Physiology & Behavior. Vol. 58, No. 3, pp. 615-618, 1995 Copyright ~ 1995 Elsevier Science Ltd Printed in the USA. All rights reserved 0031-9384/95 $9.50 + .00
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Emotional Hyperthermia and Performance in Humans EDUARDO
BRIESE
Universidad de Los Andes, Apartado 109, M~rida 5101, Venezuela R e c e i v e d 14 J a n u a r y 1 9 9 4 B RIESE, E. Emotional hyperthermia and performance in humans. PHYSIOL BEHAV 58(3) 615-618, 1995.--This study was carried out to see whether or not the stress induced by an academic examination raises the central temperature. A secondary object of the study was to see if examination stress might be related to the examination scores. Mean oral temperature in 108 medical students prior to examination was significantly higher than that before a laboratory demonstration. This establishes the existence of emotional hyperthermia in humans. A small but significant correlation was found between the grades obtained by the students and the difference between pre-examination and pre-demonstration temperature, higher scores being associated with larger temperature differences. However, the temperature prior to examination was practically the same in the students with the highest grades as in the students with the lowest grades. The difference between pre-examination and pre-demonstration temperature was larger in the students with the highest grades because they had a significantly lower temperature prior to the practical demonstration. On the other hand, in the lowest scoring students, temperature prior to the practical demonstration was almost as high as that prior to examination. This suggests that emotion per se does not influence the performance which apparently is related to the adequate triggering and management of the emotional response. Emotion Students
Psychological stress Humans
Examination hyperthermia
G E N T L E handling, measurement of colonic temperature, (Tc), change of cage or change of environment increases central temperature in rats (3) and mice (4). This p h e n o m e n o n has been called emotional hyperthermia, psychological stress hyperthermia, psychogenic hyperthermia, stress induced fever or emotional fever (2,5). Emotional hyperthermia has also been reported in humans. However, in contrast with the abundant literature on emotional hyperthermia in animals there are few reports on emotional hyperthermia in humans. From 1945 to 1992 I have found only seven papers on this subject and of those only three concerned healthy h u m a n subjects (7,11,12). Two works were on psychiatric patients (6,8) one was a review (10) and the remaining one (9) was a note on two female subjects whose central temperature was significantly higher after watching films. Gotsev and Ivanov (7) took the axillary temperature of 1068 students during oral examinations (in fact, mostly after the examination) . There were various examination sessions in Sofia (Bulgaria) and Budapest (Hungary) at distinct times of the year and distinct hours. Average temperature was 37.5°C in male students and 37.4 ° in females. The temperature of 40 students attending as listeners was under 37°C. There are some flaws in this work. First, the axillary temperature is difficult to measure accurately (1). Second,except for 40 students attending as listeners at some of the examinations, there was no control, since at this time temperatures above 37°C were considered as abnormal. The design of this study was based on considering temperatures under 37°C as normal and temperatures above 37°C as hyperthermic. Renbourn (12) found that before boxing contests the mean oral temperature in 12 school boys from 12 to 14 years old was 1.06°F (0.6°C) higher than the mean oral temperature before
Psychogenic hyperthermia
Oral temperature
training sessions and 1.44°F (0.84°C) higher than the mean oral temperature taken at home at the same hour of the day. Although this study shows emotional hyperthermia in humans, due to the small n u m b e r and young age of the subjects the results might not be representative of larger and older populations. More recently Marazziti et al.(11) have shown that mean axillary temperature of 22 residents, 10 to 15 min before a yearly examination in Psychiatry at Pisa University, was 0.6°C higher than the temperature taken 2 to 3 weeks later after having sat and relaxed for at least 30 min. In this study, the control situation was quite different from the experimental situation and moreover neither were uniform in their treatment of the subjects. In some of them blood was withdrawn and in others was not. The difficulty in establishing that emotional hyperthermia exists in humans consists in having as control a situation identical to the experimental one except for the supposed emotion. This condition was not fulfilled in the previous studies and, because of this and because of the scarcity of data on this subject, the phenomenon of emotional hyperthermia in humans does not appear to be well established. Consequently I investigated if, in an emotional situation, the central temperature of healthy young subjects rose significantly or not. Also because students often attribute failing an examination to emotion or anxiety, I wanted to see if there was any relationship between central temperature changes related to examination stress and the scores obtained by the students. METHODS The study was carried out, after informed consent, on 108 students registered in the second year of medical studies. There were
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FIG. 1. Regression analysis of the differences between the Tc before the examination and the Tc before the laboratory demonstration and the average grade of examination in anatomy, biochemistry and histology in the previous year of medical studies. The equation for the regression line is: y = 11 + 2.3 X; r = 0.292;p < 0.01. 98 males and 10 females. Ages ranged from 18 to 27 years, the average being 20. Oral temperature was taken in two situations. First, the oral temperature was taken immediately before a written examination (exam) in the physiology course. This course and exam are reputed, among the students, to be very hard and is considered here as an emotional or psychological stress situation. The second temperature measurement was taken at the same hour of the day (17:00) in an adjacent classroom and with the same thermometers, three days after the exam, immediately before a practical laboratory demonstration (practical), with the students as passive observers and under no apparent stress whatsoever. However, during the practical the teacher might have asked a few questions related to the subject. The measurement before this demonstration was taken as the control measurement. The students were not aware of their scores on the physiology exam at the time of the control measurement. Room temperature was 23.3°C in both circumstances. Outside temperature was 26°C.
Procedure The students were called into the examination hall and seated in alphabetical order while they waited for the exam paper. They were then instructed on the procedure to follow. On each desk each student received an envelope bearing his or her name and containing a mercury-in-glass clinical thermometer. At the sound of a bell the students opened the envelope, took the thermometer and put it under the tongue for three and a half minutes. A second bell indicated the end of the measurement when the students placed the thermometer in the envelope. Assistants collected the envelopes with the thermometers for later reading. Each thermometer was read independently by two persons and the mean of the two readings was taken as the true temperature.
Relationship Between Temperature Change Attributable to Psychological Stress and Exam Score Differences (AT) between Tc prior to exam and the Tc prior to the practical were compared with two sets of grades: those obtained at the physiology exam and the average grade obtained in the final examinations of anatomy, biochemistry and histology courses of the previous year of medical studies. A good correlation was found between both sets of scores (r = 0.784; F = 71.73, p =0.0001).
However, a higher A T might be due to a higher temperature prior to the exam or a lower temperature prior to the practical. Since, the difference, if any, between low scoring and high scoring students should be more evident at the extremes of the frequency distribution of scores, I compared successively larger groups of the highest and lowest scoring students. For instance, there were 13 students with a score equal or superior to 13.75 on the physiology exam. That constituted a group which was compared with a group of 14 students with a score equal or inferior to 2.2 (Table 1). The next two groups were constituted by the 19 students with a score equal or superior to 11.55 and the 19 students with a score equal or inferior to 2.75. O f course, the group of 19 students with scores equal or superior to 11.55 included the 13 students with scores equal or superior to 13.75. Also the group of 19 students with scores equal or inferior to 2.75 included the 14 students with scores equal or inferior to 2.2. The same method was followed to constitute the remaining 10 groups in Table 1 and Table 2. Two comparisons were made: one, the difference A T between comparable groups of high score and low score students (Table 1) and, two, the T,. prior to the exam compared with the T~ prior to practical within the same group (Table 2). RESULTS Mean oral temperature immediately before the exam was 37.4 ___ 0.033°C and the mean temperature before the nonstressful practical was 37.22 _ 0.028°C. This difference was significant (one-tailed paired t = 8.136, p < 0.0001). The mean Tc in the 98 male students was 37.47°C ___ 0.033 prior to exam and 37.21°C ___ 0.029 prior to practical. In the 10 female students the mean Tc prior to exam was 37.60°(: ___0.034 and 37.30°C ___0.03 prior to the practical. These differences between male and female students were not statistically significant (t = 0.03, N.S.). A regression analysis showed a small but significant relationship between A T and both sets of scores (physiology exam scores and average grade in the first previous year of studies). For physiology
TABLE 1 DIFFERENCE IN TEMPERATURE PRIOR TO EXAMINATION AND PRIOR TO LABORATORY DEMONSTRATION (A T): COMPARISON BETWEEN LOW SCORING STUDENTS (LS) AND HIGH SCORING STUDENTS (HS) n
A T(°C)
Physiology examination 13 HS 0.39 14 LS 0.11 19 HS 0.35 19 LS 0.18 28 HS 0.35 29 HS 0.21
t
p
2.50
0.014
2.09
0.021
1.76
0.041
Average Anatomy, Biochemistry, Histology 20 HS 0.31 2.96 0.002 20 LS 0.05 28 HS 0.35 3.24 0.001 25 LS 0.06 36 HS 0.32 2.80 0.003 31 LS 0.11 43 HS 0.32 1.56 N.S. 44 LS 0.2
EMOTIONAL HYPERTHERMIA
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TABLE 2 ORAL TEMPERATURE PRIOR TO EXAMINATION (Tex) AND PRIOR TO LABORATORY DEMONSTRATION (T dem) IN HIGH SCORING AND LOW SCORING STUDENTS n
Tex (°C)
Tdem (°C)
t
p
High Scoring Students Physiology examination 1 13 37.48 37.09 2 19 37.49 37.14 3 28 37.50 37.15
4.18 5.09 6.12
< .002 < .0002 <.0002
Average Anatomy, 4 20 5 28 6 36 7 43
5.66 6.56 6.68 7.49
< .0002 < .0002 < .0002 < .0002
Low Scoring Students Physiology examination 8 14 37.43 37.32 9 19 37.45 37.27 10 29 37.48 37.27
1.40 2.87 3.84
N.S. < .02 <.001
Average Anatomy, 11 20 12 25 13 31 14 44
1.33 1.33 1.98 4.22
N.S. N.S. <.03 <.0002
Biochemistry, Histology 37.49 37.18 37.53 37. i 8 37.49 37.17 37.50 37.18
Biochemistry, Histology 37.34 37.29 37.35 37.29 37.42 37.31 37.48 37.27
n = number of individual in successively larger groups of high and low scoring students. Each larger group includes the students from the preceding smaller group. For example in the 28 students with the high scores in row 3 the 19 of the row 2 were included; and in the 19 students of row 2 the 13 highest scoring students of row 1 were included. scores r = 0.295, F(1,55) = 5.243, p < 0.03. AT on average grades regression analysis is given in Fig. 1 (r = 0.292; F(1,85) = 7.895, p < 0.006). Table 1 shows that the difference between the Tc prior to the exam and the Tc prior to the practical (AT) was significantly larger for the high scoring students with respect to the low scoring students. However, Table 2 shows that in low scoring students the A T was smaller not because the Tc was lower prior to the exam, that is, not because they had a smaller emotional hyperthermia prior to exam, but because the Tc was almost as high prior to the practical than prior to the exam. In the extreme low scoring students the difference between the Tc prior to exam and prior to practical (rows 8, 11 and 12 in Table 2) was not significant. DISCUSSION
There are two points to be addressed here: the emotional hyperthermia and the relationship between temperature and the students' performance. The results show that in an emotional situation, as that before an academic examination, oral temperature of young healthy humans rises in an appreciable and statistically significant way. The earlier studies suggested that emotional hyperthermia may or may not exist in humans. The present report firmly establishes the phenomenon. The main problem with this kind of study is to establish a reliable reference or control situation. In other words, the dif-
ficulty is to know the " n o r m a l " temperature of the subjects in similar circumstances except for the emotion. Since emotion and anxiety variables are difficult to measure the control situation must be carefully chosen. The lack of this was an almost constant flaw in the earlier studies. For example, in Marazziti et al. (10) the difference between the stress and calm situation temperature was greater than in the present work probably because the procedures were different: in addition to temperature measurement, blood pressure was measured and 20 ml of blood was taken from 12 subjects (but not from the remaining 10). That probably increased the anxiety atmosphere in the exam room. Furthermore, in the calm situation the temperature of all subjects was not taken in the same room or at the same time of day as in the stress situation but individually, 2 or 3 weeks later, after at least 30 min of relaxation, which might have given lower figures for the control measurements and thus increase the difference. The relationship between the temperature and exam score is the second point to be addressed here and is a more complex matter. As shown in Fig. 1 the general tendency was that A T was higher for higher-scoring students. That could be interpreted as indicating that good students are more anxious before the examination than the poor ones. However a more detailed investigation showed that the A T for the high-scoring students was higher because their predemonstration Tc was lower than the predemonstration Tc of low-scoring students. In other words, A T was smaller for the low-scoring students because their predemonstration temperature was almost as high as their preexam temperature. This suggests that the preexamination and predemonstration situations were not perceived as very different by the low scoring students. If we admit that the rise in Tc might be due to anxiety the difference between high and low-scoring students might indicate that " g o o d " students adequately manage their emotions in contrast with the " p o o r " students who appear to be anxious even in ordinary, nonstressful situations. This study is based on the assumption that prior to an exam normal people are anxious. Anxiety might be concomitant with changes in sleep-activity rhythm, eating, ingestion of caffein, drugs or smoking. Each one of these factors could affect the Tc. It is not known if anxiety produces a rise in Tc directly or through one or a combination of those factors or if anxiety is the common determinant of the rise in Tc and the changes mentioned before. However this seems to be a too complex and speculative topic to be discussed here. In conclusion the present results show that an emotional situation can induce a rise in body temperature in humans as it does in animals. This rise in oral temperature was statistically significant but its magnitude may depend on the individual and on what is chosen as a control variable. On the other hand, if we admit that the rise in temperature is related to anxiety, the results suggest that a certain degree of anxiety, as revealed by the rise of body temperature, cannot, in general, explain failure in an exam. On the contrary, it seems that a certain degree of emotion or anxiety could rather be favorable to success. However, when anxiety is present in innocuous as well as stressful circumstances, it could be related to poor performance. ACKNOWLEDGEMENTS
I am most grateful to Ian Woodward and Ana C. Rojas for their help with the manuscript and to Luis Hernandez for pertinent criticisms and help with statistical analysis.
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7. Gotsev, T.; Ivanov, A. Psychogenic elevation of body temperature in healthy persons. Acta Physiol. Hungarica 1:53-62; 1950. 8. Hasan, M. K.; White, A. C. Psycogenic fever, entity or nonentity. Postgrad. Med. 66:152-154; 1979. 9. Kleitman, N. The effect of motion pictures on body temperature. Science 101:507-508; 1945. 10. Lancet. Leading articles. Body temperature and emotions. Lancet 2:475-476; 1960. 11. Marazziti, D.; DiMuro, A.; Castrogiovani, P. Psychological stress •and body temperature changes in humans. Physiol. Behav. 52:393395; 1991. 12. Renbourn, E. T. Body temperature and pulse rate in boys and young men prior to sporting contests. A study of emotional hyperthermia: With a review of the literature. J. Psycosomatic Res. 4:149-175; 1960.