Dynamic Thermography: Analysis of Hand Temperature During Exercise

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1 Annals of Biomedical Engineering, Vol. 26, pp , /98 $ Printed in the USA. All rights reserved. Copyright 1998 Biomedical Engineering Society Dynamic Thermography: Analysis of Hand Temperature During Exercise ALLA ZONTAK, SAMUEL SIDEMAN, OLEG VERBITSKY, and RAFAEL BEYAR The Heart System Research Center, The Julius Silver Institute of Biomedical Engineering, Department of Biomedical Engineering, Technion-Israel Institute of Technology, Haifa, Israel (Received 25 September 1997; accepted 10 June 1998) Abstract Exercise has a noted effect on skin blood flow and temperature. We aimed to characterize the normal skin temperature response to exercise by thermographic imaging. A study was conducted on ten healthy and active subjects (age years) who were exposed to graded exercise for determination of maximal oxygen consumption (V O 2 max), and subsequently to constant loads corresponding to 50%, 70%, and 90% of V O 2 max. The skin temperature response during 20 min of constant load exercise is characterized by an initial descending limb, an ascending limb and a quasi-steady-state period. For 50% V O 2 max, the temperature decrease rate was C/s during a time interval of s and the temperature increase rate was C/s during a time interval of s. The level of load did not influence the temperature decrease and increase rates. In contrast, during graded load exercise, a continuous temperature decrease of C/s was observed throughout the test. In summary, the thermographic skin response to exercise is characterized by a specific pattern which reflects the dynamic balance between hemodynamic and thermoregulatory processes Biomedical Engineering Society. S Keywords Skin temperature, Thermoregulation, Blood flow, Thermography, Exercise. INTRODUCTION Skin temperature is determined by complex interactions between heat conducted through central warm areas, blood perfusion in the superficial and deep skin layers, and heat exchange with the environment at the skin surface. 1,2,4 The effect of exercise on skin blood flow and temperature has been previously studied by several authors and reviewed by Johnson 6 and Kenney and Johnson. 7 Muth et al. 10 and other investigators noted a reduction in blood flow in the skin of the hand during the initial phase of leg exercises, which reversed with continued work. Kirsis 8 obtained similar results and reported more pronounced blood flow changes in subjects Address correspondence to: Professor Rafael Beyar, MD, DSc, Department of Biomedical Engineering, Technion-IIT, Haifa 32000, Israel. Electronic mail: rafael@biomed.technion.ac.il 988 involved in sports. In contrast to the data presented above, Lowenthal et al. 9 reported a significant increase in skin blood flow in the finger and hand with moderately heavy leg exercise. Christensen et al. 4 demonstrated an immediate considerable decrease in finger blood flow in subjects performing leg exercise on a bicycle ergometer. This decrease in blood flow is transient except under strenuous exercise. An initial decrease in temperature with subsequent increase later on has also been observed as reviewed previously. 6,7 According to the interpretations of Johnson 6 and Robinson, 11 at the beginning of exercise the demand of blood flow to muscles results in skin vasoconstriction; however, as body temperature rises, the thermal regulatory processes predominate and the skin blood vessels dilate, increasing blood flow and heat conduction to the skin. Infrared thermography has been widely utilized for visualizing temperature patterns on the skin surface. With the advent of thermographic imaging, it is now possible to take continuous measurements of skin surface temperatures and their changes with a high degree of accuracy. 5 Our goal was, therefore, to characterize the effect of exercise and recovery on the skin temperature responses, at well controlled exercise levels and temperature conditions, as measured by thermography. 3 Since the fingers tips are subjected to the highest temperature variability due to the rich innervation, we selected this site for temperature measurement throughout the study. We hypothesized that leg exercise influences the dynamics of the skin temperature and that the degree of this effect depends on the load. METHODS Experimental Protocol I The study was designed to measure the hand skin temperature under conditions of rest, different levels of physical load bicycle ergometry and recovery from exercise. Each study session was performed at ambient temperature (23 1 ) and humidity (60 10%). Ten active male volunteers (age years; body

2 Exercise Thermography 989 weight kg; height cm) were studied. The subjects rested in a seated position in the examination room for 15 min prior to the beginning of the exercise. Exercise testing was then performed on a calibrated bicycle ergometer MONARK Ergomedic 818E. Thermography of the back of the hands placed over a wooden surface was obtained in the sitting position. The dynamics of temperature in one image pixel covering an area of 1.4 mm 2 of the left hand middle finger were analyzed. This approach was selected since the aim of this study was an analysis of variations over time in a small skin area. The system was calibrated against a black box. Correction for skin emissivity was not required since the focus of this study was the relative changes of temperature, and not the absolute values. Determination of Work Loads by Graded Exercise Test Combined with Respiratory Gas Analysis The subjects underwent a graded exercise test with expired gas analysis prior to the submaximal exercise trials. Workloads were increased by 50 W every 3 min until volitional exhaustion. Expired gas analysis was continuously recorded and data, averaged every 30 s of exercise, were collected using a commercially available system System 4400 Metabolic and Respiratory Diagnostics. Variables included oxygen consumption, carbon dioxide production and respiratory exchange ratio. Oxygen consumption (V O 2 ) was assessed at the end of each workload and at maximum effort. The moment of physical exhaustion was considered as a moment of V O 2 max achievement. Average typical values are given in Table 1. Linear regression was used to relate oxygen consumption to the level of load. Oxygen consumption values equal to 50%, 70% and 90% of V O 2 max were calculated and loads corresponding to these values of oxygen consumption were selected. Experimental Protocol II In this session, the dynamics of hand surface temperature under conditions of rest followed by constant load 50% and 70% of V O 2 max) was studied. The recording session lasted 640 s at rest and 1280 s under load conditions. Since the total duration of the measurements was limited to a period of 20 min, slow oscillations at very low frequencies could not be detected. Every 10 s an infrared image which consisted of an average of 32 images was obtained. Since the temperature changes were relatively slow, this digitizing rate of 6 images per min was appropriate, allowing detection of temperature variations with frequencies of up to 3 per min. TABLE 1. Average V O 2 max and time to V O 2 max. AVG Statistical Procedures All the results obtained in the experiment were presented as mean and standard error of the mean SEM. Student t-tests were applied to compare between two sets of observations. Linear regression and correlations were used here to study the nature of relationship between the variables. P level of 0.05 was accepted as significant. RESULTS Graded Load Experiment (Experimental Protocol I) During the graded load experiment to determine V O 2 max, thermographic images over the initial 720 s of exercise, which was common for all subjects, were analyzed. The thermographic images with color coded temperature maps for one subject under conditions of graded load are presented in Fig. 1. Note that the finger tip temperature as well as the entire hand temperature decreases throughout the experiment. Figure 2 upper panel presents the temperature data for ten subjects, obtained from the left hand middle finger tip. Almost all the curves show a continuously decreasing trend. The average temperature SEM is presented in Fig. 2 lower panel. The average rate of temperature decrease calculated by using a linear regression for each subject was C/s. Rest and Steady State Experiments (Experimental Protocol II) SEM Age (years) Height (cm) Weight (kg) V O 2 max (ml/min) Time to V O 2 max(min) The subjects were seated at rest until steady state conditions were achieved. Figure 3 top panel presents the temperature data obtained during 640 s for the same ten subjects presented in Fig. 2. The data show that, in general, steady state is achieved 500 s after the beginning of the study. This assures that the data during exercise are all started from similar baseline conditions. Figure 3 bottom panel presents the mean temperature and standard error SEM at rest. The mean temperature at rest was C. The subjects were then subjected to a load corresponding to 50% V O 2 max for 1280 s. Three subjects did not complete the exercise protocol and only data for seven subjects are presented in Fig. 4. The finger tip temperature reached its minimum after 7 min of exercise

3 990 ZONTAK et al. FIGURE 1. An example of thermographic data, obtained under graded load conditions. Note that the hand temperature drops continuously throughout the exercise.

4 Exercise Thermography 991 FIGURE 2. Temperature curves of ten subjects during graded load upper panel and their average values with the standard error of the mean, SEM lower panel. and increases afterwards until 15 min. During the last 5 min of the study the temperature reached steady state. Five curves out of seven had a typical minimum. The rate of temperature decrease and increase and the duration of the two processes were calculated. The temperature decrease rate was C/s during a time interval of s and the temperature increase rate was C/s during a time interval of s. Under loads corresponding to 70% V O 2 max, the same characteristics of the temperature response were obtained. The average decrease rate was C/s and the average increase rate was C/s. There was no statistical difference in both the decrease and increase rates between the loads corresponding to 50% and 70% V O 2 max. The time intervals of temperature decrease and increase phases were and s, respectively. It was found that for all exercise intensities the rate of temperature decrease depended on the initial finger temperature. Figure 5 a shows the relationship between the rate of temperature decrease and the initial temperature. Note that for greater initial finger temperature, a greater FIGURE 3. Temperature curves of ten subjects under conditions of rest upper panel and their average values lower panel with the standard error of the mean, SEM. temperature decrease rate is obtained. Linear regression data for the case of graded load Fig. 5 a and for the case of load corresponding to 50% V O 2 max Fig. 5 b shows the relationships between the rate of temperature decrease and the initial finger tip temperature. While the data points are dispersed the relationship is statistically significant in the graded load experiments (n 9, p 0.05) and shows a similar trend for the 50% load experiments (n 5, p 0.1). DISCUSSION Exercise is associated with large hemodynamic changes involving multiple regulatory processes. Since exercise is tightly linked to hemodynamic changes and to heat generation within the body, marked alternations in thermoregulatory processes during exercise are expected. These thermoregulatory processes may be reflected in the dynamics of skin temperature during exercise. A comprehensive review of the thermoregulatory processes associated with exercise and their effects on skin blood

5 992 ZONTAK et al. FIGURE 4. Temperature curves of seven subjects under load corresponding to 50% V O 2 max upper panel and their averaged values with the standard error of the mean, SEM lower panel. flow and temperature has been conducted recently. 6,7 The skin plays a principal role in the maintenance of a constant body temperature. The delivery of heat from the deeper parts of the body to the skin is accomplished primarily by the blood circulation. Skin blood flow can change a hundred fold through its rich sympathetic innervation, as well as through other mechanisms, in accordance with the need for heat dissipation or conservation. In the current study, which is the first one providing thermographic imaging during exercise, it was shown that the dynamics of skin temperature response during exercise depends on the type of exercise graded versus constant load. During graded exercise, where the load on the body is constantly increasing, causing a continuously increased demand from the working organs, the temperature of the fingers continuously decreases throughout the exercise period. Since the blood pressure constantly increases during exercise, 12,13 it is likely that the continuous decrease in finger temperature is caused by a continuous skin vasoconstrictor response, due to an FIGURE 5. a Relationship between the rate of temperature decrease and the initial finger temperature for the graded load experiment. Slope , intercept p <0.05, r 0.8. b Relationship between the rate of temperature decrease and the initial finger temperature for 50% load case. Slope , intercept p<0.1, r 0.8. increase in catecholamine and other vasoconstrictor hormones as exercise intensity increases. 12 Contrary to the graded exercise, the skin temperature curve obtained during 20 min of steady load exercise can be divided into three parts: initial descending limb of min; ascending limb of min and a steady state period of min. This pattern of temperature response is consistent with previous observations. 6,7,11 It has been suggested that at the beginning of work the demand of blood flow to working muscles leads to skin reflex vasoconstriction, but as the body temperature rises, the thermal demand predominates and the skin vessels dilate, increasing heat conduction to the skin. This pattern is achieved at moderate 50% V O 2 max) or severe 70% V O 2 max) loads. This pattern may be explained by the typical skin vasoconstrictor response to the initiation of an hemodynamic load, which is then overruled by a vasodilator response, increasing blood flow to the skin. This vasodilator response is probably associated with thermal regulation of

6 Exercise Thermography 993 the body and the increase in core body temperature typically obtained during exercise. The observation that under continuously increasing load, such as occurs in the graded load experiment, there is a continuous temperature decrease without a vasodilator phase such as occurs in graded load exercise is, to the best of our knowledge, new. It is suggested that the increasing hemodynamic requirements present a dominant skin vasoconstrictor stimulus, and that thermoregulation is suppressed under these conditions. Attempts to study the changes in skin blood flow due to exercise have been reported by several authors and have been recently reviewed by Johnson 6 and Kenny and Johnson. 7 Christensen et al. 4 and others have demonstrated an immediate considerable decrease in finger blood flow in subjects performing leg exercises on a bicycle ergometer, which did not persist for longer than several minutes unless the work was very strenuous. Since the alterations occurred practically with the onset of exercise, they were attributed to neuro-reflex mechanisms. Similar results were obtained by Muth et al. 10 who noted a transient reduction in blood flow in the skin of the hand during exercises, followed by an increase, and by Kirsis et al. 8 who reported higher variations of skin blood flow in sportsmen. This is indeed consistent with our observation that in steady state load an initial temperature decrease reflecting vasoconstriction is followed by a temperature increase reflecting vasodilatation. In contrast to the above observations, Lowenthal et al. 9 reported a significant increase in skin blood flow in the finger and hand with heavy leg exercise. A flow decrease at the initial phases of exercise was not observed and the increased flow persisted throughout the 15 min period of observation. According to our results, the intensity of load does not influence the temperature decrease and increase rates and duration of descending and ascending limbs. These data may not be applicable to earlier observations by Kirsis et al. 8 who found that higher loads may be associated with higher skin blood flow levels. We found that the temperature decrease rate depends on initial hand temperature. This observation suggests that when the baseline vasodilator conditions predominate warm hands the hemodynamic recruitment of blood flow by vasoconstriction is larger leading to a more pronounced effect on both skin blood flow and temperature. SUMMARY The response of the skin temperature to exercise has been studied for the first time in normal healthy volunteers using infrared thermography. Graded load exercise results in a constant decrease of finger temperature reflecting the constantly dominating vasoconstrictor response. Steady state exercise causes a similar initial temperature decrease followed by rewarming of hands reflecting dominance of the thermoregulatory reflexes at a later stage of the exercise. The dynamic temperature response to exercise reflects the balance of hemodynamic and thermoregulatory processes and may serve as a tool to noninvasively assess the integrity of these mechanisms in circulatory or other diseases involving thermal and hemodynamic regulation. ACKNOWLEDGMENTS This study was sponsored by the Women s Division of the American Technion Society, NY, and supported by grants from the Michael and Adelaide Kennedy-Leigh Research Fund London, UK and the Deutshe Forschungs Gemeinschaft DFG Guest Professorship to Professor S. Sideman at Karlsruhe University, Germany. REFERENCES 1 Abramson, D. P. I. Circulation in the Extremities. London: Academic, Brengelmann, G. L., J. M. Johnson, L. Hermansen, and L. B. Rowell. Altered control of skin blood flow during exercise at high internal temperatures. J. Appl. Physiol : , Chabanski, S. Spectral Analysis and Filtration of Dynamic Infra-red Images of the Human Body. Technion, Israel: MSc Research Thesis, Christensen, E., M. Nielsen, and B. Hannisdahl. Investigations of the circulation in the skin at the beginning of muscular work. Acta Physiol. Scand. 4:162, Clark, R., M. Goff, and J. Culley. High resolution thermography in medicine. J. Photogr. Sci. 37: , Johnson, J. M. Exercise and the cutaneous circulation. Exercise Sport Sci. Rev. 20:59 97, Kenney, W. L., and J. M. Johnson. Control of skin blood flow during exercise. Med. Sci. Sports Exercise 24 3 : , Kirsis, F. Issledovanie kozhnogo krovotoka v nerabotaushchey konechnosti pri fizicheskoi nagruzke. Teor. Prakt. Fiz. Kul t. 8:29 31, Lowenthal, M., K. Harpuder, and S. Blatt. Peripheral and visceral vascular effects of exercise and postprandial state in supine position. J. Appl. Physiol. 4:689, Muth, H., P. Wormald, J. Bishop, and K. Donald. Further studies of blood flow in the resting arm during supine leg exercise. Clin. Sci. 17:603, Robinson, S. Temperature regulation in exercise. Pediatrics (Suppl.) 32:691, Rowell, L. B. Blood pressure regulation during exercise. Ann. Med. (Helsinki) 23:329 33, Vander, A. Human Physiology. New York: McGraw Hill, 1990, pp. 415, 596.

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