The Beneficial Effect of Nasal Breathing on ExerciseInduced Bronchoconstriction13 R. SHTURMAN-ELLSTEIN, R. J. ZEBALLOS, J. M. BUCKLEY, and J. F. SOUHRADA
SUMMARY In the first step of a study of the relation of nasal and oral breathing during moderate treadmill exercise to the onset of bronchoconstriction in young patients with perennial bronchial asthma, it was observed that most subjects spontaneously breathed with their mouths open when instructed to breathe "naturally." Subsequently, when they were required to breathe only through the nose during the exercise, an almost complete inhibition of the postexercise bronchoconstrictive airway response was demonstrated. When instructed to breathe only through the mouth during exercise, an increased bronchoconstrictive airway response occurred, as measured by spirometry, flowvolume relationships, and body plethysmography. These findings suggest that the nasopharynx and the oropharynx play important roles in the phenomenon of exercise-induced bronchoconstriction.
Introduction Exercise-induced bronchoconstriction is frequently seen in young patients with bronchial asthma. T h e degree of this bronchoconstriction is dependent on the nature (1, 2) and duration (3) of the exercise, with the bronchoconstriction developing during exercise (3) and reaching a maximum within 5 to 15 min after exercise (4). T h e bronchoconstrictive response is reproducible (5). Exercise-induced bronchoconstriction can be modified pharmacologically by use of several different agents (6, 7). T h e mechanisms responsible for the development of exercise-in(Received in original form May 11, 1977 and in revised form March 27,1978) 1 From the Department of Pediatrics and the Pulmonary Function Laboratory, National Jewish Hospital and Research Center, Denver, Colo. 80206. 2 Presented in part at the Fall Meeting of the American Physiological Society, Hollywood, Fla., October 1977. 3 Requests for reprints should be addressed to Dr. Joseph Souhrada, National Jewish Hospital and Research Center, 3800 East Colfax Ave., Denver, Colo. 80206.
duced bronchoconstriction are yet to be demonstrated. It has been observed that climatologic factors can cause bronchoconstriction in some asthmatic patients (8). Exposure to cold air leads to significant increases in both nasal and airway resistance (9, 10). Recently, it has been shown that increasing the temperature and humidity of the inspired air during exercise significantly diminishes postexercise bronchoconstriction in asthmatic patients (11). These observations are consistent with the findings of Fitch and Morton (2), who demonstrated that asthmatic patients developed less airway obstruction after swimming in a heated, indoor swimming pool than after treadmill walking or bicycling at room temperature. T h e work performed in Fitch and Morton's study (2) was the same in all 3 types of exercise. T h e differences in temperature and humidity of the inspired air in the areas where the exercise was carried out could conceivably have accounted for the lesser degree of airway obstruction that developed after swimming. Therefore, if the temperature and humidity are important factors in exercise-induced bron-
AMERICAN REVIEW OF RESPIRATORY DISEASE, VOLUME 118, 1978
65
66
SHTURMAN-ELLSTEIN, ZEBALLOS, BUCKLEY, AND SOUHRADA
choconstriction, the effect of the natural conditioning of the inspired air by the nose should be ascertained. T h i s conditioning includes humidincation, temperature adjustment, and removal of airborne particles (12, 13), which might be the necessary factors for supplying clean, warm, humid air to the lungs. W h e n only mouth breathing is relied on during exercise, there should be less resistance to air flow, but th inspired air will be cooler and less humid than during nasal breathing. These changes in air quality may influence the degree of postexercise bronchoconstriction. T o investigate this possibility, 12 young asthmatic patients were examined to determine: (1) the usual type of breathing that asthmatic patients use during exercise when not specifically instructed on what manner to breathe, and (2) whether or not the natural conditioning of air by the nose plays a role in diminishing exercise-induced bronchoconstriction.
Materials and Methods Patients. Ten boys and 2 girls, 6 to 14 years of age, with mild to moderate, nonsteroid-dependent, perennial bronchial asthma (as defined by the American Thoracic Society) were tested. Their full clinical histories were obtained from parents and patients. All patients had positive histories of allergy and exercise-induced bronchoconstriction, and the average duration of bronchial asthma was 7.5 years. At the time of the study, none had any symptoms of acute illness, and all patients could ventilate freely through both nares. The subjects had not received any medication for at least 6 hours before testing. Any sign of wheezing before testing disqualified the patient from partici-
pating in the study on that day. All patients were familiar with the techniques used in the testing. (The anthropometric and clinical characteristics of the patients are shown in table 1.) Experimental procedures. The subjects walked on a treadmill (Quinton, Seattle, Wa.) for 10 min, with the grade constantly at 15 per cent, but the speed varied between 2.8 and 3.8 mph. The average workload achieved was 2.12—0.06 watts per kg of body weight (14), which represents a moderate workload corresponding to 75 to 85 per cent of maximal heart rate (15). Each patient undertook the same workload on the 3 testing days. The heart rate was monitored at baseline, during exercise, and 1 min after exercise. Pulmonary function testing was done 5 to 10 min before exercise, and at 7 to 12 and 30 to 35 min after exercise. Within 7 min after exercise, the patients were no longer tachypneic and were capable of performing pulmonary function tests without difficulty. The pulmonary function tests included conventional spirometry and determination of maximal expiratory flow-volume curve measured with a 570 Wedge spirometer (Med. Science, St. Louis, Mo.). Thoracic gas volume (Vtg) and airway resistance (Raw) were determined, using the variable-pressure body plethysmograph (W. Collins, Braintree, Mass.), by means of the method of DuBois and associates (16, 17). All instruments were calibrated daily. Measurements in the body plethysmograph were taken 3 times in succession, and the average of these tests was reported. Spirometry, maximal expiratory flow-volume curves, and body plethysmography were directly analyzed by an on-line computer system (Healthgarde, Salt Lake City, Utah). Body plethysmography measurement was always taken before the measurement of spirometric and flow-volume data. The exercise testing of each patient was done on 3 different days at approximately the same time, and
TAB LE 1 SOME ANTHROPOMETRIC AND CLINICAL CHARACTERISTICS OF TESTED PATIENTS
Patient
Age (years)
1 2 3 4 5 6 7 8 9 10 11 12
8 7 13 8 12 6 13 9 14 7 9 7
Sex M M M M M M F M M M F M
Body Weight (kg)
Height (cm)
26 25 42 37 37 17 40 32 33 22 24 23
126 121 157 134 147 111 152 132 134 124 126 121
Duration of Asthma (years) 1 6 8 8 9 5 12 8 11 3 6 7
0.82 ± 0.03 1.05±0.10 1.00 ± 0 . 1 9 1.10±0.11 1.24 ± 0 . 0 4 1.26 ± 0 . 0 9 1.38±0.16 1.24±0.16
1.38 ± 0 . 1 1 1.44 ± 0 . 1 3 1.36 ± 0 . 1 4
1.62 ± 0 . 0 1 1.84 ± 0 . 0 3
±0.05 ±0.08 ±0.10 ±0.03 ±0.03
1.09 1.41 1.03 1.08 1.09
1.15 ± 0 . 0 3 1.97 ± 0 . 0 4
0.81 ± 0 . 0 5 1.02 ± 0 . 1 1 1.56 ± 0 . 0 7 1.14±0.01 2.33 ± 0.37
25-75
±0.15 ± 0.33 ±0.38 ±0.18 ±0.61 ±0.18 ±0.13 ±0.28 ± 0.38 ±0.15
2.68 ± 0 . 1 8 3.01 ± 0.33 2.95 ± 0.35
3.07 ± 0 . 2 5
3.65 1.89 2.02 2.47 2.75
3.01 ± 0 . 1 6
1.97 2.09 4.15 2.67 4.85
Vmax75
±0.10 ±0.19 ±0.25 ±0.08 ±0.13
±0.18 ± 0.48 ± 0.05 ± 0.03
1.67 ± 0 . 1 3 1.78 ± 0 . 2 2 1.66 ± 0 . 1 8
1.04 1.38 1.29 1.45 1.66
1.35 2.96 2.07 2.47
1.32 ± 0 . 0 5 1.40 ± 0 . 1 6 2.08 ± 0.02
Vmaxso
FUNCTION
±0.08 ±0.02 ±0.15 ± 0.07 ±0.11
0.80 ± 0.05 0.89 ± 0 . 1 3 0.77 ± 0 . 1 3
0.58 ± 0 . 0 8 0.76 ± 0 . 0 1
1.15 1.11 0.56 0.64 0.62
1.65 ± 0 . 3 1
0.89 ± 0.08 0.72 ± 0.03
0.43 ± 0 . 1 1 0.73 ± 0.03
Vmax25
TESTS
1.73±0.16
1.66±0.14 1.68 ± 0 . 1 4
1.63±0.16 ND 1.09 ± 0 . 0 5
1.44 ± 0 . 0 9 2.14±0.10 0.92 ± 0 . 1 7 2.08 ± 0 . 0 4 2.01 ± 0.09 1.93 ± 0 . 1 1
1.38 ± 0 . 0 6 1.53 ± 0 . 0 3 2.44 ± 0.05
Vtg
FOR
8.09 ± 1 . 0 2 6.77 ± 0 . 5 3 7.35 ± 1 . 1 4
0.154 ± 0 . 0 1 3
0.100 ± 0 . 0 1 0 0.101 ± 0 . 0 1 3
0.087 ± 0.008
0.076 ± 0.003 0.062 ± 0.007
6.16 ± 0 . 8 0
0.109 ± 0 . 0 0 5 0.109 ± 0 . 0 0 7 0.122 ± 0 . 0 1 4
1.35 ± 0 . 0 1 5 0.052 ± 0 . 0 1 3 0.086 ± 0.002
0.062 ± 0 . 0 1 1 0.091 ± 0 . 0 1 3 ND
± 0.76 ±2.66 ±0.06 ±0.36 ± 0.23
SGaw (liter/cm H20/sec)
±1.31 ± 0.33 ± 0.64 ±1.21 ±0.54 ND
9.57 6.36 8.28 8.88 7.06
5.58 14.01 4.78 6.41 4.34
sec)
Raw (cm H 2 0 / l i t e r /
f-l
s 0
C/5
Q
X
O
X
O 0 0
O 2
O H
NSTR
pulmonary variables.
H
JCED BRO
Definitions of abbreviations: F E V i = forced e x p i r a t o r y v o l u m e in 1 sec; F E F 2 5 - 7 5 % = f o r c e d e x p i r a t o r y f l o w in t h e m i d d l e half o f t h e f o r c e d vital c a p a c i t y ; V m a x 7 5 , V m a x 5 0 , a n d V m a x 2 5 == m a x i mial e x p i r a t o r y f l o w after e x h a l a t i o n o f , respectively, 7 5 , 5 0 , and 2 5 per c e n t of t h e f o r c e d vital c a p a c i t y ; V t g = t h o r a c i c gas5 v o l u m e ; R a w = a i r w a y resistance; S G a w = specif ic a i r w a y c o n d u c t a n c e ; N D = n o t d o n e ( p a t i e n t u n a b l e t o p e r f o r m ) . Averages w e r e based o n 3 testing d a y s ' results f o r each p a t i e n t . * Averages w e r e based on data f r o m 1 2 patients w i t h i n each d a y . By repeated measures ( t tests), t h e r e w e r e n o significant differences a m o n g d a i l y baseline values f o r a n y
8 9 10 11 12 D a i l y group values"*" "Spontaneous breathing" Nasal b r e a t h i n g M o u t h breathing
6 7
1.42 ± 0 . 0 1 2.18±0.14
1.04 ± 0 . 0 2 1.12±0.11 2.09 ± 0 . 0 2
FEF
SELECTED PULMONARY
[ING AN
5
1 2 3 4
Individual patient*
FEVX
TABLE 2 I N D I V I D U A L A N D D A I L Y G R O U P M E A N ± SE O F B A S E L I N E V A L U E S
NASAL BRE;*
68
SHTURMAN-ELLSTEIN, ZEBALLOS, BUCKLEY, AND SOUHRADA
60 £ £
40
.^?
20 175
155 -2 Ml
the testing was completed within 1 week. On the first day, the patients were allowed to breathe in the manner they preferred ("spontaneous breathing"). On the second and third testing days, they were instructed to breathe either nasally only, with the mouth tightly closed, or orally only, with noseclips applied throughout the exercise. This sequence was randomized. (Preliminary study revealed that placing tape on the mouth induced anxiety in the younger subjects and that voluntary mouth control was more satisfactory.) T h e exercise test was accomplished in a room where the air temperature ranged from 70 to 75° F and the relative humidity ranged from 25 to 30 per cent, and these were monitored every day. T h e patients and the technician testing the pulmonary functions were not aware of any possible effect that the different types of breathing might have on the outcome of the study. When patients performed an exercise test using the mouth, they inhaled room air through a Rudolph valve and expired into a Fleisch pneumotachograph (no. 3). T h e dead space of this system was 100 ml. T o measure nasal ventilation, an Ambu mask (no. 2) fitted tightly to the face was used. Through the transparent mask it was easy to observe whether the patient kept his or her lips tightly closed. A flow signal received from the pneumotachygraph was integrated into volume, using an on-line computer system (Healthgarde, Salt Lake City, Utah). End-tidal Pco 2 , tidal volume, respiratory frequency, and minute ventilation (VE) were recorded con-
* 135 w
s
• ~
115
£
a spontaneous breathing • mouth breathing • nasal breathing baseline
4
6
8
minutes of exercise
10 post exercise
Fig. 1. Changes in minute ventilation (VE), in liter per min, and heart rate during exercise and 1 min after exercise on the 3 testing days. Exercise was performed with mouth breathing (•), nasal breathing (±), and spontaneous breathing (°). Mean ± SE values are shown. tinuously during exercise and displayed on a monitor. End-tidal Pco 2 was analyzed using a mass spectrophotometer (Perkin-Elmer, Norwalk, Conn.). Analysis of data. Data for all pulmonary functions measured were expressed as percentages of daily
Mill
EUl 120
2
120
m
1 M
u spontaneous breathing • month breathing A nasal breathing 712 minutes post exercise
60
L 30-35
• spontaneous breathing • mouth breathing • nasal breathing 712
30 35
minutes post exercise
Fig. 2. Changes of the forced expiratory volume in 1 sec (FEVj) and maximal mid-expiratory flow (FEF25_75%), i.e., the forced expiratory flow in the middle half of the forced vital capacity, after exercise. Exercise was performed with mouth breathing (•), nasal breathing (•), and spontaneous breathing (a). Mean ± SE values are shown.
69
NASAL BREATHING AND EXERCISE-INDUCED BRONCHOCONSTRICTION
baseline values. Analysis of variance was done for each pulmonary function variable, expressed in absolute values, followed by a Duncan multiple range test (18) to determine the basis of any significant effects. Significance of differences was established at P < 0.05. Results
The absolute values (mean ± SE) of the pulmonary function data on each of the different testing days (for "spontaneous breathing," oral breathing only, and nasal breathing only) measured at baseline for individual patients and for the group, are shown in table 2. No significant differences were found among the individual or the group baseline values determined on the 3 testing days. Therefore, the mouth breathing only or the nasal breathing only testing day may be appropriately compared with the day when "spontaneous breathing" was used. The changes in pulmonary function after exercise are related to the baseline values obtained on that same day. All patients tolerated the exercise tests without apparent clinical symptoms. The changes in ventilation during exercise when patients used oral or nasal breathing are shown in figure 1. No significant differences in ventilation were seen between these 2 types of breathing. Similarly, during exercise, no differences in end-tidal Pco 2 were seen between these 2 types of breathing. End-tidal Pco 2 ranged between 32.5 and 33.5 mm Hg with nasal breathing; 32.7 and 33.2 mm Hg with mouth breathing. The heart rate responses on the 3 testing days are also shown in figure 1. No significant differences occurred in the heart rate responses when related to the types of breathing used; however, the lowest heart rates during exercise were achieved with nasal breathing. During the first testing day, when the patients were given no instructions on the manner of breathing, most (10) had their mouths open during the treadmill exercise. Two patients breathed consistently through their noses. On the first testing day, 7 to 12 min after exercise with "spontaneous breathing," the patients developed bronchoconstriction, demonstrated by changes in the forced expiratory volume in 1 sec (FEVj), forced expiratory flow in the middle half of the forced vital capacity (FEF25_75%), maximal expiratory flow after exhalation of 25, 50, or 75 per cent of the forced vital capacity (Vmax25, Vmax 50 , and Vmax 75 , respectively), Raw, and Vtg. By 30 min after exercise, these
values had returned almost to baseline (figures 2, 3, and 4). The changes in FEVX and FEF25-75% in the postexercise period after the 3 different types of breathing are shown in figure 2. The most significant decrease (P < 0.05) in FEVX and FEF25_75% occurred on the day when the patients used mouth breathing only during exercise. When nasal breathing only was used, there were small decreases in the values of these pulmonary functions (table 3).
spontaneous breathing • month breathing • nasal breathing 7 12
30 35
minutes post eicrcise
Fig. 3. Changes in flow-volume relationship as measured by the maximal expiratory flow after exhalation of 25, 50, and 75 per cent of the forced vital capacity (Vmax25%VC, Vmaxso%VC, and Vmax75%VC), respectively, after exercise. Exercise was performed with mouth breathing (•), nasal breathing (A), and spontaneous breathing (a). Mean ± SE values are shown.
70
SHTURMAN-ELLSTEIN, ZEBALLOS, BUCKLEY, AND SOUHRADA
Vtg
D spontaneous breathing • mouth breathing A nasal breathing
a spontaneous breathing • month breathing A nasal breathing
L 30 35
712
31 35
712 minutes post exercise
minutes post exercise
Fig. 4. Body plethysmography values for thoracic gas volume (Vtg) and airway resistance (Raw) after exercise. Exercise was performed with mouth breathing (•), nasal breathing (±), and spontaneous breathing (a), Mean ± SE values are shown. The changes in the maximal expiratory flowvolume curves measured by Vmax 25 , Vmax 50 , and Vmax 75 are shown in figure 3. The most significant decrease (P < 0.05) occurred in all 3 variables when mouth breathing only was used during the exercise. By contrast, nasal breathing had only a small, insignificant effect on these measurements. The body plethysmograph data are shown in figure 4. Again, the most significant change (P < 0.05) occurred when patients were asked to breathe orally during exercise. The changes in
Raw and Vtg of nasal breathing were not significantly different from those measurements for "spontaneous breathing." The individual FEF25_75% values, expressed as per cent of baseline, measured 7 to 12 min after exercise in the 3 testing sessions are shown in figure 5. The FEF25-75% value was chosen because it is considered to be a sensitive and relatively effort-independent measurement of airway obstruction. When mouth breathing was used during exercise, significant changes in FEF25-75% were seen in 11 of the 12 patients
TABLE 3 C O M P A R A T I V E V A L U E S FOR SIGNIFICANCE OF DIFFERENCES IN P U L M O N A R Y F U N C T I O N D A T A *
Pulmonary Function Data FEVi FEF25-75% Vmax75 Vmax50 Vmax25 Vtg Raw SGaw
"Spontaneous Breathing" "Spontaneous Breathing" Mouth Breathing versus versus versus Mouth Breathing Nasal Breathing Nasal Breathing {P values) (P values) (P values) NS f NS NS NS NS P < 0.001 NS NS
P P P P
< 0.05 < 0.05 < 0.05 < 0.05 NS NS NS NS
P P P P P P P P
< 0.005 < 0.005 < 0.001 < 0.001
SUMMARY In the first step of a study of the relation of nasal and oral breathing during moderate treadmill exercise to the onset of bronchoconstriction in young patients with perennial bronchial asthma, it was observed that most subjects spontaneously breathed with their mouths open when instructed to breathe "naturally." Subsequently, when they were required to breathe only through the nose during the exercise, an almost complete inhibition of the postexercise bronchoconstrictive airway response was demonstrated. When instructed to breathe only through the mouth during exercise, an increased bronchoconstrictive airway response occurred, as measured by spirometry, flowvolume relationships, and body plethysmography. These findings suggest that the nasopharynx and the oropharynx play important roles in the phenomenon of exercise-induced bronchoconstriction.
Introduction Exercise-induced bronchoconstriction is frequently seen in young patients with bronchial asthma. T h e degree of this bronchoconstriction is dependent on the nature (1, 2) and duration (3) of the exercise, with the bronchoconstriction developing during exercise (3) and reaching a maximum within 5 to 15 min after exercise (4). T h e bronchoconstrictive response is reproducible (5). Exercise-induced bronchoconstriction can be modified pharmacologically by use of several different agents (6, 7). T h e mechanisms responsible for the development of exercise-in(Received in original form May 11, 1977 and in revised form March 27,1978) 1 From the Department of Pediatrics and the Pulmonary Function Laboratory, National Jewish Hospital and Research Center, Denver, Colo. 80206. 2 Presented in part at the Fall Meeting of the American Physiological Society, Hollywood, Fla., October 1977. 3 Requests for reprints should be addressed to Dr. Joseph Souhrada, National Jewish Hospital and Research Center, 3800 East Colfax Ave., Denver, Colo. 80206.
duced bronchoconstriction are yet to be demonstrated. It has been observed that climatologic factors can cause bronchoconstriction in some asthmatic patients (8). Exposure to cold air leads to significant increases in both nasal and airway resistance (9, 10). Recently, it has been shown that increasing the temperature and humidity of the inspired air during exercise significantly diminishes postexercise bronchoconstriction in asthmatic patients (11). These observations are consistent with the findings of Fitch and Morton (2), who demonstrated that asthmatic patients developed less airway obstruction after swimming in a heated, indoor swimming pool than after treadmill walking or bicycling at room temperature. T h e work performed in Fitch and Morton's study (2) was the same in all 3 types of exercise. T h e differences in temperature and humidity of the inspired air in the areas where the exercise was carried out could conceivably have accounted for the lesser degree of airway obstruction that developed after swimming. Therefore, if the temperature and humidity are important factors in exercise-induced bron-
AMERICAN REVIEW OF RESPIRATORY DISEASE, VOLUME 118, 1978
65
66
SHTURMAN-ELLSTEIN, ZEBALLOS, BUCKLEY, AND SOUHRADA
choconstriction, the effect of the natural conditioning of the inspired air by the nose should be ascertained. T h i s conditioning includes humidincation, temperature adjustment, and removal of airborne particles (12, 13), which might be the necessary factors for supplying clean, warm, humid air to the lungs. W h e n only mouth breathing is relied on during exercise, there should be less resistance to air flow, but th inspired air will be cooler and less humid than during nasal breathing. These changes in air quality may influence the degree of postexercise bronchoconstriction. T o investigate this possibility, 12 young asthmatic patients were examined to determine: (1) the usual type of breathing that asthmatic patients use during exercise when not specifically instructed on what manner to breathe, and (2) whether or not the natural conditioning of air by the nose plays a role in diminishing exercise-induced bronchoconstriction.
Materials and Methods Patients. Ten boys and 2 girls, 6 to 14 years of age, with mild to moderate, nonsteroid-dependent, perennial bronchial asthma (as defined by the American Thoracic Society) were tested. Their full clinical histories were obtained from parents and patients. All patients had positive histories of allergy and exercise-induced bronchoconstriction, and the average duration of bronchial asthma was 7.5 years. At the time of the study, none had any symptoms of acute illness, and all patients could ventilate freely through both nares. The subjects had not received any medication for at least 6 hours before testing. Any sign of wheezing before testing disqualified the patient from partici-
pating in the study on that day. All patients were familiar with the techniques used in the testing. (The anthropometric and clinical characteristics of the patients are shown in table 1.) Experimental procedures. The subjects walked on a treadmill (Quinton, Seattle, Wa.) for 10 min, with the grade constantly at 15 per cent, but the speed varied between 2.8 and 3.8 mph. The average workload achieved was 2.12—0.06 watts per kg of body weight (14), which represents a moderate workload corresponding to 75 to 85 per cent of maximal heart rate (15). Each patient undertook the same workload on the 3 testing days. The heart rate was monitored at baseline, during exercise, and 1 min after exercise. Pulmonary function testing was done 5 to 10 min before exercise, and at 7 to 12 and 30 to 35 min after exercise. Within 7 min after exercise, the patients were no longer tachypneic and were capable of performing pulmonary function tests without difficulty. The pulmonary function tests included conventional spirometry and determination of maximal expiratory flow-volume curve measured with a 570 Wedge spirometer (Med. Science, St. Louis, Mo.). Thoracic gas volume (Vtg) and airway resistance (Raw) were determined, using the variable-pressure body plethysmograph (W. Collins, Braintree, Mass.), by means of the method of DuBois and associates (16, 17). All instruments were calibrated daily. Measurements in the body plethysmograph were taken 3 times in succession, and the average of these tests was reported. Spirometry, maximal expiratory flow-volume curves, and body plethysmography were directly analyzed by an on-line computer system (Healthgarde, Salt Lake City, Utah). Body plethysmography measurement was always taken before the measurement of spirometric and flow-volume data. The exercise testing of each patient was done on 3 different days at approximately the same time, and
TAB LE 1 SOME ANTHROPOMETRIC AND CLINICAL CHARACTERISTICS OF TESTED PATIENTS
Patient
Age (years)
1 2 3 4 5 6 7 8 9 10 11 12
8 7 13 8 12 6 13 9 14 7 9 7
Sex M M M M M M F M M M F M
Body Weight (kg)
Height (cm)
26 25 42 37 37 17 40 32 33 22 24 23
126 121 157 134 147 111 152 132 134 124 126 121
Duration of Asthma (years) 1 6 8 8 9 5 12 8 11 3 6 7
0.82 ± 0.03 1.05±0.10 1.00 ± 0 . 1 9 1.10±0.11 1.24 ± 0 . 0 4 1.26 ± 0 . 0 9 1.38±0.16 1.24±0.16
1.38 ± 0 . 1 1 1.44 ± 0 . 1 3 1.36 ± 0 . 1 4
1.62 ± 0 . 0 1 1.84 ± 0 . 0 3
±0.05 ±0.08 ±0.10 ±0.03 ±0.03
1.09 1.41 1.03 1.08 1.09
1.15 ± 0 . 0 3 1.97 ± 0 . 0 4
0.81 ± 0 . 0 5 1.02 ± 0 . 1 1 1.56 ± 0 . 0 7 1.14±0.01 2.33 ± 0.37
25-75
±0.15 ± 0.33 ±0.38 ±0.18 ±0.61 ±0.18 ±0.13 ±0.28 ± 0.38 ±0.15
2.68 ± 0 . 1 8 3.01 ± 0.33 2.95 ± 0.35
3.07 ± 0 . 2 5
3.65 1.89 2.02 2.47 2.75
3.01 ± 0 . 1 6
1.97 2.09 4.15 2.67 4.85
Vmax75
±0.10 ±0.19 ±0.25 ±0.08 ±0.13
±0.18 ± 0.48 ± 0.05 ± 0.03
1.67 ± 0 . 1 3 1.78 ± 0 . 2 2 1.66 ± 0 . 1 8
1.04 1.38 1.29 1.45 1.66
1.35 2.96 2.07 2.47
1.32 ± 0 . 0 5 1.40 ± 0 . 1 6 2.08 ± 0.02
Vmaxso
FUNCTION
±0.08 ±0.02 ±0.15 ± 0.07 ±0.11
0.80 ± 0.05 0.89 ± 0 . 1 3 0.77 ± 0 . 1 3
0.58 ± 0 . 0 8 0.76 ± 0 . 0 1
1.15 1.11 0.56 0.64 0.62
1.65 ± 0 . 3 1
0.89 ± 0.08 0.72 ± 0.03
0.43 ± 0 . 1 1 0.73 ± 0.03
Vmax25
TESTS
1.73±0.16
1.66±0.14 1.68 ± 0 . 1 4
1.63±0.16 ND 1.09 ± 0 . 0 5
1.44 ± 0 . 0 9 2.14±0.10 0.92 ± 0 . 1 7 2.08 ± 0 . 0 4 2.01 ± 0.09 1.93 ± 0 . 1 1
1.38 ± 0 . 0 6 1.53 ± 0 . 0 3 2.44 ± 0.05
Vtg
FOR
8.09 ± 1 . 0 2 6.77 ± 0 . 5 3 7.35 ± 1 . 1 4
0.154 ± 0 . 0 1 3
0.100 ± 0 . 0 1 0 0.101 ± 0 . 0 1 3
0.087 ± 0.008
0.076 ± 0.003 0.062 ± 0.007
6.16 ± 0 . 8 0
0.109 ± 0 . 0 0 5 0.109 ± 0 . 0 0 7 0.122 ± 0 . 0 1 4
1.35 ± 0 . 0 1 5 0.052 ± 0 . 0 1 3 0.086 ± 0.002
0.062 ± 0 . 0 1 1 0.091 ± 0 . 0 1 3 ND
± 0.76 ±2.66 ±0.06 ±0.36 ± 0.23
SGaw (liter/cm H20/sec)
±1.31 ± 0.33 ± 0.64 ±1.21 ±0.54 ND
9.57 6.36 8.28 8.88 7.06
5.58 14.01 4.78 6.41 4.34
sec)
Raw (cm H 2 0 / l i t e r /
f-l
s 0
C/5
Q
X
O
X
O 0 0
O 2
O H
NSTR
pulmonary variables.
H
JCED BRO
Definitions of abbreviations: F E V i = forced e x p i r a t o r y v o l u m e in 1 sec; F E F 2 5 - 7 5 % = f o r c e d e x p i r a t o r y f l o w in t h e m i d d l e half o f t h e f o r c e d vital c a p a c i t y ; V m a x 7 5 , V m a x 5 0 , a n d V m a x 2 5 == m a x i mial e x p i r a t o r y f l o w after e x h a l a t i o n o f , respectively, 7 5 , 5 0 , and 2 5 per c e n t of t h e f o r c e d vital c a p a c i t y ; V t g = t h o r a c i c gas5 v o l u m e ; R a w = a i r w a y resistance; S G a w = specif ic a i r w a y c o n d u c t a n c e ; N D = n o t d o n e ( p a t i e n t u n a b l e t o p e r f o r m ) . Averages w e r e based o n 3 testing d a y s ' results f o r each p a t i e n t . * Averages w e r e based on data f r o m 1 2 patients w i t h i n each d a y . By repeated measures ( t tests), t h e r e w e r e n o significant differences a m o n g d a i l y baseline values f o r a n y
8 9 10 11 12 D a i l y group values"*" "Spontaneous breathing" Nasal b r e a t h i n g M o u t h breathing
6 7
1.42 ± 0 . 0 1 2.18±0.14
1.04 ± 0 . 0 2 1.12±0.11 2.09 ± 0 . 0 2
FEF
SELECTED PULMONARY
[ING AN
5
1 2 3 4
Individual patient*
FEVX
TABLE 2 I N D I V I D U A L A N D D A I L Y G R O U P M E A N ± SE O F B A S E L I N E V A L U E S
NASAL BRE;*
68
SHTURMAN-ELLSTEIN, ZEBALLOS, BUCKLEY, AND SOUHRADA
60 £ £
40
.^?
20 175
155 -2 Ml
the testing was completed within 1 week. On the first day, the patients were allowed to breathe in the manner they preferred ("spontaneous breathing"). On the second and third testing days, they were instructed to breathe either nasally only, with the mouth tightly closed, or orally only, with noseclips applied throughout the exercise. This sequence was randomized. (Preliminary study revealed that placing tape on the mouth induced anxiety in the younger subjects and that voluntary mouth control was more satisfactory.) T h e exercise test was accomplished in a room where the air temperature ranged from 70 to 75° F and the relative humidity ranged from 25 to 30 per cent, and these were monitored every day. T h e patients and the technician testing the pulmonary functions were not aware of any possible effect that the different types of breathing might have on the outcome of the study. When patients performed an exercise test using the mouth, they inhaled room air through a Rudolph valve and expired into a Fleisch pneumotachograph (no. 3). T h e dead space of this system was 100 ml. T o measure nasal ventilation, an Ambu mask (no. 2) fitted tightly to the face was used. Through the transparent mask it was easy to observe whether the patient kept his or her lips tightly closed. A flow signal received from the pneumotachygraph was integrated into volume, using an on-line computer system (Healthgarde, Salt Lake City, Utah). End-tidal Pco 2 , tidal volume, respiratory frequency, and minute ventilation (VE) were recorded con-
* 135 w
s
• ~
115
£
a spontaneous breathing • mouth breathing • nasal breathing baseline
4
6
8
minutes of exercise
10 post exercise
Fig. 1. Changes in minute ventilation (VE), in liter per min, and heart rate during exercise and 1 min after exercise on the 3 testing days. Exercise was performed with mouth breathing (•), nasal breathing (±), and spontaneous breathing (°). Mean ± SE values are shown. tinuously during exercise and displayed on a monitor. End-tidal Pco 2 was analyzed using a mass spectrophotometer (Perkin-Elmer, Norwalk, Conn.). Analysis of data. Data for all pulmonary functions measured were expressed as percentages of daily
Mill
EUl 120
2
120
m
1 M
u spontaneous breathing • month breathing A nasal breathing 712 minutes post exercise
60
L 30-35
• spontaneous breathing • mouth breathing • nasal breathing 712
30 35
minutes post exercise
Fig. 2. Changes of the forced expiratory volume in 1 sec (FEVj) and maximal mid-expiratory flow (FEF25_75%), i.e., the forced expiratory flow in the middle half of the forced vital capacity, after exercise. Exercise was performed with mouth breathing (•), nasal breathing (•), and spontaneous breathing (a). Mean ± SE values are shown.
69
NASAL BREATHING AND EXERCISE-INDUCED BRONCHOCONSTRICTION
baseline values. Analysis of variance was done for each pulmonary function variable, expressed in absolute values, followed by a Duncan multiple range test (18) to determine the basis of any significant effects. Significance of differences was established at P < 0.05. Results
The absolute values (mean ± SE) of the pulmonary function data on each of the different testing days (for "spontaneous breathing," oral breathing only, and nasal breathing only) measured at baseline for individual patients and for the group, are shown in table 2. No significant differences were found among the individual or the group baseline values determined on the 3 testing days. Therefore, the mouth breathing only or the nasal breathing only testing day may be appropriately compared with the day when "spontaneous breathing" was used. The changes in pulmonary function after exercise are related to the baseline values obtained on that same day. All patients tolerated the exercise tests without apparent clinical symptoms. The changes in ventilation during exercise when patients used oral or nasal breathing are shown in figure 1. No significant differences in ventilation were seen between these 2 types of breathing. Similarly, during exercise, no differences in end-tidal Pco 2 were seen between these 2 types of breathing. End-tidal Pco 2 ranged between 32.5 and 33.5 mm Hg with nasal breathing; 32.7 and 33.2 mm Hg with mouth breathing. The heart rate responses on the 3 testing days are also shown in figure 1. No significant differences occurred in the heart rate responses when related to the types of breathing used; however, the lowest heart rates during exercise were achieved with nasal breathing. During the first testing day, when the patients were given no instructions on the manner of breathing, most (10) had their mouths open during the treadmill exercise. Two patients breathed consistently through their noses. On the first testing day, 7 to 12 min after exercise with "spontaneous breathing," the patients developed bronchoconstriction, demonstrated by changes in the forced expiratory volume in 1 sec (FEVj), forced expiratory flow in the middle half of the forced vital capacity (FEF25_75%), maximal expiratory flow after exhalation of 25, 50, or 75 per cent of the forced vital capacity (Vmax25, Vmax 50 , and Vmax 75 , respectively), Raw, and Vtg. By 30 min after exercise, these
values had returned almost to baseline (figures 2, 3, and 4). The changes in FEVX and FEF25-75% in the postexercise period after the 3 different types of breathing are shown in figure 2. The most significant decrease (P < 0.05) in FEVX and FEF25_75% occurred on the day when the patients used mouth breathing only during exercise. When nasal breathing only was used, there were small decreases in the values of these pulmonary functions (table 3).
spontaneous breathing • month breathing • nasal breathing 7 12
30 35
minutes post eicrcise
Fig. 3. Changes in flow-volume relationship as measured by the maximal expiratory flow after exhalation of 25, 50, and 75 per cent of the forced vital capacity (Vmax25%VC, Vmaxso%VC, and Vmax75%VC), respectively, after exercise. Exercise was performed with mouth breathing (•), nasal breathing (A), and spontaneous breathing (a). Mean ± SE values are shown.
70
SHTURMAN-ELLSTEIN, ZEBALLOS, BUCKLEY, AND SOUHRADA
Vtg
D spontaneous breathing • mouth breathing A nasal breathing
a spontaneous breathing • month breathing A nasal breathing
L 30 35
712
31 35
712 minutes post exercise
minutes post exercise
Fig. 4. Body plethysmography values for thoracic gas volume (Vtg) and airway resistance (Raw) after exercise. Exercise was performed with mouth breathing (•), nasal breathing (±), and spontaneous breathing (a), Mean ± SE values are shown. The changes in the maximal expiratory flowvolume curves measured by Vmax 25 , Vmax 50 , and Vmax 75 are shown in figure 3. The most significant decrease (P < 0.05) occurred in all 3 variables when mouth breathing only was used during the exercise. By contrast, nasal breathing had only a small, insignificant effect on these measurements. The body plethysmograph data are shown in figure 4. Again, the most significant change (P < 0.05) occurred when patients were asked to breathe orally during exercise. The changes in
Raw and Vtg of nasal breathing were not significantly different from those measurements for "spontaneous breathing." The individual FEF25_75% values, expressed as per cent of baseline, measured 7 to 12 min after exercise in the 3 testing sessions are shown in figure 5. The FEF25-75% value was chosen because it is considered to be a sensitive and relatively effort-independent measurement of airway obstruction. When mouth breathing was used during exercise, significant changes in FEF25-75% were seen in 11 of the 12 patients
TABLE 3 C O M P A R A T I V E V A L U E S FOR SIGNIFICANCE OF DIFFERENCES IN P U L M O N A R Y F U N C T I O N D A T A *
Pulmonary Function Data FEVi FEF25-75% Vmax75 Vmax50 Vmax25 Vtg Raw SGaw
"Spontaneous Breathing" "Spontaneous Breathing" Mouth Breathing versus versus versus Mouth Breathing Nasal Breathing Nasal Breathing {P values) (P values) (P values) NS f NS NS NS NS P < 0.001 NS NS
P P P P
< 0.05 < 0.05 < 0.05 < 0.05 NS NS NS NS
P P P P P P P P
< 0.005 < 0.005 < 0.001 < 0.001
