PCO2 has been shown to increase with the severity of exercise (Nielsen, 1936).
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1 554 J. Physiol. (I955) I29, THE ROLE OF BODY TEMPERATURE IN CONTROLLING VENTILATION DURING EXERCISE IN ONE NORMAL SUBJECT BREATHING OXYGEN By J. E. COTES From the Pneumoconiosis Research Unit of the Medical Research Council, Llandough Hospital, Penarth, Glamorganshire (Received 16 February 1955) The body temperature rises during exercise (Pembrey & Nicol, 1898) and in proportion to the increase in metabolism (Christensen, 1931). At rest, a rise in body temperature increases pulmonary ventilation and depresses the During exercise the effect of temperature alveolar C2 tension (Haldane, 195). on ventilation has not been studied in detail, but the ventilation at a constant PCO2 has been shown to increase with the severity of exercise (Nielsen, 1936). This finding may be explained in terms of a rise in body temperature (Gray, 195), but there is little direct evidence for the hypothesis (Comroe, 1944; Barltrop, 1954). Recently Bannister, Cunningham & Douglas (1954) have produced indirect evidence to support it. In the present investigation the body temperature has been lowered during exercise and the effect of this procedure upon ventilation observed. One subject only was studied in the time available so that the conclusions to be drawn from the findings are not necessarily generally applicable. METHOD The subject, aged 3, weight 6 kg, height 18 cm, and wearing light clothing, performed moderate stepping exercise. Oxygen was breathed to eliminate any stimulus from hypoxia. The intensity of the exercise was regulated by adjusting the height of the step and the rate of stepping; these were noted so that the same level of exercise could be reproduced on a number of occasions. The replicate variability of ventilation using this method (Hugh-Jones, 1952) in a group of twenty-six untrained subjects at 35 kg. m/min, the highest work level adopted in the present investigation, was ±5-5 % and the oxygen consumption was 1-26, 8.D. ± 7 I./min s.t.p. (Cotes, unpublished). This level of exercise was below the lactic acid threshold for the present subject (cf. Owles, 193). The oxygen consumption for each work level was determined breathing air, using an open circuit method (Haldane & Graham, 1935), and it was assumed that no appreciable change occurred breathing oxygen (Marzahn, Gilbeau & Zaeper, 1936). The experiments started from a quiet resting state with the subject breathing through a mouthpiece and blindfold to reduce visual stimulation. No active participation in the experiment other than stepping was required of the subject, and the results were not analysed until the whole series
2 BODY TEMPERATURE AND EXERCISE 555 had been completed. The rate ofbreathing, ventilation, and the end tidal CO2 tension were recorded each half minute on a 2 cu.ft. gas meter, an end tidal air sampler (Rahn & Otis, 1949) and an infrared gas analyser. The gas meter agreed with a Tissot spirometer to within + 1 %1. Ventilation measurements, averaged over 2 min, were corrected to BTPS. The Rahn-Otis sampler, mouthpiece and valve box together had a deadspace of 36 ml., and the delay from the point of sampling to full-scale deflexion on the analyser meter was 2 sec, of which 8 sec represented the time taken for the sample to reach the analyser cell, whose capacity was -3 ml. The end tidal C2 tensions obtained using this method at tidal volumes exceeding in seven experiments were, on average, -7 mm Hg (range -1-5 mm) less than Haldane samples taken at the end of expiration (cf. Bannister et al. 1954). In order to vary the end tidal CO2 tensions, carbon dioxide was added to the oxygen, the mixture then passing through a humidifier and on to a demand system requiring a suction in the mouthpiece of 1-3 and 2-2 cm H2 at flows of 3 and 1 I./min respectively. The ventilation was measured at rest and at different levels of exercise and body temperature whilst the subject was breathing the mixtures. The rectal temperature was measured at intervals with a clinical thermometer inserted to a depth of cm. All observations were made at least 3 min after the start of the exercise, and it has been assumed that when steady temperature readings were obtained under these conditions they bore a reasonably constant relationship to the temperature of arterial blood (Mead & Bonmarito, 1949; Cranston, Gerbrandy & Snell, 1954). In some experiments the subject was cooled by a spray of cold tap water which flowed off him into a shallow bath. The flow was adjuste(d by trial and error to keep the rectal temperature constant to within.1 C. This procedure was found to be relatively simple and did not cause discomfort or shivering except when the temperature was falling rapidly. RESULTS In each experiment the end tidal pco2 was stabilized at two levels, which straddled 46 mm Hg in most cases (Table 1). The relationship between ventilation, pco2, and rectal temperature at the two stages of each run are shown in Fig. 1. Assuming a linear relationship between ventilation and carbon dioxide tension over the range 4-52 mm Hg at rest (Lambertsen, Kough, Cooper, Emmel, Loeschcke & Schmidt, 1953), and during exercise (Nielsen, 1936), the regression of ventilation on carbon dioxide tension and body temperature, allowing for possible interaction between them, is the following: VE = 4-6 PACo2+ (151-1PACo2) BT-64-9, where VE = ventilation (1./min), PACO2 = end tidal carbon dioxide tension (mm Hg), BT =body temperature ( C). The standard error for the coefficient of the interaction term (.1) is This term does not significantly improve the goodness of fit of the formula to the data, and may be omitted. The regression when recalculated omitting this term then becomes VE = (1P4+.19) PACo2 + ( ) BT The ventilation breathing oxygen can thus be expressed in terms of the additive effects of two independent variables: carbon dioxide tension and body temperature. The regression coefficient of ventilation on pco2 at constant body temperature with its standard error is /min per mm change 36-2
3 556 J. E. COTES in pco2, and is apparently independent of the actual body temperature over the range studied ( C). The regression coefficient of ventilation on body temperature at constant PCO2 is 11 ±+78 1./min per C rise in body temperature and is apparently independent of carbon dioxide tension over the range studied (4-52 mm Hg). This relationship is illustrated in Fig. 2, taking an arbitrary pco2 of 46 mm Hg, and calculating from the average slope of the regression of ventilation on PCO2 what the ventilation at this pco2 would have been in each experiment. TABLE 1. Ventilation, end tidal PCO2 and body temperature at different levels of steady state exercise whilst breathing mixtures of carbon dioxide in oxygen Work level Av. 2 cons. Inspired CO2 Ventilation End tidal Rectal temp. (kg.m/min) ml./min s.t.p. (%) 1./min BTPS PCO2 (mm Hg) (O C) Rest Rest Rest *6 15*5 43* *8 37X * * *6 2* * 29* * *3 48* *4 35* * Rest Rest Rest *2 22*5 48* 37* *4 42* *6 23* * *8 41*6 38* * The rise in body temperature above the resting level is proportional to the increased metabolism. The regression coefficient of body temperature on oxygen consumption is C (95 % confidence limits ) per litre increase in oxygen consumption over the range studied (see Fig. 3). The observed increase in ventilation during exercise may be due to the rise in body temperature, or to metabolism, or to the movements associated with exercise or to some other factor. In the hope of deciding between them, the body temperature was maintained at its resting value by water cooling, whilst the subject exercised breathing oxygen at 35 kg.m/min. In three experiments, in which the rectal temperature remained constant to within.1 C, the ventilation decreased and the pco2 increased when compared with the same exercise without cooling. The averages for the exercise ventilation, PCO2 and body temperature for the three periods of exercise performed with cooling at
4 BODY TEMPERATURE AND EXERCISE 557 this work level were /min, 51-3 mm Hg and 36.8 C; the corresponding values for the six periods without cooling were 28-1 l./min, 42-6 mm Hg and 38.3 C (Table 2). The individual values are shown as dots in Fig. 4 against the regression lines of ventilation on PCO2 at different body temperatures 4 _ , ;,S' r, i ,.* _ ,.-,' -,, r ', ,, ' _ ~~~ -.~ S &I - -_- E 38-33, , 376 * - _, W *c W ',.,' , -,, --,",.'_* J ' I l l I End tidal pco2 (mm Hg) Fig. 1. Ventilation and end tidal pco2 breathing oxygen or CO2 in oxygen at different levels of body temperature obtained by steady state exercise of varying intensity. obtained from the first experiment. It can be seen that the ventilation values during cooling whilst exercising at 35 kg.m/min are close to those which would be anticipated for this subject whilst sitting at rest with the same body temperature, 36.8 C (98.3 F), and breathing a CO2 mixture adjusted to raise his PCO2 to 51 mm Hg.
5 558 J, E. COTES 4o. 3 - / * 1 I v 1 Fig Temperature (OC) Regression of ventilation at an end tidal pco2 of 46 mm Hg on body temperature at rest and during steady state exercise of varying intensity. 39 U 38 u E Qo o 37 Fig Oxygen consumption, mi./min s.t.p. 15 Regression of body temperature on oxygen consumption at rest and during steady state exercise.
6 BODY TEMPERATURE AND EXERCISE 559 Three other experiments with cooling were carried out. In one cooling was inadequate and the body temperature (and ventilation) increased to reach the normal values for the subject. In two the ventilation and pco2 stabilized at the two points marked x in Fig. 4 whilst the rectal temperature was falling over the range C. All the points obtained breathing oxygen appear to lie about a line representing the behaviour of ventilation and PCO2 for constant work at changing body temperatures. The findings suggest that had the body temperature fallen appreciably below the resting value at this work level a dangerous increase in PCO2 might have occurred. TABLE 2. Ventilation, end tidal pc2 and body temperature whilst exercising at 35 kg. m/min breathing oxygen with and without cooling during exercise Exercise ventilation, End tidal Rectal temp. I./min BTPS pco, mm Hg (C) With cooling ' Without cooling 29* *2 38*61 28* * Also included for comparison in Fig. 4 are points obtained whilst exercising at the same work level (35 kg.m/min) breathing 2-5% C2 in oxygen with a mean body temperature of 38.3 C. Under these conditions the expected increase in both ventilation and PCO2 has taken place. DISCUSSION In the present investigation the ventilatory response to C2, /min per mm rise in pco2, is below the mean value found for normal subjects at rest, but is within the normal range (Lambertsen et at. 1953; Prime & Westlake, 1954). The ventilatory response to a rise in body temperature under steady conditions of exercise at constant pco2 has not previously been reported. Nielsen (1936) has described the ventilatory response to C2 at rest and during exercise at 223 and 446 kg.m/min on a bicycle ergometer. The regressions of ventilation on PCO2 at these three levels of activity had the same coefficients (i.e. slope) which is in agreement with the present findings. The change in ventilation at constant PCO2 between rest and the lower level of exercise was greater than that between the two levels of exercise; the body temperature was not recorded. The difference might have been due to the temperature increasing in increments corresponding to the changes in ventilation.
7 56 J. E. COTES The ventilatory response to a rising body temperature at rest has been reported by a number of workers (e.g. Landis, Long, Dunn, Jackson & Meyer, 1926); few reports refer to steady conditions oftemperature, but Barltrop (1954) _ E o 3 A 4, pco2 (mm Hg) Fig. 4. Effect on ventilation and end tidal PCO2 during steady state exercise at 35 kg. m/min whilst breathing oxygen, both of water cooling during exercise, and of adding CO2 to the inspired oxygen. Points superimposed on regressions of ventilation on end tidal pco2 at different body temperatures., Body temperature constant; x, body temperature falling. found that the mean ventilation increased by /min and the mean alveolar CO2 tension fell by 4-8 mm Hg in seven normal subjects when their body temperature was raised 2 C, and Bazett & Haldane (1921) found comparable 6
8 BODY TEMPERATURE AND EXERCISE 561 changes of /min and 8-7 mm Hg when the body temperature rose 18' C under similar conditions. Assuming a mean ventilatory response to carbon dioxide of 2 I./min per mm rise in PC2' this implies an increase in ventilation at constant PCO2 of 6-7 and / C rise in body temperature in the two cases. These values are of the same order as the 111. increase here reported. The rise in body temperature during exercise of 1.9 C/1. increase in oxygen consumption in this one subject is higher than values previously reported; it may be compared with the range 6-1-3' C/1. (Lundgren, 1946), which is representative of published data. The ventilatory response to carbon dioxide at constant body temperature, the rise in body temperature with oxygen consumption, and the increase in ventilation with body temperature at constant pco2 reported in the present investigation are thus reasonably comparable with previous findings. It therefore seems probable that the findings were not grossly disturbed by the physical or psychological stimuli inherent in the design of the experiments. The data suggest that the ventilation whilst performing moderate steady exercise breathing oxygen, can be fully described in terms of the additive effects of C2 tension and body temperature. This interpretation is supported by the three experiments in which the subject's body temperature was prevented from rising above its resting level by water cooling during exercise. The ventilation was similar to that recorded at rest breathing a C2 mixture to produce the same PCO2 as that observed under the modified exercise conditions. The general applicability of this finding requires verification in a random sample of normal subjects. It appears to confirm directly, a part of the additive hypothesis propounded by Gray (195) for the control of ventilation during exercise, and to refute the suggestions both that a sensitization of the respiratory centre to C2 occurs in exercise (Lindhard, 1933) and that the stimuli arising as a result of limb movement (Harrison, Harrison, Calhoun & Marsh, 1932) play a significant part in the control of ventilation during exercise in man (Grodins, 195). SUMMARY 1. The relation between ventilation, carbon dioxide tension and body temperature has been studied in one normal subject performing moderate 'steady state' exercise breathing oxygen. 2. The ventilatory response to carbon dioxide at constant body temperature was /min per mm change in PCO2, and to body temperature at constant P /min per C rise in body temperature. The body temperature increased C (95% confidence limits 1F3-2 4)/1. increase in oxygen consumption.
9 562 J. E. COTES 3. The relationship YE = 144PACO + I 1 OBT described the behaviour of ventilation whilst breathing oxygen or C2 in oxygen at rest, during normal exercise and when the body temperature was lowered by water cooling during exercise. It is concluded that for this subject breathing oxygen, the ventilation is controlled by the additive effects of C2 tension and body temperature, and that moderate exercise only influences the ventilation indirectly via its effect on these two variables. I wish to thank Dr J. C. Gilson for encouragement, advice and the provision of facilities, Mr P. D. Oldham for the statistical analysis of the data, and Mr A. J. Merrick for invaluable technical assistance. I am also imdebted to Dr D. J. C. Cunningham who read the manuscript and to Mr F. Meade who prepared the diagrams. REFERENCES BANISTER, R. G., CuNNiGHAM, D. J. C. & DoUGLAs, C. G. (1954). The carbon dioxide stimulus to breathing in severe exercise. J. Physiol. 125, BARLTROP, D. (1954). The relation between body temperature and respiration. J. Physiol. 124, 19-2P. BAZETT, H. C. & HALDANE, J. B. S. (1921). Some effects of hot baths on man. J. Physiol. 55, 4-5. CHRISTENSEN, E. H. (1931). Beitrage zur Physiologie schwerer korperlicher Arbeit: II Mitteilung. Die K6rpertemperatur wahrend und unmittelbar nach schwerer k6rperlicher Arbeit. Arbeitsphysiologie, 4, COMROE, J. H., Jr, (1944). Hyperpnea of muscular exercise. Physiol. Rev. 24, CRANSTON, W. I., GERBRANDY, J. & SiNELL, E. S. (1954). Oral, rectal and oesophageal temperatures and some factors affecting them in man. J. Physiol. 126, GRAY, J. S. (195). Pulmonary Ventilation and its Physiological Regulation. Springfield, Illinois: Thomas. GRODINS, F. S. (195). Analysis of factors concerned in regulation of breathing in exercise. Phy8iol. Rev. 3, HALDANE, J. S. (195). The influence of high air temperatures. J. Hyg., Camb., 5, HALDANE, J. S. & GRAHAM, J. I. (1935). Methods of Air Analysis. London: Griffin. HARlISON, T. R., HARRISON, W. G., CALHouN, J. A. & MARSH, J. P. (1932). Congestive heart failure. XVII. The mechanism of dyspnea on exertion. Arch. intern. Med. 5, HUGH-JONES, P. (1952). A simple standard exercise test and its use for measuring exertion dyspnoea. Brit. med. J. i, LAMBERTSEN, C. J., KOUGH, R. H., COOPER, D. Y., EMMEL, G. L., LOESCHCKE, H. H. & SCHMIDT, C. F. (1953). A comparison of the relationship of respiratory minute volume to pco2 and ph of arterial and internal jugular blood in normal men during hyperventilation produced by low concentrations of CO2 at 1 atmosphere and by 2 at 3 atmospheres. J. appl. Physiol. 5, LANDIS, E. M., LONG, W. L., DUNN, J. W., JACKSON, C. L. & MEYER, U. (1926). Studies on the effects of baths on man. III. Effects of hot baths on respiration, blood and urine. Amer. J. Physiol. 76, LINDHARD, J. (1933). tber die Erregbarkeit des Atemzentrums bei Muskelarbeit. Arbeitsphysiologie, 7, LUNDGREN, N. P. V. (1946). The physiological effects of time schedule work on lumber-workers. Acta physiol. scand. 13, Suppl. 41, MARzAHN, H., GILBEAU, W. & ZAEPER, G. (1936). Klinische Untersuchungen uber die Funktion von Atmung und Kreislauf bei gesunden und kranken. Z. klin. Med. 129, MEAD, J. & BONMARITO, C. L. (1949). Reliability of rectal temperatures as an index of internal body temperature. J. appl. Physiol. 2,
10 BODY TEMPERATURE AND EXERCISE 563 NIELSEN, M. (1936). Untersuchungen uber die Atemregulation beim Menschen. Phy8iol. 74, Suppl. 1, Skand. Arch. OWLES, W. H. (193). Alterations in the lactic acid content of the blood as a result of light exercise, and associated changes in the C2-combining power of the blood and in the alveolar CO2 pressure. J. Phy8iol. 69, PEMBREY, M. S. & NICOL, B. A. (1898). Observations upon the deep and surface temperature of the human body. J. Physiol. 23, PRIME, F. J. & WESTLAKE, E. K. (1954). The respiratory response to CO2 in emphysema. Clin. Sci. 13, RAHN, H. & OTIS, A. B. (1949). Continuous analysis of alveolar gas composition during work, hyperpnea, hypercapnia and anoxia. J. appl. Phy8iol. 1,
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