Oronasal partitioning of ventilation during exercise in humans J. R. WHEATLEY, Thoracic Medicine
T. C. AMIS, AND L. A. ENGEL Unit, Westmead Hospital, Sydney, New South Wales 2145, Australia
WHEATLEY, J. R., T. C. AMIS, AND L. A. ENGEL. Oronasal partitioning of ventilation during exercise in humans. J. Appl. Physiol. 71(2): 546-551, 1991.-The partitioning of oronasal breathing was studied in five normal subjects during progressive exercise. Subjects performed three to five identical runs, each consisting of four 1-min work periods at increments of 50 W. Nasal and oral airflow were measured simultaneously using a partitioned face mask both during and for 4 min after exercise. Total mean flows were the sum of nasal and oral flows. At a total mean inspiratory flow of 2 l/s, the nasal fraction of total flow was 0.36 t 0.04 (SE) and decreased by 6 * 3% between total flows of 1.5 and 2.5 l/s. Throughout exercise, the nasal fraction of total mean inspiratory flow did not differ from that of total expiratory flow and was similar to that of total mean inspiratory flow during the postexercise period at a corresponding total mean flow (both P > 0.2). The results show that oronasal flow partitioning is not directly due to the exercise itself but is related to the level of ventilation and is uninfluenced by the direction of upper airway flow (i.e., inspiratory vs. expiratory). These findings suggest tightly controlled modulation of the relative resistances of the oral and/or nasal pathways. nasal resistance; racic airways
oral resistance;
oronasal
breathing;
extratho-
openstotheatmospherevia two parallel pathways, the nasal and oral cavities. These two pathways join at the level of the oropharynx, which is in series with the larynx. Over 80% of normal subjects breathe exclusively via the nose at rest (4, 11, 13, 17). However, during moderate to heavy exercise over 80% of subjects breathe oronasally, the remainder continuing to breathe only nasally (5, 11). The switching point from nasal to oronasal breathing has been shown to occur at a ventilation of 35-40 l/min in normal subjects (5, 11, 14) and may be influenced by psychological factors (14), nasal airflow resistance (II), nasal work of breathing, and nasal average power during inspiration (15). Nasal breathing permits the removal of some airborne particulate pollutants while the inspired air is warmed and humidified. However, the oral breathing offers a lower resistance to ventilation, especially when the mouth is held wide open (6). Thus during exercise the demand for increased ventilation is normally associated with combined oronasal breathing. The nasal proportion of total ventilation tends to decrease as the exercise intensity increases (5, 1l), but there is little quantitative information about the proportions of nasal and oral airflow during the different phases of the respiratory cycle. THEHUMANUPPERAIRWAY
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0161-7567/91
$1.50
Copyright
Nor is there any information about the reproducibility of these proportions within a given subject or on the effect of exercise per se on the level of partitioning. Therefore we studied the partitioning of both inspiratory and expiratory upper airway flow into oral and nasal components both during exercise and in the immediate postexercise period. METHODS
We studied five healthy normal male subjects, aged 38 t 8 (SD) yr, who were naive as to the purpose of the exercise study. They had no known medical problems, in particular no symptoms of nasal disease, and none was a trained athlete. Informed consent was obtained from each subject, and the protocol was approved by the Ethics Committee of the institution. No medications were administered. Subjects were seated on a cycle ergometer and performed three to five identical exercise runs, each of 4 min total duration and consisting of four consecutive l-min work periods at 50, 100, 150, and 200 W, respectively. The work rate of 200 W corresponded to -80% of the predicted maximum work rate for the group. Subjects breathed initially through the nose alone but could switch to oronasal breathing at will. None of the subjects breathed through the nose alone for an entire exercise run. Measurements were made both during the 4-min exercise period and for 4 min immediately after the completion of each exercise run. We used a partitioned face mask, constructed individually for each subject (18), such that nasal and oral breathing routes were kept separate. Each mask compartment was tested for air leaks by pressurizing it to 10 cmH,O and ensuring that the pressure held for 10 s. Masks were tested both before and at the conclusion of each exercise run. The mask was strapped firmly to the subject’s face and connected to two identical low-resistance breathing circuits, one each for the nasal and oral compartments. Flow was measured separately in each circuit with a heated pneumotachograph (Fleisch no. 2) coupled to a differential pressure transducer (Validyne MP 45, t10 cmH,O). A three-way stopcock (Hans Rudolph) was attached to each pneumotachograph. Both flow signals were digitized using a sampling frequency of 50 Hz and recorded in real time on a PDP-11 computer (DEC) using DAOS software. The data were stored on disk for subsequent analysis. Data analysis. The areas under both the inspiratory
@ 1991 the American
Physiological
Society
Downloaded from www.physiology.org/journal/jappl at Washington Univ (128.252.067.066) on March 3, 2019.
ORONASAL
PAKI’ITIONING
OF
547
VENTILATION
JE
Z
0.6
0 -Ic)
i
a
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s 0 I IA
LE
1
SW
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acn aZ l-
MEAN
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FLOW
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fraction of inspiratory flow plotted against mean total inspiratory flow during exercise in 5 subjects. Initial data points are taken after switch from nasal to oronasal breathing. Different symbols represent separate exercise runs. Note intrasubject reproducibility of separate exercise runs and intersubject variability of nasal flow fractions. FIG.
1. Nasal
and expiratory nasal and oral flow signals were integrated separately to give both nasal and oral inspired and expired volumes for each breath. The inspiratory and expiratory mean flows were calculated separately for each route and then summed to give total inspiratory and total expiratory mean flow, respectively. The nasal fraction of flow was calculated by dividing nasal flow by the corresponding total mean flow for each breath. Nasal and oral ventilation were calculated separately for both inspiration and expiration and summed to give total ventilation. The ventilation at the switch from nasal to oronasal breathing was the mean value of nasal ventilation from the three nasal breaths immediately preceding the switch. Data were expressed as means t SE. Statistical analysis was performed using Student’s t test for paired comparisons and an analysis of variance (ANOVA) for multiple samples together with a Scheffe F test for significance (1). RESULTS
During tidal breathing before exercise, minute ventilation (VE) was 10.7 t 1.0 l/min. This increased to 75.7 t 5.0 l/min at the end of the 4-min exercise period and then decreased to 17.1 t 0.9 l/min over the subsequent 4 min. The switch from nasal to oronasal breathing occurred in all subjects at a VE of 22.3 t 3.5 l/min. After the switch to oronasal breathing we calculated the nasal flow fraction during inspiration and related this to the total (nasal plus oral) inspiratory mean flow for each exercise run in each subject (Fig. 1). The data were highly reproducible within each individual for the three to five exercise periods. However, the absolute nasal fractions varied widely between subjects, ranging from 26 to 64% at the start of oronasal breathing. In four of the five subjects, nasal flow fractions decreased as total flow increased
(P < 0.03). In the fifth subject (SW), the nasal flow fraction increased slightly as total flow increased. Consequently, the group data showed only a 6 t 3% decrease in nasal flow fraction between total flows of 1.5 and 2.5 l/s. Nevertheless, for the same flow range, absolute nasal flow increased from 0.61 t 0.10 to 0.85 t 0.10 l/s (P < 0.01). We calculated the nasal flow fractions during exercise and in the immediate postexercise period for both inspiration and expiration, relating the values to total inspiratory or expiratory mean flow, respectively (Fig. 2). Inasmuch as the data were highly reproducible, mean values for each condition were calculated for each subject. At a total mean flow of 2 l/s the nasal flow fraction was similar during inspiration (0.36 t 0.04) and expiration (0.37 t 0.04; P > 0.2) and did not differ between the exercise (0.36 t 0.04) and postexercise periods (0.35 t 0.03; P > 0.2). In fact, in each individual, there was no difference in the nasal flow fractions at a total mean flow of 2 l/s between any of the four conditions (P > 0.05; ANOVA). At all other flows, the expiratory nasal flow fraction was similar to the inspiratory nasal fraction during both the exercise and postexercise periods (Fig. 3). Similarly, nasal flow fractions during exercise and immediately postexercise were similar for both inspiration and expiration (Fig. 4). For each subject the difference between inspired and expired nasal volumes was calculated at l-min intervals both during exercise and in the postexercise periods (Fig. 5). The pattern of this difference showed considerable interindividual variability. In only one subject did nasal inspired volume exceed the expired volume during the whole exercise period. Four subjects had a larger nasal inspired volume halfway through the exercise period, but at peak exercise the nasal expired volume was greater in four subjects. One subject always had a larger nasal ex-
Downloaded from www.physiology.org/journal/jappl at Washington Univ (128.252.067.066) on March 3, 2019.
548
ORONASAL
PARTITIONING
JE
OF
VENTILATION
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0.6
SW
MR
0.6
o.*l-?---0.0
-r
2.0
I
I
0.0
MEAN
2.0
FLOW
2. Nasal fraction of flow plotted against mean total flow during inspiration (closed symbols) both during exercise runs (circles) and postexercise period (squares) sents mean results in each category for all exercise runs. Nasal flow fraction is similar tion and not different between exercise and postexercise periods. FIG.
pired volume, the magnitude of which declined throughout the exercise and postexercise periods. However, in four of the five subjects, nasal inspired volumes were larger than the nasal expired volumes at the end of the postexercise period. DISCUSSION
The principal findings of this study show that during exercise the nasal fraction of total flow varies as a function of total flow in a reproducible manner within an individual but demonstrates significant interindividual variability. Furthermore, at a given total mean flow, the nasal fraction does not differ between inspiration and expiration and is the same during exercise and in the immediate postexercise period.
0.0
I
’
I
’
2.0
(I/s) (open symbols) and expiration in 5 subjects. Each point repreduring inspiration and expira-
There is little published data on the oronasal distribution of airflow during exercise, presumably because of the technical difficulties in measuring oral and nasal airflow simultaneously. First reports suggested that 8082% of airflow was nasal at rest and that on exercise this decreased to 60% (17). In 20 subjects who switched from nasal to oronasal breathing during exercise, the initial nasal proportion of total ventilation was 57%, declining to 39% at the end of exercise when VE was 90 l/min (11). However, no data were provided as to the consistency of the change in nasal fraction among the subjects. A subsequent study confirmed that most subjects followed this pattern of nasal ventilation during exercise but demonstrated that some subjects breathed proportionately more nasally as they exercised at higher work rates (2).
0
INSPIRATORY
n
0.4
0.8
N ASAL FRACTION
FIG. 3. Identity plots of nasal flow fraction during expiration vs. that during inspiration and after exercise (B). Each symbol represents a different subject and shows mean values increments of 0.5 l/s between 1 and 3 l/s. Note similarity of inspiratory and expiratory nasal exercise and postexercise periods.
both during exercise (A) obtained using total flow flow fractions during both
Downloaded from www.physiology.org/journal/jappl at Washington Univ (128.252.067.066) on March 3, 2019.
ORONASAL
PARTITIONING
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549
VENTILATION
0.8
0
0.4
0.8 0
EXERCISE
NASAL
0.4
0.8
FLOW FRACTION
FIG. 4. Identity plots of nasal flow fraction after exercise vs. that during exercise both during inspiration (A) and expiration (R). Each symbol represents a different subject and shows mean values obtained using total flow increments of 0.5 l/s between 1 and 3 l/s. Note similarity of exercise and postexercise nasal flow fractions during both inspiration and expiration.
This interindividual variability was confirmed in another study in which three of six normal subjects showed little change in nasal flow fraction during and after exercise, whereas the other three subjects showed a progressive decrease (5). In that study the proportion of nasal ventilation during exercise ranged between 20 and 90% (5). Thus, our data are consistent with studies that demonstrate the interindividual variability in both the absolute proportion of nasal ventilation and the pattern of change due to exercise-induced hyperpnea (2, 5). It has been suggested that the method of recording oronasal ventilation may account for some of the differences between studies (2). Niinimaa et al. (11) used a head-out exercise body plethysmograph and a nasal mask and Chadha et al. (5) used respiratory inductive
1
II CD -
EXERCISE
i II
I
-200 0
POST-EXERCISE
I 4
2
TIME
I 6
1 8
( min )
5. Difference between inspired and expired nasal volumes (per breath) plotted against time, measured from beginning of exercise period. Negative values indicate nasal expiration greater than inspiration. Four minutes denotes end of exercise period. Different symbols represent individual subjects. Note interindividual variability in difference between inspired and expired nasal volumes and difference between exercise and postexercise periods. FIG.
plethysmography and a nasal mask, whereas our study and that of Bethel et al. (2) used a two-compartment face mask. Hence the major difference between our study and most others was the use of a mask to measure oral ventilation, potentially altering the degree of mouth opening during oronasal breathing. However, it is unlikely that mouth opening was inadequate in our study, because we have shown oral resistances of ~0.5 cmH,O l 1-l s at 0.5 l/s inspiratory flow using our mask system (J. Wheatley, unpublished observations). Nevertheless, our subjects may have had their mouths open wider than normal, as suggested by the smaller initial nasal flow fractions. In addition, the face mask may have influenced the switching point from nasal to oronasal ventilation, because it was less than in previous studies (5, 11, 14). Thus we do not claim any physiological significance of our measured switching point. Our data are in agreement with other published studies showing that oronasal breathing is the normal pattern during exercise and that the absolute value of nasal ventilation increases throughout the exercise period. The proportion of nasal ventilation and its change during exercise in our study show considerable interindividual variability, as demonstrated in studies without a face mask (5). In addition, our data reveal more information about the control of oronasal partitioning. The tight relationship between the nasal flow fraction and total mean flow, related to the level of ventilation rather than the exercise itself, suggests that oronasal partitioning is probably determined by the ventilation rather than physical exercise itself. Furthermore the similar relationship between the nasal flow fraction and total mean flow during inspiration and expiration indicates that the direction of flow through the upper airway does not influence oronasal flow partitioning. The findings also suggest a tight control and modulation of the flow-partitioning mechanism in each individual. Inspired and expired nasal volume, considered on a breath-by-breath basis in each subject, differed between individuals and changed during exercise. In a given subject, either nasal inspired or nasal expired volume was
Downloaded from www.physiology.org/journal/jappl at Washington Univ (128.252.067.066) on March 3, 2019.
l
550
ORONASAL
PARTITIONING
greater, depending on the level of exercise. There was no consistent pattern for the group. This differs from the study by Niinimaa et al. (ll), where nasal inspiration consistently exceeded nasal expiration. Unfortunately, no reports of interindividual variability or of any systematic changes during exercise were provided in that study. The ultimate mechanism that determines the degree of oronasal partitioning must be the relative airflow resistances of the oral and nasal pathways. Nasal resistance during exercise and at rest has been extensively investigated (7,8, 12). From these studies. it is clear that about two-thirds of the total nasal resistance is found at the entrance to the bony cavum of the nose in the vicinity of the pyriform aperture and about one-third in the cartilaginous vestibule (3, 9). There is very little contribution from the region of the soft palate and posterior choanae during nasal breathing only (16). Thus nasal breathing does not appear to have a mechanism capable of readily modulating oronasal partitioning. In addition, nasal resistance decreases substantially during exercise (7, 8), which, in itself, should increase the nasal fraction of flow. This is opposite to that observed in the majority of subjects, which also argues against nasal resistance being the major factor controlling oronasal partitioning. Much less is known about flow resistance of the oral pathway. Oral resistance was reported to be similar to that of the nasal airway in normal subjects at rest and to decrease with increasing exercise (6). In addition, a large reduction in oral resistance was observed with wider opening of the mouth. Thus the oral airway appears to have the appropriate mechanism to control oronasal partitioning, with the ability to vary its resistance from infinity to very low values. The potential major site determining oral resistance could vary from the lips and teeth to the posterior orifice between the tongue and soft palate. In our study the mask system tended to inhibit wide opening of the mouth and jaw. Hence an internal readjustment of the soft palate and tongue was a more likely mechanism controlling oronasal partitioning. Rodenstein and Stanescu (13) used fluoroscopy to demonstrate that the soft palate could direct upper airway flow, even with the mouth open. Their data support the concept that when the mouth is open, the soft palate is responsible for the partitioning of oronasal flow and, hence, the level of oral resistance. The differences between inspired and expired nasal volume also reflect intrabreath changes in relative resistance of the nasal and oral pathways. Nasal resistance may vary between inspiration and expiration because the cross-sectional area of the nasal valve may be greater during inspiration (10). However, changes in the oral pathway resistance during inspiration and expiration are more likely to be responsible for these intrabreath changes. Inspiratory contraction of upper airway dilator muscles may cause phasic dilation of the oral airway, decreasing the oral resistance during inspiration relative to that during expiration. In addition, there may be a passive mechanical effect secondary to the alternating negative and positive pressures in the compliant oral pathway. In this case, the negative inspiratory pressures tend to increase inspiratory oral resistance and the positive pressures tend to decrease expiratory resistance. The resultant oral resistance will
OF
VENTILATION
be a balance between these two opposing forces, which can allow any combination of inspiratory and expiratory oral resistances. As ventilation increases, the level of both phasic and tonic drive to upper airway dilator muscles increases. This will decrease the oral resistance during both inspiration and expiration and hence decrease the nasal fraction of flow during progressive exercise. The similarity of the inspiratory and expiratory nasal flow fractions, in the presence of phasic dilator muscle activity, may be due to passive dilating effects in expiration secondary to positive oral pathway pressures. It should be noted that although the inspiratory and expiratory nasal flow fractions are similar at the same total mean flow, they cannot be measured within the same breath. This is because total inspiratory and expiratory mean flows are not necessarily the same within a breath. The purpose of the change in oronasal partitioning during exercise is unclear but may relate to meeting the demands of increasing ventilation while trying to minimize respiratory work (using a lower-resistance oral pathway) but still maintaining some air-conditioning function of the nasal pathway. In conclusion, we have shown that, during exercise-induced hyperpnea, oronasal flow partitioning is related to the level of ventilation rather than the exercise itself and is uninfluenced by the direction of flow through the upper airway (i.e., inspiratory vs. expiratory). The level of partitioning was highly reproducible within an individual but showed significant interindividual variability in both the absolute level and the change with exercise-induced hyperpnea. These findings suggest tightly controlled modulation of the relative resistances of the oral and/or nasal pathways. Although the mechanism of this modulation is not known, we speculate that the oral pathway resistance controls the level of oronasal flow partitioning. The authors thank Ken Isles for expertise and assistance in the construction of the face masks and Jeanette Walker for invaluable secretarial assistance. This study was supported by the National Health and Medical Research Council of Australia. Address reprint requests to J. R. Wheatley. Received
14 November
1990; accepted
in final
form
12 April
1991.
REFERENCES 1. ARMITAGE, P., AND G. BERRY. Statistical Methods in Medical Research (2nd ed.). Cambridge, UK: Blackwell, 1987. 2. BETHEL, R. A., D. J. ERLE, J. EPSTEIN, D. SHEPPHARD, J. A. NADEL, AND H. A. BOUSHEY. Effect of exercise rate and route of inhalation on sulfur-dioxide induced bronchoconstriction in asthmatic subjects. Am. Rev. Respir. Dis. 128: 592-596, 1983. 3. BRIDGER, G. P., AND D. F. PROCTOR. Maximum nasal inspiratory flow and nasal resistance. Ann. Otol. 79: 481-488, 1970. 4. CAMNER, P., AND B. BAKKE. Nose or mouth breathing? Environ. Res. 21: 394-398, 1980. 5. CHADHA, T. S., S. BIRCH, AND M. A. SACKNER. Oronasal distribution of ventilation during exercise in normal subjects and patients with asthma and rhinitis. Chest 92: 1037-1041, 1987. 6. COLE, P., R. FORSYTH, AND J. S. J. HAIGHT. Respiratory resistance of the oral airway. Am. Rev. Respir. Dis. 125: 363-365, 1982. 7. DALLIMORE, N. S., AND R. ECCLES. Changes in human nasal resistance associated with exercise, hyperventilation and rebreathing. Acta Otolaryngol. 84: 416-421, 1977. 8. FORSYTH, R. D., P. COLE, AND R. J. SHEPHARD. Exercise and nasal patency. J. Appl. Physiol. 55: 860-865, 1983.
Downloaded from www.physiology.org/journal/jappl at Washington Univ (128.252.067.066) on March 3, 2019.
ORONASAL
PARTITIONING
9. HAIGHT, J. S. J., AND P. COLE. The site and function of the nasal valve. Laryngoscope 93: 49-55, 1983. 10. HAIRFIELD, W. M., D. W. WARREN, V. A. HINTON, AND D. L. SEATON. Inspiratory and expiratory effects of nasal breathing. Cleft Palate J. 24: 183-189, 1987. 11. NIINIMAA, V., P. COLE, S. MINTZ, AND R. J. SHEPHARD. Oronasal distribution of respiratory airflow. Respir. Physiol. 43: 69-75, 1981. 12. RICHERSON, H. B., AND P. M. SEEBOHM. Nasal airway response to exercise. J. Allergy 41: 269-284, 1968. 13. RODENSTEIN, D. O., AND D. C. STANESCU. Soft palate and oronasal breathing in humans. J. Appl. Physiol. 57: 651-657, 1984. 14. SAIBENE, F., P. MOGNONI, C. L. LAFORTUNA, AND R. MOSTARDI.
OF
15. 16.
17. 18.
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Oronasal breathing during exercise. Pfluegers Arch. 378: 65-69, 1978. SCHULTZ, E. L., AND S. M. HORVATH. Control of extrathoracic airway dynamics. J. Appl. Physiol. 66: 2839-2843, 1989. TAKAGI, Y., D. F. PROCTOR, S. SALMON, AND S. EVERING. Effects of cold air and carbon dioxide on nasal flow resistance. Ann. Otol. Rhinol. Laryngol. 78: 40-48, 1969. UDDSTR~MER, M. Nasal respiration. Acta Otoluryngol. 42, Suppl.: 3-146, 1940. WHEATLEY, J. R., T. C. AMIS, AND L. A. ENGEL. Relationship between alae nasi activation and breathing route during exercise in humans. J. Appl. Physiol. 71: 124-130, 1991.
Downloaded from www.physiology.org/journal/jappl at Washington Univ (128.252.067.066) on March 3, 2019.
T. C. AMIS, AND L. A. ENGEL Unit, Westmead Hospital, Sydney, New South Wales 2145, Australia
WHEATLEY, J. R., T. C. AMIS, AND L. A. ENGEL. Oronasal partitioning of ventilation during exercise in humans. J. Appl. Physiol. 71(2): 546-551, 1991.-The partitioning of oronasal breathing was studied in five normal subjects during progressive exercise. Subjects performed three to five identical runs, each consisting of four 1-min work periods at increments of 50 W. Nasal and oral airflow were measured simultaneously using a partitioned face mask both during and for 4 min after exercise. Total mean flows were the sum of nasal and oral flows. At a total mean inspiratory flow of 2 l/s, the nasal fraction of total flow was 0.36 t 0.04 (SE) and decreased by 6 * 3% between total flows of 1.5 and 2.5 l/s. Throughout exercise, the nasal fraction of total mean inspiratory flow did not differ from that of total expiratory flow and was similar to that of total mean inspiratory flow during the postexercise period at a corresponding total mean flow (both P > 0.2). The results show that oronasal flow partitioning is not directly due to the exercise itself but is related to the level of ventilation and is uninfluenced by the direction of upper airway flow (i.e., inspiratory vs. expiratory). These findings suggest tightly controlled modulation of the relative resistances of the oral and/or nasal pathways. nasal resistance; racic airways
oral resistance;
oronasal
breathing;
extratho-
openstotheatmospherevia two parallel pathways, the nasal and oral cavities. These two pathways join at the level of the oropharynx, which is in series with the larynx. Over 80% of normal subjects breathe exclusively via the nose at rest (4, 11, 13, 17). However, during moderate to heavy exercise over 80% of subjects breathe oronasally, the remainder continuing to breathe only nasally (5, 11). The switching point from nasal to oronasal breathing has been shown to occur at a ventilation of 35-40 l/min in normal subjects (5, 11, 14) and may be influenced by psychological factors (14), nasal airflow resistance (II), nasal work of breathing, and nasal average power during inspiration (15). Nasal breathing permits the removal of some airborne particulate pollutants while the inspired air is warmed and humidified. However, the oral breathing offers a lower resistance to ventilation, especially when the mouth is held wide open (6). Thus during exercise the demand for increased ventilation is normally associated with combined oronasal breathing. The nasal proportion of total ventilation tends to decrease as the exercise intensity increases (5, 1l), but there is little quantitative information about the proportions of nasal and oral airflow during the different phases of the respiratory cycle. THEHUMANUPPERAIRWAY
546
0161-7567/91
$1.50
Copyright
Nor is there any information about the reproducibility of these proportions within a given subject or on the effect of exercise per se on the level of partitioning. Therefore we studied the partitioning of both inspiratory and expiratory upper airway flow into oral and nasal components both during exercise and in the immediate postexercise period. METHODS
We studied five healthy normal male subjects, aged 38 t 8 (SD) yr, who were naive as to the purpose of the exercise study. They had no known medical problems, in particular no symptoms of nasal disease, and none was a trained athlete. Informed consent was obtained from each subject, and the protocol was approved by the Ethics Committee of the institution. No medications were administered. Subjects were seated on a cycle ergometer and performed three to five identical exercise runs, each of 4 min total duration and consisting of four consecutive l-min work periods at 50, 100, 150, and 200 W, respectively. The work rate of 200 W corresponded to -80% of the predicted maximum work rate for the group. Subjects breathed initially through the nose alone but could switch to oronasal breathing at will. None of the subjects breathed through the nose alone for an entire exercise run. Measurements were made both during the 4-min exercise period and for 4 min immediately after the completion of each exercise run. We used a partitioned face mask, constructed individually for each subject (18), such that nasal and oral breathing routes were kept separate. Each mask compartment was tested for air leaks by pressurizing it to 10 cmH,O and ensuring that the pressure held for 10 s. Masks were tested both before and at the conclusion of each exercise run. The mask was strapped firmly to the subject’s face and connected to two identical low-resistance breathing circuits, one each for the nasal and oral compartments. Flow was measured separately in each circuit with a heated pneumotachograph (Fleisch no. 2) coupled to a differential pressure transducer (Validyne MP 45, t10 cmH,O). A three-way stopcock (Hans Rudolph) was attached to each pneumotachograph. Both flow signals were digitized using a sampling frequency of 50 Hz and recorded in real time on a PDP-11 computer (DEC) using DAOS software. The data were stored on disk for subsequent analysis. Data analysis. The areas under both the inspiratory
@ 1991 the American
Physiological
Society
Downloaded from www.physiology.org/journal/jappl at Washington Univ (128.252.067.066) on March 3, 2019.
ORONASAL
PAKI’ITIONING
OF
547
VENTILATION
JE
Z
0.6
0 -Ic)
i
a
0.4
a IA -
I
s 0 I IA
LE
1
SW
MR
0.6 -
I
acn aZ l-
MEAN
INSPIRATORY
FLOW
(I/s)
fraction of inspiratory flow plotted against mean total inspiratory flow during exercise in 5 subjects. Initial data points are taken after switch from nasal to oronasal breathing. Different symbols represent separate exercise runs. Note intrasubject reproducibility of separate exercise runs and intersubject variability of nasal flow fractions. FIG.
1. Nasal
and expiratory nasal and oral flow signals were integrated separately to give both nasal and oral inspired and expired volumes for each breath. The inspiratory and expiratory mean flows were calculated separately for each route and then summed to give total inspiratory and total expiratory mean flow, respectively. The nasal fraction of flow was calculated by dividing nasal flow by the corresponding total mean flow for each breath. Nasal and oral ventilation were calculated separately for both inspiration and expiration and summed to give total ventilation. The ventilation at the switch from nasal to oronasal breathing was the mean value of nasal ventilation from the three nasal breaths immediately preceding the switch. Data were expressed as means t SE. Statistical analysis was performed using Student’s t test for paired comparisons and an analysis of variance (ANOVA) for multiple samples together with a Scheffe F test for significance (1). RESULTS
During tidal breathing before exercise, minute ventilation (VE) was 10.7 t 1.0 l/min. This increased to 75.7 t 5.0 l/min at the end of the 4-min exercise period and then decreased to 17.1 t 0.9 l/min over the subsequent 4 min. The switch from nasal to oronasal breathing occurred in all subjects at a VE of 22.3 t 3.5 l/min. After the switch to oronasal breathing we calculated the nasal flow fraction during inspiration and related this to the total (nasal plus oral) inspiratory mean flow for each exercise run in each subject (Fig. 1). The data were highly reproducible within each individual for the three to five exercise periods. However, the absolute nasal fractions varied widely between subjects, ranging from 26 to 64% at the start of oronasal breathing. In four of the five subjects, nasal flow fractions decreased as total flow increased
(P < 0.03). In the fifth subject (SW), the nasal flow fraction increased slightly as total flow increased. Consequently, the group data showed only a 6 t 3% decrease in nasal flow fraction between total flows of 1.5 and 2.5 l/s. Nevertheless, for the same flow range, absolute nasal flow increased from 0.61 t 0.10 to 0.85 t 0.10 l/s (P < 0.01). We calculated the nasal flow fractions during exercise and in the immediate postexercise period for both inspiration and expiration, relating the values to total inspiratory or expiratory mean flow, respectively (Fig. 2). Inasmuch as the data were highly reproducible, mean values for each condition were calculated for each subject. At a total mean flow of 2 l/s the nasal flow fraction was similar during inspiration (0.36 t 0.04) and expiration (0.37 t 0.04; P > 0.2) and did not differ between the exercise (0.36 t 0.04) and postexercise periods (0.35 t 0.03; P > 0.2). In fact, in each individual, there was no difference in the nasal flow fractions at a total mean flow of 2 l/s between any of the four conditions (P > 0.05; ANOVA). At all other flows, the expiratory nasal flow fraction was similar to the inspiratory nasal fraction during both the exercise and postexercise periods (Fig. 3). Similarly, nasal flow fractions during exercise and immediately postexercise were similar for both inspiration and expiration (Fig. 4). For each subject the difference between inspired and expired nasal volumes was calculated at l-min intervals both during exercise and in the postexercise periods (Fig. 5). The pattern of this difference showed considerable interindividual variability. In only one subject did nasal inspired volume exceed the expired volume during the whole exercise period. Four subjects had a larger nasal inspired volume halfway through the exercise period, but at peak exercise the nasal expired volume was greater in four subjects. One subject always had a larger nasal ex-
Downloaded from www.physiology.org/journal/jappl at Washington Univ (128.252.067.066) on March 3, 2019.
548
ORONASAL
PARTITIONING
JE
OF
VENTILATION
SC
0.6
SW
MR
0.6
o.*l-?---0.0
-r
2.0
I
I
0.0
MEAN
2.0
FLOW
2. Nasal fraction of flow plotted against mean total flow during inspiration (closed symbols) both during exercise runs (circles) and postexercise period (squares) sents mean results in each category for all exercise runs. Nasal flow fraction is similar tion and not different between exercise and postexercise periods. FIG.
pired volume, the magnitude of which declined throughout the exercise and postexercise periods. However, in four of the five subjects, nasal inspired volumes were larger than the nasal expired volumes at the end of the postexercise period. DISCUSSION
The principal findings of this study show that during exercise the nasal fraction of total flow varies as a function of total flow in a reproducible manner within an individual but demonstrates significant interindividual variability. Furthermore, at a given total mean flow, the nasal fraction does not differ between inspiration and expiration and is the same during exercise and in the immediate postexercise period.
0.0
I
’
I
’
2.0
(I/s) (open symbols) and expiration in 5 subjects. Each point repreduring inspiration and expira-
There is little published data on the oronasal distribution of airflow during exercise, presumably because of the technical difficulties in measuring oral and nasal airflow simultaneously. First reports suggested that 8082% of airflow was nasal at rest and that on exercise this decreased to 60% (17). In 20 subjects who switched from nasal to oronasal breathing during exercise, the initial nasal proportion of total ventilation was 57%, declining to 39% at the end of exercise when VE was 90 l/min (11). However, no data were provided as to the consistency of the change in nasal fraction among the subjects. A subsequent study confirmed that most subjects followed this pattern of nasal ventilation during exercise but demonstrated that some subjects breathed proportionately more nasally as they exercised at higher work rates (2).
0
INSPIRATORY
n
0.4
0.8
N ASAL FRACTION
FIG. 3. Identity plots of nasal flow fraction during expiration vs. that during inspiration and after exercise (B). Each symbol represents a different subject and shows mean values increments of 0.5 l/s between 1 and 3 l/s. Note similarity of inspiratory and expiratory nasal exercise and postexercise periods.
both during exercise (A) obtained using total flow flow fractions during both
Downloaded from www.physiology.org/journal/jappl at Washington Univ (128.252.067.066) on March 3, 2019.
ORONASAL
PARTITIONING
OF
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VENTILATION
0.8
0
0.4
0.8 0
EXERCISE
NASAL
0.4
0.8
FLOW FRACTION
FIG. 4. Identity plots of nasal flow fraction after exercise vs. that during exercise both during inspiration (A) and expiration (R). Each symbol represents a different subject and shows mean values obtained using total flow increments of 0.5 l/s between 1 and 3 l/s. Note similarity of exercise and postexercise nasal flow fractions during both inspiration and expiration.
This interindividual variability was confirmed in another study in which three of six normal subjects showed little change in nasal flow fraction during and after exercise, whereas the other three subjects showed a progressive decrease (5). In that study the proportion of nasal ventilation during exercise ranged between 20 and 90% (5). Thus, our data are consistent with studies that demonstrate the interindividual variability in both the absolute proportion of nasal ventilation and the pattern of change due to exercise-induced hyperpnea (2, 5). It has been suggested that the method of recording oronasal ventilation may account for some of the differences between studies (2). Niinimaa et al. (11) used a head-out exercise body plethysmograph and a nasal mask and Chadha et al. (5) used respiratory inductive
1
II CD -
EXERCISE
i II
I
-200 0
POST-EXERCISE
I 4
2
TIME
I 6
1 8
( min )
5. Difference between inspired and expired nasal volumes (per breath) plotted against time, measured from beginning of exercise period. Negative values indicate nasal expiration greater than inspiration. Four minutes denotes end of exercise period. Different symbols represent individual subjects. Note interindividual variability in difference between inspired and expired nasal volumes and difference between exercise and postexercise periods. FIG.
plethysmography and a nasal mask, whereas our study and that of Bethel et al. (2) used a two-compartment face mask. Hence the major difference between our study and most others was the use of a mask to measure oral ventilation, potentially altering the degree of mouth opening during oronasal breathing. However, it is unlikely that mouth opening was inadequate in our study, because we have shown oral resistances of ~0.5 cmH,O l 1-l s at 0.5 l/s inspiratory flow using our mask system (J. Wheatley, unpublished observations). Nevertheless, our subjects may have had their mouths open wider than normal, as suggested by the smaller initial nasal flow fractions. In addition, the face mask may have influenced the switching point from nasal to oronasal ventilation, because it was less than in previous studies (5, 11, 14). Thus we do not claim any physiological significance of our measured switching point. Our data are in agreement with other published studies showing that oronasal breathing is the normal pattern during exercise and that the absolute value of nasal ventilation increases throughout the exercise period. The proportion of nasal ventilation and its change during exercise in our study show considerable interindividual variability, as demonstrated in studies without a face mask (5). In addition, our data reveal more information about the control of oronasal partitioning. The tight relationship between the nasal flow fraction and total mean flow, related to the level of ventilation rather than the exercise itself, suggests that oronasal partitioning is probably determined by the ventilation rather than physical exercise itself. Furthermore the similar relationship between the nasal flow fraction and total mean flow during inspiration and expiration indicates that the direction of flow through the upper airway does not influence oronasal flow partitioning. The findings also suggest a tight control and modulation of the flow-partitioning mechanism in each individual. Inspired and expired nasal volume, considered on a breath-by-breath basis in each subject, differed between individuals and changed during exercise. In a given subject, either nasal inspired or nasal expired volume was
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l
550
ORONASAL
PARTITIONING
greater, depending on the level of exercise. There was no consistent pattern for the group. This differs from the study by Niinimaa et al. (ll), where nasal inspiration consistently exceeded nasal expiration. Unfortunately, no reports of interindividual variability or of any systematic changes during exercise were provided in that study. The ultimate mechanism that determines the degree of oronasal partitioning must be the relative airflow resistances of the oral and nasal pathways. Nasal resistance during exercise and at rest has been extensively investigated (7,8, 12). From these studies. it is clear that about two-thirds of the total nasal resistance is found at the entrance to the bony cavum of the nose in the vicinity of the pyriform aperture and about one-third in the cartilaginous vestibule (3, 9). There is very little contribution from the region of the soft palate and posterior choanae during nasal breathing only (16). Thus nasal breathing does not appear to have a mechanism capable of readily modulating oronasal partitioning. In addition, nasal resistance decreases substantially during exercise (7, 8), which, in itself, should increase the nasal fraction of flow. This is opposite to that observed in the majority of subjects, which also argues against nasal resistance being the major factor controlling oronasal partitioning. Much less is known about flow resistance of the oral pathway. Oral resistance was reported to be similar to that of the nasal airway in normal subjects at rest and to decrease with increasing exercise (6). In addition, a large reduction in oral resistance was observed with wider opening of the mouth. Thus the oral airway appears to have the appropriate mechanism to control oronasal partitioning, with the ability to vary its resistance from infinity to very low values. The potential major site determining oral resistance could vary from the lips and teeth to the posterior orifice between the tongue and soft palate. In our study the mask system tended to inhibit wide opening of the mouth and jaw. Hence an internal readjustment of the soft palate and tongue was a more likely mechanism controlling oronasal partitioning. Rodenstein and Stanescu (13) used fluoroscopy to demonstrate that the soft palate could direct upper airway flow, even with the mouth open. Their data support the concept that when the mouth is open, the soft palate is responsible for the partitioning of oronasal flow and, hence, the level of oral resistance. The differences between inspired and expired nasal volume also reflect intrabreath changes in relative resistance of the nasal and oral pathways. Nasal resistance may vary between inspiration and expiration because the cross-sectional area of the nasal valve may be greater during inspiration (10). However, changes in the oral pathway resistance during inspiration and expiration are more likely to be responsible for these intrabreath changes. Inspiratory contraction of upper airway dilator muscles may cause phasic dilation of the oral airway, decreasing the oral resistance during inspiration relative to that during expiration. In addition, there may be a passive mechanical effect secondary to the alternating negative and positive pressures in the compliant oral pathway. In this case, the negative inspiratory pressures tend to increase inspiratory oral resistance and the positive pressures tend to decrease expiratory resistance. The resultant oral resistance will
OF
VENTILATION
be a balance between these two opposing forces, which can allow any combination of inspiratory and expiratory oral resistances. As ventilation increases, the level of both phasic and tonic drive to upper airway dilator muscles increases. This will decrease the oral resistance during both inspiration and expiration and hence decrease the nasal fraction of flow during progressive exercise. The similarity of the inspiratory and expiratory nasal flow fractions, in the presence of phasic dilator muscle activity, may be due to passive dilating effects in expiration secondary to positive oral pathway pressures. It should be noted that although the inspiratory and expiratory nasal flow fractions are similar at the same total mean flow, they cannot be measured within the same breath. This is because total inspiratory and expiratory mean flows are not necessarily the same within a breath. The purpose of the change in oronasal partitioning during exercise is unclear but may relate to meeting the demands of increasing ventilation while trying to minimize respiratory work (using a lower-resistance oral pathway) but still maintaining some air-conditioning function of the nasal pathway. In conclusion, we have shown that, during exercise-induced hyperpnea, oronasal flow partitioning is related to the level of ventilation rather than the exercise itself and is uninfluenced by the direction of flow through the upper airway (i.e., inspiratory vs. expiratory). The level of partitioning was highly reproducible within an individual but showed significant interindividual variability in both the absolute level and the change with exercise-induced hyperpnea. These findings suggest tightly controlled modulation of the relative resistances of the oral and/or nasal pathways. Although the mechanism of this modulation is not known, we speculate that the oral pathway resistance controls the level of oronasal flow partitioning. The authors thank Ken Isles for expertise and assistance in the construction of the face masks and Jeanette Walker for invaluable secretarial assistance. This study was supported by the National Health and Medical Research Council of Australia. Address reprint requests to J. R. Wheatley. Received
14 November
1990; accepted
in final
form
12 April
1991.
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ORONASAL
PARTITIONING
9. HAIGHT, J. S. J., AND P. COLE. The site and function of the nasal valve. Laryngoscope 93: 49-55, 1983. 10. HAIRFIELD, W. M., D. W. WARREN, V. A. HINTON, AND D. L. SEATON. Inspiratory and expiratory effects of nasal breathing. Cleft Palate J. 24: 183-189, 1987. 11. NIINIMAA, V., P. COLE, S. MINTZ, AND R. J. SHEPHARD. Oronasal distribution of respiratory airflow. Respir. Physiol. 43: 69-75, 1981. 12. RICHERSON, H. B., AND P. M. SEEBOHM. Nasal airway response to exercise. J. Allergy 41: 269-284, 1968. 13. RODENSTEIN, D. O., AND D. C. STANESCU. Soft palate and oronasal breathing in humans. J. Appl. Physiol. 57: 651-657, 1984. 14. SAIBENE, F., P. MOGNONI, C. L. LAFORTUNA, AND R. MOSTARDI.
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15. 16.
17. 18.
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Oronasal breathing during exercise. Pfluegers Arch. 378: 65-69, 1978. SCHULTZ, E. L., AND S. M. HORVATH. Control of extrathoracic airway dynamics. J. Appl. Physiol. 66: 2839-2843, 1989. TAKAGI, Y., D. F. PROCTOR, S. SALMON, AND S. EVERING. Effects of cold air and carbon dioxide on nasal flow resistance. Ann. Otol. Rhinol. Laryngol. 78: 40-48, 1969. UDDSTR~MER, M. Nasal respiration. Acta Otoluryngol. 42, Suppl.: 3-146, 1940. WHEATLEY, J. R., T. C. AMIS, AND L. A. ENGEL. Relationship between alae nasi activation and breathing route during exercise in humans. J. Appl. Physiol. 71: 124-130, 1991.
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