Schwabe, Emery & Griffith (1938), basing oxygen consumption on body
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1 J. Physiol. (1963), 169, pp With 3 text-figures Printed in Great Britain THE BASAL METABOLIC RATE OF COLD-ADAPTED RATS BY A. C. L. HSIEH From the Department of Physiology, University of Hong Kong, Hong Kong (Received 3 April 1963) Schwabe, Emery & Griffith (1938), basing oxygen consumption on body weight, found the metabolic rates of rats living at 7-12 C to be about 13 % higher than controls, when determinations were made at thermal neutrality (28 C). Ring (1939), basing oxygen consumption on surface area, found the metabolic rates of rats living in a refrigerator (0-5o C) to be 21 % higher than those of warm-adapted rats when determinations were made at 300 C (referred to as MR 30). Sellers, Reichman, Thomas & You (1951) also using surface area as a reference unit for oxygen consumption, obtained an MR 30 of + 17 % for rats adapted to 1.50 C. Against these findings are the observations of Cottle & Carlson (1954) who, basing oxygen consumption on body weight to the 3/4 power, found the metabolic rate of cold-adapted rats (5 C) to be similar to those living at 25 C. Chiu & Hsieh (1960) noted that the various reference units used to express the metabolic rate of rats did not satisfactorily correct for differences in size of the animals and concluded that metabolic rates of cold-adapted rats appear higher than those of warm-adapted ones because the smaller body weights of the former animals favoured this during the conversion of total oxygen consumption to metabolic rate. If one assumes that rats adapted to 50 C should have at least the same amount of metabolically active tissue as rats of the same age living in a warm environment, and compares their absolute rates of oxygen consumption, the results of Chiu & Hsieh (1960) indicate that the metabolic rate at 250 C (MR 25) of the cold-adapted rats is similar to that of warm-adapted (280 C) rats. The different conclusions cannot be entirely ascribed to different mathematical manipulations of the data. Heroux (1960), using a unit that approximately fitted his data (the square root of body weight in grams), shows a graph in which the MR 30 of rats adapted to 60 C is about + 24 %. If the absolute rates of oxygen consumption of these animals are compared, the cold-adapted rats still show an MR 30 of + 12 %. These considerations have led to an examination of the conditions under which the oxygen consumption of rats are usually determined. Ring (1939), Sellers et al. (1951) and Heroux (1960) determined oxygen 54 Physiol. 169
2 852 A. C. L. HSIEH consumption at 300 C, whereas Cottle & Carlson (1954) and Chiu & Hsieh (1960) determined oxygen consumption at 250 C. The different results may have been due to the different temperatures at which the oxygen consumptions of the animals were determined. While 300 C is the temperature at which the metabolic rate of rats living in a normal environment is minimal, this temperature may be too high for rats adapted to cold. On the other hand, 25 C may be too low for rats adapted to a warm environment. The rate of heat production of a rat at 50 C is about twice that of one living at 280 C. When such an animal is transferred to a warm room, time will be required for the rate of heat production to fall to a new level (i.e. to reach a steady state). If insufficient time is allowed for the animal to reach a steady state in its new environment, estimations of metabolic rates will be too high. The present paper describes experiments designed to determine: (1) the time required for rats living at 50 C to reach a steady state when transferred to 280 C, and (2) the effects of environmental temperature on the oxygen consumption of cold-adapted (50 C) and warm-adapted (280 C) rats. The rates of oxygen consumption of the animals have been correlated with their body and liver weights. METHODS Male albino rats were kept in individual metal cages and given food and water ad libitum. Diet consisted of 70 % corn meal, 18 % wheat gluten, 10 % brewer's yeast, 1 %/ NaCl and 1 % CaCO3. Rats to be adapted to cold were placed in a room maintained at 50C and warm-adapted controls were kept in another room at 280 C. Body weights were recorded to the nearest gram each moming at about the same hour. Rectal temperatures were recorded to the nearest 0.10 F ( C) by a thermometer inserted about 2 in. (5 cm) above the anus. Temperatures have been converted to degrees Centigrade for the purpose of this report. Oxygen consumptions were determined by a closed-circuit method previously described (Hsieh, 1962). The metabolic chambers were immersed in a large water-bath maintained at the desired temperature. Ten minutes was allowed for temperatures to reach equilibrium and oxygen consumptions recorded for two half-hour periods. The amount of oxygen consumed during the second half-hour period was used to calculate the hourly rate of oxygen consumption. Rats receiving triiodo-l-thyronine were given daily subcutaneous injections of 3:5:3'- triiodo-l-thyronine (Califomia Corporation for Biochemical Research). The hormone was dissolved in alkalinized water (distilled water adjusted to ph 8 with 0-1 N-NaOH) and concentrations arranged so that the desired amount was contained in 0-5 ml. of fluid. RESULTS Effects of stabilization time on oxygen consumption at 280 C Two groups of nine rats each, having similar average weights (about 235 g), were placed in the cold room. One group received daily injections of 5,tg triiodo-l-thyronine (T3). The body weights of the animals not
3 METABOLIC RATE OF RATS 853 receiving T3 fell by about 20 g in 3 weeks, after which a gradual increase in weight occurred. Those that received T3 lost weight during the first week of cold exposure, but then began to grow. By the third week the treated rats were about 35 g heavier than the untreated (Fig. 1). 270 r F W -c k o 230 F- co 220 I- 210 F Time (weeks) 4 5 Fig. 1. Mean body weights of rats exposed to 50 C. Untreated rats,, and rats receiving subcutaneous injections of triiodo-l-thyronine (5,ug/day) 0. Nine animals per group. Between the third and fifth weeks the rats were taken from the cold room and oxygen consumptions determined at 280 C. The rats were either placed directly in the metabolic chambers or allowed to stabilize for various periods in the warm room. The results are compared with those obtained from appropriate controls in Fig. 2. Rates of oxygen consumption of the cold-adapted rats decreased with the length of time allowed for
4 854 A. C. L. HSIEH stabilization at 28 C; after 2 hr rates were not significantly different from those of controls. The oxygen consumption of rats receiving T3 were higher than untreated animals but no increment ascribable to adaptation to cold could be observed L- E 380 C 0._ E 360 _j(5) (9) 0C 0 C 0I 340 bo x (9) (14) * Time (hr) Fig. 2. Mean oxygen consumptions of warm- and cold-adapted rats determined at 280 C after various periods at 280 C. Cold-adapted rats receiving T3 warm-adapted rats receiving T3 5,ig/day, 0; cold-adapted rats, *; warmadapted rats, F. Numbers of animals per group are in parentheses; vertical bars indicate standard errors of the means. Oxygen consumptions at 5, 20, 25, 28 and 300 C Three groups of eight rats each were placed at 50 C. One group was given 5 jtg T3/day, another 15 /tg/day and the third group received no treatment. The changes in weight on exposure to cold were similar to
5 METABOLIC RATE OF RATS those of the previous experiment. Oxygen consumptions were determined during the third and fourth week of cold exposure. When determinations were to be made at 25, 28 or 30 C the rats were first placed at 28 C for 2 hr. Determinations at 20 C were preceded by a 2 hr period at room temperature (16-20' C). For determinations at 50 C the cold-adapted rats were transferred directly to the metabolic chambers, but the warmadapted rats were first placed in the cold room for 2 hr. The oxygen consumptions of the treated and untreated cold-adapted rats were similar when measured at 5 and at 20 C. At higher temperatures rates were directly related to the dose of T3 (Table 1). TABLE 1. Oxygen consumption (ml./hr) of warm-adapted rats (W) and cold-adapted rats (C) at various environmental temperatures Environmental temperature (0 C) 855 Group W (237) (131) (120) (111) (100) C (275) (177) (119) (116) (134) C+ T3 (5 tg/day) (269) (180) (147) (148) (156) C+T3 (15 itg/day) (272) (167) (170) (175) (187) Values are the mean + standard error of the mean; n= 8 for each group. Numbers in parentheses are relative oxygen consumptions with group W at 300 C taken as 100. Oxygen consumptions of the cold-adapted rats were minimal at 25 and 280 C (Table 1). At these temperatures there was no difference between the rates of cold- and warm-adapted rats. At 30 C rates of the coldadapted rats increased whereas those of the warm-adapted group decreased. Thus at 300 C the cold-adapted rats had significantly higher rates. At 5 and 20 C the oxygen consumptions of the cold-adapted rats were also higher. Rectal temperatures of the untreated cold-adapted rats during the period of stabilization at 28 C and at the end of their sojourn in the metabolic chambers at 25, 28 and 300 C, are compared with those of control animals in Fig. 3. While the average temperature of the control animals remained relatively constant during the whole period, there was a fall of C in that of the cold-adapted group. Transfer to 250 C was followed by a further fall of C, but transfer to 300 C resulted in a rise of C. Only at 28 C could the cold-adapted animals be regarded as having a constant body temperature during the period of determination of oxygen consumption.
6 856 A.C.L.HSIEH The foregoing results suggested that cold-adapted rats have a lower neutral temperature. However, the higher oxygen consumption at 300 C may have been due to insufficient stabilization time. Oxygen consumptions of twenty-nine cold-adapted rats (5 weeks at 50 C) and twenty-nine warm-adapted rats were determined at 30 C after stabilization periods of 6 and 24 hr. After 6 hr at 280 C the average oxygen consumption of the cold-adapted group was ml./hr. This was about 18 % higher than 39- V ~~~~~~~~~30 0~~~~~~~~~~~~~~~~~~~~~ E Time (hr) Fig. 3. Mean rectal temperatures of cold-adapted rats, 0, and warm-adapted rats, 0. During the first 2 hr the animals were kept in their cages at 280 C. At 2 hr the animals were transferred to metabolic chambers kept at the temperatures indicated. Nine animals per group. that of the warm-adapted controls. After 24 hr in the warm room the average oxygen consumption of the cold-adapted group was significantly lower ( X4 ml./hr) and no longer different from that of the control group. Correlation of oxygen consumption at 300 C with body weight and liver weight Immediately after the preceding experiments the animals were killed and their body and liver weights determined. While the average body weight of the cold-adapted group was smaller than that of the warmadapted group, the average liver weight of the former group was larger (Table 2). Since the regression coefficients of log. liver weights on log. body
7 METABOLIC RATE OF RATS 857 weights of the two groups are similar, it is safe to assume that at the beginning of the experiments, when body weights were similar, liver weights of the two groups were the same. Thus cold exposure stimulates growth of the liver but retards growth of the body as a whole. Group w C TABLE 2. No. Body and liver weights of warm-adapted (W) and cold-adapted (C) rats Initial Final mean body mean body Mean liver weight (g) weight (g) weight (g) bi N.S. CP<o0.01 o P<o0001 7N.S L11L LO Relative liver ba size (%) DP< = standard error; bi = within-groups regression coefficient of log. liver weight on log. body weight; ba = average within-groups regression coefficient. Relative liver size calculated from regression equations with ba: log. liver wt. (W) = 0-73 log. body wt. (W) , (1) log. liver wt. (C) = 0-73 log. body wt. (C) , (2) log. liver wt. (C) -log. liver wt. (W) = 0-107, liver wt. (C)/liver wt. (W) = 1-28 = , Mean body and liver weights together with oxygen consumptions after 6-24 hr of stabilization at 280 C are shown in Table 3. Regression coefficients for log. oxygen consumption on log. body weight and log. liver weight have been calculated and found to be significantly different for cold-adapted and warm-adapted groups of animals. TABLE 3. Regression coefficients of log. oxygen consumption on log. body weight and log. liver weight of warm-adapted (W) and cold-adapted (C) rats after 6 hr (6) and 24 hr (24) of stabilization at 280 C Group W (6) a(6) W (24) C (24) Group W (6) C(6) W (24) C (24).No. No. Mean body weight (g) P< p<o 0-01 L Mean liver weight (g) p<o-o P<&-oo Oxygen consumptions were determined at bi=within-groups regression coefficient. Mean 02 (ml./hr) < L S. 331 _ 8-4 Mean 02 (ml./hr) p<o FN.S._ bi p<o _ F-P < 0_-01 LO bi P< P< (3) (4) 300 C; + = standard error of the mean;
8 858 A. C. L. HSIEH DISCUSSION Hsieh (1962) noted that rats living at 40 C, fed on a diet containing 0-05 % propylthiouracil and given daily doses of 5 p,g T3, grew more rapidly than normally fed rats under similar environmental conditions. The present experiments (Fig. 1) show that T3 has a similar stimulating effect on normally fed animals. At 5 and 20 C cold-adapted rats receiving T3 have rates of oxygen consumption that are similar to untreated cold-adapted rats (Table 1). This indicates that the effects of cold and T3 on energy metabolism are not additive. Only at temperatures above 20 C are the conditions of the animals 'unmasked'. At 28 C the rates of cold-adapted rats are not greater than those of warm-adapted animals given similar doses of T3 (Fig. 2). These points further suggest that exposure to cold does not increase the sensitivity of rats to T3 (see Hsieh, 1962). Given sufficient time for stabilization, the oxygen consumptions determined at 25 and 28 C of cold-adapted rats are similar to those of warmadapted ones. At an environmental temperature of 30 C the former have higher oxygen consumptions. The experiments clearly show the important part played by stabilization time and environmental temperature in influencing the magnitude of this parameter. The question then arises, at what environmental temperature and after how long a period of stabilization should the oxygen consumptions of cold-adapted rats be determined if the results are to be used in a comparison of basal metabolic rates? When comparing basal metabolic rates it seems logical to use minimal rates of oxygen consumption. However, in the present experiments this would lead to the animals being under different conditions (the cold-adapted group would be at C while the warm-adapted group would be at 30 C). The usual procedure is to make comparisons under standard conditions. Since oxygen consumptions of control animals are minimal at 30 C (Benedict & MacLeod, 19; Herrington, 1940), this will be used as the standard temperature. However, the arbitrary nature of this standard temperature should not be overlooked. For the purpose of the present discussion oxygen consumptions of cold-adapted rats determined at 300 C after a 6 hr stabilization period will be used to make comparisons of basal metabolic rates because: (a) levels are similar to those obtained after 2 hr, and (b) the reduction in rates after 24 hr at 280 C may be the result of decay in adaptational processes. The ratio of mean oxygen consumption to mean body weight of the cold-adapted group is greater than that of the warm-adapted group (1.35 ml./hr/g body weight as against 1-00 ml./hr/g body weight, after 6 hr
9 METABOLIC RATE OF RATS 859 (280 C) as shown in Table 3. Thus, if it is assumed that the total oxygen consumption of a rat is related to its total body weight, one may conclude that metabolic rates of cold-adapted rats are higher than those of the warm-adapted. But the size of the metabolically active tissues may be different in the two groups. The different effects of cold on total body weight and liver size shown in Table 2 are well known (Emery, Emery & Schwabe, 1940; Katsh, Katsh & Osher, 1955; Heroux & Gridgeman, 1958; Hale, Mefferd, Vawter & Foerster, 1959; Hannon & Vaughan, 1961). If one assumes that liver size is related to the total amount of metabolically active tissue and compares the ratios of mean oxygen consumption to mean liver weight, the metabolic rates of cold-adapted rats are similar to those of the controls (30.5 ml./hr/g liver weight for the warm-adapted group and 31-1 ml./hr/g liver for the cold-adapted group). Indeed, after 24 hr at 280 C their metabolic rates are lower than those of the controls. Thus, from the same oxygen consumption data it is possible to arrive at diametrically opposing conclusions by using different criteria for calculating metabolic rates. Kleiber (1932) plotted the logarithm of mean oxygen consumptions of groups of adult animals of different species against the logarithm of their body weights, and having obtained a straight line has advocated the use of body weight (in kg) raised to the 3/4 power as a unit of metabolic size. But it may well be that 'the seeming similarity between the different species shown by this logarithmic chart is an artificial similarity' (Benedict, 1938). It is essential to show that the within-groups (intraspecific) regression coefficients are similar. This has not been done. In the present experiments two groups of the same species are being compared. The within-groups regression coefficients (bi in Table 3) of log. oxygen consumption on log. body weight of the warm-adapted rats is This is significantly higher than 0-26, which is the value for the coldadapted rats. Approximately the same difference in bi of log. oxygen consumption on log. liver weight of the two groups is also shown. It is apparent that cold has induced a change in the underlying relation between oxygen consumption and body weight and liver weight. This points to a qualitative change in both body and liver and adjustments based on corrections for quantitative differences will not be valid. The foregoing considerations force one to conclude that it is impossible to compare the basal metabolic rates of rats adapted to 50 C for 5 weeks with those kept at 28 C, by using either body weight or liver weight as reference units. The lower temperatures at which cold-adapted rats have minimal oxygen consumption (Table 1) suggest that these animals may have a higher basal metabolic rate. However, the lower neutral temperatures
10 860 A. C. L. HSIEH 860)A.L SE may be due to the combined effects of increased metabolically active material (e.g. larger livers) and reduced surface area for heat loss (i.e. smaller body weights). SUMMARY 1. Rats kept at 50 C and given subcutaneous injections of triiodo-lthyronine (T3, 5 ug/day) grow more rapidly than controls living unider similar conditions. 2. Oxygen consumptions of cold-adapted rats (5 weeks at 50 C) receiving T. are similar to those of untreated cold-adapted rats when determinations are made at 5 and 200 C. Thus the effects of cold and T3 on energy metabolism are not additive. 3. Cold stimulates growth of livers but retards growth of the body as a whole. 4. The regression coefficient of log. oxygen consumption on log. body weight is 1x27 + 0x169 in warm-adapted rats and in coldadapted ones. 5. The regression coefficient of log. oxygen consumption on log. liver weight is 1i in warm-adapted rats and in coldadapted ones. 6. The significantly different regression coefficients point to a qualitative change in body and liver of cold-adapted rats. It is thus impossible to compare the basal metabolic rates of rats adapted to 5 C for 5 weeks with those kept at 280 C by using either body weight or liver weight as reference units. 7. Cold-adapted rats have lower neutral temperatures. This may be due to the combined effects of increased metabolically active tissue (e.g. larger livers) and reduced surface area for heat loss (i.e. smaller body weights). This work was supported in part by grants from the China Medical Board of New York and the University of Hong Kong Research Grants Committee. REFERENCES BENEDICT, F. G. (1938). In Vital Energetics, p Washington: Carnegie Inst. BENEDICT, F. G. & MAcLEoD, G. (19). The heat production of the albino rat. II. Influence of environmental temperature, age, and sex; comparison with the basal metabolism of man. J. Nutr. 1, CHu, C. C. & HsIEH, A. C. L. (1960). A comparative study of four means of expressing the metabolic rate of rats. J. Phy8iol. 150, CoTrLx, W. & CARLsoN, L. D. (1954). Adaptive changes in rats exposed to cold. Caloric exchange. Aner. J. Physiol. 178, EMRRY, F. E., EMERY, L. M. & SCHWABE, E. L. (1940). Effects of prolonged exposure to low environmental temperature on body growth and on weights of organs in albino rat. Growth, 4,
11 METABOLIC RATE OF RATS 861 HAT,E, H. B., MEFFERD, R. B. Jr., VAWTER, G. & FOERSTER, G. E. (1959). Influence of long-term exposure to adverse enviromnents on organ weights and histology. Amer. J. Physiol. 196, HANNON, J. P. & VAUGHAN, D. A. (1961). Effect of exposure duration on selected enzyme indexes of cold acclimatization. Amer. J. Physiol. 200, HEROUX, 0. (1960). The effect of intermittent indoor cold exposure on white rats. Canad. J. Biochem. Physiol. 38, HEROUX, 0. & GRIDGEMAN, R. (1958). The effect of cold acclimation on the size of organs and tissues of the rat, with special reference to modes of expression of results. Canad. J. Biochem. Physiol. 36, HERRINGTON, L. P. (1940). The heat regulation of small laboratory animals at various environmental temperatures. Amer. J. Physiol. 1, HSIEH, A. C. L. (1962). The role of the thyroid in rats exposed to cold. J. Physiol. 161, KATSH, S., KATSH, F. G. & OSHER, P. (1955). Organs of rats exposed to cold. Anat. Rec. 121, 402. KTLIBER, M. (1932). Body size and metabolism. Hilgardia, 6, RING, G. C. (1939). Thyroid stimulation by cold, including the effect of changes in body temperature upon basal metabolism. Amer. J. Physiol. 125, SELLERS, E. A., REICHMAN, S., THOMAS, N. & You, S. S. (1951). Acclimatization to cold in rats: metabolic rates. Amer. J. Physiol. 167, SCHWABE, E. L., EMERY, F. E. & GRIFFITH, F. R. Jr. (1938). The effect of prolonged exposure to low temperature on the basal metabolism of the rat. J. Nutr. 15,
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