that NC is the
best anthropometric measurement for prediction of OSAHS severity, especially in males[18]
[19]
[23]
[39]
[41]
[44]. Comparing cephalometry between male and female subjects showed a statistically
significant difference in MP-H and PNS-P measurements, which were higher in male subjects.
PNS-P measurement was correlated with AHI in males, while there were no significant
correlations in females.
In conclusion, the results of this study show a correlation of anthropometric (BMI,
NC, and WC) and cephalometric (MP-H and PNS-P) measurements with the AHI, reinforcing
their preparatory role and use as predictors of OSAHS.