Mechanisms of oronasal airflow partitioning in dogs

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Respiration Physiology 104 (1996) 169-177

Mechanisms of oronasal airflow partitioning in dogs T.C. A r n i s *, N. O ' N e i l l , T. Van d e r T o u w , A. B r a n c a t i s a n o Department of Respirato~ Medicine, Westmead Hospital Westmead, NSW 2145 Australia Accepted 26 February 1996

Abstract

We examined the integrated (MTA) electromyographic activity (EMG) of the hyoepiglotticus (HE) muscle and the soft palate muscles (SPM) during CO2 administration in 6 anaesthetised prone, mouth open dogs. As ventilation increased nasal flow ('VN) as a percentage of total flow (VT), i.e. "~N/'VT%, decreased. Breath-by-breath peak inspiratory and peak expiratory HE EMG activity was strongly and inversely correlated with VN/~'rT%(both r > 0.8, p < 0.001), whereas the correlation between SPM MTA EMG activity and VN/~'T% was highly variable. Severing of the HE muscles halved the rate at which "QN/'QT% was reduced with respect to increasing ventilation while electrical stimulation of HE muscle contraction resulted in a fall in VN/'~/T% to near zero levels. Active control of epiglottic position appears to be an important mechanism controlling the patency of the epiglottic-soft palate seal and thus the oronasal partitioning of airflow in dogs.

Keywords: Flow, oronasal, partitioning; Mammals, dog; Muscle, upper airways, hyoepiglotticus, soft palate; Upper airways, respiratory-related muscle activity 1. Introduction

The canine upper airway consists of two parallel conduits for airflow, the nasal and oral pathways. These two breathing routes combine at the level of the pharynx. At this level the typical mammalian upper airway features an overlapping soft palate and epiglottis, with the ventral surface of the epiglottic tip in contact with the dorsal surface of the soft palate (Negus, 1927). This anatomical arrangement may be regarded as a valve which, at least partially, controls the separation of the nasal and oral airways. The functional advantage of this separation has been thought to lie in the preservation of olfactory processes during feeding (Negus, 1927). * Corresponding author. Tel.: 61 (2) 845 6797, Fax: 61 (2) 893 9060.

In animals with an overlapping epiglottis and soft palate the epiglottic-soft palate seal has the potential to control the patency of the oral pathway. Indeed, in some animals (e.g. horses) the relationship between the epiglottis and soft palate is so tightly controlled that under normal circumstances these animals are thought to be incapable of using the oral route for breathing i.e. obligate nose breathers (Sisson and Grossman, 1953). The dog breathes via the nasal route at rest but develops patterns of breathing which involve both the oral and nasal route during exercise or thermally induced panting (Goldberg et al., 1981; Biewener et al., 1985). The importance of the epiglottic soft palate seal in the control of oral route airflow in dogs can be inferred from the observation of Biewener et al. (1985) that dogs may have an open mouth without any oral route airflow.

0034-5687/96/$15.00 Copyright © 1996 Elsevier Science B.V. All rights reserved. Pll S 0 0 3 4 - 5 6 8 7 ( 9 6 ) 0 0 0 2 9 - 1

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T.C. Amis et al./Respiration Physiology 104 (1996) 169-177

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Fig. 1. Schematic diagram of the experimental arrangement. Note that with the dog in the prone mouth open position, airflow may occur via the nose (VN) and/or mouth ('~M) depending on the integrity of the seal between the soft palate and epiglottis. The electromyogram (EMG) of the hyoepiglotticus (HE) and soft palate muscles (palatinus (PAL/, levator (LP), and tensor (TP/veli palatini) was measured using fine-wirebipolar electrodes. ~/Y = tracheal airflow. While the soft palate has received some attention as a structure capable of influencing oronasal partitioning of airflow (Rodenstein and Stanescu, 1986, Biewener et al., 1985), the concept of epiglottic involvement in oronasal airflow partitioning has been little explored. In dogs epiglottic position is actively controlled by the hyoepiglotticus muscle (HE) which connects the epiglottis to the ceratohyoid bone of the hyoid apparatus. Contraction of the HE purportedly moves the epiglottis ventrally (Miller et al., 1979), thus potentially disengaging it from the soft palate. In a companion paper (Amis et al., 1996), we reported that the HE muscle of the anaesthetised dog develops substantial electromyographic (EMG) activity during stimulated breathing. Under these circumstances, the epiglottis came to lie ventral to the soft palate in a position that opened the oral airway. These findings strongly suggest that the epiglottis might play an active role in the determination of oronasal airflow partitioning in dogs. The aim of the present study was to examine the relationships between the activity of those muscles controlling soft palate position, HE muscle activation and the oronasal partitioning of airflow in anaesthetised dogs.

2. Methods 2.1. Animals

We studied 6 adult crossbred dogs (2 males, 4 females, weight 15-23 kg) under general anaesthesia induced by intravenous thiopental sodium (25 mg/kg) followed by intravenous chloralose (initial dose 25 mg/kg). Anaesthesia was maintained with a continuous infusion of a 0.5% chloralose solution administered via a cannula inserted into a femoral vein. Heart rate and arterial blood pressure were monitored throughout the study. Five of the dogs were the same animals studied in a companion study of HE muscle recruitment (Amis et al., 1996). The investigation was approved by the Western Sydney Area Health Service Animal Care and Ethics Committee. 2.2. Experimental preparation

The experimental arrangement is shown in Fig. 1. The animals were studied prone with the mouth held widely open with metal bars placed behind the upper and lower canine teeth. The tongue was positioned

T.C. Amis et al./Respiration Physiology 104 (1996) 169-177

with the tip just touching the caudal surface of the lower incisor teeth and then secured with tape tied around the mandible. The trachea was divided between the fourth and fifth cartilage tings caudal to the cricoid cartilage. Separate tracheal cannulas were inserted and fastened to the cranial and caudal cut ends of the trachea. Tracheal airflow (X?T) was measured with a pneumotachograph (Fleisch no. 1) coupled to a differential pressure transducer (MP 45, 4-5 cm H20, Validyne). One end of the pneumotachograph was attached to the caudal tracheal segment while the other end was connected to the cranial tracheal segment. In this manner the animal was able to breathe through its upper airway with the pneumotachograph surgically placed in series with the trachea. Tidal volume was measured by electrical integration of the flow signal. A specially constructed mask (Amis et al., 1992) was placed over the animal's nostrils and sealed to the animal's face with a quick-setting dental impression compound (polyorganosiloxane, President Heavy Base, Coltene). A pneumotachograph (Fleisch no. 1) attached to a pressure transducer (4-10 cm H20, Celesco) measured flow through the mask, i.e. nasal route airflow (XZN).

2.3. Electromvography Bipolar Teflon-coated fine-wire electrodes (40 gauge) were inserted perorally via a 23-gauge hypodermic needle unilaterally into the HE muscle. A laryngoscope was used to visualise the paired HE as bulges beneath the hypopharyngeal mucosa at the junction between the base of the tongue and the ventral epiglottic surface. Placement of the electrodes in the HE was confirmed by visual observation of ventral movement of the epiglottis during tetanic low-voltage electrical stimulation (model $48 Grass stimulator, 5-7 volts, 2 sec duration, 40 pulses/sec, 0.2 msec/pulse) applied via the fine-wire electrodes. Correct placement of the electrodes was accepted only when substantial ventral epiglottic movements, unaccompanied by visual movement of any other hypopharyngeal structures, were observed during electrical stimulation. Fine-wire electrodes were also inserted unilaterally into the soft palate muscles (palatinus (PAL),

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levator veli palatini (LP) and tensor veli palatini (TP)) using approaches described previously (Van der Touw et al., 1994a,b). Correct placement of electrodes was confirmed by visual assessment of the occurrence of characteristic palatal movements in response to low-voltage tetanic electrical stimulation (Van der Touw et al., 1994a). The raw EMG signals were filtered (80-1000 Hz), amplified, rectified and integrated (model NT1900, Neotrace) with a time constant of lOOms to produce moving time average (MTA) EMGs. The raw EMGs were also displayed on an oscilloscope as well as transformed into an audio signal via an amplifier and loud speaker. These visual and auditory signals were used to determine the presence of action potentials in the raw EMG signal.

2.4. Data recording The flow, volume, pressure and integrated EMG signals were recorded on a strip chart recorder (model 7758B, Hewlett-Packard) and also stored on magnetic tape (model 3968A, Instrumentation Recorder, Hewlett-Packard) for subsequent analysis.

2.5. Experimental protocol After a 1 to 2 min period of quiet tidal breathing via the tracheostomy the upper airway was connected to the pneumotachograph and a further 1 to 2 min of resting breathing obtained. Ventilation was then stimulated by introducing 100% CO2 at a port in the caudal tracheal cannula. A continuous infusion of progressively increasing amounts (continuous bias flow of approximately 2 to 8 L/min) of CO2 was administered until there was no further increase in ventilation. Room air was then inspired until ventilation returned to control levels. Because of technical restrictions on the number of channels available for analysis, separate runs were recorded for SPM EMGs (measured in four dogs) and for HE EMGs (measured in five dogs).

2.6. Additional studies In four animals studies were also performed before and after bilaterally surgically severing the attachments of the HE muscle to the ventral surface of the epiglottis.

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In two dogs (with intact HE muscles) the tracheal pneumotachograph was disconnected from the tracheostomy tube, thus isolating the upper airway. The animals were then mechanically ventilated via the tracheostomy such that no HE MTA EMG activity was present. A constant airflow (420-500 ml/sec) generated by a high-impedance negative pressure source was then passed through the isolated upper airway in an inspiratory direction while HE muscle contraction was induced by graded direct unilateral electrical stimulation delivered via the HE EMG electrodes. The applied stimulus was of 2 sec duration, 40 pulses/sec, 0.2 msec/pulse, and of variable voltage (0-10 volts).

2.7. Data analysis The MTA EMG activity was quantified in arbitrary units (a.u.) above baseline (i.e. where the raw EMG did not show any action potentials). Peak inspiratory and peak expiratory EMG activity were measured as the maximum values of MTA EMG activity during inspiration and expiration, respectively. The MTA EMG activity was measured for 3-5 representative breaths during resting breathing and at minimum VN, as well as on a breath-bybreath basis, during the CO2 runs. Depending on the number of breaths necessary to achieve maximum steady state ventilation measurements were made on an every breath, up to every fifth breath, basis. Ventilation (L/min) was calculated on a breathby-breath basis as tidal volume (L) divided by TTOT (rain), where TTOT is the time for one respiratory cycle. VN was measured at peak ~rY. Oronasal airflow partitioning was expressed as percent nasal airflow i.e. "{/N/'~rT%. Inspiration and expiration were analysed separately. Steady state data from representative breaths were averaged for each dog and then pooled to determine group means. For studies involving cutting the HE, only inspiration was analysed. Statistical comparisons were made using Student's t-test or the Wilcoxon signed rank test for paired data, as appropriate. All steady state EMG comparisons were made using the Wilcoxon signed rank test. Regression analysis was used to fit exponential or linear functions to the relationships between MTA EMG activity and ~¢'N/'QT%, and ventilation and VN/'QT%; p < 0.05 was considered significant.

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VN/'QT% initially increases. However, further increases in ventilation are associated with a progressively falling VN/VT% as flow is diverted to the oral pathway. 3. Results

3.1. Oronasal airflow partitioning Ventilation during resting tidal breathing via the upper airway was 9.4 4- 1.4 L/min (mean 4- SE) and progressively increased during CO2 administration to reach a maximum value of 16.4 4- 2.6 L/min (p < 0.05). During resting breathing airflow occurred via both mouth and nose, with VN/VT% being 16.2 ± 6.2% on inspiration and 17.4 + 6.4% on expiration. With CO2 administration, peak inspiratory and peak expiratory "~T increased from 576 -4- 93 to 823 i 104 ml/sec and from 647 4- 67 to 839 4- 58 ml/sec, respectively (both p < 0.05). However, inspiratory and expiratory VN fell from 66 4- 16 ml/sec to 16 ± 4 ml/sec and from 88 4- 22 ml/sec to 9.3 4- 5.5 ml/sec, respectively (both p < 0.05). As a result VN/VT% fell progressively (Fig. 2) until virtually all airflow was via the mouth during both inspiration (VN/VT% = 1.8 ± 0.4%, p < 0.05) and expiration (VN/'VT% = 0.8 ± 0.3%, p < 0.05) (Fig. 3).

3.2. HE EMG activi~.' During increased ventilation peak HE MTA EMG activity increased progressively (Fig. 4) from 9.4 -t2.0 to 50.7 4- 16.8 a.u. during inspiration and from

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was highly variable both between individual dogs and amongst the SPM muscles themselves. Peak inspiratory MTA EMG activity did not consistently correlate with inspiratory "9N/~CT% for any SPM. In two of the three dogs studied, peak expiratory PAL, LP, and TP MTA EMG activity was inversely correlated with expiratory ~'N/VT% (all r > 0.5, p < O.O5).

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Fig. 3. Bar graph showing mean (+SE) percent nasal airflow (~/N/~rT%) in 6 dogs during inspiration (Insp.) and in 5 dogs during expiration (Exp.). Data are shown for control conditions together with the minimum "QN/VT% obtained during CO2 administration (CO_.). Note that during CO2 administration oronasal airflow partitioning changes in that mean VN/~/T% falls during both inspiration and expiration. * p < 0.05 compared to Control.

2.4 4- 1.2 to 46.2 4- 15.7 a.u. during expiration (both p < 0.05, Fig. 5). Furthermore, during both inspiration and expiration breath-by-breath HE MTA EMG activity was strongly and inversely correlated (r > 0.8, p < 0.001) with VN/VT% in a curvilinear manner in all dogs studied (Fig. 6).

3.3. SPM EMG activi~ Three dogs were studied for each SPM. During resting breathing inspiratory SPM EMG activity only occurred in one dog for PAL and TE However, inspiratory MTA EMG activity did not change with increasing ventilation for any of the SPMs (p > 0.05). In contrast, peak expiratory SPM EMG activity increased from 3.1 4- 3.1 to 15.4 4- 4.8 a.u. for PAL, from 13.4 + 10.2 to 88.4 4- 23.4 a.u. for LP and from 9.7 4- 6.5 to 18.4 4- 8.7 a.u. for TP. While peak expiratory MTA EMG activity for each SPM quantitatively increased in every dog in which it was measured, these increases failed to achieve statistical significance when each muscle was considered individually (p = 0.1). However, when the SPM muscles were considered as a group, peak expiratory MTA EMG activity increased significantly (p < 0.01) during CO2 administration. The correlation between SPM MTA EMG activity and VN/VT% during increased chemical drive

In four dogs, studies were performed before and after bilaterally severing the HE muscle. Control values for ventilation, VN and gY were not significantly different before and after cutting the HE muscles (p > 0.l). Although ~]N/~/T% was also not significantly different, there was a tendency for control values to be lower than with the HE intact. During CO2 administration ~zN/VT% fell from 7.1 4- 2.3% to 2.3 4- 0.9% (p < 0.001). This value, however, was not significantly different (p = 0,6) to that achieved with the HE muscle intact. When the HE muscles were intact and during the period while VY/~ZT% was changing, the slope of the ~rN/~,rT% versus ventilation plot was - 1.2 4- 0.3 (L rain-a) -~. However, when the HE muscles were severed this fell to - 0 . 4 8 4- 0.15 (L min-J) -1 (p < 0.05, Fig. 7).

3.5. Effect of electrical stimulation of HE muscle contraction Progressive unilateral electrical stimulation of the HE muscle resulted in a decrease in ~'N/'+'T% from 10.6 ± 1.0% at 0 volts to 0.75 4- 0.3% at 9-10 volts (Fig. 8). This was associated with a decrease in "+'Y from 44.5 -4- 4.0 ml/sec to 3.5 4- 0.9 ml/sec and increased oral route airflow (calculated as VT minus "+'N) from 375.5 4- 8.3 ml/sec to 456.5 4- 14.8 ml/sec.

4. Discussion This is the first study to quantitatively document oronasal airflow partitioning in dogs during increased respiratory drive and to link these upper airway mechanical changes with HE and soft palate muscle recruitment. The principal finding of

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this study is that active control of epiglottic position during breathing in dogs is an important determinant of oronasal airflow partitioning. Co-ordinated recruitment of both soft palate and HE muscles allows active modulation of the patency of the soft

palate-epiglottic seal which, in turn, contributes to the patency of the oral airway. The mean level of resting breathing inspiratory/expiratory oronasal airflow partitioning found in the present study was 16-17%, as measured by ~'Y/+VT%. This value has a somewhat arbitrary nature since, in the anaesthetised open mouth dog, the resting position of upper airway structures is difficult to standardise. Levels of +?N/VT% found in awake dogs can potentially vary from 0 to 100% depending on the patency of the oral and nasal breathing routes. In the anaesthetised dogs of this study, the resting anatomical relationships present were such that the majority of airflow was via the mouth. Thus at rest the epiglottic-soft palate seal was incomplete. In addition, and perhaps more importantly, we have previously shown that airflow in this model can also occur via the piriform recesses (Amis et al., 1992). Administration of CO2 in the present study resulted in almost a doubling of ventilation. This was accompanied by a shift in oronasal airflow partitioning with nasal airflow falling to 10-25% of control values. Both inspiratory and expiratory oronasal airflow partitioning were similarly affected. Visual observation through the open mouth during increased

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c h e m i c a l drive revealed d i s e n g a g e m e n t of soft palate a n d epiglottis such that, as m a x i m u m ventilatory responses were approached, the epiglottis c a m e to be held in a ventral position near the floor of the h y p o p h a r y n x . This r e p o s i t i o n i n g of the epiglottis resulted in an o p e n i n g b e i n g f o r m e d b e t w e e n the epiglottis and soft palate, thus p r o v i d i n g an increasingly p a t e n t oral p a t h w a y for airflow a n d resulting in a redistribution o f airflow from the nasal to the oral b r e a t h i n g routes. Interestingly, n o large soft palate m o v e m e n t s were visualised.

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Fig. 8. Bar graph of group mean data (+SE) for percent nasal airflow (~ZN/~'T%) at 0 and 9-10 volts of unilateral electrical stimulation of the HE muscle in 2 dogs. Note the fall of VN/'QT% to almost zero levels during electrical stimulation of HE muscle contraction.

However, s t i m u l a t e d b r e a t h i n g was associated with the progressive r e c r u i t m e n t o f both H E and S P M M T A E M G activity. The S P M E M G activity was p r e d o m i n a n t l y expiratory in nature and correlated w e a k l y and variably with oronasal partitioning. We have also previously observed variable S P M MTA E M G recruitment during augmented chemical drive in s u p i n e anaesthetised dogs b r e a t h i n g

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T.C. Amis et al./Respiration Physiology 104 (1996) 169-177

via a tracheostomy (Van der Touw et al., 1994b). The depressant effect of general anaesthesia on upper airway muscle function may be an explanation for variable SPM muscle recruitment, although the HE muscles do not seem to have been so affected. An additional factor might be lack of upper airway mechanoreceptor stimulation, since with the mouth wide open peak inspiratory negative pharyngeal pressure were likely to be quite modest. Canine SPMs are known to be recruited by upper airway negative pressure (Van der Touw et al., 1994a). However, this latter argument applies only to inspiration and does not explain variable expiratory activity. Furthermore, variable patterns of SPM EMG activity have also been reported in awake human subjects (Launois et al., 1994; Tangel et al., 1995). Thus SPM activity appears to have a somewhat looser connection with respiratory events than is the case for some other upper airway muscles. In contrast the HE muscle MTA EMG activity was strongly and inversely correlated with oronasal airflow partitioning during both inspiration and expiration in all dogs studied. This finding suggests an important role for HE muscle recruitment in the progressive promotion of oral pathway airflow during stimulated breathing. In addition, the studies in which HE muscle contraction was induced by electrical stimulation demonstrate that HE muscle action alone is capable of increasing oral route airflow at the expense of nasal airflow. It has been suggested that some level of inspiratory activation of the HE may in fact enhance the seal between the soft palate and epiglottis (Andrew, 1954). In keeping with this concept some runs in the present study showed an initial increase in "~N/VT% early in the administration of CO2 (see Fig. 2). The tendency towards lower control values for VY/VT% following severing of the HE muscles may also be indicative of a loosening of the soft palate-epiglottic seal following loss of the mechanical effect of resting HE muscle activity. However, in any case, vigorous recruitment of the HE muscles at higher ventilatory levels disrupted the seal between soft palate and epiglottis and opened the oral pathway for airflow by bringing the epiglottis to lie ventral to the soft palate thus resulting in a progressive fall in VN/VT%. Previous analyses of mechanisms of oronasal airflow partitioning in dogs have concentrated, almost

exclusively, on the role of the soft palate. In their fluoroscopic study of thermally induced panting in awake dogs Biewener et al. (1985) described soft palate movements as being the principal mechanisms determining oronasal airflow partitioning. They also describe substantial epiglottic movements with the epiglottis "coming to lie in front of and below the soft palate" during shallow panting. This repositioning of the epiglottis was ascribed a passive role related to coincident tongue movements. Clearly the present study suggests active control of epiglottic position via HE muscle recruitment and demonstrates the influence of HE muscle contraction on the regulation of upper airway airflow. However, factors other than HE muscle recruitment also contribute to oronasal airflow partitioning in dogs. Obviously mouth opening is a critical step. However, beyond that influence, the present study has shown that oronasal airflow fractionation can be altered even when the HE muscles have been severed. Indeed cutting the HE muscles did not alter the final level of oronasal partitioning achieved. However, the rate at which this level was obtained in relation to the increase in ventilation was halved. Thus removing the mechanical effect of HE recruitment decreased the 'efficiency' of the oronasal partitioning process. In some dogs this influence may well be associated with a lower initial level of VN/VT%, i.e. leaky soft palate-epiglottic seal at rest. However, in other dogs the starting level of oronasal partitioning was not reduced in relation to control values (see Fig. 7) but the slope of the VN/VT% versus ventilation plot was still reduced. Thus HE muscle involvement in oronasal airflow partitioning affects not only the resting patency of the oral airway but also influences the entire partitioning process. Activation of SPMs, particularly the PAL and LE can elevate the soft palate into the nasopharynx, thus opening the oral pathway and potentially obstructing the nasopharynx. This, together with protrusion of the tongue, is thought to be the major mechanism by which oronasal partitioning is achieved in adult humans (Rodenstein and Stanescu, 1986) and is also the analysis which has been applied to dogs (Biewener et al., 1985). Airflow via the piriform recesses can also contribute to oronasal airflow partitioning in dogs. In this context, widening of the piriform recesses associated with recruitment of the

T.C. Amis et aL /Respiration Physiology 104 (1996) 169-177

cricothyroid muscles (Amis et al., 1992) allows airflow via the mouth by bypassing the epiglottic-soft palate seal. Consequently oronasal partitioning of airflow in response to increased respiratory drive is a complex process. It involves the coordinated recruitment of a n u m b e r of mechanisms which combine to reduce nasal route airflow and promote oral route airflow. In summary we have shown that in anaesthetised, prone, mouth open dogs during increased chemical drive, the HE and soft palate muscles demonstrate progressively increasing respiratory-related E M G activity. This is associated with diversion of airflow from the nasal to oral pathways. Active control of epiglottic position appears to be an important mechanism controlling the patency of the epiglottic-soft palate seal. Thus oronasal airflow partitioning in species with an overlapping epiglottis and soft palate involves active coordinated movements of a n u m b e r of upper airway structures including tongue, piriform recesses, soft palate and epiglottis.

Acknowledgements This study was supported by the National Health and Medical Research Council of Australia and by a Harry Windsor Research Grant from the C o m m u n i t y Health and Anti-Tuberculosis Association of New South Wales.

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