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J Appl Physiol 104: 998-1005, 2008. First published January 3, 2008; doi:10.1152/japplphysiol.00146.2007
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Comparison of hyperthermic hyperpnea elicited during rest and submaximal, moderate-intensity exercise

Naoto Fujii,1 Yasushi Honda,1 Keiji Hayashi,1 Hideaki Soya,1 Narihiko Kondo,2 and Takeshi Nishiyasu1

1Institute of Health and Sports Science, University of Tsukuba, Tsukuba City; and 2Faculty of Human Development, Kobe University, Kobe, Japan

Submitted 3 February 2007 ; accepted in final form 29 December 2007


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
We tested the hypothesis that, in humans, hyperthermic hyperpnea elicited in resting subjects differs from that elicited during submaximal, moderate-intensity exercise. In the rest trial, hot-water legs-only immersion and a water-perfused suit were used to increase esophageal temperature (Tes) in 19 healthy male subjects; in the exercise trial, Tes was increased by prolonged submaximal cycling [50% peak O2 uptake (VO2)] in the heat (35°C). Minute ventilation (VE), ventilatory equivalent for VO2 (VE/VO2) and CO2 output (VE/VCO2), tidal volume (VT), and respiratory frequency (f) were plotted as functions of Tes. In the exercise trial, VE increased linearly with increases (from 37.0 to 38.7°C) in Tes in all subjects; in the rest trial, 14 of the 19 subjects showed a Tes threshold for hyperpnea (37.8 ± 0.5°C). Above the threshold for hyperpnea, the slope of the regression line relating VE and Tes was significantly greater for the rest than the exercise trial. Moreover, the slopes of the regression lines relating VE/VO2, VE/VCO2, and Tes were significantly greater for the rest than the exercise trial. The increase in VE reflected increases in VT and f in the rest trial, but only f in the exercise trial, after an initial increase in ventilation due to VT. Finally, the slope of the regression line relating Tes and VT or f was significantly greater for the rest than the exercise trial. These findings indicate that hyperthermic hyperpnea does indeed differ, depending on whether one is at rest or exercising at submaximal, moderate intensity.

thermoregulation; evaporative heat loss; ventilatory pattern

IN MANY SPECIES OF MAMMALS and birds, an elevation in body temperature stimulates ventilation and increases evaporative heat loss for thermoregulation with a two-phase panting response (26, 33). In animals such as the sheep and dog, this panting response can include two distinct patterns of breathing, often referred to as first- and second-phase panting (7, 12, 13, 26, 33). In the first phase, respiratory frequency (f) is maximized, while tidal volume (VT) is minimized, and arterial blood gases are not perturbed (33). The second phase is only evident with an increase in core temperature, and VT and f are increased, so that alveolar ventilation is increased, resulting in hypocapnia and respiratory alkalosis (33). In 1905, Haldane (11) was the first to report that hyperthermia also increases ventilation in humans. The recent review by White (33) suggested that since increased ventilation by hyperthermia in humans increases alveolar ventilation so that respiratory alkalosis occurs, a hyperthermia-induced increase in ventilation in humans is likely to be the second phase of panting. However, the mechanisms and the physiological significance of this response in humans are not fully understood.

When body temperature is increased in resting humans, minute ventilation (VE) reportedly increases linearly (slope ~25 l·min–1·°C–1) with an increase in esophageal temperature (Tes) from 38.6 to 39.0°C (3). However, this response only occurs after a critical threshold (38.1–38.6°C) has been reached (3, 29). On the other hand, Hayashi et al. (14) recently reported that, during prolonged submaximal exercise [50% peak O2 uptake (VO2 peak)] in the heat, VE increased linearly (slope ~6.1 l·min–1·°C–1) with no threshold with an increase in Tes from 37.2 to 39.0°C. Similarly, Nybo and Nielsen (23) reported a linear relationship between Tes and VE (slope ~12.5 l·min–1·°C–1) in the range ~38.0–40.0°C during prolonged submaximal exercise (57% VO2 peak) in the heat with a superimposed hyperthermia. These findings suggest that hyperthermic hyperpnea differs depending on whether the subject is resting or exercising at submaximal, moderate intensity. Indeed, hyperthermia increases ventilation, and this response might be attenuated by submaximal, moderate-intensity exercise, although this possibility has not been directly tested in humans.

The relationship between core temperature and ventilatory response has been investigated in animals (e.g., sheep) at rest (7, 12, 13) and during submaximal exercise (6), but the responses of resting and exercising animals have not been investigated concurrently. In two studies, however, the relationship between core temperature and ventilatory response was obtained at rest and during submaximal, moderate-intensity exercise and was compared using the same animals (dogs and goats) (4, 22). Those studies showed that the slope of the regression line relating core temperature and respiratory evaporative water loss (Eres, an index of the panting response) was smaller during exercise than at rest. Furthermore, it was suggested that there is a core temperature threshold for the increase in Eres at rest and during exercise and that the threshold is lower during exercise than at rest (4, 22). Moreover, separately reported core temperature thresholds for hyperthermic hyperpnea during incremental exercise (37.4–37.9°C) (27, 34, 35) were lower than those during passively induced hyperthermia (38.1–38.6°C) (3, 29) in humans. We suggest that the features of the hyperthermic hyperpnea reported in the above-mentioned animal studies are also true for humans.

In resting humans, increases in ventilation elicited by increases in body temperature reportedly can be induced by an increase in VT (3, 29), an increase in f (15, 16, 24), or increases in VT and f (1, 2, 9, 17, 18). It therefore remains unclear how ventilatory patterns in humans change in response to an increase in core temperature under resting conditions. On the other hand, in humans exercising for long durations at submaximal, steady states, after an initial increase in ventilation due to an increase in VT, subsequent increases in ventilation caused by hyperthermia are reportedly due to increases in f (14, 19, 20). These findings suggest that even though hyperthermia changes ventilatory patterns, these changes can be modified by exercise. Bearing this in mind, we hypothesized that hyperthermic hyperpnea in humans differs depending on whether one is at rest or exercising; that is, hypothermic hyperpnea at rest can be attenuated by submaximal, moderate-intensity exercise in humans. To test that idea, core temperature was increased using hot-water lower body immersion and a water-perfused suit (rest trial) or by submaximal, moderate-intensity exercise in the heat (exercise trial), and the relationships between core temperature and ventilation were compared.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Subjects.   Nineteen healthy male subjects [age = 24.4 ± 2.1 (SD) yr, height = 170.0 ± 3.4 cm, body weight = 65.7 ± 6.6 kg, VO2 peak = 49.4 ± 6.2 ml·kg–1·min–1] participated in the present study, which was approved by the Human Subjects Committee of the University of Tsukuba. All participants provided written informed consent. None of the subjects were smokers, and none were taking medication. Before any data were collected, the subjects were allowed to practice the cycle exercise until they became accustomed to the exercise routine.

VO2 peak test.   Several days before beginning the experiments, the subjects came to the laboratory (in the morning or afternoon) and performed an incremental cycling exercise to volitional exhaustion to determine VO2 peak (model 818E, Monark; customized for semirecumbent cycling). The subjects initially performed a light warm-up (30 W, 60 rpm) for 3 min and then 1 min later performed the incremental cycling exercise. The exercise was started at 60 W, then the load was increased at a rate of 15 W/min throughout the exercise period. The subjects pedaled at 60 rpm, and volitional fatigue was defined as an inability to pedal at >50 rpm. The subjects breathed from a mask, which covered the mouth and nose (inside volume of the mask = 80 ml). A mass flow sensor (hot-wire type) and a gas-sampling tube (sampling volume rate <0.2 l/min) were connected to the mask, and the expired volume and gases were analyzed using an electric gas flowmeter (model RM300i, Minato Medical Science). Dead space, resistance of the respiratory apparatus, and loss of volume caused by the gas sampling were sufficiently small that we considered their effects on the data to be negligible. The flowmeter was calibrated with the aid of an appurtenant calibration instrument able to blow a fixed volume (2 liters) of reference gases of known concentration. VE, O2 uptake (VO2), and CO2 output (VCO2) were calculated at 60-s intervals. The respiratory exchange ratio (RER) was calculated as VCO2 ÷ VO2. VO2 peak was taken as the highest value of VO2 achieved by a subject, inasmuch as some subjects did not achieve a plateau (even though RER exceeded 1.1 at VO2 peak). The VO2 peak test was performed in an environmental chamber (Fujiika, Chiba, Japan) maintained at 25°C and 50% relative humidity. Room air was ventilated to prevent any increase in the CO2 concentration. Wind speed in the room was <0.2 m/s.

Experimental design.   Beginning ≥2 days after the VO2 peak test, two trials in which body temperature was increased while the subject was at rest (rest trial) or during submaximal, moderate-intensity exercise (exercise trial) were carried out in random order separated by ≥6 days. For both the trials, each subject came to the laboratory at 8:30 AM. Subjects were asked to abstain from strenuous exercise, alcohol, and caffeine for 24 h before each trial. To standardize the subjects' hydration status, we asked them to consume the same meal and drink 500 ml of water on the night before each trial. In addition, the subjects consumed only a light breakfast and 300 ml of water 2 h before each trial.

Rest trial.   After arriving at the laboratory, subjects rested, sitting in a chair, for 30 min (ambient temperature = 25°C, relative humidity = 50%). During this time, a thermocouple was inserted via the nasal passage to a distance equivalent to one-fourth of the subject's height to measure esophageal temperature (Tes). After thermocouples for measuring skin temperature (Tsk) were attached, the subject put on a water-perfusable suit that covered the upper body, except the face and hands, moved into a water-filled bathtub, and sat in a chair for 30 min. The temperature of water in the bathtub was set to ~35°C with aid of a heater, and the subject was immersed to the level of the iliac crest. As determined from pilot experiments, it was difficult to increase core temperature above 2.0°C with only a water-perfusable suit; therefore, in addition, the lower legs were immersed in hot water. The water in the bathtub was also circulated through the water-perfusable suit, and a mask for measurement of respiratory gases and volume was attached. After all measurements were started, the subject rested for 5 min. Then the water in the bathtub was replaced with the aid of a pump to set the water temperature to ~41°C, which caused the subject's body temperature to rise. During the trial, the temperature of the water was kept constant with the aid of the heater. When Tes reached 39.0°C or the subject could no longer endure the heat, the subject was allowed to move out of the bathtub.

Exercise trial.   In the exercise trial, the procedure was the same as that described for the resting trial with the following exceptions. After a thermocouple was inserted for measurement of Tes, the subjects voided urine and moved to the environmental chamber (ambient temperature = 35°C, relative humidity = 50%, wind speed < 0.2 m/s), where they sat in a chair behind the ergometer to rest for 30 min. After all the pieces of equipment, which were the same as those used in the rest trial, were attached, the subject rested for 5 min and then exercised on a cycle ergometer continuously for 40–60 min at 50% VO2 peak. When Tes reached 39.0°C or the subject could not cycle at 60 rpm, the trial ended.

Measurements.   Tes and Tsk data were collected via copper-constantan thermocouples, sampled and recorded on a computer (ThinkPad A21p, IBM, Chiba, Japan) at 1-s intervals via a data logger system (model WE7000, Yokogawa, Tokyo, Japan), and averaged over 30-s periods. Tsk was measured at seven sites (chest, upper back, lower back, abdomen, thigh, calf, and forearm), and mean Tsk (Tsk) was calculated by the method of Taylor et al. (30). Expired gas was measured using the same analyzers used in the VO2 peak test (see above). From the analyzers, VE, VT, f, VO2, VCO2, and end-tidal PCO2 (PETCO2) were recorded over 30-s periods.

Data analysis.   To assess the relationship between respiratory parameters (VE, VE/VO2, VE/VCO2, VT, f, and PETCO2) and Tes, we plotted respiratory parameters as a function of Tes and conducted linear regression analysis (14). Because ~4 min are required from the start of the exercise to steady-state VE, only data obtained after the first 5 min of the exercise were used for the regression analysis in the exercise trial. Tes threshold for the increase in VE was determined by computer algorithm as the point where the two regression lines crossed, as outlined in a previous study (14). To calculate the best-fit two regression lines, we chose the two regression lines with the smallest residual sums of squares. Since breath-by-breath data were too scattered to allow detection of the threshold, we used 30-s averaged data. The slope of the regression line relating VE and Tes (VE slope) was considered to be an index of the ventilatory response to the increase in core temperature. VE/VO2, VE/VCO2, VT, f, and PETCO2 slopes were similarly evaluated. Several subjects repeated the rest and exercise trials, and we found high and significant repeatability of Tes threshold for the increase in VE (r = 0.83, P < 0.05) and VE slope (above the threshold; r = 0.97, P < 0.05) in the rest trial (n = 9) and VE slope in the exercise trial (r = 0.93, P < 0.05, n = 13). VE, VT, and f were selected as important indexes, and for the comparison of means, minimum sample sizes were calculated on the basis of 80% power and a significance level of 0.05 (5). Effect sizes, which we set on the basis of our pilot experiments, were 1.13 for VE, 1.05 for VT, and 0.95 for f. The minimum sample sizes were estimated to be 7, 8, and 9 for VE, VT, and f, respectively. In that experiment, a large sample size (n = 19) was used to account for attrition of study subjects with increases in heating time; the resultant smallest sample size (n = 11) was larger than the estimated minimum sample sizes.

Time-dependent data were analyzed using two-factor repeated-measures ANOVA. After determination of the main effects, pairwise differences were identified using Tukey's honestly significant difference post hoc procedure. Data were collected for 40 min during the rest trials and 50 min during the exercise trials. Beyond these times, the numbers of subjects remaining in the trials were too small for useful analysis. When the number of subjects was reduced (after 35 min), we used only the remaining subjects for the ANOVA. Two-tailed paired t-tests were used to compare the slopes (VE, VE/VO2, VE/VCO2, VT, f, and PETCO2) between the two trials. Values are means ± SD. P < 0.05 was considered significant.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Body temperatures.   Tsk was measured in 18 of the 19 subjects, and Tes was measured all 19 subjects; both increased steadily during the two trials. In the rest trial, at the times indicated in Fig. 1, A and B, Tsk and Tes were significantly higher, by 0.8–3.5°C from 5 to 40 min (Tsk) and by 0.18–1.94°C from 10 to 40 min (Tes), than the respective time 0 (Pre) values. In the exercise trial, they were significantly higher, by 0.2–0.9°C from 15 to 40 min (Tsk) and by 0.26–1.57°C from 15 to 40 min (Tes), than the respective 10-min values. Tsk was significantly higher, by 0.5–2.0°C from 10 to 40 min, in the exercise than in the rest trial, and Tes was significantly higher, by 0.23–0.48°C, between time 0 (Pre) and 20 min. By the end of the heating sessions, Tes had increased 2.2 ± 0.5°C from time 0 (Pre) in the rest trial and 2.1 ± 0.4°C in the exercise trial. The rate of increase in Tes was significantly higher in the rest than in the exercise trial (3.3 ± 0.5 vs. 2.5 ± 0.6°C/h, P < 0.05).


Figure 1
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  		Fig. 1. Time-dependent changes in mean skin temperature and esophageal temperature (Tes) during rest and exercise trials. Numbers adjacent to symbols indicate number of subjects remaining. Pre, time 0. *P < 0.05, rest vs. exercise at the same time or time points. {dagger}P < 0.05 vs. Pre in rest trial. $P < 0.05 vs. 10 min in exercise trial.

 
VE, VT, f, and PETCO2.   VE, VT, f, and PETCO2 were measured in all 19 subjects. At the times indicated in Fig. 2, VE, VT, f, and PETCO2 were significantly higher in the exercise than in the rest trial. VE and f in the exercise trial gradually increased, and VE after 20 min of exercise and f after 25 min of exercise were significantly higher than the 10-min values in the exercise trial. In the rest trial, VE, VT, and f were significantly higher after 25 min than at time 0. In the rest trial, PETCO2 was significantly lower at 20–40 min than at time 0; in the exercise trial, PETCO2 gradually declined after 5 min and was significantly different from the 10-min values after 25 min of exercise (Fig. 2D).


Figure 2
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  		Fig. 2. Time-dependent changes in minute ventilation, tidal volume, respiratory frequency, and end-tidal PCO2 (PETCO2) during rest ({blacktriangleup}) and exercise ({circ}) trials. Numbers adjacent to symbols indicate number of subjects remaining. *P < 0.05, rest vs. exercise at the same time point. {dagger}P < 0.05 vs. Pre in rest trial. $P < 0.05 vs. 10 min in exercise trial.

 
Tes-dependent changes in VE, VE/VO2, VE/VCO2, VT, f, and PETCO2.   Ventilatory parameters plotted against Tes from rest to the end of the heating session are shown in Fig. 3. During the exercise trial, VT was increased during the first few minutes of the exercise, with only a small change in Tes. Thereafter, in all subjects, VT steadily and gradually declined, while VE, VE/VO2, VE/VCO2, and f increased linearly, with increases in Tes. In contrast, during the rest trial, 14 of the 19 subjects showed a clear threshold for hyperpnea (Fig. 3A), while the remaining 5 did not (Fig. 4). The average temperature of the threshold was 37.8 ± 0.5°C. To compare the ventilatory responses to the increase in core temperature during the rest and exercise trials, we divided the Tes range into subranges spanning the temperatures below and above the threshold observed in the rest trial (Fig. 3). In each Tes subrange, the slope of the regression lines relating Tes and VE, VE/VO2, VE/VCO2, VT, f, and PETCO2 were evaluated in each subject (Fig. 3), and the average slopes are shown in Table 1. Below the threshold, VE, VE/VO2, VE/VCO2, and f slopes were significantly lower and the PETCO2 slope was significantly higher in the rest than in the exercise trial. Above the threshold, VE, VE/VO2, VE/VCO2, VT, and f slopes were significantly higher and the PETCO2 slope was significantly lower in the rest than in the exercise trial.


Figure 3
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  		Fig. 3. Tes-dependent changes in minute ventilation, ventilatory equivalent for O2 uptake (VE/VO2), ventilatory equivalent for CO2 output (VE/VCO2), tidal volume, respiratory frequency, and PETCO2 during rest and exercise trials in 14 subjects who showed a core temperature threshold for hyperpnea during passively induced hyperthermia. bullet, Averaged threshold in rest trial. Dashed lines, regression lines for respective subranges below and above threshold in both trials.

 

Figure 4
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  		Fig. 4. Tes-dependent changes in minute ventilation in rest ({blacktriangleup}) and exercise ({circ}) trials of 5 subjects who did not show a core temperature threshold for hyperpnea during passively induced hyperthermia.

 

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  		Table 1. Slopes of regression lines calculated after ventilatory parameter was plotted vs. Tes in subjects with a core temperature threshold for hyperpnea in the rest trial

 
Figure 5 shows the VE slopes for the rest (above the threshold) and exercise trials in the 14 subjects who showed a core temperature threshold for hyperpnea. The VE slope was higher for the rest than for the exercise trial in 11 of the 14 subjects (Fig. 5); in the remaining 3 subjects, the slope was slightly higher for the exercise than for the rest trial.


Figure 5
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  		Fig. 5. Minute ventilation (VE) slopes for rest (above threshold) and exercise trials of the 14 subjects who showed a core temperature threshold for hyperpnea during passively induced hyperthermia. bullet, Averaged data.

 
For the five subjects who did not show a threshold, only regression lines across the entire Tes range were evaluated (only VE is shown in Fig. 4); these slope values are shown in Table 2. VE, VE/VO2, VE/VCO2, and f slopes were significantly lower and the PETCO2 slope was significantly higher in the rest than in the exercise trial.


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  		Table 2. Slopes of regression lines calculated after ventilatory parameter was plotted vs. Tes in subjects without a core temperature threshold for hyperpnea in the rest trial

 
VO2, VCO2, and RER.   VO2, VCO2, and RER were measured in all 19 subjects. VO2 and VCO2 increased from time 0 during the rest trial and from the 10-min value during the exercise trial at the times indicated in Fig. 6, A and B. RER increased from time 0 during the rest trial but declined from the 10-min value during the exercise trial at the times indicated in Fig. 6C. In addition, VO2 and VCO2 were significantly higher during the exercise than during the rest trial at the times indicated in Fig. 6, A and B, whereas RER was significantly higher during the rest than during the exercise trial at the times indicated in Fig. 6C.


Figure 6
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  		Fig. 6. Time-dependent changes in O2 uptake, CO2 output, and respiratory exchange ratio during rest ({blacktriangleup}) and exercise ({circ}) trials. Numbers adjacent to symbols indicate number of subjects remaining. *P < 0.05, rest vs. exercise at the same time point. {dagger}P < 0.05 vs. Pre in rest trial. $P < 0.05 vs. 10 min in exercise trial.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Hyperthermic hyperpnea at rest and during submaximal, moderate-intensity exercise.   In the present study, the VE slope at temperatures above the threshold at rest (rest trial, 26.7 l·min–1°·C–1) was significantly greater than that during submaximal, moderate-intensity exercise (exercise trial, 7.9 l·min–1·°C–1). Although, to our knowledge, the ventilatory responses to increases in core temperature during rest and submaximal, moderate-intensity exercise have not been compared in humans, the responses of resting (3) and exercising (14, 23) subjects have been investigated separately. For instance, it was reported that after a certain threshold was reached in resting subjects, VE increased linearly with increases in Tes (slope ~25 l·min–1·°C–1) (3) in the range 38.6–39.0°C. In addition, Hayashi et al. (14) recently reported that when subjects carried out submaximal, moderate-intensity exercise (50% VO2 peak) in the heat, VE increased linearly with increases in Tes (slope ~6.1 l·min–1·°C–1) in the range 37.2–39.0°C. Similarly, Nybo and Nielsen (23) reported that, during submaximal, moderate-intensity exercise (57% VO2 peak) in the heat with a superimposed hyperthermia, VE increased linearly with increases in Tes (slope ~12.5 l·min–1·°C–1) in the range 38.0–40.0°C. Collectively, the results of these earlier studies are consistent with our present findings. Analogous observations were also made in two animal studies (4, 22).

Earlier reports suggest that increases in VE in response to increasing body temperature at rest could be accomplished via increases in VT (3, 29), f (15, 16, 24), or VT and f (1, 2, 9, 17, 18). We found in the present study that, during the rest trial, increases in VE reflected increases in VT and f. During the exercise trial, by contrast, after an initial increase in ventilation due to VT, subsequent increases in ventilation reflected increases in f (Fig. 2, A–C, and Fig. 3, A, D, and E, Table 1). This suggests that, for passively induced hyperthermia, increases in core temperature above the threshold for hyperpnea at rest drive increases in VT and f and that submaximal, moderate-intensity exercise modifies this change as reflected by the finding that only f increases once VT has reached its maximal value. At rest, therefore, larger increases in VE are elicited in response to increases in core temperature.

Core temperature threshold for hyperpnea.   When we compared the relationships between core temperature and ventilation in subjects at rest (rest trial) and during submaximal, moderate-intensity exercise (exercise trial), in 14 of 19 subjects we observed a threshold temperature for hyperpnea in the rest trial. This is similar to findings reported earlier, although the threshold observed in the present study (37.8 ± 0.5°C on average) is lower than those reported earlier. Previously reported threshold temperatures for hyperpnea at rest were 38.1°C (tympanic temperature) (3) and 38.5°C (Tes) (3). In addition, Petersen and Vejby-Christensen (25) reported that, even at rectal temperatures of 38.4–38.7°C, VE was unchanged from the value seen before heating at rest, which suggests that the core temperature threshold for hyperpnea at rest was >38.4–38.7°C. The reason(s) for the variation in the threshold values is unclear, although differences in the experimental setup likely contribute to it. We used hot-water legs-only immersion to the iliac crest and a water-perfusable suit to raise core temperature in the present study. Previously, investigators used exercise at 44°C in an environmental chamber (25) and hot-water (41°C) immersion to the shoulder (3). In addition, it has been suggested that the effects of rapid transients in core temperature, exercise, and environmental conditions on Tes, rectal temperature, tympanic temperature, and temperature at the auditory meatus differ (28), which suggests that differences in the site of core temperature measurement may also have affected apparent temperature thresholds for hyperpnea.

We did not observe a core temperature threshold for the increase in VE in any of the subjects during the exercise trial; instead, VE increased linearly with increasing Tes. Similarly, Nybo and Nielsen (23) reported that VE increased with increases in Tes in the range 38.0–40.0°C during constant-workload exercise (57% VO2 peak) with a superimposed hyperthermia, but they made no reference to the existence of a threshold. Moreover, Hayashi et al. (14) observed a threshold during submaximal, moderate-intensity constant-workload exercise (50% VO2 peak), but in only 2 of 13 subjects. On the contrary, it also has been reported that when Tes exceeded 37.4–37.9°C during incremental exercise, ventilatory equivalents for O2 and CO2 (i.e., VI/VO2 and VI/VCO2, respectively) increased linearly with increasing Tes (27, 34, 35). However, because these studies used increasing workload to increase temperature, the effect of an anaerobic threshold (31) on ventilatory responses cannot be excluded. In addition, although Petersen and Vejby-Christensen (25) suggested that there is a core temperature threshold for increases in VE/VO2 and VE/VCO2 during constant-workload exercise, they did not evaluate that threshold in their study. Even though in the present study we analyzed VI/VO2 and VI/VCO2 data collected from the start to the end of the exercise, as in previous studies in which incremental workload exercise was used (27, 34, 35), we did not detect a Tes threshold for increases in VI/VO2 and VI/VCO2. It thus remains unclear whether there is a core temperature threshold for hyperpnea during submaximal, moderate-intensity constant-workload exercise in humans.

Although core temperature thresholds during rest and submaximal exercise have not been systematically compared in humans, two such studies have been carried out in animals (4, 22). It was reported that the spinal temperature threshold for the increase in Eres (an index of panting response) was 45°C at rest and 39.1–40.1°C during submaximal exercise in two dogs (4). In addition, the hypothalamic temperature threshold for an increase in Eres was 40.18°C at rest and 38.94°C during submaximal exercise in two goats, whereas the abdominal aortic temperature threshold for the increase in Eres was 39.06°C at rest and 38.69°C during submaximal exercise in three goats (22). It is certainly plausible that the core temperature threshold for hyperpnea is also lower during submaximal, moderate-intensity exercise in humans. If the core temperature threshold for hyperpnea in the exercise trial was below the preheating Tes (36.6°C), it would be ≥1.2°C lower than during the rest trial (the temperature of the threshold in the rest trial was 37.8°C). To determine the threshold temperature for hyperpnea during constant-workload, submaximal, moderate-intensity exercise in humans, it may be necessary to reduce core temperature before exercise, for example, by using cold-water immersion (10).

Possible mechanisms and physiological significance of the difference in hyperthermic hyperpnea between rest and submaximal, moderate-intensity exercise.   Our results suggest that, in humans exercising for long periods at submaximal, steady levels, there is an initial increase in ventilation due to VT, after which exercise attenuates hyperthermic hyperpnea (evaluated as VE slope), and this attenuation is mainly due to prevention of an increase in VT. How does exercise modify hyperthermic hyperpnea? One possibility is that, during submaximal, moderate-intensity exercise, maximum VT is achieved at a submaximal exercise intensity. Gallagher et al. (8) reported that, during incremental cycling exercise, ventilation initially increased as a result of increases in VT and f, but at >61.4% maximum VO2, a further increase in ventilation was almost completely due to increases in f, and a plateau in VT was seen. Since the exercise intensity in the present study (50% VO2 peak) was close to that at which VT reaches a plateau (8), a hyperthermia-evoked increase in VT (at 50% VO2 peak) may have been inhibited. In addition, the respiratory pattern in the exercise trial could reflect a smaller decrease in PETCO2 than in the rest trial (Fig. 3). That is, if the increased ventilation is induced only by f, it might lead to a smaller increase in alveolar ventilation than if it was induced by VT and f (as seen in resting conditions). Another possible explanation is related to water conservation. Because of the higher VE, water loss from the respiratory tract during exercise is greater than at rest. As a result, hyperthermic hyperpnea during exercise might be inhibited to protect water balance. Alternatively or in addition, a change in chemoreceptor sensitivity may modify the hyperthermic ventilatory response during exercise. It has been suggested that hyperthermia increases ventilation by augmenting respiratory drive signaled by peripheral and/or central chemoreceptors (33). It also has been suggested that exercise changes peripheral and central chemoreceptor sensitivities, which is reflected in increased hypoxic (21, 32) and hypocapnic (32) ventilatory responses. Taken together, the effect of chemoreceptors on ventilation during hyperthermia may be changed by exercise, and this may contribute to the difference in hyperthermic hyperpnea in humans at rest and during submaximal, moderate-intensity exercise.

Limitations.   Although the range of Tsk (35–37 vs. 35–39°C) and the rate of increase in Tes (2.5 and 3.3°C/h) significantly differed between the rest and exercise trials in the present study, the differences were relatively small and well within the range in the study of Hayashi et al. (14), in which the difference in Tsk (35–39°C) and the rate of increase in Tes (1.9–3.6°C/h) during submaximal, moderate-intensity exercise at 50% VO2 peak (same as the present study) did not affect the VE slopes (l·min–1·°C–1). Although White and Cabanac (35) reported that the rate of increase in core temperature affected hyperthermic hyperpnea, the difference in the rates (3.8 and 6.3°C/h) was much greater than in the present study. In addition, to increase the rate of rise in core temperature, they changed the rate of increase in workload. Consequently, the augmented increase in VE they observed could reflect the increase in workload, and not simply the increase in core temperature.

Five subjects did not show a threshold for hyperpnea in passively induced hyperthermia. The VE slope at rest for these subjects was 0.8 ± 0.7 l·min–1·°C–1, which is considered to be equivalent to the before-threshold value for the other 14 subjects (0.5 ± 0.8 l·min–1·°C –1). We therefore speculate that these five subjects have a threshold for hyperpnea >39.0°C, the temperature at which, for ethical reasons, we stopped heating. To compare the slope of the hyperpnea between rest and submaximal, moderate-intensity exercise, we analyzed the 14 subjects who had a clear threshold in the rest trial. Further studies are needed to describe the mechanisms underlying the large individual differences in the hyperthermic hyperpnea response in humans.

In summary, we compared the relationships between core temperature and ventilatory response in humans at rest and during submaximal, moderate-intensity exercise. Above the threshold for hyperpnea, the slope of the regression line relating VE and Tes was significantly greater in the rest than in the exercise trial. Moreover, the slopes of the regression lines relating VE/VO2, VE/VCO2, and Tes were significantly greater in the rest than in the exercise trial. The slope relating VT and f (respiratory pattern) to the increases in Tes also was significantly greater in the rest than in the exercise trial; thus the increase in VE was accomplished via changes in VT and f in the rest trial, but only f (after an initial increase in ventilation due to VT) in the exercise trial. Our results suggest that hyperthermia-induced increases in ventilation are attenuated by submaximal, moderate-intensity exercise, and this attenuation likely reflects limitations on further increases in VT imposed by an unknown mechanism(s).


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This study was supported by grants from the Center of Excellence projects and Ministry of Education, Science, and Culture of Japan.


   ACKNOWLEDGMENTS
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We sincerely thank the volunteer subjects.


   FOOTNOTES
 

Address for reprint requests and other correspondence: Takeshi Nishiyasu, Institute of Health and Sports Science, Univ. of Tsukuba, Tsukuba City, Ibaraki 305-8574, Japan (e-mail: nisiyasu{at}taiiku.tsukuba.ac.jp)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


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  1. Baker JF, Goode RC, Duffin J. The effect of a rise in body temperature on the central-chemoreflex ventilatory response to carbon dioxide. Eur J Appl Physiol 72: 537–541, 1996.[CrossRef][Web of Science]
  2. Bazett HC. Studies of the effects of baths on man. Am J Physiol 70: 412–429, 1924.[Free Full Text]
  3. Cabanac M, White MD. Core temperature thresholds for hyperpnea during passive hyperthermia in humans. Eur J Appl Physiol 71: 71–76, 1995.[CrossRef][Web of Science]
  4. Clough DP, Jessen C. The role of spinal thermosensitive structures in the respiratory heat loss during exercise. Pflügers Arch 347: 235–248, 1974.[CrossRef][Web of Science][Medline]
  5. Cohen J. Statistical Power Analysis for the Behavioral Sciences (2nd ed.). Hillsdale, NJ: Erlbaum, 1988.
  6. Entin PL, Robertshaw D, Rawson RE. Thermal drive contributes to hyperventilation during exercise in sheep. J Appl Physiol 85: 318–325, 1998.[Abstract/Free Full Text]
  7. Findlay JD, Hales JR. Hypothalamic temperature and the regulation of respiration of the ox exposed to severe heat. J Physiol 203: 651–663, 1969.[Abstract/Free Full Text]
  8. Gallagher CG, Brown E, Younes M. Breathing pattern during maximal exercise and during submaximal exercise with hypercapnia. J Appl Physiol 63: 238–244, 1987.[Abstract/Free Full Text]
  9. Gaudio R Jr, Abramson N. Heat-induced hyperventilation. J Appl Physiol 25: 742–746, 1968.[Free Full Text]
  10. González-Alonso J, Teller C, Andersen S, Jensen FB, Hyldig T, Nielsen B. Influence of body temperature on the development of fatigue during prolonged exercise in the heat. J Appl Physiol 86: 1032–1039, 1999.[Abstract/Free Full Text]
  11. Haldane JS. The influence of high air temperatures. J Hyg 5: 494–513, 1905.
  12. Hales JRS. Changes in respiratory activity and body temperature of the severely heat-stressed ox and sheep. Comp Biochem Physiol 31: 975–985, 1969.[Medline]
  13. Hales JR, Webster ME. Respiratory function during thermal tachypnoea in sheep. J Physiol 190: 241–260, 1967.[Abstract/Free Full Text]
  14. Hayashi K, Honda Y, Ogawa T, Kondo N, Nishiyasu T. Relationship between ventilatory response and body temperature during prolonged submaximal exercise. J Appl Physiol 100: 414–420, 2006.[Abstract/Free Full Text]
  15. Hey EN, Lloyd BB, Cunningham DJC, Jukes MGM, Bolton DPG. Effects of various respiratory stimuli on the depth and frequency of breathing in man. Respir Physiol 1: 193–205, 1966.[CrossRef][Web of Science][Medline]
  16. Hill L, Flack M. The influence of hot baths on pulse frequency, blood pressure, body temperature, breathing volume and alveolar tensions of man. J Physiol 38: 57P–61P, 1909.
  17. Laitinen LA, Lindqvist A, Heino M. Lungs and ventilation in sauna. Ann Clin Res 20: 244–248, 1988.[Web of Science][Medline]
  18. Landis EM, Long WL, Dunn JW, Jackson CL, Meyer U. Studies on the effects of baths on man. Am J Physiol 76: 35–48, 1926.[Free Full Text]
  19. Martin BJ, Morgan EJ, Zwillich CW, Weil JV. Control of breathing during prolonged exercise. J Appl Physiol 50: 27–31, 1981.[Abstract/Free Full Text]
  20. Martin BJ, Morgan EJ, Zwillich CW, Weil JV. Influence of exercise hyperthermia on exercise breathing pattern. J Appl Physiol 47: 1039–1042, 1979.[Abstract/Free Full Text]
  21. Martin BJ, Weil JV, Sparks KE, McCullough RE, Grover RF. Exercise ventilation correlates positively with ventilatory chemoresponsiveness. J Appl Physiol 45: 557–564, 1978.[Abstract/Free Full Text]
  22. Mercer JB, Jessen C. Control of respiratory evaporative heat loss in exercising goats. J Appl Physiol 46: 978–983, 1979.[Abstract/Free Full Text]
  23. Nybo L, Nielsen B. Middle cerebral artery blood velocity is reduced with hyperthermia during prolonged exercise in humans. J Physiol 534: 279–286, 2001.[Abstract/Free Full Text]
  24. Petersen ES, Vejby-Christensen H. Effects of a rise in body temperature on the pattern of breathing in man. J Physiol 250: 40P–41P, 1975.[Medline]
  25. Petersen ES, Vejby-Christensen H. Effect of body temperature on steady state ventilation and metabolism in exercise. Acta Physiol Scand 89: 342–351, 1973.[Web of Science][Medline]
  26. Robertshaw D. Mechanisms for the control of respiratory evaporative heat loss in panting animals. J Appl Physiol 101: 664–668, 2006.[Abstract/Free Full Text]
  27. Sancheti A, White MD. Reproducibility of relationships between human ventilation, its components and oesophageal temperature during incremental exercise. Eur J Appl Physiol 96: 495–504, 2006.[CrossRef][Web of Science][Medline]
  28. Sawka MN, Wenger CB, Pandolf KB. Thermoregulatory responses to acute exercise-heat stress and heat acclimation. In: Handbook of Physiology. Environmental Physiology. Bethesda, MD: Am. Physiol. Soc, 1996, sect. 4, vol. 1, chapt. 9, p. 157–185.
  29. Saxton C. Respiration during heat stress. Aviat Space Environ Med 52: 281–286, 1975.
  30. Taylor WF, Johnson JM, O'Leary D, Park MK. Effect of high local temperature on reflex cutaneous vasodilation. J Appl Physiol 57: 191–196, 1984.[Abstract/Free Full Text]
  31. Wasserman K, Whipp BJ, Casaburi R. Respiratory control during exercise. In: Handbook of Physiology. The Respiratory System. Control of Breathing. Bethesda, MD: Am. Physiol. Soc, 1986, sect. 3, vol. II, pt. 2, chapt. 17, p. 595–619.
  32. Weil JV, Byrne-Quinn E, Sodal IE, Kline JS, McCullough RE, Filley GF. Augmentation of chemosensitivity during mild exercise in normal man. J Appl Physiol 33: 813–819, 1972.[Free Full Text]
  33. White MD. Components and mechanisms of thermal hyperpnea. J Appl Physiol 101: 655–663, 2006.[Abstract/Free Full Text]
  34. White MD, Cabanac M. Core temperature thresholds for ventilation during exercise. Adv Exp Med Biol 393: 173–177, 1995.[Medline]
  35. White MD, Cabanac M. Exercise hyperpnea and hyperthermia in humans. J Appl Physiol 81: 1249–1254, 1996.[Abstract/Free Full Text]



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