Heat loss responses in rats acclimated to heat loaded intermittently OSAMU SHIDO AND TETSUO NAGASAKA Department of Physiology, School of Medicine, Kanazawa University, SHIDO, OSAMU, AND TETSUO NAGASAKA. He& 10~s responses in ruts acclimated to heat loaded intermittently. J. Appl. Physiol.

68(l): 66-70, 1990.-The present study examined the heat loss responseof heat-acclimatedrats to direct body heating with an intraperitoneal heater or to indirect warming by elevating the ambient temperature (T,). The heat acclimation of the rats was attained through exposure to T, of 33 or 36°C for 5 h daily during 15 consecutive days. Control rats were kept at T, of 24°C for the sameacclimation period. Heat acclimation lowered the body core temperature at T, of 24”C, and the core temperature level was lowered as acclimation temperature increased. When heat was applied by direct body heating, the threshold hypothalamic temperature (Thy) for the tail skin vasodilation wasalsolower in heat-acclimatedrats than in the control rats. However, the amount of increasein Thy from the resting level to the threshold wasthe samein all three groups. When heat was applied by indirect warming, threshold Thy was slightly higher in heat-acclimatedthan in control rats. The amount of increase in Thy from the resting level to the threshold was significantly greater in heat-acclimated rats. In addition, T, and the skin temperature at the onset of skin vasodilation were significantly higher in heat-acclimated rats. The results indicate that heat-acclimatedrats werelesssensitiveto the increase in skin temperature in terms of threshold Thy. The gain constant of nonevaporative heat loss responsewas assessedby plotting total thermal conductanceagainstThy. When heat was appliedby direct body heating, the regressionlines showingthe relationship betweenthermal conductanceand Thyweresteeper in the heat-acclimated than in the control rats. Furthermore the maximal level of thermal conductancewas greater in heatacclimated rats. When heat was applied by indirect warming, however, there was no difference in the slopesbetween the heat-acclimated and control rats. Although heat acclimation improved the capacity of nonevaporative heat dissipation, the rats acclimated to daily intermittent heat exposureswere less sensitivein heat lossresponseto the rise in environmental and skin temperaturesthan nonacclimatedsubjects. direct and indirect calorimetry; nonevaporative heat loss;thermal conductance;threshold temperature

ACCLIMATION shifts the thermoneutral zone and set point in temperature regulation (5, 8, 9, 14), and it facilitates heat loss response to acute heat stress in animals and humans (2, 6, 10, 11, 19). In our previous study, nonevaporative heat loss (R + C + K) response to a rise in ambient temperature (TB) was enhanced in rats acclimated to continuous heat exposure (17). However, this augmented heat loss response was not observed when the core temperature was raised directly through a heater implanted in the peritoneal cavity of rats. Direct body

HEAT

66

016L7567/90

$1.50

Copyright

Kunazawa 920, Japan

heating quickly raises the body core temperature at a constant Ta. When the body temperature is indirectly raised, however, the initial changes are in T, and skin temperature. These results suggest that heat-acclimated rats have a more sensitive heat loss response to the rise in environmental temperature than nonacclimated subjects. Differences in thermal history also affect physiological adaptation in animals (1). Our recent study has shown that acclimation to continuous heat exposure increases the diurnal body temperatures of rats during and after a heat exposure period whereas acclimation to daily intermittent heat exposures lowers body temperature (18). In the present study, therefore, we examined the thermoregulatory responses to two kinds of acute heat exposures and attempted to determine how different methods of heat acclimation affect the nonevaporative heat loss mechanism in rats. METHODS

AnimaZs and preparations. Male Wistar rats (Std: Wistar/ST), initially weighing 280-290 g, were used. A 22gauge stainless steel cannula was stereotaxically implanted into the median preoptic-anterior hypothalamus under pentobarbital sodium anesthesia (50 mg* kg-’ ip). After surgery, they were transferred and maintained for 2 days in an animal room with T, of 24.0 t 0.4*C. Then they were divided into three groups: the control (C,> group was kept at T, of 24.O”C throughout the experiment and the heat-acclimated groups were intermittently exposed to T, of 33.0°C (HI) or 36.0°C (Hg). In the H1 and H2 groups, the room temperature was quickly raised from 24.0°C to respective T, at 0900 h and maintained, then lowered to 24.O”C at 1400 h. This intermittent heat exposure was made every day for at least 15 consecutive days. Rats were housed in individual cages and were provided laboratory rat chow and tap water ad libitum with a 12:12-h light-dark cycle (lights on at 0600 h). During this acclimation period, each rat was loosely restrained in a cylindrical wire cage for 4 h almost every day. Two days before the experiments, a laparotomy was performed under pentobarbital anesthesia (50 mg kg-’ ip) with a l&cm median incision for inserting an intraperitoneal electric heater (IPEH) into the peritoneal cavity. A copper-constantan thermocouple (0.1 mm) was inserted into the hypothalamic cannula and fixed to the cannula with dental cement. Lead wires were passed subcutaneously and exteriorized at the nape. In addition,

0 1990 the American

l

Physiological

Society

Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on December 25, 2018.

ACCLIMATION

TO INTERMITTENT

HEAT

EXPOSURE

67

content. Metabolic heat production (1M) was calculated from O2 consumption and the caloric equivalent for 02 (4.823 kcal 1-l). Hypothalamic temperature (Thy), coionic temperature, and tail skin temperature (T& were continuously monitored on a potentiometer. Heart rate (HR) was counted every minute from ECG recordings. The temperature of the wall (Tw&, the jacket water, and the outlet air from the calorimeter were also monitored by thermocouples. All parameters except those for HR were sampled every minute through an analog-to-digital converter (ADC-12IB, Kanazawa Control Kiki, Kanazawa) connected to a personal computer (PC-98OlVX, NEC, Tokyo). Heat loads. After a 2-h control period at 24”C, the rats were subjected to acute heat stress by heating IPEH implanted in the peritoneal cavity [internal heating (IH)] or increasing T, [external warming (EW) 1. IPEH was made of a closely coiled insulated constantan wire (1.5 m, 23 Q) covered with a polyethylene tube (35 cm long, 1.5 mm 00). The rats received a heat load of 6.5 We kg-l, which was based on our previous data (16), for 30 min through an IPEH. EW was performed by raising the jacket water temperature surrounding the calorimeter chamber. Water temperature was continuously raised for 80 min at a constant rate of O.lS°C l rein? The details of (R + C + K) estimation during EW have been described elsewhere (17). After the experiment, the body was checked for saliva and urine and those rats with wet skin surfaces were discarded from the results. Rats were tested for both kinds of heat stress on separate days. Data analysis and statistics. As T, was raised in EW, T,k rose gradually for a while and then sharply, making a bend on the T,k curve. At the time of the bend, Thy was determined by someone who did not know the purpose of the study. Total thermal conductance was calculated as (R + c + K)/(Th, - T,d. Resting values were established as the means of 5-min data before heat loading at a T, of 24’C. A linear regression line showing the relationship between the total thermal conductance and Thy from the onset of the tail skin vasodilation was obtained by the method of least squares from the mean values of successful measurements. The results are presented as means t SE and statistical evaluations were assessed by one-way analysis of variance (ANOVA) and Scheffe’s multiple comparison test. The statistical significance of the difference between l

o-

Cn

H2

1. Resting (closed bars) and threshold (open bars) hypothalamic temperatures (Thy) of 3 groups of rats: C,, control rats; HI, rats acclimated to 33°C by intermittent exposures; Ha, rats acclimated to 36°C by intermittent exposures. IH, intraperitoneal heating; EW, external warming. Values are means ,t SE. * Difference bet.ween resting and threshold Thy was significant among groups. FIG.

four copper electrodes for electrocardiogram (ECG) recordings were sutured on the chest. At the termination of the experiments, the rats were killed with a large dose of anesthetics and the location of the hypothalamic cannula was checked. Measurements. Each rat was loosely restrained in a cylindrical wire cage the same size as the cage used during the acclimation period. One thermocouple covered with a polyethylene tube was inserted 6 cm into the colon and fixed with surgical tape wrapped around the tail. Another thermocouple was placed longitudinally along the middle of the tail and held in place by one turn of the tape, which covered the thermocouple junction. The rat in the cage was then transferred into a gradient layer direct calorimeter (12). An acrylic pan filled with vegetable oil was set under the cage to collect the rats’ wastes to prevent unwarranted evaporation. The calorimeter wall temperature (T,,n) was initially set at 24°C with an accuracy of t0.02”C. Fresh dry air was introduced into the calorimeter chamber at a constant rate of 2.0 1. min. (R + C + K) was measured by the calorimeter, and evaporative heat loss (E) was calculated from the flow and humidity of the air monitored with a humidity sensor (MHI-11, Vaisala, Helsinki). A fraction of air (100 ml min-‘) withdrawn from the calorimeter chamber was sent into a zirconia 02 analyzer (LC700E, Toray, Tokyo), and O2 consumption was calculated from measurements of O2 l

I

..

.

..

EW FIG. 2. Changes in tail skin temperature (T& during IH and EW from 30 to 80 min after onset of EW in C,, Hr, and Hz rats. Values are means. SEs are not shown to simplify the figure. * Significantly different between C, and Hg rats; * significantly different between C, and H1 rats and between C, and Hz rats.

..

40

$0 Time

sb

io

a0

(mid

Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on December 25, 2018.

68

ACCLIMATION

regression coefficients was performed was considered significant.

TO INTERMITTENT

by F test. P < 0.05

RESULTS

Figure 1 shows Thy measured before (resting Thy) and at the time when TBk rose sharply (threshold Thy) after acute heating in all three groups of rats. Resting and threshold Thy of H1 and H2 rats became lower than that of C, rats. Values for other parameters [Tsk, E, (R + C + K), metabolic heat production (A4) and HR] at T, of 24°C did not differ among the groups. When warmed by EW, the threshold Thy for each group was nearly the same. In the latter experiment, tail skin vessels started to dilate at 60.6 t 2.0, 72.6 $- 2.1, and 73.8 t 2.4 min after the onset of warming (corresponding Tsk were 30.80 t 0.55, 32.28 t 0.49, 33.26 + 0.48"C) in C,, HI, and H2 rats, respectively (Fig. 2). This significantly slower response of tail skin vasodilation appeared to contribute to the significantly greater difference between threshold Thv and resting Thy in Hl and H2 rats. Figure 3 shows changes in T hy and total thermal conductance after the rats were subjected to IH or EW. After the start of IH, Thy rose rather sharply for the first several minutes, and then the rise of the temperature was retarded as tail skin vasodilation occurred. For the last 12 min of IH heating, Thy in H2 rats became significantly lower than in the control rats. EW significantly increased Thy and total thermal conductance. Thy was lower in HI and HZ rats than in the control rats, but the difference between the groups was not statistically significant. The total thermal conductance increased earlier in the control than in the other two groups. Figure 4 summarizes the relationship between total thermal conductance and Thy after tail skin vasodilation that occurred in IH and EW experiments. When body heating was made by IH, the slope of the regression line showing the relationship between the total thermal conductance and Thy was steeper in the heat-acclimated

HEAT

EXPOSURE

than in the control rats. Estimated values for the slope were 1.691,5.086, and 3.405 W l rnD2. “C-l for C,, HI, and HP rats. After body warming by EW, total thermal conductance increased, and slopes of the regression lines were then calculated. There was no apparent difference in the slopes (3.03, 3.00, and 3.20 W l rnB2* ‘C-l) among groups. When total thermal conductance was plotted against mean body temperature, which was computed from Thy and TBk by weighing factors for T,k from 0.1 to 1.0 at steps of 0.1, the slopes of the regression lines did not differ from each other. After IH started, M decreased slightly but not significantly in all groups. When subjected to EW, M was significantly suppressed from 28, 27, and 30 min after the start of EW in C,, HI, and Hz rats, respectively. The low level of M was then consistent in heat-acclimated rats. In C, rats, however, M returned to the preheating level 58 min after the onset of EW. DISCUSSION At a thermoneutral temperature of 24”C, the Thy before the heat load and the threshold Thy for tail skin vasodilation defined during IH were lower in heat-acclimated rats than in nonacclimated subjects. Fox et al. (2) have shown that in human subjects oral temperature decreases by -0.19”C after acclimation to daily body warming in a water bath for 12-24 days. Shido et al. (18) have reported that in rats repeated heat exposures for 5 h daily for 10 consecutive days lower body core temperature. Furthermore, there is evidence that shows a downward shift of threshold core temperature for heat loss response in heatacclimated or physically trained human subjects (6, 11, 13, 19). All these reports may be consistent with the present observations and suggest that acclimation to repeated daily heat exposures shifts the set point in temperature regulation to a lower level. When Thy was raised by the elevation of T,, however, the threshold Thy became slightly higher in the heat-

39.0 38.6 ,G -38.2 >, c' 37.8

-bf

FIG. 3. Changes in Thyand total thermal conductance (C) after IH or EW. * Significantly different among groups; * significantly different between C, and Hz rats; * significantly different between C, and HI rats and between C, and Ha rats.

OH1 hH2

. AA

--f&&&&~~&p t . f.

30 Time

(min)

40

50

Time

.

.

60

70

t 80

(mid

Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on December 25, 2018.

ACCLIMATION

TO INTERMITTENT

EW l

/

/

HEAT

/ /‘@ ‘m

EXPOSURE

69

43 d

y’

0,‘o

l ,’ o,R’ ’ 0 /-, Q o/’ p Y /‘oA/ ’ 9 al / l Cn 0 0’ 0 HI P AH2 4” A A/ l ./

1

38.0

38.2

38.4 Thy ("cl

38.6

38.8

I .

. .

38.5

. .

38.7

..

FIG. 4. Changes in relationship between C and Thy in rats acutely heated by IH or warmed by EW. Dashed lines, regression lines showing relationship between C and Thy in each group. * Significantly different from slope for control rats.

I

38.9

Thy(‘C)

acclimated rats than in the control rats. TSk at which tail skin vessels dilated was also significantly higher in the heat-acclimated rats. IH first raised the body core temperature of the rat without much elevation of shell temperature. In contrast, EW elevated shell temperature first and then body core temperature, The results, therefore, suggest that, in terms of threshold Thy for nonevaporative heat loss, repeated intermittent heat exposures reduce sensitivity to a rise in skin temperature. Nonevaporative heat-loss response to heat stress should be assessed by total thermal conductance rather than (R + C + K) measured by direct calorimetry because (R + C + K) is affected by the temperature difference between the body core and the calorimeter chamber wall (17). Although the rise in total thermal conductance in control rats was retarded near the end of IH, it continued to rise throughout this period in heat-acclimated rats, so the difference between the total thermal conductance of the control and heat-acclimated rats became significant at the end of IH. This result suggests that acclimation to intermittent heat exposure enhances the capacity of nonevaporative heat loss, which mainly depends on cutaneous blood flow. This conclusion is comparable to the previous reports in human subjects showing that thermal conductance (13) and hand and forearm blood flow (2) are kept greater during heat stress in heat-acclimated subjects than in the controls. Horowitz (7) reported that in rats, plasma and extracellular fluid volume increased lo-28 days after the start of heat exposure. There are several reports showing that cardiovascular adjustments occur in heat-acclimated subjects and distribute more blood to peripheral organs that are related strongly to heat dissipation (2,8,15, 19). The increased capacity for nonevaporative heat loss in the present heat-acclimated rats may therefore be attributed to an increased ability to supply blood to the cutaneous tissue. In the IH experiment, the slope of the regression line showing the relationship between thermal conductance and Thy (mean body temperature) became steeper after acclimation to repeated intermittent heat exposures, which indicates that (B + C + K) response per unit increase in central thermal drive becomes greater after heat acclimation. This augmented sensitivity of heat loss response to IH in heat-acclimated rats may be attributed,

at least partly, to an increased capacity of blood supply to cutaneous tissue (2, 13). When body temperature was raised by EW, however, no such difference in heat loss response was observed between heat-acclimated and control rats. H1 or Hz rats were subjected to 33 or 36°C of T,, respectively, for 5 h daily during at least 15 consecutive days. Glaser and Whittow (4) reported that responses to an experimental stimulus were progressively decreased when the procedure was repeated. Such “habituation” was observed in the cold defensive response of rats to repeated cold stimuli applied to the tail (3). Thus there is a possibility that rats exposed to daily intermittent heat exposures become less sensitive to T,k rise due to habituation to the gradual rise in T,. T, and T,k at the onset of tail skin vasodilation were higher in heat-acclimated rats by 1.5-2.4’C than in the control rats. This also supports the conclusion that rats acclimated to intermittent heat exposure become less sensitive to Tsk rise than nonacclimated rats. In the previous study (17), we observed that rats acclimated to continuous heat exposure were more sensitive to the rise in T,k both in (R + C + K) response and in threshold core temperature for cutaneous vasodilation than nonacclimated rats. Thus it appears that the manner of temperature acclimation in heat loss mechanisms is greatly affected by the schedule of heat exposure in rats. Changes in M during IH and EW in the present rats were similar to those in rats acclimated to continuous heat exposures (17); i.e., IH had practically no effect on A4 in both heat-acclimated and control rats, and EW suppressed A4 greatly in heat-acclimated rats. The difference in the heat exposure schedule appears to have a strong influence on the manner of acclimation in nonevaporative heat loss but not in metabolic heat production in rats. In summary, acclimation to repeated daily heat exposures lowers resting body core temperature and threshold temperature for cutaneous vasodilation and increases the capacity of (R + C + K) in rats. However, it appears that heat-acclimated rats are less sensitive to the rise in environmental and skin temperatures in heat loss response. These observations are completely different from the results in rats acclimated to continuous heat exposure

Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on December 25, 2018.

70

ACCLIMATION

TO

INTERMITTENT

(17). It is likely that the methods of heat exposure for heat acclimation greatly influence the thermoregulatory mechanisms, especially (R + C + K) response, in rats. The authors are grateful to Yoriko Yoneda for assistance in the experiments. This study was supported by Ministry of Education, Science, and Culture of Japan Grants-in-Aid for Scientific Research 61870009 and 63770104.

Address reprint requests to 0. Shido. Received 21 March 1989; accepted in final form 31 August 1989. REFERENCES K., W. WONNENBERG, H. GALLMEIER, AND B. ZIEHM. Shift of threshold temperature for shivering and heat polypnea as a mode of thermal adaptation. PfEuegers Arch. 321: 159-172, 1970. Fox, R. H., R. GOLDSMITH, D. J. KIDD, AND H. E. LEWIS. Blood flow and other thermoregulatory changes with acclimatization to heat. J. Physiol. Lond. 166: 548-562, 1963. GLASER, E. M., AND J. P. GIFFIN. Influence of the cerebral cortex on habituation. J. Physiol. Land. 160: 429-445, 1962. GLASER, E. M., AND G. C. WHITTOW. Evidence for a non-specific mechanism of habituation. J. Physiol. Lond. 122: 43-44, 1953. GWOSDOW, A. R., AND E. L. BESCH. Effect of thermal history on the rat’s response to varying environmental temperature. J. Appl.

1. BRUCK,

2.

3. 4. 5.

Physiol. 59: 413-419, 6. HENANE, R., AND

1985.

J. L. VALATX. Thermoregulatory changes induced during heat acclimatization by controlled hyperthermia in man. J. Physiol. Lond. 230: 255-271, 1973. 7. HOROWITZ, M. Acclimation of rats to moderate heat: body water distribution and adaptability of the submaxillary gland. Pfluegers Arch.

366: 173-176,1976,

HEAT

EXPOSURE

8. HOROWITZ, M., D. ARGOV, AND D. MIZRAHI. Interrelationships between heat acclimation and salivary cooling mechanism in conscious rats. Comp. Biochem. physiol. A Comp. Physiol. 74: 945-949, 1983. 9. HOROWITZ, M., AND U. MEIRI. Thermoregulatory activity in the rat: effects of hypohydration, hypovolemia and hypertonicity and their interaction with short-term heat acclimation. Comp. Biochem. Physiol. A Camp. Physiol. 82: 577-582, 1985. 10. HOROWITZ, M., Y. SHIMONI, S. PARNES, M. S. GOTSMAN, AND Y. HASIN. Heat acclimation: cardiac performance of isolated rat heart. J. AppZ. Physiol. 60: 9-13, 1986. 11. NADEL, E. R., K. B. PANDOLF, M. F. ROBERTS, AND J. A. J. STOLWIJK. Mechanism of thermal acclimation to exercise and heat. J. Appl. Physiol. 37: 515-520, 1974. 12. NAGASAKA, T., K. HIRATA, Y. SUGANO, AND H. SHIBATA. Heat balance during physical restraint in rats. Jpn. J. Physiol. 29: 383392,1979* 13. PIWONKA, R. W., AND S. ROBINSON. Acclimatization of highly trained men to work in severe heat. J. AppZ. Physiol. 22: g-12,1967. 14. RAND, R. P., A. C. BURTON, AND T. ING. The tail of the rat in temperature regulation and acclimatization. Can. J. Physiol. Pharmacol. 43: 257-267, 1965. 15. ROWELL, L. B. Human cardiovascular adjustments to exercise and thermal stress. Physiol. Rev. 54: 75-159, 1974. 16. SHIDO, O., AND T. NAGASAKA. Thermal balance during intraperitoneal electric heating at various ambient temperatures in rats. J. Aerosp. Environ. Med. 23: 27-32, 1986. 17. SHIDO, O., AND T. NAGASAKA. Thermoregulatory responses to

acute body heating in rats acclimated to continuous heat exposure. J. Appl. 18. SHIDO,

Physiol. 68: 59-65, 1990. O., Y. YONEDA, AND T. NAGASAKA.

Changes in body temperature of rats acclimated to heat with different acclimation schedules. J. AppZ. Physiol. 67: 2154-2157, 1989. 19. WYNDHAM, C. H. Effect of acclimatization on the sweat rate-rectal temperature relationship. J. AppZ. Physiol. 22: 27-30, 1967.

Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on December 25, 2018.

Heat loss responses in rats acclimated to heat loaded intermittently.

The present study examined the heat loss response of heat-acclimated rats to direct body heating with an intraperitoneal heater or to indirect warming...
1MB Sizes 0 Downloads 0 Views