S.E.M.). None of the subjects had any symptoms suggestive of nasal, upper airway, sleep or respiratory disorders. The protocol was approved by the Western Sydney Area Health Service Ethics and Radiation Safety Committees, and all subjects gave their informed written consent.
X-ray fluoroscopy
A lateral projection of the upper airway was imaged using an X-ray image intensifier (BV 25, Philips, North Ryde, NSW, Australia). Subjects were seated with the right side of their head and neck facing the X-ray beam. A 1·0 mm copper filter was used to reduce the dose of radiation received at the skin and to improve the resolution of the air contrast image. The total thyroid radiation dose in each subject was measured by thermoluminescent dosimetry using lithium fluoride chips and was less than 0·29 mSv.
Experimental protocol
Each subject was studied in the seated posture breathing via a tight fitting nasal mask (Sullivan nasal CPAP mask, ResMed, Sydney, NSW, Australia) or via a standard mouthpiece. The use of a standard mouthpiece for oral route breathing ensured a standard absolute degree of mouth opening between subjects. In addition, head and neck position were kept constant throughout the study by clamps attached to the nasal mask or mouthpiece and by a fixed head support. Studies were performed during relaxed tidal breathing without any additional load other than the measurement apparatus (unloaded breathing, UB) and then during breathing via a resistive load common to inspiration and expiration and sufficient to produce a peak inspiratory nasal or mouth pressure of -1·47 kPa (RL). Measurements were obtained during both exclusive nasal and exclusive oral breathing achieved by occluding the alternative pathway with a tap. This arrangement allowed the mouthpiece to remain in situ for both nasal (mouthpiece occluded) and oral (nasal mask occluded) breathing. Thus, jaw position was kept constant for all conditions studied.
Inspiratory and expiratory oral or nasal airflow were monitored with pneumotachographs (Fleisch no. 2) coupled to pressure transducers (±0·98 kPa; Celesco, IDM Instruments, Dandenong, Victoria, Australia) and the signals displayed on an oscilloscope (Model 511, Tektronix). The flow signals were used to relate epiglottic, corniculate cartilage and hyoid bone position to the phase of respiration. Nasal mask pressure or mouth pressure was measured with a pressure transducer (±9·8 kPa, Celesco) during resistive loaded breathing.
Using an approach we have employed previously (Wheatley et al. 1991), the oscilloscope screen was imaged using a video camera, the output of which was mixed with that from the image intensifier, displayed on a television monitor, and stored on videotape for subsequent analysis.
Data analysis
The simultaneous record of upper airway fluoroscopic image and airflow allowed us to relate displacements of upper airway structures to the phase of respiration. A video analyser (model 321, Colorado Video) and computer were used to measure the epiglottic, laryngeal and hyoid movements during breathing from the recorded images. Vertical and horizontal distances on the recorded images were calibrated using a steel ball marker of known dimensions which was taped to the subject's skin anteriorly over the larynx, and included on the fluoroscopic images. In the lateral projection, we measured the antero-posterior (A-P) and cranio-caudal (C-C) position of the epiglottic tip, corniculate cartilages of the larynx and hyoid bone relative to the antero-cranial edge of the fourth cervical vertebra (C4, Fig. 1). Airway diameter at the tip of the epiglottis was also measured. Measurements were made at zero flow (ZF), peak inspiratory (PI) and peak expiratory (PE) flow for nasal and oral, unloaded and resistive loaded breathing.
Data were calculated as the mean of four to five consecutive breaths. Statistical comparisons were examined using one factor repeated measures analysis of variance (ANOVA) with Fisher's PLSD used as a multiple comparison technique. Simple linear regression analysis was used to examine correlations between epiglottic, laryngeal and hyoid displacements. P < 0·05 was considered significant.
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Figure 1. X-ray image of upper airway
Lateral projection X-ray image from one subject showing the epiglottic tip (E), hyoid bone (H) and corniculate cartilage (C) of the larynx. The position of these structures was measured in the antero-posterior (left-right) and cranio-caudal (top-bottom) direction relative to the antero-cranial edge (0,0) of the fourth cervical vertebra (C4). Positions cranial and anterior to C4 were regarded as positive while positions caudal to C4 were regarded as negative.
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RESULTS |
Nasal breathing
Epiglottic movements. During unloaded breathing via the nose there was minimal change in epiglottic tip position in most subjects (Fig. 2). However, there was a tendency for the epiglottic tip to move slightly cranially during inspiration and slightly caudally during expiration, such that, for the group as a whole, the position of the epiglottic tip at PE was 0·7 ± 0·3 mm more caudal than at PI (P < 0·05, Fig. 4A). There were no significant movements in the antero-posterior direction.
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Figure 2. Epiglottic tip movements during nasal breathing
Epiglottic tip position during unloaded breathing and breathing against a fixed resistive load via the nose at peak inspiratory flow (PI), zero flow (ZF), and peak expiratory flow (PE) in seven normal subjects. Different symbols represent individual subjects. Epiglottic tip position was measured in the antero-posterior and cranio-caudal directions (relative to C4).
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During resistive loading there was considerable inter-subject variability, with some relatively large changes in the position of the epiglottic tip characterized by caudal movement of the epiglottis on inspiration and cranial movement on expiration (Fig. 2). Thus, for the group, during resistive loading the epiglottic tip at PE was 2·6 ± 1·3 mm cranial to its position at PI and 3·5 ± 0·1 mm cranial to its position at PE during unloaded breathing (P < 0·05, Fig. 4A). There were no significant movements in the antero-posterior direction.
Corniculate cartilage movements. During unloaded breathing via the nose, the group mean position of the corniculate cartilage at PE was 1·1 ± 0·2 mm anterior and 1·0 ± 0·3 mm caudal to its position at PI (P < 0·05, Fig. 4B). This was primarily because of anterior and caudal movement during expiration such that the corniculate cartilage at PE was 0·9 ± 0·3 mm anterior to its position at ZF (P < 0·05, Fig. 4B).
During resistive loading, results were more variable with some subjects exhibiting relatively large changes in corniculate cartilage position. These movements were particularly characterized by posterior movement of the corniculate cartilages during inspiration in most subjects. Thus, the corniculate cartilages at PI during resistive loading were 2·5 ± 0·4 mm and 1·8 ± 0·4 mm more posterior than at PE and ZF, respectively (P < 0·05, Fig. 4B).
Hyoid movements. During unloaded breathing there were no significant movements of the hyoid detected in either the antero-posterior or cranio-caudal directions. However, during resistive loading the hyoid moved in a caudal and posterior direction in most subjects during inspiration. For the group, the hyoid was 4·2 ± 2·2 mm caudal and 1·5 ± 0·6 mm posterior at PI when compared with its position at ZF, and 6·0 ± 2·3 mm caudal and 1·5 ± 0·7 mm posterior when compared with its position at PE (P < 0·05, Fig. 4C).
Oral breathing
Epiglottic movements. During exclusively oral route unloaded breathing, there was no significant respiratory-related change in the position of the epiglottic tip in either the antero-posterior or cranio-caudal directions (Figs 3 and 4A).
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Figure 3. Epiglottic tip movements during oral breathing
Epiglottic tip position during unloaded breathing and breathing against a fixed resistive load via the mouth at peak inspiratory flow (PI), zero flow (ZF), and peak expiratory flow (PE) in seven normal subjects. Different symbols represent individual subjects. Epiglottic tip position was measured in the antero-posterior and cranio-caudal directions (relative to C4).
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During resistive loaded breathing, there was considerable inter-subject variability particularly in regard to cranio-caudal movements. However, for the group, there was, again, no significant respiratory-related change in epiglottic tip position detected (Figs 3 and 4A) although the epiglottic tip at PE during resistive loading was 3·2 ± 0·1 mm cranial to its position at PE during unloaded breathing (P < 0·05, Fig. 4A).
Corniculate cartilage movements. During oral unloaded breathing the corniculate cartilage at PI had moved posteriorly by 1·0 ± 0·2 mm and 0·8 ± 0·2 mm compared with its position at ZF and PE, respectively (P < 0·05, Fig. 4B). There were no significant movements in the cranio-caudal direction.
Under resistive load conditions, the PI position was 1·5 ± 0·4 mm posterior to the ZF position (P < 0·05, Fig. 4B). There was also a significant anterior movement during expiration such that the PE position was 1·1 ± 0·6 mm anterior to the ZF position (P < 0·05, Fig. 4B). Movements in the cranio-caudal direction were marked in some subjects, especially during inspiration, but no consistent pattern emerged.
Hyoid movements. There were no significant antero-posterior or cranio-caudal movements of the hyoid detected during unloaded breathing via the mouth (Fig. 4C). However, during resistive loading the hyoid moved posteriorly and caudally during inspiration such that the PI position was 1·3 ± 0·6 mm and 3·5 ± 1·7 mm posterior and caudal, respectively, to the ZF position and 1·5 ± 0·6 mm and 4·2 ± 1·7 mm posterior and caudal, respectively, to the PE position (P < 0·05, Fig. 4C).
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Figure 4. Epiglottic movements during breathing
Group mean data for antero-posterior and cranio-caudal co-ordinates (relative to C4) for the epiglottic tip (A), corniculate cartilage (B) and hyoid bone (C) during each breathing condition, together with resultant inspiratory (I) and expiratory (E) displacement vectors. Shown are the zero flow (ZF) position co-ordinates ( , UB mouth;  , UB nose;  , RL mouth;  , RL nose) together with those resultant displacement vectors having a significant (P < 0·05 antero-posterior and/or cranio-caudal displacement component during breathing (i.e. significant difference between ZF and PE or PI positions or between PI and PE positions). See text for discussion. UB, unloaded breathing; RL, resistive loaded breathing. Closed arrowheads, movements during nasal breathing; open arrowheads, movements during mouth breathing.
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Position of upper airway structures at zero airflow
During nasal breathing there was no significant effect of resistive loading (compared with unloaded breathing) on the ZF position of the epiglottic tip, corniculate cartilage or hyoid bone. During oral breathing the epiglottic tip and hyoid bone were positioned 2·9 ± 1·2 mm and 4·3 ± 2·1 mm, respectively, more cranially during resistive loaded breathing than during unloaded breathing (P < 0·05, Fig. 4A and C). However, there was no significant effect of oral resistive loading on corniculate cartilage position compared with oral unloaded breathing (Fig. 4B).
There was no significant effect of route of breathing on the position of the epiglottic tip at ZF in the antero-posterior direction (Fig. 4A). In the cranio-caudal direction the major effect was a significant (P < 0·05) caudal shift in the ZF position of the epiglottic tip with unloaded mouth breathing compared with unloaded nasal breathing (Fig. 4A). However, when the resistive load was applied during mouth breathing, the epiglottic tip ZF position was similar to that during tidal nasal breathing. There was no significant effect of route of breathing on the ZF position of the corniculate cartilages (Fig. 4B). For the hyoid, the major effect was a significant caudal shift of the ZF position during unloaded breathing via the mouth when compared with any other condition (Fig. 4C).
Breathing route: airway diameter at epiglottic tip
Group mean data for airway diameter at the epiglottic tip are shown in Fig. 5A and B. There was no significant effect of phase of respiration (i.e. PI, ZF, PE) on upper airway diameter measured at the epiglottic tip during either unloaded or resistive loaded breathing via the nose or mouth (Fig. 5A and B).
The airway diameter at the epiglottic tip at PI was unaffected by the route of breathing or by resistive loading. At ZF the airway diameter was smallest during unloaded breathing via the mouth (8·8 ± 0·8 mm) and largest during resistive loaded breathing via the nose (10·7 ± 1·0 mm, P < 0·05). At PE the airway diameter during oral breathing was significantly greater during resistive loading than during unloaded breathing (Fig. 5B). Furthermore, at PE the airway diameter at the epiglottic tip was greatest during resistive loaded breathing via the nose (10·7 ± 0·9 mm) and least with unloaded breathing via the mouth (8·6 ± 0·7 mm).
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Figure 5. Airway diameter at epiglottic tip
Bar graph showing mean data (+ 1 S.E.M.) for airway diameter measured at the epiglottic tip in seven normal subjects during nasal (A) and oral route (B) breathing. Data for unloaded breathing () and resistive loaded breathing ( ) are shown for peak inspiratory flow (PI), zero flow (ZF), and peak expiratory flow (PE) conditions. * P < 0·05 compared with ZF nasal resistive loaded breathing (A);  P < 0·05 compared with PE nasal unloaded and resistive loaded breathing (A) and oral resistive loaded breathing (B).
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Relationship of epiglottic movements to those of other structures
The only significant group mean epiglottic tip movements detected in the present study were in the cranio-caudal plane and related to the difference between the epiglottic position at PI and that at PE for nasal breathing. During resistive loaded breathing via the nose, this difference was found, strongly and positively, to correlate with both corniculate cartilage and hyoid movements in the same plane (both r > 0·84, where r is the correlation coefficient, P < 0·02). When the inspiratory and expiratory movements were considered individually for this condition (i.e. PI-ZF and PE-ZF), the strongest correlation during inspiration was with cranio-caudal movements of the hyoid bone (r = 0·96, P < 0·0001), although a strong correlation with corniculate cartilage movement was also found (r = 0·91, P = 0·002). During expiration, cranio-caudal epiglottic movements correlated with corniculate cartilage movements (r = 0·80, P < 0·03) (but not hyoid) in the same plane.
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DISCUSSION |
The principal findings in this study were that in seated normal subjects: (1) there was minimal (especially in the antero-posterior direction) movement of the epiglottic tip during unloaded breathing via nose or mouth; however, (2) some individuals demonstrated relatively large cranio-caudal epiglottic movements during resistive loaded breathing via either route, although this was more marked for nasal route breathing. In addition, upper airway diameter at the epiglottic tip did not change during either nose or mouth breathing, but was smallest during oral unloaded breathing and largest during resistive loaded breathing via the nose.
The cranio-caudal movements of the epiglottic tip, detected during nasal breathing, correlated strongly and positively with both corniculate cartilage and hyoid bone movements in the same plane. Another finding was that with oral route unloaded breathing all three upper airway structures at ZF were positioned substantially caudal to their position during nasal breathing. Adding a resistive load to the oral pathway resulted in a repositioning of these structures to the nasal route breathing position.
Previous studies using the same measurement approach as the present study (Collett et al. 1986; Wheatley et al. 1991) have estimated the accuracy of the technique to be of the order of 0·8 to 1·2 mm. Thus, we were probably unable to distinguish displacements of less than 1 mm. In the present study, the displacements measured during unloaded breathing were of this order and were thus at the limit of the resolution of the technique. However, during resistive loading, displacements were 1·3-6·0 times this distance and were thus easily within the measurement ability of our approach. Movement of the head and neck of the subject during the study is another potential source of error. However, subjects were positioned with the back of their heads in contact with a rigid board and instructed to maintain position constant throughout the study. In addition, the connections to the nasal mask were sufficiently rigid to restrict any head movement. Finally, no evidence of subject movement was detected on any of the videotape images, suggesting that movement was an unlikely source of error. Jaw position is another potential influence on the position of upper airway structures; however, this was held constant for all conditions by having a standard mouthpiece in place throughout the study.
In a comparative anatomical study, Negus (1927) concluded that the epiglottis was not necessary for deglutition, respiration or phonation. He suggested that the role of the epiglottis was to preserve nasal airflow while the mouth was open (as occurs during feeding) and thus allow olfactory sensing of inhaled gas to continue whilst the oral route was used for eating purposes. This arrangement would seem of considerable advantage to grazing animals since olfactory detection of predators can then continue during feeding. Consequently, typical mammalian upper airway anatomy (found in carnivores, ungulates and non-human primates) places the epiglottis dorsal to the soft palate, thus directing airflow to and from the nasopharynx while separating the respiratory and feeding passages in the upper airway. In effect, this anatomical arrangement 'locks' the laryngeal airway into the nasopharyngeal airway during feeding and prevents oral route breathing.
This anatomical arrangement is found in the human infant up to about 6 months of age, following which contact between the soft palate and epiglottis is lost (Sasaki et al. 1977). This modification of neonatal upper airway anatomy during growth is thought to be related to the development of phonatory ability by allowing the pharynx to participate in speech production (Laitman et al. 1977). In their comparative study of the human and monkey epiglottis Laitman et al. (1977) concluded that the function of the epiglottis was to 'guide the larynx upwardly behind the soft palate so it can lock into the nasopharynx' and preserve nasal route breathing.
Both Negus (1927) and Fink et al. (1979) speculated that epiglottic shape and position may reflect adaptation for the high ventilatory rates associated with exercise, implying that epiglottic position may modify upper airway resistance. In the present study we were unable to demonstrate any consistent and significant epiglottic movements in the antero-posterior direction during unloaded or resistive loaded breathing via either nose or mouth. Consistent with this finding was the lack of any change in the diameter (at the epiglottic tip) of the upper airway during breathing. These results suggest that epiglottic movements in this plane are not recruited, either because the mechanisms do not exist or because they were not activated by the stimulus imposed. This contrasts with our findings in dogs (Amis et al. 1996b), where negative upper airway pressure (similar to the peak levels achieved in the present study) resulted in substantial recruitment of inspiratory hyo-epiglotticus muscle activity, large ventral movements of the epiglottis and a fall in upper airway resistance.
The major epiglottic movements detected in the present study were in the cranio-caudal direction during nasal breathing, with some individuals demonstrating relatively large displacements. These movements strongly correlated with displacements of the whole larynx (as measured by corniculate cartilage position) and with movements of the hyoid bone. In the present study cranio-caudal movements of the corniculate cartilage were of about the same magnitude as those for the epiglottic tip but were more variable and did not achieve significance.
A feature of the results in the present study was the effect of route of breathing and resistive loading on the overall position and movement of the upper airway structures that we examined. In particular, it was evident that, in comparison to nasal route breathing, oral route breathing was associated with: (1) a much more caudal position of these structures at ZF, and (2) no consistent respiratory-related movements of the epiglottis. However, this result may not be due to the use of the oral route for breathing alone, but rather to the level of upper airway resistance, since addition of a resistive load to the oral route returned the resting upper airway to its nasal route configuration, although it did not restore the breathing-related movements (see Fig. 4). Further studies in which oral and nasal route resistances are measured and varied in relation to one another in a known manner are required to confirm this hypothesis.
It is also not possible from the present study to distinguish between active and passive mechanisms responsible for the position and movement of the structures examined. Thus, for example, the effects of caudal traction on the trachea during inspiration (Van de Graaff, 1991) may have contributed to caudal movement of the epiglottic tip during resistive loading and nasal breathing; however, so may have inspiratory contraction of infrahyoid muscles (van Lunteren & Strohl, 1988). Furthermore, the lack of consistent epiglottic tip movements during mouth breathing implies recruitment of an opposing force to both of these processes. Consequently, further studies will also be required to define the precise mechanisms involved in determining the position of the epiglottis during breathing.
We conclude that there is little respiratory-related movement of the human epiglottis during unloaded breathing. However, individual subjects may adopt different strategies during resistive loaded breathing, especially via the nose, resulting in cranio-caudal displacements of the epiglottis. Oral route breathing results in a more caudal positioning of the epiglottis and less consistent respiratory-related movements. In addition, when present, epiglottic movements during breathing do not appear to be independent of those of the larynx and hyoid. Although route of breathing modifies the position of the epiglottis, we speculate that this phenomenon may be related to the level of upper airway resistance to airflow.
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Acknowledgements
This study was supported by the National Health and Medical Research Council of Australia and by a Harry Windsor Research Grant from the Community Health and Anti-Tuberculosis Association of New South Wales. The authors would like to thank the Department of Radiology at Westmead Hospital for technical assistance with the fluoroscopy and Michael Rynn for assistance with the development of computer software.
Corresponding author
T. C. Amis: Department of Respiratory Medicine, Westmead Hospital, Westmead NSW 2145, Australia.
Email: terencea{at}westgate.wh.usyd.edu.au
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