J Med Dent Sci 2010； 57： 147－154

Corresponding Author: Risa TamuraGeneral Dentistry, Department of Comprehensive Oral Health Care, Division of Oral Health Sciences, Graduate School Tokyo Medical and Dental University 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-0034, JapanTel & Fax: +81-3-5803-5765E-mail: yellowcube.gend@tmd.ac.jpReceived January 29；Accepted March 12, 2010

Original Article

Association between positional changes in laboratory values and severity in subjects with obstructive sleep apnea syndrome

Risa Tamura1, Takashi Ono2,3, Mitsuo Sato4, Makoto Hasegawa1, Keiji Moriyama2,3 and Kouji Araki5

1) General Dentistry, Department of Comprehensive Oral Health Care, Division of Oral Health Sciences, Graduate School, Tokyo Medical and Dental University2) Maxillofacial Orthognathics, Graduate School, Tokyo Medical and Dental University3) “International Research Center for Molecular Science in Tooth and Bone Diseases”, Global Center of Excellence (GCOE) Program, Tokyo Medical and Dental University4) Behavioral Dentistry, Department of Comprehensive Oral Health Care, Division of Oral Health Sciences, Graduate School, Tokyo Medical and Dental University5) Center for Education Research in Medicine and Dentistry, Tokyo Medical and Dental University

Key words: obstructive sleep apnea syndrome; OSAS severity; cephalometric radiograph; facial axis; neck depth

INTRODUCTION

  Obstructive sleep apnea syndrome (OSAS) is characterized by recurrent obstruction or narrowing of the upper airway during sleep. Gravitational pull against oropharyngeal soft tissue such as the tongue, soft palate and uvula, and sleep-related depression of the muscle tone,1 are responsible for this condition. Nasal cont inuous posit ive airway pressure and oral appliances have been established as effective treatment modalities of OSAS. The etiology and common risk factors for OSAS include obesity, middle-age, male gender and a constricted mandible 2.  Upper airway obstruction mainly occurs in the supine position during sleep, whereas clinical examinations are usually performed in the upright position while the subject is awake. Several papers have examined positional changes in cephalometric measurements3-5 and nasal resistance is also influenced by body position. Shepard et al.6 found that the expiratory nasal resistance in subjects with OSAS increases when the body position is altered from upright to supine. This may occur because the oropharyngeal soft t issue compromises the upper airway due to gravity7.  The aim of the study was to investigate the association between the difference (defined as the remainder, Rm) in laboratory values in the upright and

  Introduction : The aim of the study was to investigate the association between the difference (defined as the remainder, Rm) in laboratory values determined in the upright and supine positions and the severity of obstructive sleep apnea syndrome (OSAS). Materials and Methods: Thirty-three Japanese male subjects with OSAS [apnea/hypopnea index (AHI: the number of apneas and hypopneas per hour) ≥ 5] underwent cephalometric analysis and measurements of nasal resistance in the upright and supine positions. Several parameters in a dental model and physical features were also analyzed. Results: Significant associations of the logarithmic AHI, with neck depth, Rm for the facial axis, and the minimum airway behind the tongue in the supine position were found in multiple linear regression analysis. Conclusion: Our results suggest that neck depth, Rm for the facial axis and the minimum airway behind the tongue in the supine position may be determinants of the severity of OSAS.

148 J Med Dent SciR. Tamura et al.

supine positions and the severity of OSAS. A second goal was to stimulate cooperation between the medical and dental fields in the diagnosis and treatment of OSAS.

MATERIALS AND METHODS

Subjects  Thirty-three Japanese male subjects with OSAS par-ticipated in the study. The subjects underwent full-night polysomnography at sleep clinics and were diagnosed with OSAS [apnea/hypopnea index (AHI: the number of apneas and hypopneas per hour2.) ≥ 5 /h]. They were then referred to the Department of Dental Sleep Medi-cine, Tokyo Medical and Dental University Dental Hos-pital, for treatment. The study was approved by the in-stitutional ethics committee (approval number: 396) and all subjects provided written informed consent. Inclu-sion criteria were subjects with established molar oc-clusion and without continuum missing teeth on the maxillary and mandibular arches. The subjects were classified into subgroups according to the severity of OSAS in reference with the guideline reported by the American Academy of Sleep Medicine Task Force8; 14 subjects were mild OSAS (5 ≤ AHI < 15), 11 were moderate OSAS (15 ≤ AHI < 30) and 8 were severe OSAS (30 ≤ AHI) (Table 1).

Body position and pillow height  Subjects were requested to assume their most relaxed head and neck positions with their back straight on a dental chair in the sitting position. In the supine position, they were asked to lie down on the dental chair or a wooden bed with a soft mat (only for recording of the supine cephalometric radiograph). The same examiner measured the neck and occipital depths in the relaxed standing position in each subject using a “Press-shaper” (Fig. 1; Nishikawa Sangyo Co., Ltd., Tokyo) , just i f ied with i ts lower border at the

suprascapular level and held against the subject’s back. A standard pillow (neck height: 6 cm, occipital height: 4 cm, content: polystyrene beads, Nishikawa Sangyo) was adjusted to fit the neck and occipital depths in each subject with or without use of an

VariableTotal (n=33) Mild OSAS (n=14) Moderate OSAS (n=11) Severe OSAS (n=8)

Mean±SD Range Mean±SD Range Mean±SD Range Mean±SD Range

Age (year) 52.9±13.8 28.0-75.0 47.7±16.9 28.0-75.0 54.6±11.2 36.0-74.0 59.6±6.8 48.0-67.0

Height (cm) 170.2±5.4 159.0-181.0 172.2±4.8 164.0-181.0 169.3±4.2 164.0-177.5 167.8±7.2 159.0-181.0

Weight (kg) 69.9±8.9 55.0-96.0 72.3±11.3 58.0-96.0 69.4±5.4 60.0-75.0 66.6±8.0 55.0-82.0

BMI (kg/m2) 24.1±2.3 20.1-30.8 24.3±3.1 20.1-30.8 24.2±1.5 22.3-26.9 23.6±1.3 21.8-25.5

AHI (events/h) 24.0±17.6 5.1-78.7 11.2±3.2 5.1-14.9 21.7±3.5 16.7-26.0 49.7±16.9 30.7-78.7

Figure 1 : Apparatus for laboratory measurements. (a) Device for measuring neck (lower arrow) and occipital (upper arrow) depths. (b) Standard pillow and adjustable seat.

Table 1. Demographic data. AHI (apnea hypopnea index), the number of apneas and hypopneas per hour; Mild OSAS, 5 ≤ AHI < 15; moderate OSAS, 15 ≤ AHI < 30; severe OSAS, 30 ≤ AHI

(b)

(a)

149Positional changes and severity of obstructive sleep apnea syndrome

adjustable seat (Fig. 1; height: 1 cm, fabric: urethane foam, Nishikawa Sangyo). Normal respiration is occasionally disturbed in the supine position due to the gravitational difference to the head and neck area by the positional change. The pillow fills a gap between the bed and the neck curvature because of its shock-absorbing function. Individualization of the pillow height was designed to stabilize cervical vertebra and yield relaxation on the electroencephalogram, resulting in decreased muscle tone of the neck and shoulders9, 10. Thus, we attempted to minimize the influence of excessive neck flexure on the upper airway.

Neck circumference  The neck circumference of each subject at the level of the cricothyroid cartilage was measured in the upright and supine positions.

Cephalometric radiographs  Supine and upright cephalometric radiograms were

taken with the jaw relaxed to mimic the mandibular position during sleep. The upright radiogram was taken in the natural head position, whereas the supine radiogram was taken while the subject was lying on a wooden bed with a soft mat, with the head placed on the adjusted pillow. In each body position, the ear rods were not inserted into the bilateral external auditory meatuses. Subjects were requested to swallow their saliva, and the radiograph was taken at the end of expiration. All cephalometric radiograms were analyzed through measurements of 12 parameters related to the mandibular position in the Ricketts’ cephalometric analysis11 (Fig. 2) and 8 parameters that reflect the status of the airway and the hyoid bone (Fig. 3).

Figure 2 : Ricketts’ cephalometric analysis. 1, Overjet (horizontal overlap of upper and lower incisor teeth); 2, overbite (vertical overlap of upper and lower incisor teeth); 3, inter-incisal angle; 4, lower facial height; 5, occlusal plane to ramus (Xi to occlusal plane); 6, occlusal plane inclination; 7, facial height; 8, facial axis; 9, facial taper; 10, mandibular plane angle; 11, ramus position; 12, mandibular arc. Abbreviations: N, nasion; Or, orbitale; Ba, basion; Pog, pogonion; Po, porion; Gn, gnathion; ANS, tip of the anterior nasal spine; CF, polar center; Pt, pterygoid; PTV, pterygoid vertical (point Pt to FH plane); Xi, ramus center.

Figure 3 : Landmarks and parameters for cephalometric analysis of the upper airway and hyoid bone. 1, Most anteroinferior point on the third cervical vertebra; 2, the point on the posterior pharyngeal wall where the postpalatal airway is at its narrowest; 3, the point on the posterior pharyngeal wall opposite the tip of the soft palate; 4, the point on the posterior pharyngeal wall where the postlingual airway is at its narrowest; 5, the point on the posterior surface of the soft palate where the postpalatal airway is at its narrowest; 6, the tip of the soft palate; 7, the point on the posterior surface of the tongue where the postlingual airway is at its narrowest; 8, most anterior point on the tongue; 9, the tip of the upper incisor; 10, the most anterior point on the hyoid bone. Point 2 to point 5, minimum airway behind the soft palate; point 3 to point 6, minimum airway at tip of the soft palate; point 4 to point 7, minimum airway behind the tongue; point 10 to Go, hyoid-Go; point 10 to Me, hyoid-Me; point 1 to point 10, third cervical vertebra-hyoid; PNS to point 6, soft palate length; point 8 to point 9, tongue-upper incisal edge. Abbreviations: Go, gonion; Me, menton; PNS, tip of the posterior nasal spine.

150 J Med Dent SciR. Tamura et al.

Nasal Resistance  A multifunctional spirometer HI-801 (Chest M.I., Inc., Tokyo) was used to measure nasal resistance in the upright and supine positions using the anterior-mask method. Since the expiratory nasal resistance has been reported to change in association with the body position12, this value was used for analysis.

Model analysis  Alginate impressions of the upper and lower dentitions were taken and plaster models were made for each subject. Model analysis was performed using 13 parameters (Fig. 4) including the dental arch sizes, which have previously been shown to be significantly correlated with oral volume13 and tongue size14.

Statistical analysis  Rm values were calculated as differences between laboratory values recorded in the upright and supine positions. One-way analysis of variance and multiple comparison of Tukey HSD were used to determine the significance of the association of laboratory mean values with the severity of OSAS. Correlations between laboratory values and the normal-distributed AHI, calculated in the logarithm (log-AHI), which has the relationship with the severity of OSAS, were examined by Pearson correlation analysis. Stepwise method of multiple linear regression analysis was used to examine the strength of relationships between Rm or laboratory values and the log-AHI. All analyses were performed using SPSS for Windows (v. 18.0, SPSS Inc., Chicago, IL, USA).

RESULTS

  Significant differences for mean of neck depth were found between subjects with mild and moderate OSAS and between those with mild and severe OSAS (Table 2). For measurements in the supine position, mean of facial depth differed significantly between subjects with moderate and severe OSAS, and mean of point 4-7 differed significantly between those with mild and severe OSAS (Table 2). Significant correlations of log-AHI were found with facial depth in the upright position, mandibular arc in both the upright and supine position, point 4-7 in the supine position, maxillary arch length, mandibular arch length, neck depth and occipital depth. Multiple linear regression analysis revealed that neck depth, Rm for the facial axis, and point 4-7 in the supine position were significant independent variables associated with the log-AHI (Table 3).

DISCUSSION

  Kondo et al. have shown that the volumetric ratio between the tongue and oral cavity is significantly larger in subjects with OSAS than in those without OSAS using magnetic resonance imaging (MRI)15. MRI is effective for diagnosis of obstruction or narrowing in the oropharyngeal area, but it also has several disadvantages, including a long acquisition time, artifacts caused by metallic restoration, contraindications for claustrophobic subjects, and the expense of the facility. Hence, we sought a more convenient, low-cost, and specific method for diagnosis of OSAS.

Figure 4 : Model analysis. Distance between bilateral 1, Deepest point of palatal side, upper canine (U3N); 2, buccal cusp, upper first premolar (U4); 3, deepest point of palatal side, upper first premolar (U4N); 4, deepest point of palatal side, upper first molar (U6N); 5, cusp, lower canine (L3); 6, deepest point of lingual side, lower canine (L3N); 7, buccal cusp, lower first premolar (L4); 8, deepest point of lingual side, lower first premolar (L4N); 9, buccal cusp, lower second premolar (L5); 10, deepest point of lingual side, lower second premolar (L5N); 11, mesial buccal cusp, lower first molar (L6); 12, maxillary arch length; 13, mandibular arch length

151Positional changes and severity of obstructive sleep apnea syndrome

ItemMild vs. Moderate

Moderate vs. Severe

Mild vs. Severe

Correlation with log-AHI

Age 0.411 0.702 0.125 0.066

BMI 0.993 0.841 0.768 0.413

Neck depth 0.023* 1.000 0.042* 0.003**

Occipital depth 0.502 0.704 0.165 0.033*

Maxillary arch length 0.587 0.983 0.529 0.045*

Mandibular arch length 0.078 0.952 0.208 0.020*

ItemMild vs. Moderate Moderate vs. Severe Mild vs. Severe Correlation with log-AHI

Rm Up Sp Rm Up Sp Rm Up Sp Rm Up Sp

Neck circumference 0.655 0.834 0.998 0.855 0.897 0.992 0.968 0.998 0.997 0.833 0.844 0.801

Overjet 0.945 0.952 0.988 0.937 0.804 0.876 0.997 0.920 0.923 0.824 0.871 0.765

Overbite 0.924 0.750 0.739 1.000 0.497 0.496 0.944 0.855 0.862 0.922 0.626 0.736

Inter-incisal angle 0.761 0.798 0.884 0.948 0.957 0.986 0.602 0.658 0.821 0.269 0.216 0.342

Lower facial height 0.821 0.423 0.273 0.629 0.975 0.981 0.906 0.363 0.444 0.974 0.090 0.080

Occlusal plane to ramus 0.962 0.597 0.422 0.598 0.874 0.378 0.717 0.928 0.963 0.624 0.805 0.889

Occlusal plane inclination 0.525 0.215 0.137 0.389 0.989 0.515 0.915 0.346 0.807 0.996 0.190 0.395

Facial depth 0.157 0.622 0.741 0.157 0.436 0.030* 0.962 0.095 0.098 0.910 0.045* 0.072

Facial axis 0.984 0.985 0.915 0.070 0.276 0.883 0.077 0.190 0.990 0.052 0.090 0.922

Facial taper 0.798 0.698 0.645 0.899 0.972 0.991 0.992 0.597 0.614 0.717 0.514 0.504

Mandibular plane angle 0.187 0.673 0.994 0.383 0.739 0.450 0.972 0.279 0.368 0.841 0.210 0.273

Ramus position 0.520 0.999 0.546 0.190 0.903 0.107 0.660 0.912 0.440 0.542 0.805 0.424

Mandibular arc 0.229 0.552 0.116 0.143 0.520 1.000 0.864 0.105 0.157 0.762 0.041* 0.022*

Point 2-5 0.761 0.930 0.468 0.951 0.573 0.280 0.943 0.745 0.848 0.741 0.823 0.942

Point 3-6 0.996 0.312 0.125 0.875 0.295 0.330 0.824 0.968 0.946 0.911 0.705 0.711

Point 4-7 0.998 0.583 0.562 0.154 0.996 0.275 0.145 0.586 0.038* 0.142 0.201 0.012*

Point 10-Go 0.271 0.906 0.662 0.320 0.423 0.966 0.994 0.617 0.549 0.808 0.382 0.218

Point 10-Me 0.887 0.990 0.978 0.295 0.838 0.857 0.480 0.885 0.926 0.674 0.560 0.800

Point 1-10 0.968 1.000 0.981 0.132 0.936 0.692 0.167 0.921 0.769 0.134 0.921 0.263

PNS-point 6 0.995 1.000 0.997 0.924 0.987 0.927 0.880 0.984 0.894 0.228 0.905 0.385

Point 8-9 0.979 0.642 0.771 0.848 0.951 0.988 0.918 0.869 0.716 0.965 0.240 0.288

Nasal resistance 0.268 0.662 0.390 0.667 0.684 0.865 0.855 0.234 0.204 0.861 0.208 0.260

Table 2. Comparisons in OSAS severity and correlation between all items and the log-AHI. Comparisons in OSAS severity were performed by one-way analysis of variance, multiple comparison of Tukey HSD and correlation were examined by Pearson correlation analysis. Each data were shown in p-value.Rm, remainder of measured value; Up, measured value in upright position; Sp, measured value in supine position. *: p<0.05, **: p<0.01

152 J Med Dent SciR. Tamura et al.

  We found that three parameters, neck depth, facial depth in the supine position, and point 4-7 in the supine position, showed a significant difference between the severity of OSAS. Bivariate correlations were found for two of these parameters (i.e., neck depth and point 4-7 in the supine position), and six others (i.e., occipital depth, maxillary arch length, mandibular arch length, mandibular arc in both upright and supine position and facial depth in the upright position). These eight parameters with Rm for the facial axis, which showed a tendency of correlation with the log-AHI, were analyzed by the stepwise method of the multiple linear regression analysis with the log-AHI as the dependent variable. Indeed, a previous study showed the facial axis in the upright position was a significant determinant of OSAS18. It was thus assumed that the Rm for the facial axis might have a possible relationship with OSAS. This led us to include the Rm for the facial axis in the multiple linear regression analysis. As a result, significant associations were found for neck depth, Rm for the facial axis, and point 4-7 in the supine position, while the other parameters were eliminated. To explain this contradiction, partial correlation analysis was performed using the nine parameters. True significant correlations were found for Rm for the facial axis with AHI (p=0.023), and for Rm for the facial axis (p=0.028) and point 4-7 in the supine position (p=0.043) with the severity of OSAS.

Neck circumference  The absence of a relationship between neck circumference and the severity of OSAS found in this

study differs from findings in a previous study in which the subjects were older and had a greater BMI16. These differences may account for the discrepancy between the two studies, since neck circumference is influenced by reduced metabolism that leads to obesity and a decrease in muscle tone. Sasanabe et al.17 also studied neck circumference in subjects with and without OSAS, but did not examine the relationship with the severity of OSAS. Despite the association of neck circumference and OSAS reported in many studies, we found no significant relationship of the severity of OSAS (i.e., AHI and log-AHI) with neck circumference in each body position or with the Rm value. This may be attributable to the homogeneity of BMI in our subjects, since neck circumference is influenced by obesity.

Nasal resistance  Narrowing and obstruction of the upper airway caused by posterior displacement of the tongue and soft palate by gravitational pull or tissue swelling are significant factors that increase nasal resistance. In the positional change from upright to supine, engorgement and swelling of the nasal tissue occurs due to leveling with the heart, which may induce upper airway narrowing and obstruction. In our study, an increase in nasal resistance was found in most subjects in association with the change in body position, but no correlation was found between nasal resistance and the log-AHI.

Ricketts’ cephalometric analysis  A significant difference in the facial axis between subjects with and without OSAS has been reported18. This indicates that Ricketts’ cephalometric analysis is useful for identifying characteristic craniofacial morphology in subjects with OSAS. However, the previous study was performed using a standard cephalometric radiograph taken in the upright position, and without consideration of the severity of OSAS18. In contrast, we recorded upright and supine cephalometric radiographs taken with a natural head position and focused on Rm values. Our results confirm that the facial axis is an important factor in diagnosis of OSAS. Previous studies have also reported a significant difference in facial depth in subjects with and without OSAS18, 19, but we found no true relationship between facial depth and log-AHI in multiple linear regression analysis. Despite that there were no significant correlations in mandibular arc in subjects with and without OSAS reported in previous studies18, 19, we found significant correlations of the severity of OSAS

Standard regression coefficient

Neck depth 　0.459**

Rm for the facial axis -0.372**

Point 4-7in the supine position -0.334*

Occipital depth NS

Facial depth in the upright position NS

Mandibular arc in the upright position NS

Mandibular arc in the supine position NS

Maxillary arch length NS

Mandibular arch length NS

Multiple correlation coefficient (R) 　0.710**

Determination coefficient (R2) 　0.504**

Table 3. Associations with the log-AHI in mutiple linear regression analysis. Stepwise method; F(3,29)=9.823, p<0.001. *: p<0.05, **: p<0.01, NS: not significant

153Positional changes and severity of obstructive sleep apnea syndrome

(i.e., AHI and log-AHI) with mandibular arc in each body position.

Cephalometric analysis of the upper airway and hyoid bone  There was a significant difference in point 4-7 in the supine position between subjects with mild and moderate OSAS, and this value was also correlated with the log-AHI. Moreover, a statistically significant relationship (p=0.025) between point 4-7 in the supine position and log-AHI was found in multiple linear regression analysis. However, a previous report found no significant relationship of cephalometric variables in the upper airway and hyoid bone with severity of OSAS20.  The significance of upper airway and hyoid variables may be influenced by the conditions under which radiographs are taken and may also depend on ethnic differences in craniofacial morphology. No Rm values for cephalometric variables related to the upper airway and hyoid bone showed a significant correlation with the log-AHI. However, a significant relationship between point 4-7 in the supine position and log-AHI was found in multiple linear regression analysis. Thus, we believe that supine cephalometry is superior to conventional upright cephalometry for evaluation of subjects with OSAS.

Model analysis  Subjects with OSAS have been reported to have narrower and shorter dental arches compared to healthy controls21, 22. We found that there was no significant difference in the parameters of a model analysis with reference to the severity of OSAS, except for correlations with the maxil lary arch length (r =-0.351, p =0.045) and mandibular arch length (r=-0.403, p=0.020).

Clinical significances of the findings   The neuromuscular system involuntarily secures the human upper airway. Based on the definition of a “retro-excursion margin” constructed from the mandible, the hyoid bone and the tongue-soft tissue complex, a different retro-excursion margin may be present in subjects with and without OSAS. Our findings that an increase in neck depth, a decrease in Rm for the facial axis, and a decrease in point 4-7 in the supine position were significantly associated with increased log-AHI which has the relationship with the severity of OSAS may be explained in light of the retro-excursion margin, as follows. A subject with OSAS advances the chin with

the head tilted as the log-AHI increases. On the other hand, posterior displacement of the mandible, the hyoid bone and the tongue-soft tissue complex against the upper airway decreases with a positional change. This indicates that the range of the retro-excursion margin decreases as the log-AHI increases. This, in turn means that the mandible, hyoid bone and tongue-soft tissue complex in subjects with lower log-AHI may originally be set anteriorly and that the range of action may be greater than that in subjects with higher log-AHI. This may account for the differential effectiveness of oral appliances. Further studies are needed to confirm the relationship between laboratory values and the AHI or severity of OSAS and to investigate the dependence of the effect of oral appliances on the severity of OSAS from the perspective of the retro-excursion margin.

CONCLUSION

  Our results suggest that neck depth, Rm for the facial axis and the minimum airway behind the tongue in the supine position may be determinants of the severity of OSAS.

ACKNOWLEDGEMENTS

  We thank Ryuji Chiba and Hiroshi Tanaka (Tokyo Medical and Dental University, Dental Hospital, Department of Oral and Maxillofacial Radiology) for recording of X-rays; Shuhei Nakamura, Kaori Harada, Ayaka Inakazu and Shirou Mataki (Tokyo Medical and Dental University, Dental Hospital, Department of Oral Diagnosis and General Dentistry / Dental Sleep Clinic) for clinical support; Yoshiyuki Sasaki (Tokyo Medical and Dental University, Faculty of Dentistry, Center for Education and Research in Oral Health Care) for statistical advice; and Nishikawa Sangyo Co.,Ltd., (Tokyo) for providing the tools for this study.

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