thoroughly trained to permit this kind of treatment. Thus, an attempt body; e.g. oral, rectal and axillary temperatures are often used clinically

Transcription

1 206 J. Phy8iol. (1964), 174, pp With 6 t&xt-fig4ure8 Printed in Great Britain A STUDY OF DIURNAL TEMPERATURE PATTERNS IN SHEEP BY V. E. MENDEL* AND G. V. RAGHAVANt From the Department of Animal Science, University of Alberta, Edmonton, Alberta, Canada (Received 14 February 1964) The constant body temperature of homeotherms is the net result of the balance between heat production and heat loss. This balance is achieved through changes in physical and chemical functions mediated by neural mechanisms. Body temperature can be measured at a number of sites on the animal body; e.g. oral, rectal and axillary temperatures are often used clinically to indicate the deep body temperature. However, Benzinger (1961) suggests that because of its considerable thermal inertia, rectal temperature is not a reliable index of deep body temperature and although it may be a useful clinical indicator, it is not truly representative of the temperature which stimulates the heat-production or heat-conservation mechanisms. While it is unlikely that the temperature of any one location is truly representative of the deep body temperature, that of the blood supplying the brain seems to provide a better measure of the changes which affect thermoregulatory mechanisms than do any of the sites where body temperature is commonly measured. However, it was not until Bligh (1957 a) successfully implanted thermocouples in the bicarotid trunk of sheep tbat it became possible to keep the temperature of the blood flowing to the brain under constant observation for prolonged periods in the intact, conscious animal. This procedure has the disadvantage of requiring surgery which limits its application to a small number of animals at any given time. On the other hand, the non-surgical technique of measuring the temperature of the tympanic membrane (Benzinger, 1959) does not readily lend itself to animal research because each animal must be thoroughly trained to permit this kind of treatment. Thus, an attempt was made in this study to find a readily accessible location on the body of sheep which closely follows the temperature of the internal carotid artery and which could be used under a variety of experimental conditions. * Present address: Imperial Valley Field Station, University of California, Route 1, Box 121 El Centro, California, U.S.A. t Present address: Department of Animal Science, University of Manitoba, Winnipeg, Manitoba, Canada.

2 DIURNAL TEMPERATURE PATTERNS 207 In addition to short-range thermoregulatory responses to changes in environmental temperature, body temperature of most adult homeotherms follows a characteristic diurnal pattern, and since the diurnal cycle covers a range of temperatures it becomes important for experimental purposes to define the limits of this temperature cycle. Therefore, an additional objective of this study was to characterize and to measure quantitatively the diurnal temperature pattem in adult sheep. METHODS Two 4-year-old wethers fitted with rumen cannulae (Jarret, 1948) were used. The animals were kept in special cages in a holding room with a moderate daily-temperature variation (22-28 C). They were each fed 250 g of oats and 1000 g hay daily. A copper-constantan thermocouple (25 S.W.G.) enclosed in a polyethylene-clad sheath (1.5 mm O.D. and 1 mm. I.D.) was introduced into the internal carotid artery, in an animal anaesthetized with sodium pentabarbital, by a modification of Bligh's (1957a) technique. The common carotid artery was located and traced anteriorly in order to locate the internal carotid artery. A collateral vessel was found arising from the internal carotid artery which passed into the brachiocephalicus muscle. A small incision was made in the collateral vessel and the thermocouple pushed through the incision into the internal carotid artery until it stopped at the brain-to-mandible bifurcation. Two ligatures around the collateral vessel served to anchor the thermocouple and to prevent blood from seeping out of the incision. Continuing posteriorly, the thermocouple lead wires were brought out and lead along the common carotid artery for a distance of about 4 in. at which point two loose ligatures were placed around the thermocouple lead and a few fibres of the underlying omohyoidius muscle. A 2 in. vertical incision was then made through the skin, well above the jugular furrow and at the base of the neck. Two separate sutures, 2 in. apart, were placed around the thermocouple, now lying under the skin, and a few fibres of the trapezius muscle. The thermocouple lead was then passed farther under the skin to a second incision at the withers where it was finally brought to the surface and tied to the wool; at this point two more sutures were placed around a few fibres of the trapezius muscle and the thermocouple and the incision closed. Experiments were started with each sheep 7 days after the operation, by which time the edges of the incision had joined. At the conclusion of the experiment, 3 months later, each animal was bled to death from the right common carotid artery and the head fixed in 10 % formalin. The heads were later dissected and in each case the end of the thermocouple was found to be lying in the mid-stream position, at the point of bifurcation of the internal carotid artery, and free from blood clots. Internal carotid artery temperatures were recorded by a potentiometer (Leeds and Northrup Co., 4901 Stenton Avenue, Philadelphia 44, Pa) with a calibrated accuracy of 0-01 mv. Skin temperatures were measured at fourteen body sites each of which was 11 cm. in diameter. The wool at each location was removed and the skin shaved to promote good contact by a 'banjo-type' thermistor probe. The subcutaneous and external-jugular blood temperatures were measured by an hypodermic thermistor probe, rumen and rectal temperatures were measured with tubular thermistor probes. All thermistor probes were plugged into a twelve-channel telethermometer (Yellow Springs Instrument Co., Yellow Springs, Ohio).

3 208 V. E. MENDEL AND 0. V. RAGHA VAN Experimental 8ChedULe In the first part of the experiment an attempt was made to locate a site on the body which closely followed the temperature of the internal carotid artery. During this 10-day experimental period, temperature measurements were taken twice daily concurrently with the feeding periods, when it was believed the body temperatures would be changing most rapidly. Temperatures were measured at half-hour intervals, begirming 30 min before feeding and ending 1 hr after feeding. Owing to equipment limitations whereby one probe was used to measure the temperature at several sites, the following arbitrary sequence for measuring body temperatures was adopted: internal carotid artery, external jugular vein, skin and subcutaneous tissues, rumen and rectum. The temperatures of the skin and subcutaneous tissues were measured starting from the left ear (E) and moving posteriorly to the left neck (LN), left shoulder (LS), sternum (St), front left flank (FLF), rear left flank (RLF), back thorax (BS), back lumbar (BL), back sacral (BS), left upper thigh (LUT), right upper thigh (RUT), right rear flank (RRF), right front flank (RFF) and right shoulder (RS). Subcutaneous temperatures were not measured in the ear and sternum. In a later experiment the diurnal temperature patterns of these body sites were studied. The sequence of temperature measurements, feeding and management were the same as before except that temperature measurements were made at each site, at 2 hr intervals, for 24 hr, on 4 alternate days. In order to eliminate the possible effects of feeding on diurnal temperature patterns, similar 2 hr measurements were made for 2 alternate days after 19 hr of fast. RESULTS Short term variations in temperature The temperature relations which exist in the various tissues during feeding are shown in Fig. 1. In the interests of brevity and clarity the results obtained for each tissue are reported separately. Temperatures rose in the external jugular vein and internal carotid artery during the feeding period but remained constant between the morning and afternoon feeds, though at a level somewhat higher than before feeding (Figs. 1 A, B). There were only slight differences between the mean temperatures of the internal carotid artery (40.100C) and of the external jugular vein (40.09 C) (Table 1). Intraruminal temperature decreased by C during the morning feeding period then increased by 015' C (Fig. 1A). Rumen temperatures varied between the morning and afternoon feeding period when it began to rise (Fig. 1B). Bailey, Hironaka & Slen (1962) have also reported a rise in the intraruminal temperature during the feeding period of sheep. Average rectal temperature was 2-25 and higher than the skin and subcutaneous temperatures, respectively. There were fluctuations in the intravascular, skin, subcutaneous, and rumen temperatures following feeding, whereas the rectal temperature remained fairly constant throughout this experiment (Figs. 1 A, B). Rectal temperatures of both sheep were about 03 C lower than the intravascular temperature, which is

4 DIURNAL TEMPERATURE PATTERNS 209 similar to the observations of Eichna (1949) in humans. The difference between rectal and carotid artery temperatures in Jersey cattle has been reported to be C (Bligh, 1957b). There were differences in skin temperatures at different locations. The temperatures were progressively lower on the dorsal surface of the abdomen, from thoracic (37.20 C) to sacral (37.08 C) regions (Table 2) A B _.r U)3990 _ 0 % ' _, u,._ 3970 _ _ C D a.m. 9 l l 10 l 11 l 1 p.m. 2 l 3 Fig. 1. Temperature relations of various body structures during the feedingperiod. A, B, -, Internal carotid artery; x - x, external jugular vein; --- -, rumen; , rectum. C, D, Subcutaneous tissue. In this, and in subsequent figures, 250 g oats were given between the first two arrows and 1000 g hay between the second two arrows. Skin and subcutaneous temperatures gradually rose during the day, coincident with a slight rise in the holding-room temperature, with little evidence that they were following the internal carotid artery temperatures (Fig. 1 C, D, see also Fig. 2 for average holding-room temperature). Kibler & Brody (1950) have observed a similar increase in the surface temperature of cattle. Noteworthy are the additional increases in the surface temperatures concomitant with feeding (Figs. 1 C, D). The mean subcutaneous temperature of all body sites was found to be 0.630C higher than the average skin temperature and as would be expected the temperatures were progressively lower from thoracic ( C) to

5 .- ~~~~~~~~~~~~~A 210 V. E. MENDEL AND G. V. RAGHA VAN sacral (37.56 C) regions (Table 3). The subcutaneous temperatures of the thigh and: neck regions were 0 60 C higher than the average dorsal and C higher than the average lateral abdominal-surface temperatures. TABLE 1. Mean intravascular, rumninal and rectal temperatures (0 C) averaged over all ten days of the expt. a.m. p.m. Before During After Before During After feeding feeding feeding feeding feeding feeding Mean + S.D. Internal ' O O carotid artery Jugular Ruimen X X Rectum 39* TABLr 2. Mean skin temperature ( C) at each of the 14 locations averaged over all ten days of the expt. a.m. p.m. Before During After Before Dung After feeding feeding feeding feeding feeding feeding Mean + S.D. BT BL ' BS * FLF * *23 RFF * RLF RRF * * LS RS LIUT 36* RUJT * E LN * St <16 TABLi 3. Mean subcutaneous temperature (0C) at each of the twelve locations averaged over all ten days of the expt. a.m. p.m. Before During After Before During After feeding feeding feeding feeding feeding feeding Mean + S.D. BT BL BS *41 37* FLF * RFF RLF *83 37*86 37* * RRF * LS RS LUT * * RUT x28 38x32 35x45 38@60 38@ LN 38*04 38*20 38*32 38*35 38* *32 0*18

6 DIURNAL TEMPERATURE PATTERNS 211 Diurnal temperature patterns The plots of the average subcutaneous temperatures were monophasic (Fig. 2), attaining their maximum and minimum values at 4 p.m. and 4 a.m. respectively. These curves are similar to those seen in humans. In the absence of food, a similar but lower trend was observed. For example, the skin and subcutaneous tissue temperature range varied, respectively, 0.80 and C throughout the day in the animals which were fed and 0-36 and 0.22 C in those which were fasted _ O 38-00/ \ _ / 37-80_ /\ /_ ~ -_ 3750 _'_ l l l l l l e 8a.m p.m a.m. 4 8 Fig. 2. Diurnal temperature patterns of subcutaneous tissues in fed (full line) and fasted sheep (broken line). The values across the top of the graph are the mean temperatures of holding room (0 C). In fed sheep the internal carotid artery temperature patterns were polyphasic (Fig. 3) with maxima at 10 a.m., 2 p.m. and 8 p.m. After the last peak there was a progressive decline to a minimum value between 2 and 4 a.m. The peaks occurring at 10 a.m. and 2 p.m. were associated with the ingestion of food. A similar rise in the temperature of the carotid artery (Findlay & Ingram, 1961) and jugular vein (Ingram & Whittow, 1962) also occurs in cattle as a result of feeding. The reason for the third peak at 8 p.m. is not evident. The temperature of external jugular blood in this trial generally followed that of the internal carotid blood but did not follow it in detail. On the average, carotid temperature exceeded jugular temperature by only C. However, at 10 a.m., 2 p.m. and 8 p.m. there were average differences of 0-16, 0-15 and C, respectively. In the absence of food the intravascular temperatures gave a monophasic plot, attaining maximum values of and C at 4 p.m. in the carotid artery and external jugular vein, respectively (Fig. 4). 14 Physiol. 174

7 212 V. E. MENDEL AND G. V. RAGHAVAN Marked drops in rumen temperature occurred at 10 a.m. and 2 p.m. coincident with periods of feeding (Fig. 5). After the second drop, rumen temperature rose gradually during the night to a maximum of at 2 a.m. Brody, Dale & Stewart (1955) and Nangeroni (1954) have also reported temperature rises in the rumen of cattle around 4 a.m _- 8a.m. 12 _t4 p.m a.m _ --_ Fig. 3. Diurnal temperature patternls of jugular (- x- x) and carotid blood (full line) in fed sheep u39.90 _/ 39-80, I l l l l l l l 8am. 12 4p.m. 8 12a.m. 4 Fig. 4. Diurnal temperature patterns of jugular (-x --- x -) and carotid blood (broken line) of fasted sheep. Rumen temperatures in the fasted animals showed only the slightest tendency to rise during the day and remained relatively unchanged throughout each 24 hr period. Rectal temperature (Fig. 6) gradually rose from 6 a.m. to a maxrimum of C at 6 p.m. then declined to a low of C at 4 a.m. A similar pattern was observed in the fasted animals exrcept that the maximum temperature was reached 2 hr earlier, at 4 p.m., and the minimum temperature 2 hr later, at 6 a.m. These results are in close agreement with those of Beakley &; Findlay (1955b) and of Quartermain (1962).

8 DIURNAL TEMPERATURE PATTERNS /_ l l 8a.m. l 12 l l l 4p.m. 8 12am. 4 Fig. 5. Diurnal temperature patterns of the rumen contents in fed (full line) and fasted sheep (broken line) _ )39-70/ Fig , a.m p.m. 8 12a.m. 4 Diurnal temperature patterns of the rectum in fed (full lihe) and fasted sheep (broken line). DISCUSSION The temperature difference between the rectum and skin (RS) has been shown to vary in different breeds of cattle (Beakley & Findlay, 1955a). At an environmental temperature of 400 C the Brahman has been shown to have an RS of 1.50 C, while, at the other extreme, the Brown Swiss was found to have an RS of 3.00 C (Worstell & Brody, 1953). In the present work the RS was found to be approximately 2.30 C, which indicates that the heat loss through the skin of the sheep is at least as effective as it is in some species of cattle. There were consistent differences in the skin and subcutaneous temperatures at different locations on the animal body. However, the temperature at none of these locations followed the internal carotid artery temperature; instead, they seemed to follow that of the holding room. The temperature of the external jugular vein, on the other hand, very closely followed the fluctuations of the internal carotid-artery temperature under all experimental conditions. High ambient temperatures have been shown to influence the temperature of the blood in the external jugular vein (Ingram & Whittow, 1962) but always the shapes of the curves for 14-2

9 214 V. E. MENDEL AND G. V. RAGHA VAN external jugular and internal carotid blood are similar. Therefore, it is suggested that the external jugular vein can be used as a convenient and reliable site for measuring the average blood temperature of the brain, under both field and experimental conditions. This is not a satisfactory substitute for measuring brain temperature in every situation but should be useful in many applied experiments. The diurnal rhythms of skin and subcutaneous temperature in the present investigation could be related to the average activity of the animal coupled with the environmental temperature. A gradual rise in the body temperature during the day is expected, because all the organs are thrown into activity with the consumption of food and a more alert attitude generally. The decline in skin and subcutaneous temperatures during the night might possibly be attributed to a decrease in activity of most of the organs, even though in this case the animals were never allowed to sleep for extended periods. An interesting relation between the temperature of the internal carotid artery and the rumen in fed sheep was noticed. The curves are nearly perfect mirror images of one another for the period 8 a.m. to 6 p.m. (Figs. 3, 5). The reasons for this relation are not evident although it could mean that heat production is increased parallel to a fall in rumen temperature. A marked rise in rumen temperature during the night, when the skin, subcutaneous, rectal and intravascular temperatures were falling, emphasizes the importance of rumen heat production in the maintenance of a constant body temperature in a cool environment. The reasons for this rise are not known but possibly the rate of fermentation increases for several hours after feeding with an accompanying rise in the average temperature of the rumen. In support of this idea it can be seen that in the absence of food the rumen temperature was lower (Fig. 4) and quite constant with no nocturnal increase. Rectal temperature did not seem to be affected by the ingestion of food and only roughly followed the temperature patterns of the rumen and intravascular system. It is, therefore, suggested that rectal temperatures should not be used to evaluate the internal temperature changes which are responsible for regulating body temperature. SUMMARY 1. An improved technique for implanting thermocouples in the internal carotid artery is described. Thermocouples implanted by this method remained functional for at least 3 months. When the animals were slaughtered, 3 months after implantation, the thermocouples were found

10 DIURNAL TEMPERATURE PATTERNS 215 to be lying at the brain-to-mandible bifurcation of the internal carotid artery and to be completely devoid of clots. 2. Experiments were conducted with two mature wether sheep in an attempt to locate an external body site more readily accessible for measurement than the internal carotid artery but which closely follows its temperature. 3. Body sites selected for temperature measurements were: rumen, rectum, jugular vein, internal carotid artery and fourteen points on the skin and twelve sites in the subcutaneous tissue. 4. The temperatures of the skin, subcutaneous and rectal tissues did not follow that of the internal carotid artery, but the temperature of the external jugular vein paralleled that of the internal carotid artery under all experimental conditions. It was suggested that the external jugular vein provides a convenient site for measuring brain blood temperature. 5. Diurnal temperature patterns of the same sites were plotted, both in the fed and fasted condition. The temperature curves of the skin, subcutaneous tissue and rectum were monophasic, reaching maxima and minima at 4 p.m. and 4 a.m., respectively, in the fed animals. In the fasted animals lower maxima and minima were reached at approximately the same times. Arterial curves were polyphasic with peaks at 10 a.m., 2 p.m. and 8 p.m. but were monophasic in the fasted animals with a maximum at 4 p.m. and in both cases a minimum at 4 a.m. Rumen temperatures remained constant in the fasted animals but fell in the fed animals at each feeding then gradually rose to a maximum at 2 a.m. REFERENCES BAILEY, C. B., HIRONAxA, R. & SLEN, S. B. (1962). Effects of the temperature of the environment and the drinking water on the body temperature and water consumption of sheep. Can. J. anim. Sci. 42, 1-8. BEAKTLEY, W. R. & FINDLAY, J. D. (1955a). The effect of environmental temperature and humidity on the skin temperature of Ayrshire calves. J. agric. Sci. 45, BEAKLTEY, W. R. & FINDLAY, J. D. (1955b). The effect of environmental temperature and humidity on the rectal temperature of calves. J. agric. Sci. 45, BENZINGER, T. H. (1959). On physical heat regulation and the sense of temperature in man Proc. nat. Acad. Sci., Wa8h., 45, BENZINGER, T. H. (1961). The quantitative mechanism and the sensory receptor organ of human temperature control in warm environment. Ann. intern. Med. 54, BLIGH, J. (1957a). The relationship between the temperature in the rectuim and of the blood in the bicarotid trunk of the calf during thermal polypnoea. J. Phy8iol. 136, BLIGH, J. (1957b). A comparison of the temperature of the blood in the pulmonary artery and in the bicarotid trunk of the calf during thermal polypnoea. J. Phy8iol. 136, BRODY, S., DALE, H. E. & STEWART, R. E. (1955). Environmental physiology and shelter engineering with special reference to domestic animals. XXXIV. Interrelations between temperatures of rumen (at various depths), rectum, blood, and environmental air; and the effects of an antipyretic, feed and water consumption. Res. Bull. Mo. agric. Exp. Sta. no EICHNA, L. W. (1949). Thermal gradients in man: Comparison of temperatures in the femoral arteries and femoral vein with rectal temperatures. Arch. phys. Med. 30,

11 216 V. E. MENDEL AND G. V. RAGHA VAN FniDLAY, J. D. & ING.RAM, D. L. (1961). Brain temperature as a factor in the control of thermal polypnoea in the ox (Bo8 tauru8). J. Phyqiol. 155, INGRAm, D. L. & WHITTOW, G. C. (1962). The effects of variations in respiratory activity and in the skin temperatures of the ears on the temperature of the blood in the external jugular vein of the ox (Bo8 tauru8). J. Phy8iol. 163, JAIRET, J. G. (1948). The production of rumen and abomasal fistulas in sheep. J. coun. Sci. indu8t. Re8. 21, KIBLER, H. H. & BiRoDY, S. (1950). Environmental physiology and shelter engineering with special reference to domestic animals. X. Influence of temperature 5 to 980 F on the evaporative cooling and exterior body surfaces in Jersey and Holstein cows. Re8. Bull. Mo. agric. Exp. Sta. no NANGERONI, L. J. (1954). Variations in intraruminal temperatures of sheep during normal and abnormal conditions. CorneU Vet. 44, QUARTERMAIN, A. R. (1962). Physiological variation in New Zealand Jersey cows during summer. 1. Repeatabilities of the measurements and diurnal variations. N.Z. J. agric. Res. 5, WORSTELL, D. M. & BRODY, S. (1953). Environmental physiology and shelter engineering with special reference to domestic animals. XX. Comparative physiological reactions of European and Indian cattle to changing temperature. Res. Bull. Mo. agric. Exp. Sta. no. 515.