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(Chest. 2003;124:212-218.)
© 2003 American College of Chest Physicians

Cephalometric Analysis in Obese and Nonobese Patients With Obstructive Sleep Apnea Syndrome*

Xiujun Yu, MD; Keisaku Fujimoto, MD; Kazuhisa Urushibata, MD; Yukinori Matsuzawa, MD and Keishi Kubo, MD, FCCP

* From the First Department of Internal Medicine, Shinshu University School of Medicine, Matsumoto, Japan.

Correspondence to: Keisaku Fujimoto, MD, First Department of Internal Medicine, Shinshu University School of Medicine, 3-1-1, Asahi, Matsumoto, 390-8621 Japan; e-mail: Keisaku{at}hsp.md shinshu-u.ac.jp


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: The aims of this study were to comprehensively evaluate the cephalometric features of patients with obstructive sleep apnea syndrome (OSAS), and to elucidate the relationship between cephalometric variables and severity of the apnea-hypopnea index (AHI).

Patients: The study population consisted of 62 male patients with OSAS, classified into 33 obese patients (body mass index [BMI] >= 27) and 29 nonobese patients (BMI < 27), and 13 male simple snorers (AHI < 5 events per hour).

Method and measurements: Diagnostic polysomnography and measurements of 22 cephalometric variables were carried out for all patients and simple snorers.

Results: Patients with OSAS in both subgroups showed several significant cephalometric features compared with simple snorers: (1) inferiorly positioned hyoid bone, (2) enlarged soft palate, and (3) reduced upper airway width at soft palate. More extensive and severe soft-tissue enlargements including anteriorly positioned hyoid bone and a longer tongue were found in the obese patients. In the nonobese patients, the anteroposterior distances of the bony nasopharynx and oropharynx were significantly smaller than those of simple snorers and obese patients. Stepwise regression analysis showed that anterior displacement of the hyoid bone and retroposition of the mandible were the dominant overall determinants for AHI in patients with OSAS, and that narrowing of the bony oropharynx and inferior displacement of the hyoid bone were dominant determinants for AHI in nonobese patients. A significant regression model for AHI using cephalometric variables could not be obtained for the obese patients, but the BMI proved to be the most significant determinant.

Conclusion: Characteristics of the craniofacial bony structure such as narrowing of the nasopharynx and oropharynx and enlargement of the soft tissue in the upper airway may be important risk factors for the development of OSAS in nonobese patients. In obese patients, the deposition of adipose tissue in the upper airway may aggravate the severity of OSAS.

Key Words: cephalometry • facial bone • hyoid bone • obesity • obstructive sleep apnea syndrome • pharynx • polysomnography • snoring • soft palate


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Obstructive sleep apnea syndrome (OSAS) is a serious and potentially life-threatening disorder that is far more common than generally believed. Excessive daytime sleepiness and loud snoring during sleep are the principal symptoms of the disorder, and are seen in nearly all such patients. The mechanisms responsible for upper airway obstruction in patients with OSAS are highly complicated and as yet not fully understood. Craniofacial anatomic risk factors are said to play a role in OSAS, together with the mechanism of upper airway compliance and muscle function.1 Over the past 3 decades, a number of studies have used cephalometric analysis to assess the craniofacial morphologic features of patients with OSAS. Certain forms of craniofacial anatomic defects, including mandibular deficiency, tongue and soft palate enlargement, and inferior displacement of the hyoid bone, have been suggested as predisposing factors for upper airway obstruction during sleep.2 3 4 5 6 Earlier observations were generally based on small sample groups without adequate control groups. More recent studies,4 7 8 9 10 11 however, have examined cephalometric abnormalities in patients with OSAS in a more systematic way, and the possibility that body mass index (BMI) influences cephalometric measurements has gained acceptance. However, results from previous studies have not always agreed with regard to craniofacial bony structure abnormalities in nonobese patients with OSAS.7 8 10 11 Furthermore, the etiology of OSAS in obese patients may be different from that in nonobese patients.7 8 11 It has been suggested that the discrepancy in these cephalometric measurements may also depend on sex,12 age,13 and race.14 15 16 OSAS in Asian men has been found more frequently in nonobese patients, despite the presence of severe illness, when compared with white male patients with OSAS.14

Asian patients with OSAS have also demonstrated greater abnormalities of the craniofacial anatomy16 ; however, only a few cephalometric studies11 15 16 of Asian patients with OSAS have been reported. Furthermore, it is unclear whether there are differences in cephalometric measurements between patients with OSAS and simple snorers. Although loud snoring during sleep is the principal symptom seen in virtually all patients with OSAS, not all snorers have OSAS. The differences between patients with OSAS and simple snorers are more interesting and important regarding the mechanisms responsible for upper airway obstruction than those between patients with OSAS and normal nonsnorers. For this reason, we have used simple snorers as control subjects in this study.

The objectives of the present study were to make a systematic and detailed cephalometric analysis of male patients with OSAS with and without obesity, and to compare these analyzed variables with those obtained from male simple snorers without morbid sleep apnea and hypopnea in a Japanese population. Another objective was to clarify the relationship between cephalometric variables and the severity of the apnea-hypopnea index (AHI) in patients with OSAS.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Population
Sixty-two Japanese male patients with OSAS, consecutively referred to Shinshu University Hospital between April 2000 and December 2001, who recorded AHI >= 10 events per hour during an overnight polysomnographic study and who complained of habitual snoring and daytime sleepiness, were recruited for this study. They were classified into two subgroups according to BMI: obese OSAS (BMI >= 27, n = 33) and nonobese OSAS (BMI < 27, n = 29).11 Thirteen healthy male simple snorers without daytime sleepiness and without morbid sleep apnea/hypopnea were recruited as control subjects. The simple snorers were chosen on the basis of the following criteria to be sure that they were free from sleep-disordered breathing: AHI < 5/h, oxygen saturation nadir > 90%, absence of sleep disturbance (including arousal observed on an EEG during an overnight polysomnographic study), and absence of the symptoms related to disordered breathing during sleep. To eliminate any potential confounding variables between male and female subjects, female subjects were excluded from the study.12 A sleep study and lateral cephalometry were performed on all of the patients and simple snorers. The characteristics and the polysomnographic data for the patients and simple snorers are presented in Table 1 . There was no significant difference in BMI or age between the nonobese patients with OSAS and simple snorers. This study was approved by the local research ethics committee, and informed consent was obtained from all patients and simple snorers.


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  		Table 1.. Patient Characteristics*

 
Polysomnography
All patients with OSAS and simple snorers underwent a sleep study consisting of an overnight polysomnographic examination, which included an EEG (C3-A2, C4-A1, O2-A1, and O3-A2), bilateral electrooculogram, chin and lower leg electromyogram, nasal and mouth airflow, thoracic and abdominal respiratory movements recorded by inductive plethysmography, ECG, oxygen saturation measured by finger oximetry, and body position. For this study, a polysomnography system (Alice III; Chest Ltd; Tokyo, Japan) was used. The episodes of apnea were defined as complete cessation of airflow for >= 10 s, and hypopnea consisted of a > 50% reduction in oronasal airflow accompanied by a reduction in oxygen saturation measured by pulse oximetry of at least 4%. Apnea events were classified as obstructive, mixed, or central, according to the presence or absence of breathing efforts with thoracoabdominal paradox. AHI was determined by the frequency of these events per hour during sleep time based on the results of the overnight polysomnography.

Cephalometric Analysis
A lateral cephalogram (left to right view) without swallowing by the patient was obtained in the sitting position during the end-expiration phase. Image plates (Veraview Epocs X550; Morita Ltd; Tokyo, Japan) were used to record the cephalogram. A cephalostat was used to keep the subject’s head in a position such that the Frankfort horizontal line was parallel to the floor during exposure. A total of 22 variables related to both craniofacial skeletal and soft tissue morphology were measured as angular (degrees) or linear (millimeters) by a single observer in a single-blind manner. Every measurement was made three times by the same observer, who did not know the clinical status of the patient, and the mean value of the two most proximate measurements was used for the statistical analyses to ensure reliability.

The cephalometric landmarks and reference lines are defined in Table 2 and illustrated anatomically in Figure 1 . The following angles and dimensions were measured: SNA, the angle between S-N and N-A; SNB, the angle between S-N and N-B; ANB, the angle between N-A and N-B; NSBa (cranial base flexure), the angle between S-N and a line from S to Ba; BMeH, the angle between B-Me and Me-H; GoMeN, the angle between Go-Me and Me-N; G-VL, the linear distance along a perpendicular plane from G to VL; S-N, the distance between S and N; N-Ba, the distance between N and Ba; ANS-PNS, the distance between ANS and PNS; PNS-AA (bony oropharynx), the distance between PNS and AA; PNS-Ba (bony nasopharynx), the distance between PNS and Ba; MP-H, the linear distance along a perpendicular plane from H to MP; H-VL, the linear distance along a perpendicular plane from H to VL; PNS-P, the distance between PNS and P; MPT, the greatest thickness of the soft palate; TGL, the distance between V and TT; TGH, the linear distance along the perpendicular bisector of the V-TT line to the tongue dorsum; AW1, the narrowest part of the airway between PNS and P; AW2, the narrowest part of the airway between P and Go; IAS, the airway width along the Go-B plane; AWest, the smallest of the three measurements, AW1, AW2 and IAS.


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  		Table 2.. Definitions of Cephalometric Landmarks and Reference Lines

 


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  		Figure 1.. Cephalometric landmarks and reference lines. For definitions, see Table 2 .

 
Statistical Analysis
All data are presented as mean ± SEM. In view of the influence of BMI on cephalometric measurements, the OSAS population was further classified into an obese and a nonobese OSAS group by BMI using the cut-off point of >= 27 and < 27 (Table 3 ). Comparison among the groups was performed with a one-way analysis of variance, followed by multiple comparisons with the unpaired t test or Mann-Whitney U test when appropriate. The correlation between variables was examined by calculating the Pearson product correlation coefficient. A multiple, stepwise, linear regression analysis was also performed to identify which cephalometric variables most satisfactorily explained the variance of AHI independently. This analysis was performed for all patients with OSAS and for each predefined subgroup of BMI. All of the statistical analyses were performed with a software program (Stat Flex version 5.0; Artech Ltd; Osaka, Japan). Statistical significance was assessed at p < 0.01 and p < 0.05.


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  		Table 3.. Cephalometric Measurements in Simple Snorers and in Nonobese and Obese Patients with OSAS*

 

   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The characteristics of the subjects are presented in Table 1 . The obese patients with OSAS were younger and showed more severe AHI and oxygen desaturation compared with nonobese patients with OSAS. All cephalometric variables could be measured in most patients; however, we could not find the hyoid bone on a cephalogram of one obese patient, nor obtain an exact measurement of AW1 for four obese patients and three nonobese patients because of enlarged tonsils. When compared with BMI-matched simple snorers, nonobese patient with OSAS showed the following craniofacial anatomical characteristics: (1) inferior position of the hyoid bone (MP-H); (2) a reduction in the anteroposterior upper airway width at the soft palate; (3) enlargement of the soft palate, chiefly due to an increase in its length; and (4) reduction in the anteroposterior width of the bony nasopharynx (PNA-Ba) and oropharynx (PNS-AA). All of these soft-tissue and airway defects, except for those of the anteroposterior width of the bony nasopharynx and oropharynx, were also found in obese patients. In addition, obese patients had a longer tongue (TGL) and more anteriorly displaced hyoid bones (H-VL) than did simple snorers. The facial A-P distance at the maxilla levels (ANS-PNS) was greater, and the mandible (G-VL) more anteriorly displaced in obese patients than in simple snorers. Furthermore, a comparison with nonobese patients showed a more anteriorly displaced hyoid bone and a longer tongue and soft palate in obese patients. However, nonobese patients had significantly shorter G-VL, N-Ba, and ANS-PNS, and significantly narrower bony nasopharynx and oropharynx than obese patients.

The correlations of the cephalometric measurements and BMI with the AHI and percentage of total sleep time occupying pulse oximetric saturation < 90% (%SpO2< 90%) for all patients with OSAS and for each subgroup of obese and nonobese patients are shown in Table 4 . In all patients with OSAS, the AHI showed a significant positive correlation with H-VL, TGL, and the retroposition of the mandible (ANB°), and a negative correlation with PNS-AA. In the nonobese subgroup, the AHI showed a significant positive correlation with TGL, and a negative correlation with the PNS-AA. However, cephalometric measurements did not significantly correlate with AHI in the obese subgroup. The %SpO2< 90%, an index for severity of desaturation, showed a significant positive correlation with H-VL, G-VL, PNS-AA, and PNS-P in all patients with OSAS; but in the obese subgroup, it did not. In the nonobese subgroup, the %SpO2< 90% showed a significant positive correlation with G-VL, PNS-AA, and MP-H, while in all patients with OSAS as well as in the obese patient subgroup, both the AHI and %SpO2 < 90% significantly correlated with BMI.


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  		Table 4.. Correlations of Cephalometric Measurements and BMI With AHI and %SpO2 < 90%*

 
Stepwise regression analysis of AHI and %SpO2 < 90% using the preselected cephalometric variables were performed for all patients with OSAS and each subgroup, except for the eight patients for whom not all cephalometric variables could be obtained as mentioned earlier. For all patients with OSAS, the regression model for AHI was significant (n = 54, model R = 0.521, R2 = 0.271, F = 4.56, p = 0.003) with the following determinants: H-VL (partial R2 = 0.184, p = 0.006), ANB° (partial R2 = 0.068, p = 0.028), PNS-AA (partial R2 = 0.083, p = 0.376), and AW1 (partial R2 = 0.001, p = 0.470). For obese patients, we could not obtain a significant regression model for AHI, while nonobese patients, the regression model could account for 39.5% of the variance of AHI (n = 26, R = 0.629, F = 3.43, p = 0.026) with the following determinants: PNS-AA (partial R2 = 0.152, p = 0.031), ANB° (partial R2 = 0.104, p = 0.062), MP-H (partial R2 = 0.048, p = 0.028), and AW1 (partial R2 = 0.0002, p = 0.155). The regression model for %SpO2 < 90% was significant for all OSAS (n = 61, model R = 0.555, R2 = 0.309, F = 8.48, p = 0.0001) with the following determinants: H-VL (partial R2 = 0.201, p = 0.00009), TGH (partial R2 = 0.045, p = 0.027), and ANB° (partial R2 = 0.048, p = 0.086). For the obese subgroup, the regression model accounted for 41.9% of the variance (n = 32, R = 0.647, F = 3.750, p = 0.011) with the following determinants: ANB° (partial R2 = 0.108, p = 0.020), BaSN (partial R2 = 0.106, p = 0.031), MP-H (partial R2 = 0.0001, p = 0.093), TGH (partial R2 = 0.020, p = 0.045), and H-VL (partial R2 = 0.094, p = 0.153). For the nonobese subgroup, the regression model accounted for 33.3% of the variance (n = 29, R = 0.578, F = 6.52, p = 0.005) with the following determinants: MP-H (partial R2 = 0.133, p = 0.027) and PNS-AA (partial R2 = 0.193, p < 0.01).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The segments of upper airway narrowing in the evolution of OSAS have attracted much attention. Since narrowing may be present in various segments of upper airway, knowledge of its location is central to an understanding of the pathogenesis of OSAS.2 3 11 In this study, a comparison with simple snorers showed that obese and nonobese patients with OSAS were commonly characterized by the following craniofacial anatomical features: a longer soft palate, upper airway narrowing at the soft palate, and an inferiorly positioned hyoid bone. Enlargement of the soft palate was more significant in obese than in nonobese patients, and contributed to extensive upper airway narrowing, so that it may be an important factor in obstruction of the upper pharyngeal airway during sleep. In fact, multiple stepwise regression analysis revealed upper airway narrowing to be one of the determinants for severity of apnea and hypopnea.

In obese patients, on the other hand, tongue length (TGL) was significantly greater than in simple snorers and nonobese patients. In the supine position, the tongue is projected posteriorly by gravity (perhaps displacing the elongated soft palate) and obstructs the hypopharyngeal space. This posterior encroachment by the tongue is counteracted only by the tone of the genioglossal muscle. Thus, a longer tongue is more likely to cause obstruction of the upper airway. Our data also showed that the hyoid bone was more inferiorly positioned in both obese and nonobese patients, as well as anteriorly positioned in obese patients, as also observed in many previous studies.1 11 17 The position of the hyoid bone is important because it serves as a central anchorage for the tongue muscles and thereby partly determines the position of the tongue. The lower position of the hyoid bone may thus be a compensatory mechanism to accommodate the greater tongue volume.8 18 The inferior and anterior displacement of the hyoid bone in obese patients may therefore be the result of the greater tongue mass and the deposition of adipose tissue. In nonobese patients, the hyoid bone was positioned lower as well; however, there was no significant difference in tongue length between nonobese patients and simple snorers. It has been reported that other tongue measurements such as tongue area, and the ratio of the tongue area to the internal maxillary area significantly correlate with MP-H.8 This means that the tongue mass may increase relative to the internal maxillary area in nonobese patients. This relative or absolute increase in tongue volume in the hypopharyngeal area may also interact with abnormal neuromuscular regulatory mechanisms.19 Multiple regression analysis showed that anterior displacement of the hyoid bone in all patients with OSAS and its inferior displacement in nonobese patients were significant determinants for the severity of AHI or desaturation. One report describes sleep apnea in an acromegalic patient with macroglossia, which was successfully treated with reduction plasty of the tongue.20 Tongue-retaining devices, designed to keep the tongue slightly forward, have been shown to substantially reduce the number and duration of apnea periods and normalize disorganized sleep patterns.21

With regard to bony structures in nonobese patients, the anteroposterior width of the bony nasopharynx and oropharynx were significantly reduced compared with that of simple snorers and obese patients. No significant characteristics of bony structures which might contribute to OSAS were found in obese patients. The narrowing of the bony oropharynx significantly correlated with the severity of apnea/hypopnea and desaturation. Multiple stepwise regression analysis confirmed that narrowing of the bony oropharynx is a dominant and independent predictor of AHI and desaturation during sleep. The smaller width of the bony pharynx may reflect a posterior positioning of the maxilla, and together with an enlarged soft palate may contribute to upper airway narrowing. No significant differences were observed in our study between the other bony structures of nonobese patients and simple snorers. Some investigators have reported that the facial A-P distance, as measured by S-N, and ANS-PNS is reduced in nonobese OSAS patients, and G-VL shorter than in obese OSAS patients and normal subjects.5 8 11 18 22 However, some reports1 23 maintain that there are no significant differences in these cephalometric variables between patients with OSAS and simple snorers. Sakakibara et al11 demonstrated a reduction in the facial A-P distance at the cranial base, maxilla, and mandible levels in nonobese Japanese with OSAS compared to nonsnoring control subjects. This indicates that there may be differences in cephalometric variables between snorers and nonsnorers.24 In this study, 46.8% of the Japanese patients with OSAS were nonobese, which was higher than the nonobesity rate of white men with OSAS.15 16 This finding seems to indicate that the characteristics of the craniofacial skeletal anatomy are important risk factors for Japanese for the development of OSAS. A comparison of the cephalometric data for nonobese white men with OSAS and their Japanese counterparts pointed out certain characteristics of the craniofacial skeletal anatomy, although there were no significant differences from those of simple snorers. Nonobese Japanese patients were characterized by wider angles of SNA and SNB, that is, greater maxillomandibular protrusion. Their ANB angle was also wider than that of white men with OSAS, which means that the mandible is more posteriorly positioned relative to the maxilla. The maxillomandibular protrusion in Asian patients with OSAS has been identified as a racial difference in the craniofacial skeletal anatomy.25 The posterior position of the mandible relative to the maxilla may also be a racial characteristic of Japanese OSAS and snorers. It may contribute to the narrowing of the hypopharyngeal space as well as the susceptibility for developing OSAS, because multiple stepwise regression analysis indicated that the ANB angle was an independent predictor of AHI and nocturnal desaturation.

From a cephalometric point of view, obese and nonobese patients with OSAS may be characterized by different pathogeneses. Narrowing of the bony oropharynx, an enlarged soft palate, and shifting of the tongue mass to the hypopharyngeal space may combine to play an important role in the development of OSAS in nonobese patients. In obese patients, however, more extensive and severe enlargement of soft tissues were found such as an enlarged soft palate, an anteriorly positioned hyoid bone, and a longer tongue. However, these findings did not show a significant correlation with the severity of OSAS, nor could a significant regression model be obtained. Only BMI showed a significant correlation with the severity of OSAS. These findings suggest that soft-tissue enlargements do not occur independently and are closely associated with obesity. In other words, the cephalometric characteristics found in obese patients were mainly the result of the deposition of adipose tissue in the upper airway. Adipose tissue may thus play an important role in the development of OSAS and may aggravate the severity of OSAS in obese patients.

In conclusion, the characteristics of craniofacial bony structures such as narrowing of the nasopharynx and oropharynx and of enlargement of soft tissue in the upper airway may be important risk factors for the development of OSAS in nonobese patients. In obese patients, soft-tissue enlargement in the upper airway resulting from the deposition of adipose tissue may play an important role in the development of OSAS.


   Footnotes
 
Abbreviations: AHI = apnea-hypopnea index; BMI = body mass index; OSAS = obstructive sleep apnea syndrome; %SpO2< 90% = percentage of total sleep time with pulse oximetric saturation < 90%

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (e-mail: permissisons{at}chestnet.org).

Received for publication June 5, 2002. Accepted for publication January 29, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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