Influence of exercise hyperthermia on exercise breathing pattern BRUCE J. MARTIN, AND JOHN V. WEIL
EDWARD
Cardiovascular Pulmonary Denver, Colorado 80262
J. MORGAN,
Research Laboratory,
MARTIN, BRUCE J., EDWARD J. MORGAN, CLIFFORD W. ZWILLICH, AND JOHN V. WEIL. Influence of exercise hyperthermia on exercise breathing pattern. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 47(5): 1039-1042, 1979.-Passive elevation of the body core temperature (T,) induces rapid, shallow breathing in resting man. We wondered if exercise-induced T, elevation would also lead to decreased tidal volume (VT) and increased breathing frequency (f) during exercise. To investigate this question, 10 subjects each performed 47 min of cycle ergometer exercise at 50-60% of the maximal aerobic capacity, with the work rate adjusted to maintain ventilation (VE) constant. This long ride raised mean T, (rectal) 0.8OC. Before and immediately after the long ride, ranges of VE and VT were obtained from short 6-min rides that progressed from unloaded pedaling to the anaerobic threshold. At the constant VE of the long ride, f rose and VT fell as T, rose ( P < 0.05). The fall in VT was associated with a fall in inspiratory time (TI); drive (VT/ TI) and timing (Tr/Ttot)components of VE were unchanged. These effects were consistent over the entire range of ‘\j~ obtained from the short 6-min rides. Passive heating in warm water to produce equal T, elevation in the same subjects yielded similar exercise breathing-pattern changes. These findings suggest that increased T, mediates the VT fall during prolonged exercise, possibly through stimulation of the central respiratory pacemaker. inspiratory time; expiratory quency; ventilation
time; tidal volume;
breathing
fre-
ELEVATES the body core temperature (T,) of humans. Although the influence of this T, rise on ventilation (TE) has been studied (5, 9)) little is known of its effect on breathing pattern. Knowledge of the depth and rate of breathing, and of the lengths of inspiration and expiration, provides additional insight into ventilatory control (2, 7, 14). Investigations in anesthetized cats (8) and in resting man (10, 17) indicate that passive elevation of the T, leads to rapid, shallow breathing. Similar changes in breathing pattern, if induced by T, rise during prolonged exercise, would have implications for the adequacy of gas exchange during long-term exercise. To assessthe influence of exercise hyperthermia on respiratory pattern, we studied the pattern of breathing during long-term exercise with the work rate adjusted to provide constant VE. We found that during prolonged exercise, rapid shallow breathing developed in parallel with the rise in rectal
EXERCISE
0161-7567/79/0000-Oooo$Ol.25
Copyright
CLIFFORD
0 1979 the American
Physiological
University
W. ZWILLICH, of Colorado
Medical
Center,
temperature. This correlation may indicate a direct effect of exercise-induced T, rise on respiratory pattern since we also found that passive heating produced similar exercise breathing-pattern changes. METHODS
Ten subjects in excellent health were studied after giving their informed consent. All experiments were performed in the morning in a cool room (23°C) in Denver (altitude 1,600 m), with the subject having refrained from exercise that day. For distraction, subjects wore headphones and watched television while exercising. Short-ride protocol. In each experiment the subject first performed 5-7 min of exercise on a Monark mechanically braked cycle ergometer. Exercise intensity was progressively increased so that respiratory pattern could be compared over a wide range of \jE. A pedaling rate of 50 rpm controlled by speedometer was chosen because of recent work indicating that this mode of exercise provides minimal entrainment of breathing frequency with pedaling rate (3). After 2 min of loadless pedaling, work rate was increased by lo-15 W each 30 s until PETCO, began to fall. Work was terminated at this point to avoid hypocapnia-induced changes in ventilatory pattern (13). End-tidal CO2 and 02 tensions were obtained by continuous sampling by an infrared CO2 analyzer (Godart) and a fuel-cell 02 analyzer (21) from a Rudolph respiratory valve (Collins). Ventilation was measured by a hot-film anemometer (Thermal Systems Inc.) and rectal temperature (T,) was measured by a thermistor inserted to a depth of 10 cm. Outputs from the anemometer and thermistor together with outputs from the gas analyzers were fed into a Nova 1200 computer (Data General Corp.). The data emerged as continuous oscilloscopic plots of PETCO,, PETO,, VE, tidal volume (VT), breathing frequency (f ), inspiratory time (TI), and T,,; 30-s means of each variable at each level of exercise were used for data analysis. This short ride was performed before and immediately after elevation of T, by either 47 min of exercise or warm-water immersion. Although the short ride itself tended to elevate T,, the average rise in T,, was less than O.l”C. It is possible, however, that the slowly responding temperature of the rectum might have failed to reflect accurately the temperature of the respiratory Society
1039
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (129.186.138.035) on January 16, 2019.
1040
MARTIN,
MORGAN,
ZWILLICH,
AND
WEIL
center or other sensory regions capable of influencing breathing pattern. Work comparing rectal with arterial temperature (I), a presumably more accurate index of respiratory-center temperature, has shown that while T,, tends to lag arterial temperature in the transition from rest to work, this lag is small For example, abrupt transition from rest to steady-state work at 60% of the maximal aerobic capacity (Voz max) results in a rate of arterial temperature rise of O.O3”C/min (L. H. Aulick, r I 1 personal communication). Thus the maximum potential 1 37.0 374 37.8 38.2 arterial temperature rise induced by the short 6-min ride T,e ("Cl in this study should be less than 0.2OC. Elevation of Tre with either exercise or warm-water FIG. 1. Significant negative correlation of exercise tidal volume (VT) (T,,) at constant high VE of long 47-min ride. immersion. After completion of the initial short 6-min with rectal temperature ride, the subject exercised for 47 min at a work rate Each point represents mean of data obtained from 10 subjects. chosen to provide a steady -state VE similar to that attained at the end of the 6-min ride. This work rate 1.24 averaged 50-60s of the Vo2 max;47 min of exercise proTi vided a T,, rise of nearly 1°C without exhausting the (seconds) subject. Ventilation and related variables were measured 1.18 after 1-2 min of exercise because previous work i.ndicates that a steady ’ st‘ate of VE during heavy exercise i.S reached at this time (22). Every 7 min thereafter,% and related 1.12 variables were m.easured after adjustment of work load l for maintenance of constant VE. The mean work load required to maintain VE constant fell slowly from 12 to t 1 I 1 370 374 3Z8 382 47 min of work (P < 0.05), with the mean reduction 5%. At the end of 47 min of work and after 2 min of rest, the Tre ( OC) short 6-min ride was repeated. The brief rest was inserted FIG. 2. Significant negative correlation of inspiratory time (TI) with to allow metabolic rate to falI so that the VE range rectal temperature (T,,) at constant high VE of long 47-min ride. Each a lo-subject mean. This TI decrease was associated obtained during this short ride would be comparable to point represents with a tidal volume (VT) decrease; ratio of TI to total breath duration that found in the previous short ride. Several days later, T,, was elevated by immersion to (T1’Ttot) wasunchanged* the neck in 38%39.5”C water for 15-40 min. The same 25 BATH HEATING EXERCISE HEATING . 0 0 10 subjects were utilized, and the T, rise in the bath for 0 each was matched to that observed during exercise. The “T same short 6-min rides were performed before bath im(liters BTPS) mersion and after drying on leaving the bath. In all subjects T,, remained constant or rose O.l”C during the @PRE @PRE 6-min ride after the bath. 1.01 l POST l POST Data were analyzed by analysis of variance. A Student70 20 0 70 Newman-Keuls test (18) was applied to treatment means, \;; (Vmin BTPS) VE (Ihnin f3Tps) with P < 0.05 regarded as significant.
1
1
1
0
I
1
l
I
1
20
RESULTS
Ventilatory pattern during 47-min ride. At the constant VE of this long ride, T,, rose and VT fell significantly with time (P < 0.05). The decrease in VT was correlated with the rise in T,, (P < 0.05; Fig. 1). The mean rise in Tre was 0.8OC in the 10 subjects, with a range from 0.5 to 1.4”C. The extent of individual changes in VT failed to correlate with the magnitude of individual rises in T,,. The VT fall per degree Celsius rise averaged 13%, with no suggestion that a threshold temperature had to be reached before VT changes occurred. The fall in VT was associated with a fall in TI that was also correlated with the T,, rise (P < 0.05; Fig. 2). Division of VE into “drive” (VT/TI) and “timing” (TI/Ttot) components (14) revealed that neither changed during the 47-min ride. TI/ Ttot averaged 0.524 t 0.017 after 12 min of exercise and 0.521 t 0.014 after 47 min of exercise (P = NS); VT/TI
FIG. 3. Values of tidal volume (VT) obtained as short 6-min rides in a typical subject. Elevating T, or warm-water immersion led to decreased VT at to these data showed in 10 subjects that mean VT was lowered by both exercise (P < 0.02) and bath neither maneuver changed - mean slope of lines.
TE was varied
during with either exercise any VE. Fitting lines intercept at zero i7E (P = 0.07) heating;
averaged 1.95 t 0.08 l/s at 12 min of exercise and 1.98 t 0.09 l/s after 47 min of work (P = NS). There was a significant fall in PETIT, from 39.1 t 1.1 Torr at the beginning of the long ride to 36.1 t 1.0 Torr at the end of the ride (P < 0.05). PETE, was unchanged at 84 TOM”. Ventilatory pattern durbzg short 6-min rides. The changes in VT and f seen at the high VE of the long ride were also present during the short 6-min rides that followed elevation of T, with prolonged exercise. At any VE, increasing T,, with exercise lowered VT by lowering TI (Fig. 3); VT/TI and TI/Ttot were unchanged. The mean VE range obtained extended from 20 to 60 l/min BTPS. The absolute effect of increased T,, on VT and f
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (129.186.138.035) on January 16, 2019.
TEMPERATURE
AND
EXERCISE
TIDAL
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VOLUME
was similar over the range of VE studied (Fig. 3). Thus linear regression lines of VT as a function of VE were shifted to lower VT without a change in slope. After exercise heating, the extrapolated VT intercept at zero J?E was shifted from 0.74 t 0.15 to 0.43 t 0.08 liters BTPS (P < O.OZ),while the slope was unchanged. Plotting VT as a function of TI showed that the extrapolated TI intercept at zero VT was significantly lowered by exercise heating from 2.3 t 0.3 to 1.6 t 0.3 s (P < 0.001). Mean PETIT, fell from 38.5 t 1.1 to 36.0 t 0.9 Torr after heating (P c 0.05); PETE, was unchanged at 81 Torr. Warm-water heating also raised average T,, by 0.8OC. Bath hyperthermia induced changes in ventilatory pattern that were similar to those seen with exercise heating: VT was reduced after heating because of decreased TI; VT/TI and TI/Ttot were unchanged. As after exercise heating, the absolute magnitude of these effects was equal over the VE range studied (Fig. 3) so that the slope of VT-VE plots was unchanged, while the extrapolated VT intercept at zero \j~ was reduced from 0.60 t 0.07 to 0.48 t 0.06 lit ers BTPS (P = 0.07). Similarly, the extrapolated TI intercept at zero VT was reduced from 2.2 t 0.2 to 2.0 t 0.2 s (P = 0.18). Mean PETIT, was lower after T,, elevation (38.0 t 1.0 vs. 39.4 t 0.9 Torr; P < 0.05), while PETE, was unchanged at 80 Torr. DISCUSSION
In this study we found that exercise hyperthermia was associated with increased f and decreased VT during exercise. An equal T,, rise produced passively in warm water provided a similar result. In previous work on exercisin .g man, progressive tachypnea developed in association with t he T, rise d.uring heavy long-term work (5). However, this tachypnea occurred as TE rose, leaving open the possibility that the increase in f was simply that expected from the VE increase alone. Our results indicate that prolonged exercise with an increase in T, results in progressive tachypnea, even with VE held constant. The behavior of VT and f during other forms of endurance exercise such as treadmill running may be altered due to entrainment of f with step rate in many subjects (3). Support for the conclusion that the T, rise in exercise caused the changes in VT and f comes from our finding that heating in warm water provided similar results. The reverse experiment of blocking the T, rise during prolonged exercise to block the development of tachypnea has not been performed. While this maneuver prevents the steady increase in VE during long-term work (6)) its effects on breathing pattern are unknown. Other studies of the influence of external heating on exercise respiratory pattern are conflicting, showing either unchanged f
and VT (9) or elevated f and decreased VT (16). Variability of results among studies may relate in part to use of different modes of endurance exercise (3). Our result agrees with previous work in resting man (10, 17) and anesthetized cats (8) showing that passive heating leads to rapid, shallow breathing. The influence of T, elevation on VT and f in this study is of comparable magnitude to its effect on heart rate (11). It is possible that some other effect common to exercise and warm-water heating caused the breathing-pattern changes. Skin temperature changes may be ruled out because the two modes of heating probably produced quite different skin temperatures (9, 12). Another possibility is that falling PETCO, may have lowered VT and raised f as it does during exercise above the anaerobic threshold (13). However, the PETIT, fall may have been the effect and not the cause of the f increase (20). In addition, the PET co, changes were small in comparison with those required in an earlier study to produce significant VT and f changes (13). The mechanism by which increased T, induces rapid, shallow breathing remains unknown. Previous work has ascribed the generation of the respiratory pattern to both a central pacemaker and to vagal and other inputs (4, 8, 15, 23). The present results are similar to those found in anesthetized cats (8), with increased temperature decreasing the extrapolated TI intercept at zero VT. Such results have previously been interpreted as indicating an effect of increased T, on the central pacemaker (8). Two potential difficulties with this interpretation should be mentioned. The first is that the present data only include tidal volumes above 1 liter BTPS. Thus, extrapolation to zero VT involves more risk of error than if VT were also measured at resting levels. Second, the concept of respiratory-center autorhythmicity has recently been challenged by evidence in dogs showing its almost complete dependence on afferent input (19). The implications of the development of tachypnea during prolonged exercise remain to be explored. Ventilation climbs throughout long-term constant-load exercise for poorly understood reasons (5). Rapid, shallow breathing could contribute to the overall VE rise if it increases dead-space ventilation. In conclusion, evidence that passive elevation of the T, lowers VT and raises f at rest prompted this study. We found that these effects also occur as T, rises during prolonged exercise. The authors thank the subjects for their Charlotte B. Feicht for technical assistance. This study was supported by National Institute Grant HL 14985. Received
16 November
1978; accepted
in final
spirited
participation,
Heart,
Lung,
form
25 June
and
and Blood
1979.
REFERENCES 1. AULICK, L. H., S. ROBINSON, S. P. TZANKOFF, AND B. J. MARTIN. Arteriovenous temperature gradients in the limbs of men during treadmill work (Abstract). Federation Proc. 33: 441, 1974. 2. BARCROFT, J., AND R. MARGARIA. Some effects of carbonic acid on the character of human respiration. J. Physiol. London 72: 175196, 1931. 3. BECHBACHE, R. R., AND J. DUFFIN. The entrainment of breathing frequency by exercise rhythm. J. Physiol. London 272: 553-561, 1977.
4. CLARK, F. J., AND C. VON EULER. On the regulation of the depth and rate of breathing. J. Physiol. London 222: 267-295, 1972. 5. DEMPSEY, J. A., N. GLEDHILL, W. G, REDDAN, H. V. FORSTER, P. G. HANSON, AND A. D. CLAREMONT. Pulmonary adaptation to exercise: effects of exercise type and duration, chronic hypoxia, and physical training. Ann. NY Acad. Sci. 301: 243-261, 1977. 6. DEMPSEY, J. A., J. M. THOMSON, S. C. ALEXANDER, H. V. FORSTER, AND L. W. CHOSY. Respiratory influence on acid-base status and their effects on 02 transport during prolonged muscular work. In:
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7.
8.
9.
10.
11.
12.
13.
14.
Metabolic Adaptation to Prolonged PhysicaL Exercise. Basel; Birkhauser, 1975, p. 56-64. GAUTIER, H., AND J. H. GAUDY. Changes in ventilatory pattern induced by intravenous anesthetic agents in human subjects. J. AppZ. Physiot.: Respirat. Enuiron. Exercise Physiol. 45: 171-176, 1978. GRUNSTEIN, M. M., W. M. FISK, L. A. LEITER, AND J. MILIC-EMILI. Effect of body temperature on respiratory frequency in anesthetized cats. J. AppZ. Physiol. 34: 154-159, 1973. HENRY, J. G., AND C. R. BAINTON. Human core temperature increase as a stimulus to breathing during moderate exercise. Respir. Physiol. 21: 183-191, 1974. HEY, E. N., B. B. LLOYD, D. J. C. CUNNINGHAM, M. G. M. JUKES, AND D. P. G. BOLTON. Effects of various respiratory stimuli on the depth and frequency of breathing in man. Respir. Physiol. 1: 193205, 1966. JOSE, A. D., F. STITT, AND D. COLLISON. The effects of exercise and changes in body temperature on the intrinsic heart rate in man. Am. Heart J. 79: 488-497, 1970. MACDOUGALL, J. D., W. G. REDDAN, C. R. LAYTON, AND J. A. DEMPSEY. Effects of metabolic hyperthermia on performance during heavy prolonged exercise. J. Appl. Physiol. 36: 538-544, 1974. MARTIN, B. J., AND J. V. WEIL. CO2 and exercise tidal volume. J. AppZ. Physiol.: Respirat. Environ. Exercise Physiol. 46: 322-325, 1979. MILIC-EMILI, J., AND M. M. GRUNSTEIN. Drive and timing components of ventilation. Chest 70: 131-133, 1976.
MARTIN,
MORGAN,
ZWILLICH,
AND
WEIL
15. MITCHELL, R. A., AND A. J. BERGER. Neural regulation of respiration. Am. Rev. Respir. Dis. 111: 206-224, 1975. 16. PETERSON, E. S., AND H. VEJBY-CHRISTENSEN. Effects of body temperature on steady-state ventilation and metabolism in exercise. Acta Physiol. &and. 89: 342-351, 1973. 17. PETERSON, E. S., AND H. VEJBY-CHRISTENSEN. Effects of body temperature on ventilatory response to hypoxia and breathing pattern in man. J. AppZ. Physiol.: Respirat. Environ. Exercise Physiol. 42: 492-500, 1977. 18. SOKAL, R. R., AND F. J. ROHLF. Biometry. The Principles and Practice of Statistics in BioZogicaZ Research. San Francisco, CA: Freeman, 1969. 19. SULLILVAN, C. E., L. F. KOZAR, E. MURPHY, AND E. A. PHILLIPSON. Primary role of respiratory afferents in sustaining breathing rhythm. J. AppZ. Physiol.: Respirat. Environ. Exercise Physiol. 45: 11-17, 1978. 20. WASSERMAN, K., AND B. J. WHIPP. Exercise physiology in health and disease. Am. Rev. Respir. Dis. 112: 219-249, 1975. 21. WEIL, J. V., I. E. SODAL, AND R. P. SPECK. A modified fuel cell for the analysis of oxygen concentration of gases. J. AppZ. Physiol. 23: 419-422, 1967. 22. WHIPP, B. J., AND K. WASSERMAN. Oxygen uptake kinetics for various intensities of constant load work. J. AppZ. Physiol. 33: 35l356, 1972. 23. WYMAN, R. J. Neural generation of the breathing rhythm. Annu. Rev. Physiol. 39: 417-448, 1977.
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EDWARD
Cardiovascular Pulmonary Denver, Colorado 80262
J. MORGAN,
Research Laboratory,
MARTIN, BRUCE J., EDWARD J. MORGAN, CLIFFORD W. ZWILLICH, AND JOHN V. WEIL. Influence of exercise hyperthermia on exercise breathing pattern. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 47(5): 1039-1042, 1979.-Passive elevation of the body core temperature (T,) induces rapid, shallow breathing in resting man. We wondered if exercise-induced T, elevation would also lead to decreased tidal volume (VT) and increased breathing frequency (f) during exercise. To investigate this question, 10 subjects each performed 47 min of cycle ergometer exercise at 50-60% of the maximal aerobic capacity, with the work rate adjusted to maintain ventilation (VE) constant. This long ride raised mean T, (rectal) 0.8OC. Before and immediately after the long ride, ranges of VE and VT were obtained from short 6-min rides that progressed from unloaded pedaling to the anaerobic threshold. At the constant VE of the long ride, f rose and VT fell as T, rose ( P < 0.05). The fall in VT was associated with a fall in inspiratory time (TI); drive (VT/ TI) and timing (Tr/Ttot)components of VE were unchanged. These effects were consistent over the entire range of ‘\j~ obtained from the short 6-min rides. Passive heating in warm water to produce equal T, elevation in the same subjects yielded similar exercise breathing-pattern changes. These findings suggest that increased T, mediates the VT fall during prolonged exercise, possibly through stimulation of the central respiratory pacemaker. inspiratory time; expiratory quency; ventilation
time; tidal volume;
breathing
fre-
ELEVATES the body core temperature (T,) of humans. Although the influence of this T, rise on ventilation (TE) has been studied (5, 9)) little is known of its effect on breathing pattern. Knowledge of the depth and rate of breathing, and of the lengths of inspiration and expiration, provides additional insight into ventilatory control (2, 7, 14). Investigations in anesthetized cats (8) and in resting man (10, 17) indicate that passive elevation of the T, leads to rapid, shallow breathing. Similar changes in breathing pattern, if induced by T, rise during prolonged exercise, would have implications for the adequacy of gas exchange during long-term exercise. To assessthe influence of exercise hyperthermia on respiratory pattern, we studied the pattern of breathing during long-term exercise with the work rate adjusted to provide constant VE. We found that during prolonged exercise, rapid shallow breathing developed in parallel with the rise in rectal
EXERCISE
0161-7567/79/0000-Oooo$Ol.25
Copyright
CLIFFORD
0 1979 the American
Physiological
University
W. ZWILLICH, of Colorado
Medical
Center,
temperature. This correlation may indicate a direct effect of exercise-induced T, rise on respiratory pattern since we also found that passive heating produced similar exercise breathing-pattern changes. METHODS
Ten subjects in excellent health were studied after giving their informed consent. All experiments were performed in the morning in a cool room (23°C) in Denver (altitude 1,600 m), with the subject having refrained from exercise that day. For distraction, subjects wore headphones and watched television while exercising. Short-ride protocol. In each experiment the subject first performed 5-7 min of exercise on a Monark mechanically braked cycle ergometer. Exercise intensity was progressively increased so that respiratory pattern could be compared over a wide range of \jE. A pedaling rate of 50 rpm controlled by speedometer was chosen because of recent work indicating that this mode of exercise provides minimal entrainment of breathing frequency with pedaling rate (3). After 2 min of loadless pedaling, work rate was increased by lo-15 W each 30 s until PETCO, began to fall. Work was terminated at this point to avoid hypocapnia-induced changes in ventilatory pattern (13). End-tidal CO2 and 02 tensions were obtained by continuous sampling by an infrared CO2 analyzer (Godart) and a fuel-cell 02 analyzer (21) from a Rudolph respiratory valve (Collins). Ventilation was measured by a hot-film anemometer (Thermal Systems Inc.) and rectal temperature (T,) was measured by a thermistor inserted to a depth of 10 cm. Outputs from the anemometer and thermistor together with outputs from the gas analyzers were fed into a Nova 1200 computer (Data General Corp.). The data emerged as continuous oscilloscopic plots of PETCO,, PETO,, VE, tidal volume (VT), breathing frequency (f ), inspiratory time (TI), and T,,; 30-s means of each variable at each level of exercise were used for data analysis. This short ride was performed before and immediately after elevation of T, by either 47 min of exercise or warm-water immersion. Although the short ride itself tended to elevate T,, the average rise in T,, was less than O.l”C. It is possible, however, that the slowly responding temperature of the rectum might have failed to reflect accurately the temperature of the respiratory Society
1039
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (129.186.138.035) on January 16, 2019.
1040
MARTIN,
MORGAN,
ZWILLICH,
AND
WEIL
center or other sensory regions capable of influencing breathing pattern. Work comparing rectal with arterial temperature (I), a presumably more accurate index of respiratory-center temperature, has shown that while T,, tends to lag arterial temperature in the transition from rest to work, this lag is small For example, abrupt transition from rest to steady-state work at 60% of the maximal aerobic capacity (Voz max) results in a rate of arterial temperature rise of O.O3”C/min (L. H. Aulick, r I 1 personal communication). Thus the maximum potential 1 37.0 374 37.8 38.2 arterial temperature rise induced by the short 6-min ride T,e ("Cl in this study should be less than 0.2OC. Elevation of Tre with either exercise or warm-water FIG. 1. Significant negative correlation of exercise tidal volume (VT) (T,,) at constant high VE of long 47-min ride. immersion. After completion of the initial short 6-min with rectal temperature ride, the subject exercised for 47 min at a work rate Each point represents mean of data obtained from 10 subjects. chosen to provide a steady -state VE similar to that attained at the end of the 6-min ride. This work rate 1.24 averaged 50-60s of the Vo2 max;47 min of exercise proTi vided a T,, rise of nearly 1°C without exhausting the (seconds) subject. Ventilation and related variables were measured 1.18 after 1-2 min of exercise because previous work i.ndicates that a steady ’ st‘ate of VE during heavy exercise i.S reached at this time (22). Every 7 min thereafter,% and related 1.12 variables were m.easured after adjustment of work load l for maintenance of constant VE. The mean work load required to maintain VE constant fell slowly from 12 to t 1 I 1 370 374 3Z8 382 47 min of work (P < 0.05), with the mean reduction 5%. At the end of 47 min of work and after 2 min of rest, the Tre ( OC) short 6-min ride was repeated. The brief rest was inserted FIG. 2. Significant negative correlation of inspiratory time (TI) with to allow metabolic rate to falI so that the VE range rectal temperature (T,,) at constant high VE of long 47-min ride. Each a lo-subject mean. This TI decrease was associated obtained during this short ride would be comparable to point represents with a tidal volume (VT) decrease; ratio of TI to total breath duration that found in the previous short ride. Several days later, T,, was elevated by immersion to (T1’Ttot) wasunchanged* the neck in 38%39.5”C water for 15-40 min. The same 25 BATH HEATING EXERCISE HEATING . 0 0 10 subjects were utilized, and the T, rise in the bath for 0 each was matched to that observed during exercise. The “T same short 6-min rides were performed before bath im(liters BTPS) mersion and after drying on leaving the bath. In all subjects T,, remained constant or rose O.l”C during the @PRE @PRE 6-min ride after the bath. 1.01 l POST l POST Data were analyzed by analysis of variance. A Student70 20 0 70 Newman-Keuls test (18) was applied to treatment means, \;; (Vmin BTPS) VE (Ihnin f3Tps) with P < 0.05 regarded as significant.
1
1
1
0
I
1
l
I
1
20
RESULTS
Ventilatory pattern during 47-min ride. At the constant VE of this long ride, T,, rose and VT fell significantly with time (P < 0.05). The decrease in VT was correlated with the rise in T,, (P < 0.05; Fig. 1). The mean rise in Tre was 0.8OC in the 10 subjects, with a range from 0.5 to 1.4”C. The extent of individual changes in VT failed to correlate with the magnitude of individual rises in T,,. The VT fall per degree Celsius rise averaged 13%, with no suggestion that a threshold temperature had to be reached before VT changes occurred. The fall in VT was associated with a fall in TI that was also correlated with the T,, rise (P < 0.05; Fig. 2). Division of VE into “drive” (VT/TI) and “timing” (TI/Ttot) components (14) revealed that neither changed during the 47-min ride. TI/ Ttot averaged 0.524 t 0.017 after 12 min of exercise and 0.521 t 0.014 after 47 min of exercise (P = NS); VT/TI
FIG. 3. Values of tidal volume (VT) obtained as short 6-min rides in a typical subject. Elevating T, or warm-water immersion led to decreased VT at to these data showed in 10 subjects that mean VT was lowered by both exercise (P < 0.02) and bath neither maneuver changed - mean slope of lines.
TE was varied
during with either exercise any VE. Fitting lines intercept at zero i7E (P = 0.07) heating;
averaged 1.95 t 0.08 l/s at 12 min of exercise and 1.98 t 0.09 l/s after 47 min of work (P = NS). There was a significant fall in PETIT, from 39.1 t 1.1 Torr at the beginning of the long ride to 36.1 t 1.0 Torr at the end of the ride (P < 0.05). PETE, was unchanged at 84 TOM”. Ventilatory pattern durbzg short 6-min rides. The changes in VT and f seen at the high VE of the long ride were also present during the short 6-min rides that followed elevation of T, with prolonged exercise. At any VE, increasing T,, with exercise lowered VT by lowering TI (Fig. 3); VT/TI and TI/Ttot were unchanged. The mean VE range obtained extended from 20 to 60 l/min BTPS. The absolute effect of increased T,, on VT and f
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (129.186.138.035) on January 16, 2019.
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1041
VOLUME
was similar over the range of VE studied (Fig. 3). Thus linear regression lines of VT as a function of VE were shifted to lower VT without a change in slope. After exercise heating, the extrapolated VT intercept at zero J?E was shifted from 0.74 t 0.15 to 0.43 t 0.08 liters BTPS (P < O.OZ),while the slope was unchanged. Plotting VT as a function of TI showed that the extrapolated TI intercept at zero VT was significantly lowered by exercise heating from 2.3 t 0.3 to 1.6 t 0.3 s (P < 0.001). Mean PETIT, fell from 38.5 t 1.1 to 36.0 t 0.9 Torr after heating (P c 0.05); PETE, was unchanged at 81 Torr. Warm-water heating also raised average T,, by 0.8OC. Bath hyperthermia induced changes in ventilatory pattern that were similar to those seen with exercise heating: VT was reduced after heating because of decreased TI; VT/TI and TI/Ttot were unchanged. As after exercise heating, the absolute magnitude of these effects was equal over the VE range studied (Fig. 3) so that the slope of VT-VE plots was unchanged, while the extrapolated VT intercept at zero \j~ was reduced from 0.60 t 0.07 to 0.48 t 0.06 lit ers BTPS (P = 0.07). Similarly, the extrapolated TI intercept at zero VT was reduced from 2.2 t 0.2 to 2.0 t 0.2 s (P = 0.18). Mean PETIT, was lower after T,, elevation (38.0 t 1.0 vs. 39.4 t 0.9 Torr; P < 0.05), while PETE, was unchanged at 80 Torr. DISCUSSION
In this study we found that exercise hyperthermia was associated with increased f and decreased VT during exercise. An equal T,, rise produced passively in warm water provided a similar result. In previous work on exercisin .g man, progressive tachypnea developed in association with t he T, rise d.uring heavy long-term work (5). However, this tachypnea occurred as TE rose, leaving open the possibility that the increase in f was simply that expected from the VE increase alone. Our results indicate that prolonged exercise with an increase in T, results in progressive tachypnea, even with VE held constant. The behavior of VT and f during other forms of endurance exercise such as treadmill running may be altered due to entrainment of f with step rate in many subjects (3). Support for the conclusion that the T, rise in exercise caused the changes in VT and f comes from our finding that heating in warm water provided similar results. The reverse experiment of blocking the T, rise during prolonged exercise to block the development of tachypnea has not been performed. While this maneuver prevents the steady increase in VE during long-term work (6)) its effects on breathing pattern are unknown. Other studies of the influence of external heating on exercise respiratory pattern are conflicting, showing either unchanged f
and VT (9) or elevated f and decreased VT (16). Variability of results among studies may relate in part to use of different modes of endurance exercise (3). Our result agrees with previous work in resting man (10, 17) and anesthetized cats (8) showing that passive heating leads to rapid, shallow breathing. The influence of T, elevation on VT and f in this study is of comparable magnitude to its effect on heart rate (11). It is possible that some other effect common to exercise and warm-water heating caused the breathing-pattern changes. Skin temperature changes may be ruled out because the two modes of heating probably produced quite different skin temperatures (9, 12). Another possibility is that falling PETCO, may have lowered VT and raised f as it does during exercise above the anaerobic threshold (13). However, the PETIT, fall may have been the effect and not the cause of the f increase (20). In addition, the PET co, changes were small in comparison with those required in an earlier study to produce significant VT and f changes (13). The mechanism by which increased T, induces rapid, shallow breathing remains unknown. Previous work has ascribed the generation of the respiratory pattern to both a central pacemaker and to vagal and other inputs (4, 8, 15, 23). The present results are similar to those found in anesthetized cats (8), with increased temperature decreasing the extrapolated TI intercept at zero VT. Such results have previously been interpreted as indicating an effect of increased T, on the central pacemaker (8). Two potential difficulties with this interpretation should be mentioned. The first is that the present data only include tidal volumes above 1 liter BTPS. Thus, extrapolation to zero VT involves more risk of error than if VT were also measured at resting levels. Second, the concept of respiratory-center autorhythmicity has recently been challenged by evidence in dogs showing its almost complete dependence on afferent input (19). The implications of the development of tachypnea during prolonged exercise remain to be explored. Ventilation climbs throughout long-term constant-load exercise for poorly understood reasons (5). Rapid, shallow breathing could contribute to the overall VE rise if it increases dead-space ventilation. In conclusion, evidence that passive elevation of the T, lowers VT and raises f at rest prompted this study. We found that these effects also occur as T, rises during prolonged exercise. The authors thank the subjects for their Charlotte B. Feicht for technical assistance. This study was supported by National Institute Grant HL 14985. Received
16 November
1978; accepted
in final
spirited
participation,
Heart,
Lung,
form
25 June
and
and Blood
1979.
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