The changing thermal response to endurance exercise during pregnancy James F. Clapp III, MD Burlington, Vermont This study was designed to test the hypothesis that the thermal response to endurance exercise is altered by the thermal adaptations to pregnancy. Accordingly, rectal temperature was monitored in 18 recreational athletes before, during, and after 20 minutes of continuous exercise before conception and every 6 to 8 weeks during pregnancy. Mean exercise intensity was 64% of V02 max before conception and did not change during pregnancy. However, the peak rectal temperature reached during exercise decreased by 0.3 0 C at 8 weeks and then fell at a rate of 0.10 C per lunar month through the thirty-seventh week. This appeared to be related to changes in resting temperature, thermal mass, sweating threshold, and venous capacitance that began early in pregnancy. These data suggest that the magnitude of any exercise-associated thermal stress for the embryo and fetus is markedly reduced by the maternal physiologic adaptations to pregnancy. (AM J OBSTET GVNECOL 1991 ;165:1684-9.)
Key words: Exercise, pregnancy, temperature Female recreational runners have been shown to routinely have an increase in rectal temperature to 39° to 39.5° C during exercise, 1.2 and under conditions of high environmental temperature and humidity, the increase exceeds this level at much lower exercise intensities. 3 During pregnancy an increase in maternal rectal temperature to these levels places the embryo and fetus at theoretical teratogenic and metabolic risk! For this and other reasons, sanctioned guidelines recommend that exercise duration be limited to 15 minutes and that pulse rate be kept under 140 during pregnancy.s However, the data currently available suggest that the thermoregulatory adaptations to both regular exercise and pregnancy maintain the level of thermal stress below the level of concern when recreational runners continue to run at higher intensities for more protracted periods of time during pregnancy. I. 6, 7 The current study was undertaken to explore these early observations through serial studies of well-conditioned recreational athletes who maintained a regular exercise regimen of running, aerobics, or cycling throughout pregnancy. It was specifically designed to From the Department of Obstetrics and Gynecology, University of Vermont College of Medicine, Supported in part by National Institutes of Health grant No, Hd21268 and by grant No, 6-464 from the National Foundation March of Dimes and The Harry W. Chandler Memorial Research Fund, Presented in part at the Thirty-seventh Annual Meeting of the Society For Gynecologic Investigation, St, Louis, Missouri, March 21-24, 1990, Reprint requests: James F, Clapp Ill, MD, Department of Reproductive Biology, Case Western University School of Medicine, Room A219, MetroHealth Medical Center, 2295 Scranton Road, Cleveland, OH 44109, 616130569
1684
test the hypothesis that the thermal response to endurance exercise is altered by the thermal adaptations to pregnancy.
Material and methods Subjects. Eighteen well-conditioned recreational athletes were studied during their chosen form of exercise (eight ran, seven performed aerobics, and three cycled) before conception and every 6 to 8 weeks during the subsequent pregnancy. They were between the ages of 27 and 34 years, in excellent health, of upper-middle or upper socioeconomic status, and worked regularly outside the home. All had been exercising regularly (at least three times a week for ~30 minutes) for ~2 years before study, were fit at enrollment as assessed by percent body fat (range, 10% to 19%) and Vo 2 max (range, 47 to 67 mI· kg-I. min-I), and maintained a regular exercise regimen throughout pregnancy. Exercise performance during pregnancy was monitored and averaged 85% ± 8% (range, 68% to 104%) of preconceptional performance. All pregnancies were singleton, clinically normal, and accurately dated. Experimental protocol. On each occasion testing was conducted 1 to 3 hours after eating, the subject wore the same exercise apparel, and body weight was obtained on a balance-beam scale to the nearest 100 gm after voiding. Then measurements of rectal temperature and oxygen consumption were obtained during an initial 10-minute period of quiet standing or sitting (cyclists only) rest and during the 20 minutes of exercise and 10 minutes of recovery that followed. Although absolute workload varied from session to session, during each exercise session the treadmill speed and grade were held constant for the runners, the cyclists biked
Thermal response to endurance exercise in pregnancy
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on a Monark cycle ergometer at a constant pedal frequency and load , and the remainder followed a specially designed constant intensity aerobics routine that was displayed on a video monitor. Environmental conditions were held relatively constant for all tests (dry bulb temperature, 19° to 21 ° C; relative humidity, 30% to 55%; no added air flow). Measurement techniques. Rectal temperature was monitored continuously and recorded each minute throughout the study with a precalibrated YSI thermistor (Yellow Springs Instrument Co., Yellow Springs, Ohio) with a reproducibility of ± 0.02° C that was held in place 13 cm above the anal verge by taping it to a perineal pad. Oxygen consumption was monitored continuously throughout the last 10 minutes of exercise with a respiratory calorimetry system with a reproducibility under test conditions of ± 3%."' 9 The onset of sweating was determined by each individual's subjective sensation of sweating (occurs within 30 seconds of that determined with a resistance hygrometer sweat capsule). Exercise intensity was calculated from the mean oxygen consumption during the last IO minutes of exercise and expressed as a percentage of Vo 2 max, which was determined preconceptionally with a constant speed, progressive grade treadmill protocol."· 9 Statistics. The data were analyzed by means of repeated-measures analysis of variance and linear regression. Significance was set at the 0.01 level.
Results As shown in Fig. 1, exercise intensity did not change significantly from one study to the next, with mean value for the group ranging between 61 % and 64 % of Vo 2 max over the six study periods. However, the respiratory exchange ratio during exercise rose significantly (p < 0.01) from 0.86 ± 0.03 (mean ± SD) be-
fore conception to 0.91 ± 0.03 by the seventh week , representing a 1.5% increase in the caloric equivalent for oxygen. It remai ned near that level for the remainder of the pregnancy. In spite of the evidence of consistent or slightly increased energy expenditure in the exercise sessions during pregnancy, the maximum rectal temperature reached during exercise (Fig. 2) fell 0 .3° C by the seventh week of pregnancy and then continued to decrease linearly at an average rate of 0.1 °C per lunar month . The range of individual R2 s for this decremental change was 0.69 to 0.99 with a mean group R2 of 0.890 ± 0.094. This longitudinal change was significant at the p < 0.0001 level. In addition, beginning early in pregnancy, there was a steady increase in body weight (Fig. 3) that averaged 1.7 kg per lunar month (group R2 = 0.994, weight = 59.8 + 1.75 kg· lunar month - I) and a steady fall in rectal temperature at rest (Fig. 4) that averaged 0 .05° C per lunar month (group R2 = 0.983, temperature = 37 .64° C - 0.05° C' lunar month-I). Both were significant at the p < 0.000 I level. As shown in Fig. 5, the rectal temperature at which sweating began during exercise fell progressively at a rate of 0.08° C per lunar month (R2 = 0.993, temperature = 37.80 - 0.09° C . lunar month-I) and the increase in rectal temperature between rest and the onset of sweating decreased abruptly by the seventh week (0.19° to 0.06° C), as did the temperature difference between rest and the peak temperature during exercise (0.80° to 0.54° C). Again, these changes were highly significant. Finally, before conception rectal temperature consistently began a linear increase during the first 2 minutes of exercise. This disappeared during pregnancy and actually reversed itself for the first few minutes of ex-
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ercise beginning in the eighth week . This became more pronounced with advancing gestation. Thus in the thirty-seventh week rectal temperature fell 0.10 C at the onset of exe rcise and did not return to control levels until minute 8 to 10 of exercise. The overall magnitude of the impact of these factors on the potential for embryonic and fetal thermal stress was assessed by calculating the area under the rectal temperature curve that exceeded 37.6° C during the 20 minutes of exercise and the 10 minutes of recovery and by expressing it in degree' min - I. The area calculated from the d ata obtained before conception was compared with that obtained during the seventh and thirty-first weeks of gestation. Before conception the area was 12.3 degree· min - I, in the seventh week the
value was only 35% (4.3 degree' min - I) of the preconceptional value, and it was 8 % (1.0 degree' min - I) at 31 weeks. Comment
These data su pport the initial h ypothesis and indicate that multiple thermal adaptatioits to pregnancy alter both the magnitude of the thermal response and the peak temperature attained when continuous, moderate- to high-intensity exercise is performed during pregnancy. Furthermore, as all the changes noted appear early in pregnancy and progress , they appear to provide thermal protection for the embryo and fetus. With one exception, these findings are similar to those reported from this la boratory earlie r. I The ex-
Thermal response to endurance exercise in pregnancy
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ception is that the decrease in resting temperature was not observed in the earlier study. The explanation probably lies in the fact that environmental temperature was a bit lower in the current study, which probably enhanced heat loss with a resultant lowering of rectal temperature. Indeed, other data'O suggest that it may have been lowered to the point where it actually may have induced heat generation. It is probable that either the lack of preconceptional values coupled with differences in exercise intensity or environment also explain the discrepancy between the current findings and the data obtained by J o nes et al. 6 in an apparen tly similar small group of women. The data indicate that multiple pregnancy-associated adaptations contributed to the modified thermal response . First, maternal weight gain increased the
quantity of heat necessal-y to raise the body temperature the same amount by 1 % to 1.5% at 7 weeks and by 12% to 14% near term simply because of the thermal inertia created by the increased tissue mass." This increase in thermal inertia was furth er acce ntuated by the pregnancy-associated decrease in rectal temperature at the onset of exercise, discussed in detail below. Second , the progressive fa ll in resting rectal temperature and the more pronounced fall in the rectal temperature at which sweating began suggests that these two thermoregulatory set points decrease progressively with advancin g gestation. Physiologically, these changes are not unusual, as they normally occur nocturnally' " and as p art of the overall thermal acclimation to regular exercise in a hot, humid environment.' Presently the mechanisms underlying these changes are unclear.
1688
Clapp
December 1991 Am J Obstet Gynecol
However, they are felt to represent the normal adaptive response to changes in nonthermoregulatory metabolic heat production and have both central and peripheral components. As pregnancy is associated with an increase in metabolic rate, these changes probably represent a normal physiologic response to increased heat production. In any case, they clearly diminish the impact of any additional heat generation and improve the ability to dissipate heat. Given that basal body temperature during pregnancy remains elevated until the mid second trimester, 13.14 the fall in resting temperature in early pregnancy was a surprise. The discrepancy suggests that the decremental change was obscured in the basal body temperature studies until later in the pregnancy by the thermal insulation inherent in the "basal conditions" described. In the current study the clothing and environmental temperature offered no such insulation and would encourage heat loss, allowing early recognition of the thermal adaptations to the increased heat production of pregnancy. The marked pregnancy-associated increase in skin temperature and blood flow,l 5.,7 coupled with the approximate 3 L increase in minute ventilation, should have improved convective, radiant, conductive, and evaporative avenues of heat loss. Although not measured in this study, the pregnancy-associated increase in distal extremity temperature at rest is reported to exceed 4 C and hand, forearm, and calf blood flows double . All else being equal, this should have improved the efficiency of heat transfer from the body core to the skin and increase convective and radiant heat loss from the extremities by between 12% and 17%.'8 However, as the pregnancy-associated change in mean skin temperature has not been measured and the distal extremities only contribute 15 % to mean skin temperature, it is likely that the overall increase in convective and radiant heat loss from the skin would have been no more than 5% to 7%. The percentage increase in evaporative heat loss from the respiratory tract should have varied inversely with minute ventilation. The pregnancy-associated rise in minute ventilation should have increased respiratory evaporative heat loss between 25% and 40% at rest, but, during exercise at the levels encountered in the current study, it would have increased only 5% to 8%. The impact of these various adaptations on overall heat dissipation at the ambient temperature used in the current study can be approximated using the partitioning of heat loss estimates obtained in nonpregnant individuals. '8 Before pregnancy, assuming a weight of 55 kg, a rise in core temperature of 0.8 C, a power output of 700 W (10 kcallmin) from exercise and an ambient temperature of 19 to 21 C, approximately 15 % (100 W) of the heat generated should be retained 0
0
0
0
to account for the increase in core temperature. Of the remainder, 40% should be lost to the environment by convection (240 W), 5% by radiation (30 W), 5% as respiratory evaporative loss (30 W) , and 50% by the evaporation of sweat (300 W). During the seventh week of pregnancy the thermal adaptation of a fall in resting core temperature (0.1 C) coupled with the increase in weight (3 kg) provided an additional amount of thermal inertia which should have buffered approximately 2% (15 W) of the heat generated before core temperature returned to its preconception resting level. The remaining increase in core temperature (0.44 C) should have stored an additional 9% (63 W) of the heat produced. Thus, at 7 weeks, total maternal heat storage should have decreased by approximately 22%. The increase in skin temperature and skin blood flow should have increased convective heat loss by approximately 5% to 252 Wand radiant heat loss to 32 W. Evaporative loss from the lungs should have increased approximately the same amount (32 W), whereas, in spite of the lower body temperature, evaporative loss by sweating should have increased slightly, to 306 W. This could not have occurred without the observed downward shift in the sweating threshold. By the thirty-first week the overall decrease in resting core temperature of 0.43 0 C, coupled with the initial 0.10 C fall in core temperature and the 14 kg increase in body weight, should have provided an overall increase in thermal inertia, which by itself would buffer approximately 13% (89 W) of the heat generated in elevating core temperature to preconception resting levels. By this time point, the efficiency of convective heat loss should have increased approximately 7% to about 257 W, with the avenues of radiant and respiratory evaporative heat loss continuing to account for approximately 64 W. As maximum core temperature only rose to the value recorded at rest before pregnancy (37.65 0 C%), the remainder of the power generated (290 W) should have been lost as heat through sweat evaporation. Again this was possibly due to an overall downward shift in the sweating threshold, which actually exceeded the shift observed in resting core temperature (0.68 0 vs 0.43 0 C). Finally, the initial fall in rectal temperature at the onset of exercise during pregnancy is puzzling but suggests that an increase in venous capacitance probably occurs early in pregnancy. With this change, additional blood would pool at rest in the periphery and cool down . At the onset of exercise its return to the central circulation would decrease central temperature and effectively buffer the initial heat generated. A similar response has been observed by Hong and Nadel'9 during exercise in the cold. In summary, in fit women who continue a regular exercise program during pregnancy, the adaptations to pregnancy appear to modulate the thermal response 0
0
Volume 165 Number 6, Part 1
Thermal response to endurance exercise in pregnancy
to exercise by several mechanisms, First, a pregnant woman's thermal inertia is increased as a result of pregnancy-associated progressive decrease in resting temperature that is magnified at the onset of exercise by the return of an increased volume of cool blood from the periphery and a progressive increase in body mass. Second, a downward shift in the central thermal threshold for sweating allows evaporative heat loss to proceed at lower core temperatures. Third, the pregnancy-associated increase in skin blood flow and skin temperature enhances heat transfer from the core to the skin and increases the thermal gradient between the individual and her environment, creating a significant increase in heat loss through convection and radiation. Finally, the rise in minute ventilation slightly increases heat loss from the respiratory tract. As a result of these changes, the maximum rectal temperature attained during 20 minutes of sustained exercise that generates approximately 10 kcall min of heat is progressively reduced. In early pregnancy the maximum rise is reduced by >30%, progressing to >70% near term.
5. American College of Obstetricians and Gynecologists. Exercise in pregnancy. Washington: American College of Obstetricians and Gynecologists, 1985; Technical bulletin no 58. 6. Jones RL, Botti ]], Anderson WM, Bennett NL. Thermoregulation during aerobic exercise in pregnancy. Obstet Gynecol 1985;65:340-5. 7. Nadel ER, Pandolf KB, Roberts MF, Stolwijk A]. Mechanisms of thermal acclimation to exercise and heat.] Appl Physiol 1974;37:515-20. 8. Clapp ]F. The effects of maternal exercise on early pregnancy outcome. AM ] OBSTET GYNECOL 1989;161: 1453-7. 9. Clapp ]F. Oxygen consumption during treadmill exercise before, during, and after pregnancy. AM] OBSTET GyNECOL 1989;161:1458-64. 10. Clapp ]F, Seaward BL, Sleamaker RH, Hiser]. Maternal physiologic adaptations to early human pregnancy. AM] OBSTET GYNECOL 1988;159:1456-60. 11. Kleiber M. The fire of life. Huntington, West Virginia: Krieger Publishing, 1975. 12. Wenger CB, Roberts MF, Stolwijk ]A], Nadel ER. Nocturnal lowering of thresholds for sweating and vasodilation.] Appl Physiol 1976;41:15-9. 13. Benjamin F. Basal body temperature recordings in gynaecology and obstetrics. ] Obstet Gynaecol Br Emp 1960;67:177-92. 14. Stewart HL. Oral basal temperatures and diagnosis of pregnancy. West] Surg Gynecol Obstet 1949;57: 192-200. 15. Burt C. Peripheral skin temperature in normal pregnancy. Lancet 1949;2:787-90. 16. Herbert CM, Banner EA, Wakim KG. Variations in the peripheral circulation during pregnancy. AM ] OBSTET GYNECOL 1958;76:742-5. 17. Katz M, Sokal MM. Skin perfusion in pregnancy. AM ] OBSTET GYNECOL 1980;137:30-3. 18. Mitchell]W. Energy exchanges during exercise. In: Nadel ER, ed. Problems with temperature regulation during exercise. New York: Academic Press, 1977: 11-26. 19. Hong SI, Nadel ER. Thermogenic control during exercise in cold environment.] Appl PhysioI1979;47:1084-9.
REFERENCES 1. Clapp ]F, Wesley M, Sleamaker RH. Thermoregulatory and metabolic responses to jogging prior to and during pregnancy. Med Sci Sports Exerc 1987;19:124-30. 2. Rozycki T]. Oral and rectal temperatures in runners. Phys Sportsmed 1984;12:105-8. 3. Palone AM, Wells CH, Kelly GT. Sexual variations in thermoregulation during heat stress. Aviat Space Environ Med 1978;49:715-9. 4. Clapp ]F. Pregnancy. In: Franklin BA, Gordon S, Timmis GC, eds. Exercise in modern medicine. Baltimore: Williams & Wilkins, 1989:268-79.
1689
Key words: Exercise, pregnancy, temperature Female recreational runners have been shown to routinely have an increase in rectal temperature to 39° to 39.5° C during exercise, 1.2 and under conditions of high environmental temperature and humidity, the increase exceeds this level at much lower exercise intensities. 3 During pregnancy an increase in maternal rectal temperature to these levels places the embryo and fetus at theoretical teratogenic and metabolic risk! For this and other reasons, sanctioned guidelines recommend that exercise duration be limited to 15 minutes and that pulse rate be kept under 140 during pregnancy.s However, the data currently available suggest that the thermoregulatory adaptations to both regular exercise and pregnancy maintain the level of thermal stress below the level of concern when recreational runners continue to run at higher intensities for more protracted periods of time during pregnancy. I. 6, 7 The current study was undertaken to explore these early observations through serial studies of well-conditioned recreational athletes who maintained a regular exercise regimen of running, aerobics, or cycling throughout pregnancy. It was specifically designed to From the Department of Obstetrics and Gynecology, University of Vermont College of Medicine, Supported in part by National Institutes of Health grant No, Hd21268 and by grant No, 6-464 from the National Foundation March of Dimes and The Harry W. Chandler Memorial Research Fund, Presented in part at the Thirty-seventh Annual Meeting of the Society For Gynecologic Investigation, St, Louis, Missouri, March 21-24, 1990, Reprint requests: James F, Clapp Ill, MD, Department of Reproductive Biology, Case Western University School of Medicine, Room A219, MetroHealth Medical Center, 2295 Scranton Road, Cleveland, OH 44109, 616130569
1684
test the hypothesis that the thermal response to endurance exercise is altered by the thermal adaptations to pregnancy.
Material and methods Subjects. Eighteen well-conditioned recreational athletes were studied during their chosen form of exercise (eight ran, seven performed aerobics, and three cycled) before conception and every 6 to 8 weeks during the subsequent pregnancy. They were between the ages of 27 and 34 years, in excellent health, of upper-middle or upper socioeconomic status, and worked regularly outside the home. All had been exercising regularly (at least three times a week for ~30 minutes) for ~2 years before study, were fit at enrollment as assessed by percent body fat (range, 10% to 19%) and Vo 2 max (range, 47 to 67 mI· kg-I. min-I), and maintained a regular exercise regimen throughout pregnancy. Exercise performance during pregnancy was monitored and averaged 85% ± 8% (range, 68% to 104%) of preconceptional performance. All pregnancies were singleton, clinically normal, and accurately dated. Experimental protocol. On each occasion testing was conducted 1 to 3 hours after eating, the subject wore the same exercise apparel, and body weight was obtained on a balance-beam scale to the nearest 100 gm after voiding. Then measurements of rectal temperature and oxygen consumption were obtained during an initial 10-minute period of quiet standing or sitting (cyclists only) rest and during the 20 minutes of exercise and 10 minutes of recovery that followed. Although absolute workload varied from session to session, during each exercise session the treadmill speed and grade were held constant for the runners, the cyclists biked
Thermal response to endurance exercise in pregnancy
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on a Monark cycle ergometer at a constant pedal frequency and load , and the remainder followed a specially designed constant intensity aerobics routine that was displayed on a video monitor. Environmental conditions were held relatively constant for all tests (dry bulb temperature, 19° to 21 ° C; relative humidity, 30% to 55%; no added air flow). Measurement techniques. Rectal temperature was monitored continuously and recorded each minute throughout the study with a precalibrated YSI thermistor (Yellow Springs Instrument Co., Yellow Springs, Ohio) with a reproducibility of ± 0.02° C that was held in place 13 cm above the anal verge by taping it to a perineal pad. Oxygen consumption was monitored continuously throughout the last 10 minutes of exercise with a respiratory calorimetry system with a reproducibility under test conditions of ± 3%."' 9 The onset of sweating was determined by each individual's subjective sensation of sweating (occurs within 30 seconds of that determined with a resistance hygrometer sweat capsule). Exercise intensity was calculated from the mean oxygen consumption during the last IO minutes of exercise and expressed as a percentage of Vo 2 max, which was determined preconceptionally with a constant speed, progressive grade treadmill protocol."· 9 Statistics. The data were analyzed by means of repeated-measures analysis of variance and linear regression. Significance was set at the 0.01 level.
Results As shown in Fig. 1, exercise intensity did not change significantly from one study to the next, with mean value for the group ranging between 61 % and 64 % of Vo 2 max over the six study periods. However, the respiratory exchange ratio during exercise rose significantly (p < 0.01) from 0.86 ± 0.03 (mean ± SD) be-
fore conception to 0.91 ± 0.03 by the seventh week , representing a 1.5% increase in the caloric equivalent for oxygen. It remai ned near that level for the remainder of the pregnancy. In spite of the evidence of consistent or slightly increased energy expenditure in the exercise sessions during pregnancy, the maximum rectal temperature reached during exercise (Fig. 2) fell 0 .3° C by the seventh week of pregnancy and then continued to decrease linearly at an average rate of 0.1 °C per lunar month . The range of individual R2 s for this decremental change was 0.69 to 0.99 with a mean group R2 of 0.890 ± 0.094. This longitudinal change was significant at the p < 0.0001 level. In addition, beginning early in pregnancy, there was a steady increase in body weight (Fig. 3) that averaged 1.7 kg per lunar month (group R2 = 0.994, weight = 59.8 + 1.75 kg· lunar month - I) and a steady fall in rectal temperature at rest (Fig. 4) that averaged 0 .05° C per lunar month (group R2 = 0.983, temperature = 37 .64° C - 0.05° C' lunar month-I). Both were significant at the p < 0.000 I level. As shown in Fig. 5, the rectal temperature at which sweating began during exercise fell progressively at a rate of 0.08° C per lunar month (R2 = 0.993, temperature = 37.80 - 0.09° C . lunar month-I) and the increase in rectal temperature between rest and the onset of sweating decreased abruptly by the seventh week (0.19° to 0.06° C), as did the temperature difference between rest and the peak temperature during exercise (0.80° to 0.54° C). Again, these changes were highly significant. Finally, before conception rectal temperature consistently began a linear increase during the first 2 minutes of exercise. This disappeared during pregnancy and actually reversed itself for the first few minutes of ex-
1686 Clapp
December 1991
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ercise beginning in the eighth week . This became more pronounced with advancing gestation. Thus in the thirty-seventh week rectal temperature fell 0.10 C at the onset of exe rcise and did not return to control levels until minute 8 to 10 of exercise. The overall magnitude of the impact of these factors on the potential for embryonic and fetal thermal stress was assessed by calculating the area under the rectal temperature curve that exceeded 37.6° C during the 20 minutes of exercise and the 10 minutes of recovery and by expressing it in degree' min - I. The area calculated from the d ata obtained before conception was compared with that obtained during the seventh and thirty-first weeks of gestation. Before conception the area was 12.3 degree· min - I, in the seventh week the
value was only 35% (4.3 degree' min - I) of the preconceptional value, and it was 8 % (1.0 degree' min - I) at 31 weeks. Comment
These data su pport the initial h ypothesis and indicate that multiple thermal adaptatioits to pregnancy alter both the magnitude of the thermal response and the peak temperature attained when continuous, moderate- to high-intensity exercise is performed during pregnancy. Furthermore, as all the changes noted appear early in pregnancy and progress , they appear to provide thermal protection for the embryo and fetus. With one exception, these findings are similar to those reported from this la boratory earlie r. I The ex-
Thermal response to endurance exercise in pregnancy
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23
31
•1 T
37
AGE (wks)
Fig. 5. Rectal temperature at which subjective onset of sweating occurred before and during pregnancy. Data are presented as mean ± SEM . PTP, Before pregnancy.
ception is that the decrease in resting temperature was not observed in the earlier study. The explanation probably lies in the fact that environmental temperature was a bit lower in the current study, which probably enhanced heat loss with a resultant lowering of rectal temperature. Indeed, other data'O suggest that it may have been lowered to the point where it actually may have induced heat generation. It is probable that either the lack of preconceptional values coupled with differences in exercise intensity or environment also explain the discrepancy between the current findings and the data obtained by J o nes et al. 6 in an apparen tly similar small group of women. The data indicate that multiple pregnancy-associated adaptations contributed to the modified thermal response . First, maternal weight gain increased the
quantity of heat necessal-y to raise the body temperature the same amount by 1 % to 1.5% at 7 weeks and by 12% to 14% near term simply because of the thermal inertia created by the increased tissue mass." This increase in thermal inertia was furth er acce ntuated by the pregnancy-associated decrease in rectal temperature at the onset of exercise, discussed in detail below. Second , the progressive fa ll in resting rectal temperature and the more pronounced fall in the rectal temperature at which sweating began suggests that these two thermoregulatory set points decrease progressively with advancin g gestation. Physiologically, these changes are not unusual, as they normally occur nocturnally' " and as p art of the overall thermal acclimation to regular exercise in a hot, humid environment.' Presently the mechanisms underlying these changes are unclear.
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However, they are felt to represent the normal adaptive response to changes in nonthermoregulatory metabolic heat production and have both central and peripheral components. As pregnancy is associated with an increase in metabolic rate, these changes probably represent a normal physiologic response to increased heat production. In any case, they clearly diminish the impact of any additional heat generation and improve the ability to dissipate heat. Given that basal body temperature during pregnancy remains elevated until the mid second trimester, 13.14 the fall in resting temperature in early pregnancy was a surprise. The discrepancy suggests that the decremental change was obscured in the basal body temperature studies until later in the pregnancy by the thermal insulation inherent in the "basal conditions" described. In the current study the clothing and environmental temperature offered no such insulation and would encourage heat loss, allowing early recognition of the thermal adaptations to the increased heat production of pregnancy. The marked pregnancy-associated increase in skin temperature and blood flow,l 5.,7 coupled with the approximate 3 L increase in minute ventilation, should have improved convective, radiant, conductive, and evaporative avenues of heat loss. Although not measured in this study, the pregnancy-associated increase in distal extremity temperature at rest is reported to exceed 4 C and hand, forearm, and calf blood flows double . All else being equal, this should have improved the efficiency of heat transfer from the body core to the skin and increase convective and radiant heat loss from the extremities by between 12% and 17%.'8 However, as the pregnancy-associated change in mean skin temperature has not been measured and the distal extremities only contribute 15 % to mean skin temperature, it is likely that the overall increase in convective and radiant heat loss from the skin would have been no more than 5% to 7%. The percentage increase in evaporative heat loss from the respiratory tract should have varied inversely with minute ventilation. The pregnancy-associated rise in minute ventilation should have increased respiratory evaporative heat loss between 25% and 40% at rest, but, during exercise at the levels encountered in the current study, it would have increased only 5% to 8%. The impact of these various adaptations on overall heat dissipation at the ambient temperature used in the current study can be approximated using the partitioning of heat loss estimates obtained in nonpregnant individuals. '8 Before pregnancy, assuming a weight of 55 kg, a rise in core temperature of 0.8 C, a power output of 700 W (10 kcallmin) from exercise and an ambient temperature of 19 to 21 C, approximately 15 % (100 W) of the heat generated should be retained 0
0
0
0
to account for the increase in core temperature. Of the remainder, 40% should be lost to the environment by convection (240 W), 5% by radiation (30 W), 5% as respiratory evaporative loss (30 W) , and 50% by the evaporation of sweat (300 W). During the seventh week of pregnancy the thermal adaptation of a fall in resting core temperature (0.1 C) coupled with the increase in weight (3 kg) provided an additional amount of thermal inertia which should have buffered approximately 2% (15 W) of the heat generated before core temperature returned to its preconception resting level. The remaining increase in core temperature (0.44 C) should have stored an additional 9% (63 W) of the heat produced. Thus, at 7 weeks, total maternal heat storage should have decreased by approximately 22%. The increase in skin temperature and skin blood flow should have increased convective heat loss by approximately 5% to 252 Wand radiant heat loss to 32 W. Evaporative loss from the lungs should have increased approximately the same amount (32 W), whereas, in spite of the lower body temperature, evaporative loss by sweating should have increased slightly, to 306 W. This could not have occurred without the observed downward shift in the sweating threshold. By the thirty-first week the overall decrease in resting core temperature of 0.43 0 C, coupled with the initial 0.10 C fall in core temperature and the 14 kg increase in body weight, should have provided an overall increase in thermal inertia, which by itself would buffer approximately 13% (89 W) of the heat generated in elevating core temperature to preconception resting levels. By this time point, the efficiency of convective heat loss should have increased approximately 7% to about 257 W, with the avenues of radiant and respiratory evaporative heat loss continuing to account for approximately 64 W. As maximum core temperature only rose to the value recorded at rest before pregnancy (37.65 0 C%), the remainder of the power generated (290 W) should have been lost as heat through sweat evaporation. Again this was possibly due to an overall downward shift in the sweating threshold, which actually exceeded the shift observed in resting core temperature (0.68 0 vs 0.43 0 C). Finally, the initial fall in rectal temperature at the onset of exercise during pregnancy is puzzling but suggests that an increase in venous capacitance probably occurs early in pregnancy. With this change, additional blood would pool at rest in the periphery and cool down . At the onset of exercise its return to the central circulation would decrease central temperature and effectively buffer the initial heat generated. A similar response has been observed by Hong and Nadel'9 during exercise in the cold. In summary, in fit women who continue a regular exercise program during pregnancy, the adaptations to pregnancy appear to modulate the thermal response 0
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Volume 165 Number 6, Part 1
Thermal response to endurance exercise in pregnancy
to exercise by several mechanisms, First, a pregnant woman's thermal inertia is increased as a result of pregnancy-associated progressive decrease in resting temperature that is magnified at the onset of exercise by the return of an increased volume of cool blood from the periphery and a progressive increase in body mass. Second, a downward shift in the central thermal threshold for sweating allows evaporative heat loss to proceed at lower core temperatures. Third, the pregnancy-associated increase in skin blood flow and skin temperature enhances heat transfer from the core to the skin and increases the thermal gradient between the individual and her environment, creating a significant increase in heat loss through convection and radiation. Finally, the rise in minute ventilation slightly increases heat loss from the respiratory tract. As a result of these changes, the maximum rectal temperature attained during 20 minutes of sustained exercise that generates approximately 10 kcall min of heat is progressively reduced. In early pregnancy the maximum rise is reduced by >30%, progressing to >70% near term.
5. American College of Obstetricians and Gynecologists. Exercise in pregnancy. Washington: American College of Obstetricians and Gynecologists, 1985; Technical bulletin no 58. 6. Jones RL, Botti ]], Anderson WM, Bennett NL. Thermoregulation during aerobic exercise in pregnancy. Obstet Gynecol 1985;65:340-5. 7. Nadel ER, Pandolf KB, Roberts MF, Stolwijk A]. Mechanisms of thermal acclimation to exercise and heat.] Appl Physiol 1974;37:515-20. 8. Clapp ]F. The effects of maternal exercise on early pregnancy outcome. AM ] OBSTET GYNECOL 1989;161: 1453-7. 9. Clapp ]F. Oxygen consumption during treadmill exercise before, during, and after pregnancy. AM] OBSTET GyNECOL 1989;161:1458-64. 10. Clapp ]F, Seaward BL, Sleamaker RH, Hiser]. Maternal physiologic adaptations to early human pregnancy. AM] OBSTET GYNECOL 1988;159:1456-60. 11. Kleiber M. The fire of life. Huntington, West Virginia: Krieger Publishing, 1975. 12. Wenger CB, Roberts MF, Stolwijk ]A], Nadel ER. Nocturnal lowering of thresholds for sweating and vasodilation.] Appl Physiol 1976;41:15-9. 13. Benjamin F. Basal body temperature recordings in gynaecology and obstetrics. ] Obstet Gynaecol Br Emp 1960;67:177-92. 14. Stewart HL. Oral basal temperatures and diagnosis of pregnancy. West] Surg Gynecol Obstet 1949;57: 192-200. 15. Burt C. Peripheral skin temperature in normal pregnancy. Lancet 1949;2:787-90. 16. Herbert CM, Banner EA, Wakim KG. Variations in the peripheral circulation during pregnancy. AM ] OBSTET GYNECOL 1958;76:742-5. 17. Katz M, Sokal MM. Skin perfusion in pregnancy. AM ] OBSTET GYNECOL 1980;137:30-3. 18. Mitchell]W. Energy exchanges during exercise. In: Nadel ER, ed. Problems with temperature regulation during exercise. New York: Academic Press, 1977: 11-26. 19. Hong SI, Nadel ER. Thermogenic control during exercise in cold environment.] Appl PhysioI1979;47:1084-9.
REFERENCES 1. Clapp ]F, Wesley M, Sleamaker RH. Thermoregulatory and metabolic responses to jogging prior to and during pregnancy. Med Sci Sports Exerc 1987;19:124-30. 2. Rozycki T]. Oral and rectal temperatures in runners. Phys Sportsmed 1984;12:105-8. 3. Palone AM, Wells CH, Kelly GT. Sexual variations in thermoregulation during heat stress. Aviat Space Environ Med 1978;49:715-9. 4. Clapp ]F. Pregnancy. In: Franklin BA, Gordon S, Timmis GC, eds. Exercise in modern medicine. Baltimore: Williams & Wilkins, 1989:268-79.
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