American Journal of Respiratory and Critical Care Medicine Vol 166. pp. 760-764, (2002)
© 2002 American Thoracic Society
Prone Position Increases Collapsibility of the Passive Pharynx in Infants and Small Children
Teruhiko Ishikawa,
Shiroh Isono,
Junko Aiba,
Atsuko Tanaka and
Takashi Nishino
Department of Anesthesiology (B1), Graduate School of Medicine, Chiba University, Chiba, Japan
Correspondence and requests for reprints should be addressed to Shiroh Isono, M.D., Department of Anesthesiology (B1), Graduate School of Medicine, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba 260-8670, Japan. E-mail: isonos{at}ho.chiba-u.ac.jp
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ABSTRACT
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On the basis of two observations that avoiding prone sleeping decreased incidence of sudden infant death syndrome and that obstructive sleep apnea is closely linked with the syndrome, we hypothesized that the prone position may increase upper airway collapsibility in infants and small children. Passive pharyngeal collapsibility of 19 infants and small children (10–101 weeks old) was examined in three postures: supine with face straight up, supine with neck rotated, and prone with neck rotated. The collapsibility was evaluated with the maximal distension of the most collapsible region, pharyngeal stiffness, and pharyngeal closing pressure, estimated from static pressure–area relationship of the passive pharynx. No significant changes in pharyngeal stiffness were detected; however, maximal distension was reduced in the prone position (mean ± SD, 0.56 ± 0.26 versus 0.44 ± 0.20 cm2; supine with face straight up versus prone position, p < 0.05). Pharyngeal closing pressure increased at neck rotation in the supine position (-4.5 ± 2.4 versus -2.8 ± 2.3 cm H2O; supine with face straight up versus supine with neck rotated, p < 0.05), and a further increase was observed in the prone position (-0.3 ± 2.9 cm H2O, p < 0.05 versus supine with neck rotation). Pharyngeal closing pressure in the prone position was above atmospheric pressure in half of our subjects, whereas all subjects had negative pharyngeal pressure in the supine position. We conclude that the prone position increases upper airway collapsibility, although the mechanism is yet unclear.
Key Words: prone position • upper airway collapsibility • infants • small children
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INTRODUCTION
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Sudden infant death syndrome (SIDS) is recognized as more than a medical problem; SIDS has become a nursing, social, ethical, and legal problem (1, 2). Presumably, obscurity of the etiology makes the syndrome such a multidisciplinary issue. Some epidemiologic studies have reported that prone sleeping is one of the most important risk factors for SIDS (3, 4). Public campaigns that recommend not laying babies on their stomach have succeeded in reducing the incidence rate of SIDS in some countries (5); nevertheless, the mechanism underlying this result is yet unclear.
Incidentally, obstructive sleep apnea (OSA) is frequently observed in SIDS victims, their siblings, and near-miss infants (6–9). OSA is characterized by symptoms such as hypoxia, hypercarbia, bradycardia, and pulmonary, and/or systemic hypertension, all of which may lead to fatal results in infants without arousal response. Vulnerable upper airway collapsibility significantly contributes to the development of OSA while the etiology of OSA has not fully been understood (10).
On the basis of the two previously mentioned important observations that avoiding prone position decreased the incidence rate of SIDS and that SIDS may be closely associated with OSA, we hypothesized that the prone position might decrease upper airway patency in infants and small children when compared with the supine position. To test the hypothesis, we evaluated the effects of the prone position on upper airway collapsibility of infants and small children, under general anesthesia with complete paralysis, eliminating neuromuscular compensatory mechanisms.
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METHODS
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Subjects
After obtaining approval from the Ethics Committee of our institution and written informed consents from parents, 19 infants and small children (mean ± SD, age: 46 ± 26 weeks; weight: 8.4 ± 1.9 kg; height: 70.4 ± 7.3 cm; 14 boys and 5 girls) were enrolled in this study. All the subjects were patients who were scheduled for elective minor surgeries, under general anesthesia, but were otherwise healthy children. The surgical procedures included inguinal hernia repair (9), plastic surgery (5), urogenital surgery (2), and others (3). Patients with craniofacial or oropharyngeal anomaly were excluded from the study. None of the subjects was observed to snore during sleep or to have any clinical evidences suggestive of sleep-disordered breathing, which was mainly confirmed by careful interviews of their parents. The parents were inquired about past history of apnea in their children and whether any incidence of choking or skin color changes during their sleep had been observed.
Evaluation of Collapsibility of Passive Pharyngeal Airway
The subjects had standard fasting time and no preanesthetic medication. General anesthesia was induced by making the subjects inhale sevoflurane in conjunction with nitrous oxide and oxygen. After establishing an intravenous line, atropine sulfate (0.01 mg/kg, minimum 0.1 mg intravenously) and vecuronium bromide, a muscle relaxant (0.1–0.2 mg/kg, intravenously) were administered. Anesthesia was then maintained with sevoflurane (1–2%) in oxygen, and vecuronium was added as necessary to maintain complete paralysis. The airway was managed by board-certified skilled pediatric anesthesiologists with a custom-made nasal mask that had a self-sealing diaphragm for insertion of a fine fiber-optic endoscope (3.5-mm outer diameter, FB10X; Pentax Inc., Tokyo, Japan). The fiberscope was passed through the diaphragm and then a naris to visualize the most collapsible area of the pharyngeal structure. After the subjects were fully oxygenated, mask ventilation was ceased while the airway pressure (PAW) was changed in step decrements of 1 cm H2O starting at 20 cm H2O by a custom-made pressure control system until the pharyngeal closure was visually observed with the scope. The distance between the tip of the scope and the narrowing site was measured with a wire passed through the aspiration channel of the scope. This procedure was completed in the supine position with face straight up, supine with neck rotated to the left, and prone with neck rotated to the left. In the prone position, the degree of neck rotation was maintained as close to equivalent to that in the supine position as possible. Neck rotation in the supine position was performed to observe the effects of neck rotation alone on pharyngeal patency. In each position, the images of the pharynx were videotaped using a closed-circuit video system (ETV8; Nisco, Saitama, Japan). We identified the most collapsible region and obtained the pressure–cross-sectional area relationship of the region.
Data Analysis
Only the set of pressure–cross-sectional area relationship of the most collapsible region was analyzed for each subject. To convert the monitor image to an absolute value of cross-sectional area of the pharynx (A, Equation 1), the magnification of the imaging system was estimated at intervals of 1.0 mm in the range of 5–30 mm between the tip of the endoscope and the object. 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 the 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. For a constant distance, the measured areas were systematically deviated from actual areas. The largest known area tested (0.95 cm2) was underestimated by 11% due to image deformation in the outer image area, and the smallest known area tested (0.03 cm2) was overestimated by 13% due to reduction in the image resolution. As we previously reported (11), the As are well fitted with a nonlinear least square method by the following equation:
 | (1) |
where  is the fitted cross-sectional area, Amax is the maximum cross-sectional area obtained, PAW is the airway pressure, and B and K are constants. In the fitting procedure, we used the mean value of cross-sectional areas corresponding to the highest three PAW values (18, 19, and 20 cm H2O) as the value of Amax. Constant K represents the shape of the fitted curve and serves as an index of upper airway compliance. These fitting procedures were performed with S-PLUS 2000 (MathSoft, Seattle, WA). We estimated airway closing pressure P'close from the fitted curve by solving an equation
 | (2) |
derived from Equation 1 by substituting 0 for Â.
Statistical Analysis
All values are expressed as mean ± SD. The mean values of Amax, K, and P'close were compared among the postures using multivariate analysis of variance followed by contrast analysis. To analyze the correlations between the three parameters and age, linear regression studies were performed. p Values less than 0.05 were considered significant.
Considerations for Subject Safety
The protocol was executed by at least two board-certified skilled anesthesiologists in addition to a resident in anesthesiology, in the presence of surgeons who were in charge of the operative procedure of the subject. Among the routine cardiorespiratory parameters monitored, arterial oxygen saturation was especially closely monitored, and the procedure was interrupted when the oxygen saturation decreased down to 96% and restarted after adequate reoxygenation.
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RESULTS
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The retropalatal segment was the most collapsible region of the pharynx in all subjects. Oxygen desaturation below 90% was not reported during the procedures.
Figure 1
shows the representative static pressure–area relationship curves of the pharynx in one subject. The pressure–area curve of the prone position is clearly revealed to be located below that of the supine position. Moreover, a significant decrease of Amax and increase of P'close above atmospheric pressure was revealed in the prone position.
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Figure 1. Representative static pressure–area relationships of the pharynx in one subject. The subject is 55 weeks old, 78 cm in height, and 8.6 kg in weight. PAW, airway pressure. (A) Cross-sectional area of the most collapsible region of the pharynx. Open circles represent measured pressure–area data points in supine position with face straight up, whereas closed circles represent those in prone position. Curves are from the nonlinear regression study using Equation 1 (see text). Note that the pressure–area curve in prone position locates below that in supine position and that prone position significantly decreased Amax and increased P'close to a value close to the atmospheric pressure, indicating that pharyngeal collapsibility is greater in prone position than in supine position.
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Figure 2
shows endoscopic images of the pharynx in concurrence with pressure–area relationships of the retropalatal segment obtained from a subject in three different positions. At each airway pressure value, the cross-sectional area of the retropalatal segment was found to be greater in the face straight-up supine position than in the neck-rotated supine and prone positions; a change in body position from face straight-up supine position produces a right shift of the pressure–area curve. Notably, the pharyngeal airway appears to be distorted by neck rotation as evidenced by the discordance of the lateral axes between the level of the retropalatal segment and that of the epiglottis.
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Figure 2. An illustration of sets of endoscopic images of the pharynx together with pressure–area relationships of the retropalatal segment obtained from one individual subject (36 weeks old, 77 cm in height, and 11.0 kg in weight) in three different positions. From the first row, the fitted pressure–area curve and the retropalatal endoscopic images in supine face straight up (S), those in supine neck rotated (SR), and those in prone position (P). The corresponding curve is represented as a thick line in each position. The same abbreviations as in Figure 1 were used for airway pressure and cross-sectional area. Two reference lines indicate frontal planes at the retropalatal area and the epiglottis. Note that neck rotation results in significant distortion of the pharynx.
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Table 1
summarizes the values of the static mechanics variables obtained by exponential curve-fitting analyses at three different positions. As indicated by the relatively high R2 values, the exponential function reasonably well fitted the measured pressure–area relationship. A significant decrease in Amax was evident in the prone position as compared with the supine position with face straight up. Posture changes did not seem to have a significant effect on pharyngeal stiffness because no changes were detected in K. In contrast, P'close significantly differed among the three postures, revealing a minimum value of P'close in the supine with face straight-up position, a slight but significant increase in P'close in the neck-rotated position, and a further significant increase in P'close in the prone position.
Figure 3
shows the P'close value of the three postures for each subject. P'close of the supine position, regardless of neck position, was below atmospheric pressure in all subjects; however, P'close of the prone position increased above atmospheric pressure in half of the subjects. This indicates the existence of a collapsed upper airway in the prone position without neuromuscular compensatory mechanisms at atmospheric pressure. No differences in age, body weight, or sex were evident between prone subjects with or without P'close value above atmospheric pressure.
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Figure 3. Changes in P'close among the three postures for each subject. S, supine with face straight up; SR, supine with neck rotated; P, prone with neck rotated. Significant differences are indicated by square brackets with corresponding p values. Note that no subjects have positive pharyngeal closing pressure regardless of neck position, whereas one half of the subjects do.
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Table 2
presents correlations between age and the three parameters, i.e., Amax, K, and P'close for each position. Significant correlation was evident between the three parameters and age in supine position, where younger infants and children revealed smaller Amax, larger K, and larger P'close. In contrast, only the correlation between age and Amax was evident in neck rotation and prone positions.
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TABLE 2. Coefficient of determination as an index of goodness of regression between age and static pharyngeal mechanics parameters
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In Figure 4
, each P'close was plotted against the corresponding observed closing pressure (Pclose). Although reasonable correlation was indicated (R2 = 0.956, p < 0.01), P'close was significantly larger than Pclose, with a difference of 0.85 ± 0.57 cm H2O (mean ± SD). Magnitudes of the differences were insignificant among the three postures.
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Figure 4. The estimated pharyngeal closing pressure (P'close) is plotted against the observed closing pressure (Pclose). Most of the points are placed above the identity line, indicating that the estimated closing pressure is larger than the real closing pressure. Among three postures, no significant difference was detected in the magnitude of the difference between the estimated and observed pharyngeal closing pressure.
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DISCUSSION
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The major findings of our study in completely paralyzed infants and small children under general anesthesia include (1) prone position decreased the maximal distension of the most collapsible region of the pharynx and increased pharyngeal closing pressure compared with supine position, (2) neck rotation increased pharyngeal closing pressure compared with supine position, (3) effects of maturation on pharyngeal collapsibility were not detected in prone position, and (4) one half of the subjects had positive closing pressure in the prone position. To our knowledge, this is the first study demonstrating that prone position has deleterious effects on pharyngeal patency.
Study Design and Methodology
Current concepts of upper airway maintenance suggest that neural regulation of the upper airway dilating muscle activities (neural mechanisms) and structural properties of the upper airway (anatomic mechanisms) are major determinants of upper airway patency. Because of methodologic difficulty in examining the two factors separately, estimation of the contribution of each of these factors to upper airway maintenance is difficult. In our study, as we previously reported, we completely eliminated the neural mechanisms by administrating neuromuscular blockade, which enabled us to purely evaluate anatomic properties of the upper airway (11).
In this study, we characterize the mechanics of the passive pharynx by obtaining the pressure–area curve of the most collapsible region. The position and the slope of the curve can determine the collapsibility of the pharynx. The position is represented by the closing pressure (P'close), that is the intercept of the curve on the pressure axis, and by the maximal area (Amax), that is the upper limit value of the curve. The constant K in Equation 1 denotes the shape of the curve, representing the stiffness of the pharynx in the entire range of airway pressure. We compared the pharyngeal collapsibility with the three variables that characterize the curve. Although these three variables can be mutually dependent on each other, each variable seems to have different collapsibility characteristics.
A possible weakness of our method was that we did not control the lung volume during step reduction of airway pressure, which also affects lung volume during the measurements. Lung volume has been reported to influence pharyngeal collapsibility (12, 13); thus, alteration in the static pressure–cross-sectional area relationship may have resulted.
The neck was rotated in the prone position in our study to simulate the actual sleeping posture of small children. The detrimental effects of the prone position on pharyngeal patency may be attributed to two factors: neck rotation and/or prone position. To assess the independent effect of neck rotation, we evaluated pharyngeal collapsibility in the supine position with neck rotation. Although equivalent neck rotations were attempted in both postures, we did not perform angle measurements of the neck rotation. Consequently, estimation of the precise degree of contribution of each factor against increased collapsibility in the prone position with neck rotation is difficult.
In our previous studies on adults and older children with sleep-disordered breathing, no significant differences between actual and estimated pharyngeal closing pressures were evident (14, 15). Subjects in the current study frequently demonstrated sigmoid rather than simple exponential pressure–area curves, which is also reported in our previous study in normal children (14). The sigmoid pressure–area curve may be indicative of a significant difference in actual and estimated closing pressures.
Possible Mechanisms of Increased Pharyngeal Collapsibility in Prone Position
The underlying mechanisms by which prone sleeping aggravates pharyngeal patency in our experimental condition have not been fully disclosed in this study. Because the neural mechanisms were eliminated in our experimental setting, only the structural changes caused by neck rotation and prone position could account for the increased upper airway collapsibility. The upper airway is a collapsible conduit surrounded by soft tissue inside the mandibular bony enclosure. Increase in tissue pressure has been suggested to cause upper airway narrowing in patients with OSA (16). Although we did not measure tissue pressure, the pressure increase by neck rotation may have resulted from squeezing and shifting of soft tissue into the mandibular enclosure. The theory is well supported by the images obtained from fiber-optic endoscope (Figure 2), where the pharynx is distorted by neck rotation and the space available for the airway is significantly reduced. Although neck rotation did have a significant effect on pharyngeal collapsibility, the effect was not strong enough to explain the impairment of upper airway patency in the prone position. In the supine position, the possible increase in the soft tissue pressure by neck rotation may be partially offset because the tissue could expand to the perisubmandibular area; however, in the prone position, the compensation may be limited by bedding materials. Furthermore, in the prone position, bedding items and heavy structures such as the head and vertebrae may have directly compressed the compliant submandibular area, increasing the tissue pressure as demonstrated by Koenig and Thach (17). This mass on the submandibular area increased the upper airway closing pressures in anesthetized and paralyzed rabbits (17).
Another possible mechanism of collapse is the difference in lung volume between supine and prone positions and its potential to affect the patency of the pharynx, which would be in keeping with some reports indicating an inverse relationship between pharyngeal collapsibility and lung volume (12, 13, 18). Changes in posture could have an effect on lung volume; however, whether the prone position decreases lung volume of infants is controversial (19–21).
Clinical Implications
The recommendation to avoid laying babies in the prone position has succeeded in reducing the incidence rate of SIDS (5). This fact may indicate that the sleeping posture has important pathophysiologic effects on the incidence of the syndrome; however, the mechanism by which the prone position leads certain infants to the syndrome has not been fully elucidated.
According to our results, posture did have a significant impact on pharyngeal patency in our experimental condition in which the prone position significantly decreased pharyngeal space and increased pharyngeal closing pressure. The vulnerability of the upper airway to collapse indicates that, without any compensation, the subjects may be at risk of developing OSA, possibly leading to arterial oxygen desaturation and bradycardia. These two symptoms are recognized as life-threatening events that are closely related to SIDS. The pharyngeal patency will improve as infants mature (11); however, postural effects were serious even in larger children because developmental effects were abolished by neck rotation and prone position.
We found positive pharyngeal closing pressure in half of our subjects in the prone position; nonetheless, they were supposedly normal infants and children without any clinical evidences of sleep-disordered breathing. This is in significant contrast with the fact that positive closing pressure of the passive pharynx was significantly associated with the presence of OSA in adult humans. One possible explanation is the difference in the relative contribution of neural mechanisms to upper airway patency between the two generations. In infants and small children, the neural compensatory mechanisms, such as reflex dilatation of upper airway, augmented breaths, startles, and arousal responses (22), may be more important for the maintenance of upper airway.
In conclusion, although underlying mechanisms are still unclear, we clearly demonstrated that prone position increased collapsibility of the passive pharyngeal airway.
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Acknowledgments
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The authors express great appreciation to the infants and children for their participation in this study, to Drs. J. E. Remmers and B. T. Thach for their constructive comments, and to Dr. S. Shimizu for the improvement of this manuscript. The authors are also grateful to the staffs of the Division of Operation Theater, the Department of Plastic Surgery, and the Department of Pediatric Surgery for their cooperation.
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FOOTNOTES
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Supported by grant-in-aid 14571421 and 10671402 from the Ministry of Education, Japan.
Received in original form September 21, 2001;
accepted in final form May 31, 2002
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ABSTRACT
INTRODUCTION