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The switching point from nasal to oronasal breathing
Respiration Physiology (1980) 42, 61-71 © Elsevier/North-Holland Biomedical Press
THE SWITCHING POINT FROM NASAL TO ORONASAL BREATHING*'**
V. NIINIMAA 1, P. COLE 2, S. MINTZ 2 and R.J. SHEPHARD I 1 Department of Preventive Medicine and Biostatistics, University of Toronto, Toronto and 2 Gage Research Institute, Toronto, Canada
Abstract. The switching point from nasal to oronasal breathing during incrementally graded submaximal exercise was determined in 30 (14 M, 16 F) healthy adult volunteers. Nasal airflow was measured by a pneumotachograph attached to a nasal mask. Oral airflow was determined as the difference between nasal airflow and total pulmonary airflow, the latter being measured by a head-out exercise body plethysmograph. The airflow and pressure signals were sampled every 20 msec by a microprocessor, which calculated respiratory volumes and nasal work of breathing, and produced an on-line print-out. Twenty of the 30 subjects (normal augmenters) switched from nasal to oronasal breathing at submaximal exercise of 105.0 W (SD=30.1), four subjects (mouth breathers) breathed habitually oronasally, five subjects (nose breathers) persistently breathed through the nose only, and one subject showed no consistent nose/mouth breathing pattern. In normal augmenters, the onset of oronasal breathing (VE 35.3 + 10.8 1 • min- 1) was quite consistent individually, but varied considerably between individuals without showing a significant sex difference. The factors most closely related to the switching point were rating of perceived exertion of breathing and nasal work of breathing.
Exercise Nasal work of breathing
Ventilation
There are three possible ways for respiratory air to reach the lungs of a normal healthy subject, namely through the nose, mouth or a combination of both routes. Most people breathe through the nose at rest, switching to oronasal breathing at higher respiratory minute volumes. The present study sought to determine the switching point from nasal to oronasal breathing, and to establish the determinants of the switching point, examining physical characteristics of subjects, intensity of exercise, ventilatory variables, nasal work of breathing and the psychophysical evaluation of the effort of breathing (Borg, 1973). A problem faced in the study of Accepted.[or publication 19 May 1980 * Based in part on material presented by one of us (V.N.) in fulfillment of the requirements of a Ph.D. degree within the University of Toronto. ** This work was supportedin part by a grant from Physicians Services Inc. Foundation of Ontario, Canada. Address for reprint requests: Dr. V, Niinimaa, The University of Calgary, Faculty of Physical Education, 2500 University Drive N.W., Calgary, Alberta T2N 1N4, Canada. 61
62
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oronasal airflows is the separate and simultaneous measurement of the two airflows without disturbance of the spontaneous breathing pattern or the natural choice of airflow route by the subject. In the present study, nasal ventilation was measured by a pneumotachograph attached to a mask which covers the nose and the eyes. Airflow through the mouth was determined indirectly as the difference between total respiratory minute volume, as determined by a head-out exercise body plethysmograph (Niinimaa et al., 1979), and nasal ventilation. Respiratory minute volume was increased by having the subject pedal against graded resistances provided by an externally mounted electrically braked ergometer. Switching point was defined as the beginning of oral augmentation of nasal breathing, which occurs with increasing respiratory minute volume. A 'normal augmenter' breathes through the nose at rest, and switches to oronasal breathing with increasing respiratory minute volume. A 'nose breather' respires only nasally both at rest and during strenuous submaximal exercise. A "mouth breather" habitually breathes oronasally both at rest and during exercise.
Methods SUBJECTS
Subjects comprised of men and women in the age range of 15 to 35 years, recruited from the University community. All were non-smokers. During the initial visit, every subject was examined by an otolaryngologist who excluded subjects with obstructive abnormalities of the nose, throat and lower airway. Subjects performed a forced vital capacity manoeuvre and from the resulting flow-volume curve forced vital capacity (FVC), one sec forced expiratory volume (FEV~0) and flow rate at 50~0 FVC ('ks0) were determined. The subjects were then tested at three submaximal workloads on a cycle ergometer (Quinton Ideal Ergometer, Model 870) in order to predict their maximal physical working capacity (PWC(max)) and maximum oxygen intake (Vow(max)) at the age related predicted maximum heart rate (nomogram of Astrand, 1960).
EQUIPMENT
A head-out exercise body plethysmograph enabled the measurement of total pulmonary airflow both at rest and during graded exercise. Simultaneous independent measurement of nasal airflow were made with the aid of a modified U.S. Divers scuba mask that covered the face from the upper lip to the forehead. The tempered glass window o f the mask was replaced by a plexiglass plate, on which a # 2 Fleisch pneumotachograph was mounted. The oropharyngeal pressure signal was detected by a Validyne MP-45 transducer.
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63
TEST P R O T O C O L
After entering the plethysmograph, the mask was placed on the subject's face, and the seal was tested by having the subject attempt to breathe nasally through the blocked pneumotachograph. The subject was then instructed to 'breathe through the nose or mouth, whichever feels more comfortable'. The test was done in eight stages, each two minutes in duration. Ten consecutive breaths during the last 30 sec of each stage were analyzed. The respiratory variables, heart rate and the rating of perceived exertion of breathing (RPE(resp), Borg, 1973) were recorded at rest and while pedalling at ergometer power settings of 0, 10, 20 . . . . . 60~o of the subject's predicted PWC(max). Switching point values for the measured variables were determined as an average of the values observed immediately before and after the switch to oronasal breathing had occurred. Nasal work of breathing was measured at rest and during submaximal exercise on a cycle ergometer. Tests were carried out 15 min after completion of the oronasal airflow distribution determination. The mask was placed on the subject's face, and checked for an absence of air leakage. The measurements were made at rest and pedalling at 0, 10, 20 . . . . . 70~o of the subject's predicted PWC(max). Respiratory variables were recorded for 5 consecutive breaths during the last 20 sec of each 2-min stage. The transnasal pressure was measured by a per oral tube (3 cm i.d.), which was placed as deeply as possible into the mouth immediately before the measurement. The nasal pressure-flow curve was monitored on an oscilloscope to ensure that the oropharyngeal airway remained unobstructed during the tests. Oronasal airflow distribution and work of nasal breathing determinations were done on two separate days not more than seven days apart. At the completion of all tests, a debriefing questionnaire was administered to the subjects. This explored previous breathing instruction the subject might have received, together with the subject's opinions on nose/mouth breathing at rest and during exercise.
C A L C U L A T I O N OF R E S U L T S
The flow and pressure signals were sampled by a microprocessor every 20 msec. Flow was integrated to yield volume, and (since work = pressure x volume), the nasal work of breathing was obtained by integrating the product of the pressure difference across the nose and the nasal respired volume for each 20 msec interval (Cole et al., 1979a,b). Peak flows were estimated from respiratory minute volumes as suggested by Silverman et al. (1951). The microprocessor also calculated the values of the respiratory vaciables and nasal work of breathing, printing the results on-line.
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Results PHYSICAL CHARACTERISTICS
Physical characteristics of the 30 subjects (14 males, 16 females) are shown in table 1. Body surface area (BSA) was calculated from the subjects' height (cm) and mass (kg), using the equation of DuBois (1927). TABLE 1 Physical characteristics of the subjects (X ± SD)
n Age (years) Height(cm) Body m a s s ( k g ) BSA(m2) "~o,(max)(l. m i n - J)* (ml.kg I-rain-I)* PWC(max)(W)*
Men
Women
14 21.6 _+ 3.8 178.0 + 4.4 70.5 ± 9.1 1.87+_ 0.12 4.03_+ 1.02 57.6 ± 1 4 . 4 289.2 +_+70.8
16 22.9 _+ 5.4 165.4 ± 5.9 59.6 ± 5.3 1.66+_ 0.09 2.71 ± 0.51 45.6 +_ 7.8 185.0 +_34.6
* Predicted values. PWC(max), Maximal physical working capacty at age related m a x i m u m heart rate.
PULMONARY FUNCTION
Predicted values were determined from the norms of Goldman and Becklake (1959) and Lapp and Hyatt (1967). In the men, results for the three pulmonary function measurements (FVC, FEV~,, Vm) were very close to predicted values (97.3 to 103.4 Jo), whereas values for the women were insignificantly higher than predicted (105.2 to 112.Tj'%). o /
SWITCHING POINT
A majority of the subjects (67%, normal augmenters) switched from nasal to orally augmented breathing at a reproducible value as respiratory minute volume was increased above its resting level (table 2). Four subjects (13%L mouth breathers) breathed oronasally even at rest, and continued to do so throughout the test. By contrast, five subjects (17},~, nose breathers, all females) breathed solely through the nose both at rest and throughout the submaximal exercise period. One subject's nose/mouth breathing pattern was unpredictable and inconsistent in four tests; this subject's data were excluded from further analysis.
65
SWITCHING POINT TABLE 2
Tabulation of subjects by mode of breathing
Normal augmenters
Mouth breathers Nose breathers Irregulars
Men
Women
Total
~
10 3 0 1
10 1 5 0
20 4 5 1
67 13 17 3
TABLE 3
Characteristics of the key variables at the switching point from nasal to oronasal breathing (x + SD)
V E ( 1 . m i n J) VT (1 BTPS) fR(breath.min -j) fh ( b e a t s . m i n -1)
Work rate(W) ~oPWC(max) RPE(resp) Av. flow (insp 1 • sec- l) Av. flow(exp 1 . s e c -1) Peak flow (insp 1 .'sec l) Peakflow(expl.sec -l) Nasalwork ( J . l - j ) of breathing ( J . m i n - j ) (J.breath -l)
Men (n = 10)
W o m e n (n = 10)
Combined (n = 20)
36.3 + 1 0 . 0 1.57 + 0.49 23.1 + 7.0 125.1 + 19.7 108.8 + 3 0 . 2 37.8 + 12.1 12.5 + 2.0 1.34 +_ 0.32 1.14+ 0.35 1.66+_ 0.46 1.75+ 0.48 0 . 9 1 + 0.20 89.0 _+72.7 3.96_+ 3.18
34.4 +_ 11.9 1.55 + 0.39 22.3 + 4.1 145.7 + 20.1 101.1 + 30.0 54.9 +_ 12.7 13.9 + 2.2 1.23 + 0.38 1.10+ 0.41 1.58-+ 0.55 1.66_+ 0.58 0.73+ 0.24 117.8 + 157.9 4.71_+ 7.19
35.3 + 10.8 1.56 + 0.43 22.7 + 5.6 * 105.0 _+ 30.1 * ]3.2 + 2.2 1.29 + 0.35 1.12+ 0.37 1.62 + 0.49 1.71+ 0.52 0.82+ 0.23 102.7 + 118.8 4.32+ 5.30
* Combined value not given because of a statistically significant sex difference RPE(resp), Rating of perceived exertion of breathing (Borg, 1973). ~ P W C ( m a x ) , Percentage of predicted m a x i m u m physical working capacity.
A description of the switching point, based upon the averaged results of two tests on each individual subject, is shown in table 3. Augmentation of nasal breathing occurred at approximately the same respiratory minute volume and the same rate of work in both sexes. A one-way analysis of variance showed that among the ventilatory variables intra-individual variation ranged from 15.9 to 17.1 ~ of the total variation. For the work rate related terms, the proportion was somewhat higher (19.3 to 26.7~o). The relationships between the measured variables and the switching point were investigated by discriminant analysis (Nie et al., 1975), using data from the stages immediately before and after the switching point. Rating of perceived exertion of breathing and total nasal work of breathing (inspired + expired) per unit volume (J. I-') were related significantly to the switching point, these two terms alone having a predictive capability of 68.9~.
66
V. N I I N I M A A ~'t a/.
Total and inspired nasal work of breathing (,-
II
3.0
2.5
~4
Mouthbreathers
----.
Normal augmenters
----Nose
~
.~.e.~,:*~r*"
breathers
,~*
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2.0
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.~***
~.~...
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1.5
• *•
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~).~ < 7 . ~
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:.~."
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RESPIRATORYMINUTEVOLUME {l,min -I E~TPE)
Fig. 1. Total and inspired nasal ork of breathing (J • I I).
The total nasal work of breathing (inspired and expired) per unit volume is shown in fig. 1. The nasal work of breathing did not differ significantly between the nose breathers and normal augmenters: however, it was significantly higher (P < 0.05) in the mouth breathers than in the other two groups (fig. 1). The linearity of the relationship between nasal work of breathing (J. 1 t) and respiratory minute volume was suggested by a mean correlation coefficient of 0.98 + 0.02 in 60 groups of observation (9 observations per set, 30 subjects tested twice). The linearity was further confirmed through multiple regression techniques, eliminating the possibility that an exponential function would describe this relationship more accurately. The physical characteristics of males in the group of 4 (3 M, 1 F) mouth breathers differed from normal augmenters only in aerobic power (Vow(max), ml- kg ] • rain ~), the three men being significantly (P < 0.05) fitter than the 10 normal augmenters. All four mouth breathers participated in regular physical training to prepare for rigorous endurance such as distance running or crosscountry skiing. The physical characteristics of the five nose breathers, all of whom were females, did not differ significantly from the 10 normal female augmenters.
Discussion of results SUBJECT MATERIAL
The height and mass of both men and women in the present study did not differ significantly from values for average Canadians of the same age (table 4). The lung
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67
TABLE 4 Comparison of the physical characteristics of the average Canadian and subjects of the present study (~ _+SD) Males
Present study
Bailey et al. (1974)
n Age (years) Height (cm) Body mass (kg) Pred. ~/o2(max) (ml. kg- 1 . min- 1, STPD)
14 21.6 + 3.8 178.0 + 4,4 70.5 +_ 9,1 57.6 + 14.4
104 25.7 +_ 2.8 176.9 + 7.3 77.5 + 10.6 36.4 + 8.0
16 22.9 +_ 5.4 165.4 + 5.9 59.6 + 5.3 45.6 + 7.8
138 23.8 +_2.9 162.1 + 5.6 57.4 +_7.0 30.6 + 7.2
Significance (2-tailed t-test)
***
***
Females n Age (years) Height (cm) Body mass (kg) Pred. "V'o~.(max) (ml. kg- 1. min- 1, S'rPD) *** P < 0.001.
f u n c t i o n values for b o t h m e n a n d w o m e n d i d n o t v a r y significantly f r o m p r e d i c t e d values. A e r o b i c p o w e r o f b o t h m e n a n d w o m e n was significantly higher ( P < 0.001) t h a n that o f the average C a n a d i a n (table 4). H o w e v e r , it is unlikely t h a t the h i g h e r average fitness level o f o u r subjects affected the switching p o i n t , for the p r e d i c t e d Vo2(max) d i d n o t emerge as a d e t e r m i n i n g factor for the switching point, a n d very fit subjects were i n c l u d e d a m o n g b o t h nose a n d m o u t h b r e a t h e r s as well as in the normal augmenters.
DESCRIPTION OF THE SWITCHING POINT In the p r e s e n t study, the switch to o r o n a s a l b r e a t h i n g o c c u r r e d at ~/E o f 3 5 . 3 + 10.8 1 . m i n - ' BTPS, w h i c h c o n c u r s well with the s t a t e m e n t o f C a m p b e l l e t al. (1970, p. 102). Saibene e t al. (1978) i n d i c a t e d t h a t the switch occurs at VE o f 40.2 1. min-~. T h e i r higher value was p r o b a b l y due to the 10 1 . m -~ i n c r e m e n t s in v e n t i l a t i o n the subjects s u r p a s s i n g the switching p o i n t b y an average o f 5 1. m i n - ' . Saibene e t al. (1965) n o t e d t h a t the switching p o i n t o c c u r r e d at i n s p i r a t o r y a n d e x p i r a t o r y flow rates o f 2.9 a n d 3.2 1 • sec- ', respectively. T h e i r values d o n o t agree with the p r e s e n t study ( i n s p i r a t i o n : 1.34 1. sec -1 average, 1.66 1-sec -~ p e a k , e x p i r a t i o n : 1.14 1- s e c - 1 average, 1.75 1. sec- ~ p e a k , (table 3) n o r with the results o f
68
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Patrick and Sharp (1969) (inspiratory peak flow 1.14 1. s e c ATPS); the latter data concur well with the present study. Perrin et al. (1977) reported that the work rate at the switching point varied from 80-180 W. Results of the present study (105.0 + 30.1 W) fall well within this range.
VARIABILITY OF THE S W I T C H I N G P O I N T
The rather small intra-individual variation of the rating of perceived exertion of breathing, ventilatory and work related variables (13.2 to 26.7~i of total variation for a given variable) indicates that in any one person each of these variables bears a fairly consistent relationship to the switching point from day to day. The inter-individual variation of the variables measured at the switching point was quite large. The variation of "~'E at switching point (SD = 10.8 1- min) is very close to the value (9.4 I. min) reported by Saibene et al. (a978). The conclusion suggested by the present study and most of the available literature is that the switching point ranges widely from one person to another; indeed, in some (mouth breathers) the values are essentially zero and in others (nose breathers) essentially infinite. The results of the present study also suggest that unless account is taken of consistent mouth and consistent nose breathers, there is no significant sex difference in the switching point. The exceptions are the percentage of PWC(max) and heart rate, which are related to the significantly lower absolute PWC(max) of women (table 2). Uddstr6mer (1940) also concluded that no sex difference was evident in the nose/mouth breathing pattern of normal subjects.
D E T E R M I N A N T S OF THE S W I T C H I N G POINT
Discriminant analysis indicated that rating of perceived exertion of breathing and nasal work of breathing were the two significant determinants of the switching point. The role of sensation is supported by Gamberale et al. (1978), who reported that there is a linear relationship between added respiratory resistance and magnitude of perception, and that subjects are able to make meaningful quantitative judgments of added respiratory resistances. The sensory input may be explained by the length: tension appropriateness theory (Campbell, 1966). The relationship of nasal resistance to the switching point has been assessed in a number of studies. Some investigators have concluded that nasal resistance influences the switching point (Saketkhoo et al., 1979; Korinkova et al., 1978; Patrick and Sharp, 1970; Saibene et al., 1965). Others minimized the role of nasal resistance (Perrin et al., 1977; Takagi et al., 1969), and recently Saibene et al. (1978) showed no correlation between nasal resistance and the switching point.
SWITCHING POINT
69
Results of the present study support the view that nasal resistance has some influence on the switching point, but the perception of effort in breathing is the most significant determinant. However, these two variables predicted the switching point with only 68.9~o accuracy, suggesting that there may be determinants other than those investigated in the present study. Results of the present study do not support the view that the switch to oronasal breathing is triggered by a collapse of the anterior nares (Bouhuys, 1977, p. 28 ; Proctor, 1977), for there is no indication of a change in slope of the nasal work of breathing-respiratory minute volume relationship at the switching point ('V'E 35.3 1- min -~, fig. 1). The alar muscles appear to function during inspiration to prevent the collapse of the nares (Mann et al., 1977; Sasaki and Mann, 1976).
MOUTH BREATHERS
Previous studies have indicated the proportion of mouth breathers in young male subjects as 10.5 to 15.8~ (Uddstr6mer, 1940) and 15.8~ (Saibene et al., 1978). Their results agree with the present study (13~). Neither Saibene et al. (1978) nor Uddstr6mer (1940) put forth any hypothesis to explain reasons for habitual mouth breathing. Comparison of mouth breathers (3 males) with normal augmenters of the same sex showed that the aerobic power (ml. kg -j. min -1) was significantly (P < 0.05) higher in the mouth breathers, as was their nasal work of breathing (fig. 1). All mouth breathers also indicated taking part in vigorous physical training for endurance competition. This would suggest that if increased nasal resistance forces these subjects to breathe oronasally at lower respiratory minute volume, and the "~'E is elevated above switching point daily during training, these subjects habituate themselves to oronasal breathing. The view that mouth breathing is a learned behavior is supported by the literature (Bouhuys, 1977, p. 28; Williams, 1970, p. 42; Polgar and Kong, 1965).
NOSE BREATHERS
In the present study, 17~o (5 out of 30) of the subjects (all females) breathed nasally both at rest and throughout the range of submaximal exercise. The proportions of nose breathers cited in previous studies of males are 7.6~ (Uddstr6mer, 1940) and 7.9~ (Saibene et al., 1978). Neither author offered any explanation for the preference of some subjects for nasal breathing. The present study showed no significant differences in either the physical characteristics or in nasal work of breathing (fig. 1) between the nose breathers and normal augmenters. The debriefing survey showed that although some of the nose breathers (3 out of 5) felt that more air would be available through the mouth, they preferred to breathe through the nose either because the subject was more comfortable with nasal breathing,
70
v. NIINIMAA ~': a/.
o r beca~ase o r o n a s a l that
the stimuli
breathing
to switch
was associated
to oronasal
with gasping
breathing
may
f o r air. T h i s s u g g e s t s
be overridden
by higher
centres of the brain.
References ~strand, 1. (1960). Aerobic work capacity in men and women with special reference to age. Acta Physiol. Scand. 49 (Suppl. 169): 1 91. Borg, G. A. V. (1973). Perceived exertion: a note on "history' and methods. Med. Sci. Sport.s 5:90 93. Bouhuys, A. (1977). The Physiology of Breathing. A textbook for medical students. New York, Grune and Stratton. Campbell, E . J . M . (1966). The relationship of the sensation of breathlessness to the act of breathing. In: Breathlessness, edited by J.B.L. Howell and E.J.M. Campbell. Oxford, Blackw Scientific Publication, pp. 55 64. Campbell, E . J . M . , E. Agostoni and J. Newsom Davis (1970). The Respiratory Muscles. London. Lloyd-Luke. Cole, P., S. Mintz, V. Niinimaa and F. Silverman (1979a). Nasal aerodynamics. J. Otolawngol 8:191 195. Cole, P.. V. Niinimaa, S. Mintz and F. Silverman (1979b). Work of nasal breathing; Measurement of each nostril independently using a split mask. Acta Otolarvngol. 88:148 154. DuBois, E. F. (1927). Basal Metabolism in Health and Disease. Philadelphia, Lea and Febiger. Gamberale, F., 1. Holmer, A.-S. Kindblom and A. Nordstr6m (1978). Magnitude Perception of added inspiratory resistance during steady-state exercise. Ergonomics 21 : 531 538. Goldman, H.I. and M.R. Becklake (1959). Respiratory function tests: Normal values at median altitudes and the prediction of" normal results. Am. Lev. Tuherc. 79:457 467. Korinkova, S., Z. VIc and E. Hoznauerova (1978). Proudovy nosno odpor v zateaovem testa. Cesk. Otolarvngol. 27:160 164. Lapp, N. L. and R.E. Hyatt (1967). Some factors affecting the relationship of maximal expiratory flow to lung volume in health and disease. Dis. Chest 51:475 481. Mann. D.G., C.T. Sasaki, M. Suzuki, H. Fukuda and J. R. Hernandez (1977). Dilatator naris muscle. Ann. Otol. Rhinol. Laryngol. 86:362 372. Nie, N.H., C.H. HullJ. G. Jenkins, K. Steirlbrenner and D.H. Brent (1975). Statistical Packages for the Social Sciences (2nd edn.) McGraw-Hill Book Company. Niinimaa, V., P. Cole, S. Mintz and R.J. Shephard (1979). A head-out body plethysmograph. J. Appl. Physiol. 47:1336 1339. Patrick. G. A. and G. R. Sharp (1969). Oronasal distribution of in spiratory flow during various activities. Proc. Physiol. Sot., pp. 22 23. Perrin. CI., J. Lacoste and R. Marl (1977). A nasal function test: The opening of mouth during physical effort. Rhinol. 15:33 38. Polgar, G. and G. P. Kong (1965). The nasal resistance of newborn infants. J. Pediatrics 67:557 567. Proctor, D. F. (1977). The upper airways. I. Nasal physiology and defence ot" the hlngs. Am. Rev. Resp. Dis. 115:97 129. Saibene, F., P. Mognoni and G. Sant'Ambrogio (1965). Lavoro rcspiratorio e ventilazione al passagio dall respirazione nasale a quella orale. Boll. Soc. ltal. Biol. Sper. 41:1550 1552. Saibene, F., P. Mognoni, C. L. Lafortuna and R. Mostardi (1978). Oronasal breathing during exercise. p/lii~ers Arch. 378:65 69. Saketkhoo, K., I. Kaplan and M.A. Sackner (1979). Effects of exercise on nasal mucous velocity and nasal airflow resistance in normal subjects..I. Appl. Plo, siol. 46:369 371. Sasaki. C.T. and D.G. Mann (1976). Dilator naris function A useful test of Iitcial nerve integrity. Arch. Ololao'n~fol. 102: 365-367.
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71
Silverman, L., G. Lee, T. Plotkin, L.A. Sawyers and A.R. Yancey (1951). Air flow measurements on human subjects with and without resistance at several work loads. Arch. Ind. Hygiene 3:461-478. Takagi, Y., D. F. Proctor, S. Salman and S. Evering (1969). Effects of cold air and carbon dioxide on nasal air flow resistance. Ann. Otolaryngol 78: 4048. Uddstr6mer, M. (1940). Nasal respiration. Acta Otolaryngol. Suppl. 42: 3-146. Williams, H.L. (1970). Definitions of Terms Used in Rhinometry with Suggested Standard Symbols. A Handbook and Glossary. Rochester, Minn., American Academy of Ophthalmology and Otolaryngology.
THE SWITCHING POINT FROM NASAL TO ORONASAL BREATHING*'**
V. NIINIMAA 1, P. COLE 2, S. MINTZ 2 and R.J. SHEPHARD I 1 Department of Preventive Medicine and Biostatistics, University of Toronto, Toronto and 2 Gage Research Institute, Toronto, Canada
Abstract. The switching point from nasal to oronasal breathing during incrementally graded submaximal exercise was determined in 30 (14 M, 16 F) healthy adult volunteers. Nasal airflow was measured by a pneumotachograph attached to a nasal mask. Oral airflow was determined as the difference between nasal airflow and total pulmonary airflow, the latter being measured by a head-out exercise body plethysmograph. The airflow and pressure signals were sampled every 20 msec by a microprocessor, which calculated respiratory volumes and nasal work of breathing, and produced an on-line print-out. Twenty of the 30 subjects (normal augmenters) switched from nasal to oronasal breathing at submaximal exercise of 105.0 W (SD=30.1), four subjects (mouth breathers) breathed habitually oronasally, five subjects (nose breathers) persistently breathed through the nose only, and one subject showed no consistent nose/mouth breathing pattern. In normal augmenters, the onset of oronasal breathing (VE 35.3 + 10.8 1 • min- 1) was quite consistent individually, but varied considerably between individuals without showing a significant sex difference. The factors most closely related to the switching point were rating of perceived exertion of breathing and nasal work of breathing.
Exercise Nasal work of breathing
Ventilation
There are three possible ways for respiratory air to reach the lungs of a normal healthy subject, namely through the nose, mouth or a combination of both routes. Most people breathe through the nose at rest, switching to oronasal breathing at higher respiratory minute volumes. The present study sought to determine the switching point from nasal to oronasal breathing, and to establish the determinants of the switching point, examining physical characteristics of subjects, intensity of exercise, ventilatory variables, nasal work of breathing and the psychophysical evaluation of the effort of breathing (Borg, 1973). A problem faced in the study of Accepted.[or publication 19 May 1980 * Based in part on material presented by one of us (V.N.) in fulfillment of the requirements of a Ph.D. degree within the University of Toronto. ** This work was supportedin part by a grant from Physicians Services Inc. Foundation of Ontario, Canada. Address for reprint requests: Dr. V, Niinimaa, The University of Calgary, Faculty of Physical Education, 2500 University Drive N.W., Calgary, Alberta T2N 1N4, Canada. 61
62
v. NIINIMAA
ct al.
oronasal airflows is the separate and simultaneous measurement of the two airflows without disturbance of the spontaneous breathing pattern or the natural choice of airflow route by the subject. In the present study, nasal ventilation was measured by a pneumotachograph attached to a mask which covers the nose and the eyes. Airflow through the mouth was determined indirectly as the difference between total respiratory minute volume, as determined by a head-out exercise body plethysmograph (Niinimaa et al., 1979), and nasal ventilation. Respiratory minute volume was increased by having the subject pedal against graded resistances provided by an externally mounted electrically braked ergometer. Switching point was defined as the beginning of oral augmentation of nasal breathing, which occurs with increasing respiratory minute volume. A 'normal augmenter' breathes through the nose at rest, and switches to oronasal breathing with increasing respiratory minute volume. A 'nose breather' respires only nasally both at rest and during strenuous submaximal exercise. A "mouth breather" habitually breathes oronasally both at rest and during exercise.
Methods SUBJECTS
Subjects comprised of men and women in the age range of 15 to 35 years, recruited from the University community. All were non-smokers. During the initial visit, every subject was examined by an otolaryngologist who excluded subjects with obstructive abnormalities of the nose, throat and lower airway. Subjects performed a forced vital capacity manoeuvre and from the resulting flow-volume curve forced vital capacity (FVC), one sec forced expiratory volume (FEV~0) and flow rate at 50~0 FVC ('ks0) were determined. The subjects were then tested at three submaximal workloads on a cycle ergometer (Quinton Ideal Ergometer, Model 870) in order to predict their maximal physical working capacity (PWC(max)) and maximum oxygen intake (Vow(max)) at the age related predicted maximum heart rate (nomogram of Astrand, 1960).
EQUIPMENT
A head-out exercise body plethysmograph enabled the measurement of total pulmonary airflow both at rest and during graded exercise. Simultaneous independent measurement of nasal airflow were made with the aid of a modified U.S. Divers scuba mask that covered the face from the upper lip to the forehead. The tempered glass window o f the mask was replaced by a plexiglass plate, on which a # 2 Fleisch pneumotachograph was mounted. The oropharyngeal pressure signal was detected by a Validyne MP-45 transducer.
SWITCHING POINT
63
TEST P R O T O C O L
After entering the plethysmograph, the mask was placed on the subject's face, and the seal was tested by having the subject attempt to breathe nasally through the blocked pneumotachograph. The subject was then instructed to 'breathe through the nose or mouth, whichever feels more comfortable'. The test was done in eight stages, each two minutes in duration. Ten consecutive breaths during the last 30 sec of each stage were analyzed. The respiratory variables, heart rate and the rating of perceived exertion of breathing (RPE(resp), Borg, 1973) were recorded at rest and while pedalling at ergometer power settings of 0, 10, 20 . . . . . 60~o of the subject's predicted PWC(max). Switching point values for the measured variables were determined as an average of the values observed immediately before and after the switch to oronasal breathing had occurred. Nasal work of breathing was measured at rest and during submaximal exercise on a cycle ergometer. Tests were carried out 15 min after completion of the oronasal airflow distribution determination. The mask was placed on the subject's face, and checked for an absence of air leakage. The measurements were made at rest and pedalling at 0, 10, 20 . . . . . 70~o of the subject's predicted PWC(max). Respiratory variables were recorded for 5 consecutive breaths during the last 20 sec of each 2-min stage. The transnasal pressure was measured by a per oral tube (3 cm i.d.), which was placed as deeply as possible into the mouth immediately before the measurement. The nasal pressure-flow curve was monitored on an oscilloscope to ensure that the oropharyngeal airway remained unobstructed during the tests. Oronasal airflow distribution and work of nasal breathing determinations were done on two separate days not more than seven days apart. At the completion of all tests, a debriefing questionnaire was administered to the subjects. This explored previous breathing instruction the subject might have received, together with the subject's opinions on nose/mouth breathing at rest and during exercise.
C A L C U L A T I O N OF R E S U L T S
The flow and pressure signals were sampled by a microprocessor every 20 msec. Flow was integrated to yield volume, and (since work = pressure x volume), the nasal work of breathing was obtained by integrating the product of the pressure difference across the nose and the nasal respired volume for each 20 msec interval (Cole et al., 1979a,b). Peak flows were estimated from respiratory minute volumes as suggested by Silverman et al. (1951). The microprocessor also calculated the values of the respiratory vaciables and nasal work of breathing, printing the results on-line.
64
v. N I I N I M A A ~'t a/.
Results PHYSICAL CHARACTERISTICS
Physical characteristics of the 30 subjects (14 males, 16 females) are shown in table 1. Body surface area (BSA) was calculated from the subjects' height (cm) and mass (kg), using the equation of DuBois (1927). TABLE 1 Physical characteristics of the subjects (X ± SD)
n Age (years) Height(cm) Body m a s s ( k g ) BSA(m2) "~o,(max)(l. m i n - J)* (ml.kg I-rain-I)* PWC(max)(W)*
Men
Women
14 21.6 _+ 3.8 178.0 + 4.4 70.5 ± 9.1 1.87+_ 0.12 4.03_+ 1.02 57.6 ± 1 4 . 4 289.2 +_+70.8
16 22.9 _+ 5.4 165.4 ± 5.9 59.6 ± 5.3 1.66+_ 0.09 2.71 ± 0.51 45.6 +_ 7.8 185.0 +_34.6
* Predicted values. PWC(max), Maximal physical working capacty at age related m a x i m u m heart rate.
PULMONARY FUNCTION
Predicted values were determined from the norms of Goldman and Becklake (1959) and Lapp and Hyatt (1967). In the men, results for the three pulmonary function measurements (FVC, FEV~,, Vm) were very close to predicted values (97.3 to 103.4 Jo), whereas values for the women were insignificantly higher than predicted (105.2 to 112.Tj'%). o /
SWITCHING POINT
A majority of the subjects (67%, normal augmenters) switched from nasal to orally augmented breathing at a reproducible value as respiratory minute volume was increased above its resting level (table 2). Four subjects (13%L mouth breathers) breathed oronasally even at rest, and continued to do so throughout the test. By contrast, five subjects (17},~, nose breathers, all females) breathed solely through the nose both at rest and throughout the submaximal exercise period. One subject's nose/mouth breathing pattern was unpredictable and inconsistent in four tests; this subject's data were excluded from further analysis.
65
SWITCHING POINT TABLE 2
Tabulation of subjects by mode of breathing
Normal augmenters
Mouth breathers Nose breathers Irregulars
Men
Women
Total
~
10 3 0 1
10 1 5 0
20 4 5 1
67 13 17 3
TABLE 3
Characteristics of the key variables at the switching point from nasal to oronasal breathing (x + SD)
V E ( 1 . m i n J) VT (1 BTPS) fR(breath.min -j) fh ( b e a t s . m i n -1)
Work rate(W) ~oPWC(max) RPE(resp) Av. flow (insp 1 • sec- l) Av. flow(exp 1 . s e c -1) Peak flow (insp 1 .'sec l) Peakflow(expl.sec -l) Nasalwork ( J . l - j ) of breathing ( J . m i n - j ) (J.breath -l)
Men (n = 10)
W o m e n (n = 10)
Combined (n = 20)
36.3 + 1 0 . 0 1.57 + 0.49 23.1 + 7.0 125.1 + 19.7 108.8 + 3 0 . 2 37.8 + 12.1 12.5 + 2.0 1.34 +_ 0.32 1.14+ 0.35 1.66+_ 0.46 1.75+ 0.48 0 . 9 1 + 0.20 89.0 _+72.7 3.96_+ 3.18
34.4 +_ 11.9 1.55 + 0.39 22.3 + 4.1 145.7 + 20.1 101.1 + 30.0 54.9 +_ 12.7 13.9 + 2.2 1.23 + 0.38 1.10+ 0.41 1.58-+ 0.55 1.66_+ 0.58 0.73+ 0.24 117.8 + 157.9 4.71_+ 7.19
35.3 + 10.8 1.56 + 0.43 22.7 + 5.6 * 105.0 _+ 30.1 * ]3.2 + 2.2 1.29 + 0.35 1.12+ 0.37 1.62 + 0.49 1.71+ 0.52 0.82+ 0.23 102.7 + 118.8 4.32+ 5.30
* Combined value not given because of a statistically significant sex difference RPE(resp), Rating of perceived exertion of breathing (Borg, 1973). ~ P W C ( m a x ) , Percentage of predicted m a x i m u m physical working capacity.
A description of the switching point, based upon the averaged results of two tests on each individual subject, is shown in table 3. Augmentation of nasal breathing occurred at approximately the same respiratory minute volume and the same rate of work in both sexes. A one-way analysis of variance showed that among the ventilatory variables intra-individual variation ranged from 15.9 to 17.1 ~ of the total variation. For the work rate related terms, the proportion was somewhat higher (19.3 to 26.7~o). The relationships between the measured variables and the switching point were investigated by discriminant analysis (Nie et al., 1975), using data from the stages immediately before and after the switching point. Rating of perceived exertion of breathing and total nasal work of breathing (inspired + expired) per unit volume (J. I-') were related significantly to the switching point, these two terms alone having a predictive capability of 68.9~.
66
V. N I I N I M A A ~'t a/.
Total and inspired nasal work of breathing (,-
II
3.0
2.5
~4
Mouthbreathers
----.
Normal augmenters
----Nose
~
.~.e.~,:*~r*"
breathers
,~*
~e*j'
2.0
w~**"
.~***
~.~...
,Y
A ~_ <
1.5
• *•
...
~).~ < 7 . ~
.....
:.~."
.....
< 0.5
RESPIRATORYMINUTEVOLUME {l,min -I E~TPE)
Fig. 1. Total and inspired nasal ork of breathing (J • I I).
The total nasal work of breathing (inspired and expired) per unit volume is shown in fig. 1. The nasal work of breathing did not differ significantly between the nose breathers and normal augmenters: however, it was significantly higher (P < 0.05) in the mouth breathers than in the other two groups (fig. 1). The linearity of the relationship between nasal work of breathing (J. 1 t) and respiratory minute volume was suggested by a mean correlation coefficient of 0.98 + 0.02 in 60 groups of observation (9 observations per set, 30 subjects tested twice). The linearity was further confirmed through multiple regression techniques, eliminating the possibility that an exponential function would describe this relationship more accurately. The physical characteristics of males in the group of 4 (3 M, 1 F) mouth breathers differed from normal augmenters only in aerobic power (Vow(max), ml- kg ] • rain ~), the three men being significantly (P < 0.05) fitter than the 10 normal augmenters. All four mouth breathers participated in regular physical training to prepare for rigorous endurance such as distance running or crosscountry skiing. The physical characteristics of the five nose breathers, all of whom were females, did not differ significantly from the 10 normal female augmenters.
Discussion of results SUBJECT MATERIAL
The height and mass of both men and women in the present study did not differ significantly from values for average Canadians of the same age (table 4). The lung
SWITCHING POINT
67
TABLE 4 Comparison of the physical characteristics of the average Canadian and subjects of the present study (~ _+SD) Males
Present study
Bailey et al. (1974)
n Age (years) Height (cm) Body mass (kg) Pred. ~/o2(max) (ml. kg- 1 . min- 1, STPD)
14 21.6 + 3.8 178.0 + 4,4 70.5 +_ 9,1 57.6 + 14.4
104 25.7 +_ 2.8 176.9 + 7.3 77.5 + 10.6 36.4 + 8.0
16 22.9 +_ 5.4 165.4 + 5.9 59.6 + 5.3 45.6 + 7.8
138 23.8 +_2.9 162.1 + 5.6 57.4 +_7.0 30.6 + 7.2
Significance (2-tailed t-test)
***
***
Females n Age (years) Height (cm) Body mass (kg) Pred. "V'o~.(max) (ml. kg- 1. min- 1, S'rPD) *** P < 0.001.
f u n c t i o n values for b o t h m e n a n d w o m e n d i d n o t v a r y significantly f r o m p r e d i c t e d values. A e r o b i c p o w e r o f b o t h m e n a n d w o m e n was significantly higher ( P < 0.001) t h a n that o f the average C a n a d i a n (table 4). H o w e v e r , it is unlikely t h a t the h i g h e r average fitness level o f o u r subjects affected the switching p o i n t , for the p r e d i c t e d Vo2(max) d i d n o t emerge as a d e t e r m i n i n g factor for the switching point, a n d very fit subjects were i n c l u d e d a m o n g b o t h nose a n d m o u t h b r e a t h e r s as well as in the normal augmenters.
DESCRIPTION OF THE SWITCHING POINT In the p r e s e n t study, the switch to o r o n a s a l b r e a t h i n g o c c u r r e d at ~/E o f 3 5 . 3 + 10.8 1 . m i n - ' BTPS, w h i c h c o n c u r s well with the s t a t e m e n t o f C a m p b e l l e t al. (1970, p. 102). Saibene e t al. (1978) i n d i c a t e d t h a t the switch occurs at VE o f 40.2 1. min-~. T h e i r higher value was p r o b a b l y due to the 10 1 . m -~ i n c r e m e n t s in v e n t i l a t i o n the subjects s u r p a s s i n g the switching p o i n t b y an average o f 5 1. m i n - ' . Saibene e t al. (1965) n o t e d t h a t the switching p o i n t o c c u r r e d at i n s p i r a t o r y a n d e x p i r a t o r y flow rates o f 2.9 a n d 3.2 1 • sec- ', respectively. T h e i r values d o n o t agree with the p r e s e n t study ( i n s p i r a t i o n : 1.34 1. sec -1 average, 1.66 1-sec -~ p e a k , e x p i r a t i o n : 1.14 1- s e c - 1 average, 1.75 1. sec- ~ p e a k , (table 3) n o r with the results o f
68
v. N I I N I M A A cta/.
Patrick and Sharp (1969) (inspiratory peak flow 1.14 1. s e c ATPS); the latter data concur well with the present study. Perrin et al. (1977) reported that the work rate at the switching point varied from 80-180 W. Results of the present study (105.0 + 30.1 W) fall well within this range.
VARIABILITY OF THE S W I T C H I N G P O I N T
The rather small intra-individual variation of the rating of perceived exertion of breathing, ventilatory and work related variables (13.2 to 26.7~i of total variation for a given variable) indicates that in any one person each of these variables bears a fairly consistent relationship to the switching point from day to day. The inter-individual variation of the variables measured at the switching point was quite large. The variation of "~'E at switching point (SD = 10.8 1- min) is very close to the value (9.4 I. min) reported by Saibene et al. (a978). The conclusion suggested by the present study and most of the available literature is that the switching point ranges widely from one person to another; indeed, in some (mouth breathers) the values are essentially zero and in others (nose breathers) essentially infinite. The results of the present study also suggest that unless account is taken of consistent mouth and consistent nose breathers, there is no significant sex difference in the switching point. The exceptions are the percentage of PWC(max) and heart rate, which are related to the significantly lower absolute PWC(max) of women (table 2). Uddstr6mer (1940) also concluded that no sex difference was evident in the nose/mouth breathing pattern of normal subjects.
D E T E R M I N A N T S OF THE S W I T C H I N G POINT
Discriminant analysis indicated that rating of perceived exertion of breathing and nasal work of breathing were the two significant determinants of the switching point. The role of sensation is supported by Gamberale et al. (1978), who reported that there is a linear relationship between added respiratory resistance and magnitude of perception, and that subjects are able to make meaningful quantitative judgments of added respiratory resistances. The sensory input may be explained by the length: tension appropriateness theory (Campbell, 1966). The relationship of nasal resistance to the switching point has been assessed in a number of studies. Some investigators have concluded that nasal resistance influences the switching point (Saketkhoo et al., 1979; Korinkova et al., 1978; Patrick and Sharp, 1970; Saibene et al., 1965). Others minimized the role of nasal resistance (Perrin et al., 1977; Takagi et al., 1969), and recently Saibene et al. (1978) showed no correlation between nasal resistance and the switching point.
SWITCHING POINT
69
Results of the present study support the view that nasal resistance has some influence on the switching point, but the perception of effort in breathing is the most significant determinant. However, these two variables predicted the switching point with only 68.9~o accuracy, suggesting that there may be determinants other than those investigated in the present study. Results of the present study do not support the view that the switch to oronasal breathing is triggered by a collapse of the anterior nares (Bouhuys, 1977, p. 28 ; Proctor, 1977), for there is no indication of a change in slope of the nasal work of breathing-respiratory minute volume relationship at the switching point ('V'E 35.3 1- min -~, fig. 1). The alar muscles appear to function during inspiration to prevent the collapse of the nares (Mann et al., 1977; Sasaki and Mann, 1976).
MOUTH BREATHERS
Previous studies have indicated the proportion of mouth breathers in young male subjects as 10.5 to 15.8~ (Uddstr6mer, 1940) and 15.8~ (Saibene et al., 1978). Their results agree with the present study (13~). Neither Saibene et al. (1978) nor Uddstr6mer (1940) put forth any hypothesis to explain reasons for habitual mouth breathing. Comparison of mouth breathers (3 males) with normal augmenters of the same sex showed that the aerobic power (ml. kg -j. min -1) was significantly (P < 0.05) higher in the mouth breathers, as was their nasal work of breathing (fig. 1). All mouth breathers also indicated taking part in vigorous physical training for endurance competition. This would suggest that if increased nasal resistance forces these subjects to breathe oronasally at lower respiratory minute volume, and the "~'E is elevated above switching point daily during training, these subjects habituate themselves to oronasal breathing. The view that mouth breathing is a learned behavior is supported by the literature (Bouhuys, 1977, p. 28; Williams, 1970, p. 42; Polgar and Kong, 1965).
NOSE BREATHERS
In the present study, 17~o (5 out of 30) of the subjects (all females) breathed nasally both at rest and throughout the range of submaximal exercise. The proportions of nose breathers cited in previous studies of males are 7.6~ (Uddstr6mer, 1940) and 7.9~ (Saibene et al., 1978). Neither author offered any explanation for the preference of some subjects for nasal breathing. The present study showed no significant differences in either the physical characteristics or in nasal work of breathing (fig. 1) between the nose breathers and normal augmenters. The debriefing survey showed that although some of the nose breathers (3 out of 5) felt that more air would be available through the mouth, they preferred to breathe through the nose either because the subject was more comfortable with nasal breathing,
70
v. NIINIMAA ~': a/.
o r beca~ase o r o n a s a l that
the stimuli
breathing
to switch
was associated
to oronasal
with gasping
breathing
may
f o r air. T h i s s u g g e s t s
be overridden
by higher
centres of the brain.
References ~strand, 1. (1960). Aerobic work capacity in men and women with special reference to age. Acta Physiol. Scand. 49 (Suppl. 169): 1 91. Borg, G. A. V. (1973). Perceived exertion: a note on "history' and methods. Med. Sci. Sport.s 5:90 93. Bouhuys, A. (1977). The Physiology of Breathing. A textbook for medical students. New York, Grune and Stratton. Campbell, E . J . M . (1966). The relationship of the sensation of breathlessness to the act of breathing. In: Breathlessness, edited by J.B.L. Howell and E.J.M. Campbell. Oxford, Blackw Scientific Publication, pp. 55 64. Campbell, E . J . M . , E. Agostoni and J. Newsom Davis (1970). The Respiratory Muscles. London. Lloyd-Luke. Cole, P., S. Mintz, V. Niinimaa and F. Silverman (1979a). Nasal aerodynamics. J. Otolawngol 8:191 195. Cole, P.. V. Niinimaa, S. Mintz and F. Silverman (1979b). Work of nasal breathing; Measurement of each nostril independently using a split mask. Acta Otolarvngol. 88:148 154. DuBois, E. F. (1927). Basal Metabolism in Health and Disease. Philadelphia, Lea and Febiger. Gamberale, F., 1. Holmer, A.-S. Kindblom and A. Nordstr6m (1978). Magnitude Perception of added inspiratory resistance during steady-state exercise. Ergonomics 21 : 531 538. Goldman, H.I. and M.R. Becklake (1959). Respiratory function tests: Normal values at median altitudes and the prediction of" normal results. Am. Lev. Tuherc. 79:457 467. Korinkova, S., Z. VIc and E. Hoznauerova (1978). Proudovy nosno odpor v zateaovem testa. Cesk. Otolarvngol. 27:160 164. Lapp, N. L. and R.E. Hyatt (1967). Some factors affecting the relationship of maximal expiratory flow to lung volume in health and disease. Dis. Chest 51:475 481. Mann. D.G., C.T. Sasaki, M. Suzuki, H. Fukuda and J. R. Hernandez (1977). Dilatator naris muscle. Ann. Otol. Rhinol. Laryngol. 86:362 372. Nie, N.H., C.H. HullJ. G. Jenkins, K. Steirlbrenner and D.H. Brent (1975). Statistical Packages for the Social Sciences (2nd edn.) McGraw-Hill Book Company. Niinimaa, V., P. Cole, S. Mintz and R.J. Shephard (1979). A head-out body plethysmograph. J. Appl. Physiol. 47:1336 1339. Patrick. G. A. and G. R. Sharp (1969). Oronasal distribution of in spiratory flow during various activities. Proc. Physiol. Sot., pp. 22 23. Perrin. CI., J. Lacoste and R. Marl (1977). A nasal function test: The opening of mouth during physical effort. Rhinol. 15:33 38. Polgar, G. and G. P. Kong (1965). The nasal resistance of newborn infants. J. Pediatrics 67:557 567. Proctor, D. F. (1977). The upper airways. I. Nasal physiology and defence ot" the hlngs. Am. Rev. Resp. Dis. 115:97 129. Saibene, F., P. Mognoni and G. Sant'Ambrogio (1965). Lavoro rcspiratorio e ventilazione al passagio dall respirazione nasale a quella orale. Boll. Soc. ltal. Biol. Sper. 41:1550 1552. Saibene, F., P. Mognoni, C. L. Lafortuna and R. Mostardi (1978). Oronasal breathing during exercise. p/lii~ers Arch. 378:65 69. Saketkhoo, K., I. Kaplan and M.A. Sackner (1979). Effects of exercise on nasal mucous velocity and nasal airflow resistance in normal subjects..I. Appl. Plo, siol. 46:369 371. Sasaki. C.T. and D.G. Mann (1976). Dilator naris function A useful test of Iitcial nerve integrity. Arch. Ololao'n~fol. 102: 365-367.
SWITCHING POINT
71
Silverman, L., G. Lee, T. Plotkin, L.A. Sawyers and A.R. Yancey (1951). Air flow measurements on human subjects with and without resistance at several work loads. Arch. Ind. Hygiene 3:461-478. Takagi, Y., D. F. Proctor, S. Salman and S. Evering (1969). Effects of cold air and carbon dioxide on nasal air flow resistance. Ann. Otolaryngol 78: 4048. Uddstr6mer, M. (1940). Nasal respiration. Acta Otolaryngol. Suppl. 42: 3-146. Williams, H.L. (1970). Definitions of Terms Used in Rhinometry with Suggested Standard Symbols. A Handbook and Glossary. Rochester, Minn., American Academy of Ophthalmology and Otolaryngology.