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Department of Anesthesiology (B1), Graduate School of Medicine, Chiba University, Chiba 260-8670, Japan
Submitted 23 April 2003 ; accepted in final form 24 July 2003
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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airway; pharynx; obstruction; collapsibility; closing pressure
Airway obstruction at the VP leads to development of strong negative airway pressure owing to contraction of inspiratory pump muscles at the downstream region, such as the OP airway. This negative pressure causes subsequent OP narrowing during obstructive apnea in accordance with OP collapsibility as demonstrated by dynamic upper airway imaging studies (12, 15). The fact that the dorsum of the tongue is in apposition with the anterior wall of the soft palate during nasal breathing in humans (10) suggests the existence of dynamic interaction between the tongue and soft palate during obstructive apnea. Furthermore, the collapsing forces exerted from the tongue onto the soft palate may be greater in patients with a more posteriorly located tongue or with a more collapsible OP airway. We hypothesized that the dorsum of the tongue pushes the anterior wall of the soft palate posteriorly during inspiratory efforts, maintaining VP closure, particularly in patients with collapsible OP airway. To test the hypothesis, we measured pressure between dorsum of the tongue and anterior wall of the soft palate (PT&P) during experimentally induced obstructive apnea in anesthetized patients with sleep-disordered breathing (SDB) and consequently assessed the influence of OP airway collapsibility by the pattern of PT&P changes.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Informed consent was obtained from all subjects after the aim and potential risks of the study were fully explained to each. The Institutional Ethics Committee approved the investigation.
Evaluation of interaction between the tongue and soft palate during obstructive apnea. All patients were premedicated with 0.5 mg atropine given intravenously before induction of anesthesia. The study was performed with each subject in a supine position on an operating table, with the neck in a neutral position while SaO2, electrocardiogram, and blood pressure were monitored. A modified tight-fitting nasal continuous positive airway pressure (CPAP) mask was fitted on each subject. Anesthesia was induced with a bolus injection of 2 mg/kg propofol and maintained with a continuous infusion of propofol at a rate of 5–10 mg/kg. Positive-pressure ventilation was performed by a BiPAP machine (BiPAP, Respironics, Murrysville, PA). Oxygen at a flow rate of 10 l/min was mixed with air delivered by the BiPAP apparatus to maintain hyperoxemia during the experiment. After intravenous administration of succinylcholine (1 mg/kg), a thin polyethylene catheter with a side hole (6-Fr-diameter catheter, ATOM, Tokyo, Japan) was inserted through the vocal cords into the trachea by a laryngoscope. Lateral pressure of the trachea (Ptr) was measured by connecting the catheter to a pressure transducer (23NB 005G; ICsensors, San Jose, CA). PT&P was measured by an air-filled flat balloon catheter (1.5 cm x 1.5 cm polyethylene film) placed on the center of anterior wall of the soft palate, connected to a pressure transducer (23NB 005G; ICsensors). Correct position of the air-filled flat balloon was confirmed by direct observation with a laryngoscope. The balloon was inflated with 0.2 ml of air. Spontaneous breathing was then allowed to resume, and the CPAP was set at a level that prevented development of inspiratory flow limitation. Mask airway pressure (Pmask) was measured by a pressure transducer (23NB 005G; ICsensors). Ventilatory airflow was measured by a Fleisch no. 2 pneumotachograph connected to a nasal CPAP mask (4719, Hans Rudolph, Kansas City, MO) and a differential pressure transducer (TP-603T; Nihon Koden, Tokyo, Japan). Obstructive apnea for 
60 s was induced by abrupt reduction of Pmask to atmospheric pressure. All the respiratory variables before, during, and immediately after airway occlusion were recorded on an eight-channel thermal array recorder (WS 682G; Nihon Koden).
Evaluation of static pharyngeal mechanics. Our endoscopic technique and evaluation of static pharyngeal mechanics were described in a previous report (4, 5). Briefly, after completion of the measurements during dynamic pharyngeal occlusion, a muscle relaxant (vecuronium 0.2 mg/kg) was injected to produce complete paralysis throughout evaluation of the static mechanics. The pressure catheters for measurements of the PT&P and Ptr were removed, and a slim endoscope (FB 15H, Pentax, Tokyo, Japan; 3 mm OD) was inserted through the nasal mask and naris without air leak. The tip of the scope was placed at the upper airway to visualize the VP and OP. A closed-circuit camera (ETV8, Nisco, Saitama, Japan) was connected to the endoscope to record the pharyngeal images and airway pressures (Paw), measured by a water manometer, on videotape for later analysis.
To determine the pressure-area relationship of the pharynx, the BiPAP machine was disconnected from the nasal mask, which was then connected to a pressure control system capable of accurately producing a constant, preselected Paw ranging from –20 to +20 cmH2O in steps of 1 cmH2O. Cessation of mechanical ventilation resulted in apnea resulting from complete muscle paralysis. Paw was immediately increased and maintained at 20 cmH2O. While the subject remained apneic for 2–3 min, Paw was slowly reduced from 20 cmH2O to the VP closing pressure, the pressure at which the VP was seen to close completely. SaO2 remained above 95% throughout this apneic test in all subjects. This procedure of experimentally induced apnea allowed construction of static pressure-area relationship of the visualized pharyngeal segment. Distance between the tip of the endoscope and the narrowing site was measured by a wire passed through the aspiration channel of the endoscope. Measurements were taken for both VP and OP.
To convert the monitor image to an absolute value of the cross-sectional area of the pharynx, magnification of the imaging system was estimated at 1.0-mm interval distances between the endoscopic tip and the object in the range of 5–30 mm. At a defined value of Paw, the image of the pharyngeal lumen was traced and the pixels included in the area were counted (SigmaScan version 2.0, Jandel Scientific Software, San Rafael, CA). The pixel number was converted to a pharyngeal cross-sectional area according to the distance-magnification relationship. Using tubes of known diameter, we tested the accuracy of our cross-sectional area measurements (5). For a constant distance, the measured areas were systematically deviated from actual areas. Largest known area tested (0.95 cm2) was underestimated by 11% because of image deformation at the outer image area, and the smallest known area tested (0.03 cm2) was overestimated by 13% because of reduction of the image resolution. The measured luminal cross-sectional area was plotted as a function of Paw. Closing pressure was defined as pressure corresponding to the zero area. At high values of Paw, relatively constant cross-sectional areas were revealed; therefore, maximum area (Amax) was determined as the mean value of the highest three Paw values (18, 19, and 20 cmH2O). As reported previously (4, 5), the pressure-area relationship of each pharyngeal segment was fitted by an exponential function, A = Amax – B x exp(–K x Paw), where A is area and B and K are constants. A nonlinear least squares technique was used for the curve fitting, and the quality of the fitting was provided by coefficient R2 (SigmaPlot version 2.0, Jandel Scientific Software). A regressional estimate of closing pressure 
, which corresponds to an intercept of the curve on the Paw axis, was calculated from the following equation for each pharyngeal segment: 
.
On the basis of our previous findings, abnormal collapsibility of each pharyngeal segment was defined as 
, which allowed determination of pharyngeal closure types in patients with SDB. Patients with exclusively at the VP were classified as the VP-only group, and those with at both VP and OP were classified as the VP+OP group.
Statistical analysis. Mann-Whitney rank sum tests were performed for group comparisons. Changes in PT&P values during obstructive apnea were assessed by Friedman repeated-measures analysis of variance on ranks, and multiple comparisons were performed by the Student-Newman-Keuls method. The Spearman rank-order test was performed for correlation analyses between variables obtained during dynamic pharyngeal obstruction and anthropometric and oximetry data and static mechanics variables. P < 0.05 was considered to be significant. All values are expressed by median (25 to 75 percentiles).
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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at the velopharynx only and 6 demonstrated at both the velopharynx and oropharynx, as determined by pharyngeal endoscopy under general anesthesia with total paralysis. The patients were classified as the VP-only group and as the VP+OP group, respectively, according to our definitions of pharyngeal closure types. During the experimentally induced obstructive apnea, various patterns of PT&P changes were revealed (Figs. 1, 2, and 3). Figure 1 presents changes in the respiratory variables during obstructive apnea in a patient of the VP-only group together with static pressure-area relationships of the passive pharynx. Abrupt reduction of Pmask to atmospheric pressure resulted in obstructive apnea. In accordance with the Ptr changes, the negative pressure deflection of the PT&P tracing gradually augmented during obstructive apnea. In contrast, totally different PT&P changes were measured in a patient of the VP+OP group (Fig. 2). PT&P gradually increased during obstructive apnea whereas negative pressure deflection of Ptr augmented during the period. Interestingly, positive deflections of PT&P were observed in accordance with negative Ptr deflections in inspirations indicated by arrows in Fig. 2. This positive PT&P deflection pattern was more clearly demonstrated in another patient of the VP+OP group (Fig. 3). This positive PT&P deflection pattern was identified in five of six patients of the VP+OP group whereas none of the VP-only group demonstrated this pattern (P < 0.05).
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Body habitus and nocturnal oxygenation. Table 1 presents the body habitus and nocturnal oxygenation data for all patients. No statistical differences were found in age, height, weight, or severity of nocturnal oxygenation between the two groups. body mass index of the VP-only group was significantly greater than that of the VP+OP group. No oximetry variables correlated with pharyngeal closure types and static mechanical variables.
Static pharyngeal mechanics of the passive pharynx. Table 2 presents static mechanical properties of the passive pharynx for all patients. With the patient classification method used in this study, oropharyngeal closing pressure 
of the VP+OP group was above atmospheric pressure and significantly greater than that of the VP-only group. Velopharyngeal closing pressure 
of the VP+OP group was also significantly greater than that of the VP-only group. Maximum cross-sectional area at the oropharynx [Amax(OP)] tended to be smaller in the VP+OP group than the VP-only group (P = 0.08). No other variables differed between the groups.
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Dynamic interaction between the tongue and soft palate during obstructive apnea. In consideration of the variable changes in PT&P during obstructive apnea, PT&P was measured at end expiration of the first, fifth, and tenth breaths (E-1, E-5, and E-10, respectively). For subsequent inspiratory phases of these expiratory measurements, PT&P values at the peak of the inspiratory effort were measured (I-1, I-5, and I-10, respectively). Increment or decrement of these PT&P values during the period (from first to tenth breaths) was calculated for each respiratory timing [
PT&P-E = (E-10–E-1), PT&P-I = (I-10–I-1)] (Fig. 1).
Regardless of the pharyngeal closure types, all patients had positive end-expiratory PT&P, indicating close apposition of the tongue and soft palate at the end of expiration during obstructive sleep apnea. Both end-expiratory and peak-inspiratory PT&P progressively increased during obstructive apnea in the VP+OP group, whereas no significant change was observed in the VP-only group (Fig. 4). Reduction of PT&P during inspiratory effort evidenced by the progressive increase in PT&P differences during inspiratory effort for each breath [PT&P(E)–PT&P(I)] was indicated in patients of the VP-only group (Fig. 5). In contrast, significant increase in the PT&P values during inspiratory effort was evidenced by progressive decrease in the PT&P differences during inspiratory effort in the VP+OP group (Fig. 5).
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Factors influencing dynamic interaction between the tongue and soft palate. Table 3 presents results of the correlation analyses among the variables of body habitus, static pharyngeal mechanics, and PT&P. PT&P-E was significantly correlated with age and inversely correlated with Amax(OP), indicating that increase in end-expiratory PT&P values during obstructive apnea occurs in older patients with smaller Amax(OP). PT&P-I was significantly correlated with 
and 
and inversely correlated with Amax(OP) and body mass index. In other words, significant dynamic interaction between the tongue and soft palate during obstructive apnea occurs in less obese patients with smaller Amax(OP) and higher collapsibility both at the velopharynx and oropharynx (Fig. 6).
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Study design and limitation of the study. Although a standard polysomnography, including respiratory as well as sleep parameters, was not performed, nocturnal oximetry was performed. It is our belief that OSA can be safely diagnosed through oximetry data and clear clinical symptoms (3, 9). In this study, the nature and severity of SDB do not seem to be well characterized. However, the main purpose of this study was not to investigate the pathogenesis of OSA. The anesthetized patients with SDB were used as a human model, allowing us to explore the mechanisms of obstructive apnea in human subjects.
No previous study measured the PT&P in humans. Accuracy of the pressure measurement with an air-filled balloon catheter depends on the inflating air volume. Accordingly, absolute PT&P values are possibly overestimated because of space occupied by the balloon between the structures, although changes in PT&P values during obstructive apnea are not artifacts and should reflect the rate of changes of contact pressure. However, we believe that the influence of the space occupied by the balloon on PT&P measurement is negligible, because the inflation air volume was limited to 0.2 ml and the thin balloon (0.9 mm thickness on average) was placed between the compliant soft tissues.
Because the experiments were performed under general anesthesia, our results do not directly apply to behavior of the upper airway during sleep in patients with SDB. Obstructive apnea occurring either during sleep or general anesthesia, however, appears to have common mechanisms. Both sleep and anesthesia depress the upper airway muscle activity more than the activity of the diaphragm, leading to increase in collapsing forces to the upper airway (7, 13). In fact, our laboratory (4) previously reported significant association between severity of SDB and upper airway collapsibility assessed during anesthesia, and Eastwood et al. (2) recently confirmed this. Although the reflexive increase in the upper airway muscle activity during obstructive apnea could influence the interaction between the tongue and soft palate, increase in the PT&P during the obstructive apnea indicates that the augmentation of the upper airway muscle activity during obstructive apnea contributes little, at least, in anesthetized SDB patients such as adult SDB patients during sleep (11).
Dynamic interaction between tongue and soft palate. We found positive PT&P values at end expiration in all SDB patients, indicating close apposition between tongue and soft palate at the end of expiration, in accordance with the findings of Rodenstein and Stanescu (10), who observed close apposition of these structures in normal awake subjects during nasal breathing. Because our study did not include normal subjects, our results do not indicate that the SDB patients have higher PT&P values than normal subjects, whereas higher PT&P values should suggest greater posterior forces on the soft palate.
More importantly, varied extent of dynamic interaction between tongue and soft palate was indicated by the patterns of PT&P changes during obstructive apnea. Supporting our initial hypothesis, the extent of the dynamic interaction depends on the collapsibility of the retroglossal airway. As clearly demonstrated by the upper recordings of a patient in the VP-only group (Fig. 1), the PT&P fluctuates between positive and negative pressures in accordance with Ptr swings during obstructive apneas, indicating the presence of an air space between tongue and the soft palate, resulting in less interaction between them. In addition to the less collapsible OP airway under static conditions, significant recruitment of the genioglossal muscle activity in response to the negative airway pressure and hypercapnia can further stiffen the less collapsible OP airway during obstructive apnea, maintaining an air space between tongue and soft palate.
In contrast, patients with a highly collapsible OP airway revealed a totally different pattern of interaction between tongue and soft palate during obstructive apnea, as shown by Figs. 2 and 3. In this pattern, no inspiratory efforts transmitted to the balloon of the PT&P catheter and end-expiratory PT&P progressively increased during of obstruction, which suggested persistence and strengthening of the contact between the structures during obstruction. The source of this contact force is most likely from the posterior movement of the tongue as suggested by significant increase of PT&P in patients with smaller Amax(OP) and greater . Concomitant increase in end-expiratory and peak-inspiratory PT&P values suggests less contribution of negative inspiratory pressure during obstructive apnea. However, we have no clear explanation for the progressive increase in this contact pressure during obstructive apnea. Surface tension created on the OP airway and on the mucosa between tongue and soft palate may increase with extension of OP obstruction and therefore possibly play a role in the progressive increase of end-expiratory PT&P values during obstructive apnea (8, 14). In addition, significant increase of PT&P was revealed during inspiratory effort, in accordance with a positive deflection pattern of the PT&P trace. This suggests significant contribution of negative inspiratory efforts during obstructive apnea to increase in the collapsing forces of the soft palate and to prevent reopening of the VP airway during the inspiratory phase.
We evaluated dynamic interaction between the tongue and soft palate during experimentally induced obstructive apnea. A variety of interaction patterns were demonstrated, and the patterns were strongly associated with mechanical properties of the retroglossal airway. Posterior movement of dorsum of the tongue during inspiratory efforts of the obstructive apnea is likely to exert persistent posterior forces onto the soft palate, maintaining retropalatal airway closure, particularly in patients with higher retroglossal collapsibility.
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ACKNOWLEDGMENTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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REFERENCES |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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, Outlying points.
, and oropharyngeal closing pressure 
. Note that significant dynamic interaction between the tongue and soft palate during obstructive apnea occurs in less obese patients with smaller Amax(OP) and higher collapsibility both at the VP and OP.