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Effect of bilateral carotid cooling on thermal responses during cycling and arm cranking work due to identical oxygen consumption
ARTICLE IN PRESS
Journal of Thermal Biology 29 (2004) 871–876 www.elsevier.com/locate/jtherbio
Effect of bilateral carotid cooling on thermal responses during cycling and arm cranking work due to identical oxygen consumption Masafumi Toriia,, Zbigiew Szyglab, Masataka Iwashitaa a
Division of Physiological and Biochemical Adaptation, Department of Biological Functions and Engineering, Graduate School of Life Science and Systems Engineering, Kyushu Institute of Technology, Kitakyushu, Japan b Institute of Human Physiology, Department of Sports Medicine, University School of Physical Education, Krakow, Poland
Abstract 1. During the control, tympanic temperature (Tty), skin blood flow (SkBF), local sweating rate (LSR) and heart rate (HR) of the AC were markedly higher than those of the BE. No significant differences were finally observed in rectal (Tre) and mean skin (Tsk) temperatures or oxygen uptake (VO2). In contrast, mechanical work efficiency (ME) was significantly higher in the BE than in the AC. 2. During ice cooling, Tty and the increasing rate in Tty began to be suppressed at 25–35 min after the beginning in both kinds of work. During the AC, SkBF, LSR, HR and mean Tsk in the ice cooling tended to be lower compared those in the control. There were no significant difference between the control and the ice cooling in ME, VO2 or Tre in either kind of work. r 2004 Published by Elsevier Ltd. Keywords: Thermoregulation; Upper- and lower-body exercise; Sweating rate; Skin blood flow; Partial body cooling; Same oxygen consumption; Tympanic temperature
1. Introduction The regulation of heat transfer from the metabolically active tissues to the body surface is one of the most important functions of the thermoregulatory aspect (see review for Nadel, 1985). We have previously reported that the influence of bilateral carotid cooling with ice on the action in the thermoregulatory center activity may cause not only a decrease of wet-heat loss due to sweat Corresponding author. Tel./fax: 0081-93-695-6077 or 0081-
93-884-3455. E-mail addresses: [email protected], [email protected] (M. Torii). 0306-4565/$ - see front matter r 2004 Published by Elsevier Ltd. doi:10.1016/j.jtherbio.2004.08.075
evaporation but also a depression of increase in tympanic temperature (Tty) in leg work due to cycling (Torii et al., 2004, in press). It is not clear how thermoregulatory function adapts to the specific hemodynamic loads associated with this form of exercise bout (see review for Sawka, 1986). The significance of the upper part of the body in our daily living has increased. If the lower part of the body suffers an accident or lowered functioning with advanced age, we need to use the upper part of the body, especially the work of the arms. Clearly, it is important to examine human thermoregulatory responses during muscular work, particularly comparing the upper- and lower-body work. Upper-body work has many applications to the
ARTICLE IN PRESS 872
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rehabilitation and maintenance of thermophysiological responses of individuals who are unable to work their lower body. The purpose of the present study, therefore, is to compare thermoregulatory responses between upperand lower-body work of same oxygen consumption during bilateral carotid cooling with an ice pack.
2. Materials and methods 2.1. Subjects The subjects were seven healthy and untrained men, and their age: 24.774.2 yr, height: 17073 cm, weight: 68.574.0 kg, body fat percent: 12.772.4%, body surface area: 1.8070.06 m2, peak oxygen uptake (VO2peak): 2.1370.20 l min1 in arm work and 3.0970.19 l min1 in cycle work. There was a significant difference in the VO2peak between arm cranking (AC) and bicycle (BE) exercises. None of the subjects took any medication at the time of the study. After careful oral and written explanations, written consent was obtained from all subjects and all of the experimental protocols were approved by the Ethical Committee of our Institute. The experiments were conducted from 11:00 to 13:00 and the subjects came to the laboratory without breakfast. 2.2. Experimental procedures Two to three days after the preliminary test, the subjects, wearing only trunks, exercised for 40 min AC or BE. In these cases, there was no significant difference in VO2 (BE: 1.2770.09 l min1 and AC: 1 1.2370.04 l min , P40.05). Work rate was 5575 W in the AC and 9575 W in the BE (Po0.05). In the experiment the subjects received bilateral carotid cooling with an ice pack (SoftTouch, PI Medical Ltd, USA, 13 mm 120 mm 520 mm, 500 g) in both exercises. All experiments were carried out in a climatic chamber in which the ambient temperature was controlled at 32.571.4 1C, and relative humidity was maintained at a constant 5071.1%. To minimize the effect of the season (Torii et al., 1996) on thermoregulatory response, the four exercise experiments were performed between last July and August, with the order randomized. 2.3. Measurements Unilateral (right) Tty, rectal (Tre) and skin (Tsk) temperatures, skin blood flow (SkBF), local sweat rate (LSR) oxygen uptake (VO2), and heart rate (HR) were continuously measured. Tty, Tre and Tsk were spontaneously recorded every minute by a thermistor recording system (Hybrid Recorder K380, Technoseven Co., Yokohama, Japan) throughout the experimental period.
Calculations of mean Tsk and mean body temperature (Tb, 0:9T ty þ 0:1T sk and 0:8T re þ 0:2T sk ) were partially described in our previous work (Torii et al., 1996). HR was continuously recorded by an electrocardiography with a telemeter system (Life Scope 6, Nihon Koudn, Tokyo). SkBF was continuously determined by a laser Doppler flowmeter (ALF21, Advance Co., Tokyo, Japan) at rest and during exercise after the beginning of exercise. The location of the censor probe for determining SkBF was on the cervical vertebra aspect of the back, according to Smolander et al. (1991). SkBF was indicated by change of SkBF (DSkBF, %) against resting conditions. Local SR at the location as well as the censor probe for determining SkBF was continuously determined by the ventilated capsule method using a hygrometry (Kenz-Perspiro OSS-100, Suzuken, Nagoya, Japan). Air under the atmosphere was pumped through the sweat capsule (area, 1.0 cm2) at the rate of 0.3 l min1. The humidity of air gas flowing out of the capsules was measured with the hygrometer. The distance between the capsule and the humidity censor was 120 cm, and the time delay for the measurement was 0.2 s. In each experiment, the base line of the humidity (zero-point) throughout Silica Gel, medium granular with blue (Wako Pure Chemical Industries, Ltd., Osaka, Japan) was decided. VO2 was measured via open-circuit spirometry by using an automated metabolic analysis system (Benchmark, 505 Type, P.K. Morgan, UK). Measurements were obtained at rest and during exercise at 1-min intervals, breath by breath. Commercially available microcomputer-based software was used to register the data every minute and to convert the values of VO2 and CO2 production into STPD units. M was estimated by the following equation: M ¼ VO2 5:0 60=A; where VO2=oxygen consumption in l min1; 5.0 (or 4.8)=caloric value produced by consumption of l.0 l oxygen during exercise (or rest) in kcal; A=body surface area in m2. The values of M were converted into watts per m2 of the body surface (W m2). After the onset of the exercise, VO2 rapidly increased which was greater in the AC than in the BE. There was no significant difference in oxygen consumption (BE, n=14: 1.2770.09 l min1 and AC, n=14: 1.2370.04 l min1, P40.05, paired t-test) in the final stage of either exercises with or without the ice pack. Mechanical work efficiency (ME) was defined as the work rate (W) used during the 40-min exercise period divided by the Mex minus the energy expended under resting conditions (Mrest) (MexMrest). Thus, ME=W/ (MexMrest). The Mrest was calculated from the average rate of O2 during the 5 min preceding the exercise bout. These values were calculated and expressed in watts per square meter (W m2) by using the aforementioned equation.
ARTICLE IN PRESS M. Torii et al. / Journal of Thermal Biology 29 (2004) 871–876
2.4. Statistical analysis All the data were expressed as mean7SE, and statistically significant difference between mean values were assessed by one-way (control-by-experimental, bilateral carotid cooling, two-way (the cooling-by-work type) analysis of variance (ANOVA) and paired t-test. P value for significance was set at 0.05.
Tty (°C)
37.6
873
Experimental (A) F[1,36]=22.73, P=0.0001 Work type (B) F[1,36]=5.275, P=0.0278 A x B F[1,36]=0.16, P=0.6913 Two-way ANOVA test
37.4 37.2
BE-CONTROL BE-COOLING AC-CONTROL AC-COOLING
37.0 36.8
3. Results (A)
3.1. Effect of ice cooling on T ty during BE and AC
3.2. Effect of ice cooling on LSR during BE and AC As soon as the subjects started, the rise in sweat secretion was observed in all subjects, and cooling experiments in both exercises, too (Fig. 1C). The LSR tended to a greater variance between the subjects, especially in the BE. In the control experiments, LSR in the AC was significantly higher than that in the BE at the final stage (31st min to 40th min). During the BE, LSR decreased with ice cooling in comparison with the control, especially after the medium through experi-
∆Tty (°C)
Experimental (A) F[1,36]=9.572, P=0.0038 Work type (B) F[1,36]=95.75, P=0.0001 A x B F[1,36]=0.005, P=0.943
0.6 Two-way ANOVA test
0.4 0.2 0
(B) 2.5
LSR (mg . cm-2. min-1)
At the end of the rest period, Tty was 36.9470.05 1C (mean7SE, n=14) in the BE and 36.8570.08 1C (n=14) in the AC. In the later period of exercise, Tty increased linearly for both tasks of the control. During the ice cooling, the change of Tty (DTty) began to be suppressed at the 25th–35th min after the beginning of the BE, and the 20th–25th min after the beginning of the AC. Finally, throughout the AC the Tty was constantly higher than in BE (Fig. 1A). Two-way ANOVA revealed a significant difference for work type (F[1,36]=5.275, P=0.0278). Moreover, ANOVA on cooling effect revealed a significant difference between control and experimental (F[1,36]=22.73, P=0.0001). Furthermore, the DTty was significantly different higher in the AC (0.8170.13 1C, mean7SE) than in the BE (0.677 0.11 1C) (two-way ANOVA, experimental (A) F[1,36]= 9.572, P=0.0038, work type (B) F[1,36]=95.75, P=0.0001, and interaction (A B) F[1,36]=0.005, P=0.943)(Fig. 1B). The same tendency was Tb (Tty0.9+Tsk0.1) in comparison with Tty trends in both works. During the AC Tsk was relatively elevated in both tasks. At the end of the AC and BE, it was 35.470.2 1C and 35.870.3 1C, respectively, with cooling (Po0.05, vs. control, respectively). The change of Tsk was slightly greater (NS) during the AC than in the BE with the cooling. No significant differences were finally observed in Tre and mean Tsk, between the AC and the BE. There were no significant differences of final mean Tre without or with the ice cooling in either kind of work.
0.8
2.0
Two-way ANOVA test
1.5
Experimental (A) F[1,36]=147.4 P=0.0001 Work type (B) F[1,36]=121.5, P=0.0001
A x B [1,36]=91.5,
P=0.0001
1.0
0.5 EXERCISE & COOLING
0 -10 -5
(C)
0
5
10
15 20 25
30 35 40
45
TIME (min)
Fig. 1. Tympanic temperature (A, Tty), change of Tty (B, DTty), local sweating rate (C, LSR) during bicycle (BE, squares) and arm crank (AC, circles) exercise with (closed symbols) and without (open symbols) the ice cooling. The data indicate mean values, and omit one standard error of mean (SE). In A the ranges of one SE in the AC and BE are 0.16 and 0.15 1C, respectively. In B the ranges of one SE in the AC and BE are 0.17 and 0.16 1C, respectively. In C the ranges of one SE in the AC and BE are 0.53 and 0.45 mg cm2 min1, respectively. The results of an ANOVA test in the final stage are indicated at the top in the panel.
mental periods (experimental (A), F[1,36]=147.37, P=0.0001, work type (B), F[1,36]=121.54, P=0.0001, and A B F[1,36]=91.507, P=0.0001, by two-way ANOVA). In contrast, no significant difference was
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observed for LSR at the initial stage (exercise start to 10th min) in either of experimental (control vs. cooling) or work type (AC vs. BE). Two-way ANOVA revealed no significant difference of the experimental (A) F[1,36]=3.871, P=0.0568, work type (B), F[1,36]= 0.569, P=0.4556, and interaction between experimental and work type (A B), F[1,36]=0.384, P=0.5395. However, as applied one-way ANOVA in individuals, LSR in the AC- control vs. cooling did not significantly differ at the final stage (F[1,19]=1.88, P=0.186).
initial stage (F[1,19]=30.19, P=0.0001). Finally, mean DSkBF was approximately1.5- and 5.8-fold against that at rest in the BE and AC, respectively. In the control, the final HR was significantly higher (Po0.05, paired t-test) during the AC (15579) than the BE (13778). At the end of the exercise with the cooling it was 15079 and 13477 beats min1 in the AC and the BE, respectively.
3.3. Effect of ice cooling on SkBF during BE and AC (Fig. 2)
VO2 and M during both tasks increased more rapidly in the AC than in the BE at the initial stage. No significant differences were finally observed in VO2 and M. In contrast, ME was significantly higher in the BE than in the AC (Po0.05, paired t-test). No cooling effect resulted in the ME in either type of work (see Table 1). Two-way ANOVA revealed a significant difference for the experimental (A) (F[1,24]=0.116, P=0.736) and work type (B) (F[1,24]=73.17, P=0.0001) and interaction between experimental and work type (A B) (F[1,24]-0.221, P=0.642). As we estimated %VO2peak in each subject, the values of %VO2peak were significantly higher (Po0.05, paired t-test) in the AC (58.573.8%, n=14) than in the BE (40.471.7%, n=14). Table 1 shows a summary of the above data in the present experiments.
Before exercise average SkBF was 0.1670.03 (mean7SE, n=14) and 0.1570.02 (n=14) volts (P40.05, paired t-test) in the BE and AC, respectively. During the control, DSkBFs in the AC were significantly higher than those of the BE (at all stages, Po0.05 paired t-test). DSkBF increased quickly the first min at the onset of the exercise in the both works, especially in the AC, and after it accumulated progressively until the 10th min in the BE, but not in the AC. DSkBF in both the experiments (control and cooling) was reached a steady state in the BE, but DSkBF in the AC increased progressively until the end of the exercise. There were significant differences in DSkBF between the control and the ice cooling in the AC, but no cooling effect was observed in the BE in the final stage, except for the
3.4. Effect of ice cooling on M and ME
Table 1 Summary table on thermophysiological variables at the final stage (31st–40th min) in the BE and AC
600 mean±SE
AC vs. BE 400
Cooling effect AC
BE
=a o
4b oc o 4 4 = 4 4 4
+ + + + +
+ + + + +
*
200
BE-CONTROL BE-COOLING
0
AC-CONTROL AC-COOLING
EXERCISE -5
0
5
10
15
20
25
30
35
40
45
VO2 (M) in final stage (in initial stage and steady stage) % VO2peak WR ME Tty DTty Tsk LSR SkBF HR
TIME (min) Fig. 2. Skin blood flow (DSkBF, % from rest) during bicycle (BE, squares) and arm crank (AC, circles) exercise with (closed symbols) and without (open symbols) the ice cooling. Data represent mean7SE. *Po0.05, significantly different, control vs. cooling in the AC. y Po0.05, significantly different, BE vs. AC in the control. z Po0.05, significantly different, BE vs. AC in the cooling (by paired t-test, all).
+, Effect, and , no effect. VO2=Oxygen uptake, M=Metabolic rate, %VO2peak=% of peak VO2, WR=work rate, ME=mechanical work efficiency, Tty=tympanic temperature, DTty=change of Tty, LSR=local sweating rate, SkBF=skin blood flow. a No significant difference, b higher in the AC, and c higher in the BE.
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4. Discussion
4.2. Cooling vs. no cooling
The present study demonstrates the differential effect of thermoregulatory effecter responses between upperand lower-body works due to same absolute VO2, e.g., Tty, DTty, LSR, HR, and SkBF by a laser Doppler flowmeter. Furthermore, no differences are observed LSE in the AC and SkBF in the BE with bilateral carotid cooling used an ice pack.
Temperature regulation in humans during exercise reflects a control system with effector responses being proportional to afferent input, particularly the temperature of the body core and the skin (Nadel, 1985). The temperature of blood reaching the brain (Tbrain) is regarded as a major afferent stimulus for the intensity of the effector responses of sweating and vasomotor activity. To estimate Tbrain in humans, measurement sites other than the brain have frequently been utilized, including the tympanic membrane. Tty is an index of Tbrain in circulating blood in the brain (Cabanac et al., 1987). We continuously cooled with an ice pack at the bilateral carotid during upper- and lower-body exercise. As soon as our subjects started in both AC and BE, partial cooling was performed using the ice pack at the bilateral carotid (see Fig. 1A and B). Young et al. (1987) have reported that effect of varying the body surface area being cooled by a liquid microclimate system was evaluated during arm crank and locomotor exercises under heat-stress, and concluded that cooling arms during arm crank exercise provided no thermoregulatory advantage, although cooling the thigh surfaces during walking did. We previously reported thermoregulatory effector responses in healthy young men during bicycle exercise for 40 min, with and without an ice pack after 20 min of the exercise initiation (Torii et al., 2004). We tested whether partial body cooling has a positively effective when thermal responses at a given work load (60–70% of their VO2peak) increase at 30 1C and an rh of 40%. After ice cooling, core temperature (Tty) and sweating rate were significantly decreased, and thermal sensation as an index of non-autonomic regulation was significantly increased in comparison with no cooling. We concluded that the effect of bilateral carotid cooling on the action in the thermal regulatory center may be not only a decrease of wet-heat loss due to sweating rate but also a depression of increase in core temperature. Similarly, as shown in the Fig. 1 A and B and Table 1, core and skin temperature decreased with the cooling using an ice pack at the bilateral carotid in the present experiment. It is suggested that the classical hypothesis has been proposed by Robinson (1974), which is ‘‘neuromuscular reflex’’ may take part in thermoregulatory effector response, especially sweating regulation during muscular work. Moreover, Rowell (1986) suggests that central command from the motor cortex systems modulates non-thermal afferent information from peripheral sensors. Moreover, this phenomenon may combine with thermal information from lowered core and skin temperatures with the cooling. As shown in Table 1, no cooling effects were observed in thermoregulatory effector responses, LSR in the BE or SkBF in the AC, in spite of reduced core temperature.
4.1. BE vs. AC There are many results of investigations on the thermoregulation connected with the lower body exercise such as leg work like cycling or running as compared with those from upper body exercise such as arm cranking and wheel chair work, as previous reviewed by Sawka (1986). In this study, the mean values with one SE for Tty and DTty during exercise at two different work types are presented in Fig. 1A and B. After 20 min of the exercise initiation, tympanic temperature in the AC is higher than it is in the BE. In turn, ME in the AC is markedly lower than in the BE, because of Tty increases in the AC as compared with the BE, in spite of the same metabolic intensity. Our results agreed with Sawka et al. (1984). In the present study, when humans exercised with identical metabolic work loads, VO2=1.2 l min1 or physical work load, work rate=5575 W in the AC and 9575 W, in the BE, Tty, DTty, LSR, HR, and SkBF were markedly higher in the AC than in the BE. In contrast, ME was significantly higher in the BE than in the AC. Moreover, thermal responses were induced according to relative metabolic intensity (%VO2peak, 58.573.8% and 40.471.7% in the AC and in the BE, respectively). Thus, thermoregulatory effector responses may be activated in proportion to relative metabolic work intensity (%VO2peak), without regard to upper- and lower-body muscular work. However, as in our previous study, when mild heatstressed humans exercised with same relative work intensity (at 60% of HRmax), Tty and wet-heat loss responses were markedly higher in cycling-work than in arm cranking-work. In this case, work rate was 12575 (mean7SE, n=9) and 5873 (n=8) watts in the BE and AC, respectively. We suggested that thermoregulatory responses might be associated with differential muscle mass (Umeda and Torii, 2003). In circulatory regulation, the characteristics of the upper-body exercise were lower VO2 and higher HR and cardiac output at the same work intensities as for the lower-body exercise (Miles et al., 1984). In our experiment circulatory control has taken part in sympathetic neural control (Rowell, 1986) to effect rapid increase of DSkBF in the initial stage in both the tasks. Similarly, VO2, and HR accumulations also have been sharply enhanced in the upper-body exercise.
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The mechanisms underlying the increase in sympathetic nerve activity to control the activity of eccrine sweat glands and vasoconstriction and vasodilation during exercise are not completely understood. The present results, therefore, indicate that carotid cooling in the absence of a reduced core temperature is effective in reducing thermal strain and increasing the performance in a 40 min-exercise in the hot temperature conditions.
References Cabanac, M., Germain, M., Brinnel, H., 1987. Tympanic temperatures during hemiface cooling. Eur. J. Appl. Physiol. 56, 534–539. Miles, D.S., Sawka, M.N., Hanpeter, D.E., Poster Jr., J.E., Doerr, B.M., Frey, M.A.B., 1984. Central hemodynamics during progressive upper- and lower-body exercise and recovery. J. Appl. Physiol.: Respirat. Envion. Exercise Physiol. 57, 366–370. Nadel, E.R., 1985. Recent advances in temperature regulation during exercise in humans. Fed. Proc. 44, 2286–2292. Robinson, S., 1974. Physiology of muscular exercise. In: Mountcastle, V. (Ed.), Medical Physiology, vol. II. Saint Louis, The C.V. Mosby Comp., pp. 1273–1304. Rowell, L.B., 1986. Human Circulation. Regulation During Physical Stress. Oxford Univ. Press, New York. Sawka, M.N., 1986. Physiology of upper body exercise. Exer. Sprots Sci. Rev. 14, 175–211. Sawka, M.N., Pimental, N.A., Pandolf, K.B., 1984. Thermoregulatory responses to upper body exercise. Eur. J. Appl. Physiol. 52, 230–234.
Smolander, J., Saalo, J., Korhonen, O., 1991. Effect of work load on cutaneous vascular response to exercise. J. Appl. Physiol. 71, 1614–1619. Torii, M., Yamasaki, M., Sasaki, T., 1996. Effect of prewarming in the cold season on thermoregulatory responses during exercise. Br. J. Sports Med. 30 (2), 102–111. Torii, M., Adachi, K., Miyabayashi, M., Arima, T., Iwashita, M., 2004. Effect of bilateral carotid cooling with an ice on thermal responses during bicycle exercise. In: Tochihara, Y. and Ohnaka, T. (Eds.), Environmental Ergonomics: The Ergonomics of Human Comfort, Health and Performance in the Thermal Environment, Elsevier Science, London, UK, in press. Umeda, K., Torii, M., 2003. Thermoregulatory responses during upper and lower body exercise at the same relative work intensity. Proceeding of the 18th Symposium on Biological and Physiological Engineering, 6–8 October 2003, Niigata, pp. 25–28 (in Japanese). Young, A.J., Sawka, M.N., Epstein, Y., Decristofano, B., Pandolf, K.B., 1987. Cooling different body surfaces during upper and lower body exercise. J. Appl. Physiol. 63, 1218–1223.
Further reading Torii, M., Umeda, K., Arima, T., Hirakoba, K., Szygula, Z., Abe, T., 2003. Effect of fanning on evaporative heat loss and tympanic temperature during exercise under heat stress. Proceedings of the XVth Triennial Congress of the International Ergonomics Association, Vol. 4, 20–25 September 2003, Seoul, Korea, pp. 368–371.
Journal of Thermal Biology 29 (2004) 871–876 www.elsevier.com/locate/jtherbio
Effect of bilateral carotid cooling on thermal responses during cycling and arm cranking work due to identical oxygen consumption Masafumi Toriia,, Zbigiew Szyglab, Masataka Iwashitaa a
Division of Physiological and Biochemical Adaptation, Department of Biological Functions and Engineering, Graduate School of Life Science and Systems Engineering, Kyushu Institute of Technology, Kitakyushu, Japan b Institute of Human Physiology, Department of Sports Medicine, University School of Physical Education, Krakow, Poland
Abstract 1. During the control, tympanic temperature (Tty), skin blood flow (SkBF), local sweating rate (LSR) and heart rate (HR) of the AC were markedly higher than those of the BE. No significant differences were finally observed in rectal (Tre) and mean skin (Tsk) temperatures or oxygen uptake (VO2). In contrast, mechanical work efficiency (ME) was significantly higher in the BE than in the AC. 2. During ice cooling, Tty and the increasing rate in Tty began to be suppressed at 25–35 min after the beginning in both kinds of work. During the AC, SkBF, LSR, HR and mean Tsk in the ice cooling tended to be lower compared those in the control. There were no significant difference between the control and the ice cooling in ME, VO2 or Tre in either kind of work. r 2004 Published by Elsevier Ltd. Keywords: Thermoregulation; Upper- and lower-body exercise; Sweating rate; Skin blood flow; Partial body cooling; Same oxygen consumption; Tympanic temperature
1. Introduction The regulation of heat transfer from the metabolically active tissues to the body surface is one of the most important functions of the thermoregulatory aspect (see review for Nadel, 1985). We have previously reported that the influence of bilateral carotid cooling with ice on the action in the thermoregulatory center activity may cause not only a decrease of wet-heat loss due to sweat Corresponding author. Tel./fax: 0081-93-695-6077 or 0081-
93-884-3455. E-mail addresses: [email protected], [email protected] (M. Torii). 0306-4565/$ - see front matter r 2004 Published by Elsevier Ltd. doi:10.1016/j.jtherbio.2004.08.075
evaporation but also a depression of increase in tympanic temperature (Tty) in leg work due to cycling (Torii et al., 2004, in press). It is not clear how thermoregulatory function adapts to the specific hemodynamic loads associated with this form of exercise bout (see review for Sawka, 1986). The significance of the upper part of the body in our daily living has increased. If the lower part of the body suffers an accident or lowered functioning with advanced age, we need to use the upper part of the body, especially the work of the arms. Clearly, it is important to examine human thermoregulatory responses during muscular work, particularly comparing the upper- and lower-body work. Upper-body work has many applications to the
ARTICLE IN PRESS 872
M. Torii et al. / Journal of Thermal Biology 29 (2004) 871–876
rehabilitation and maintenance of thermophysiological responses of individuals who are unable to work their lower body. The purpose of the present study, therefore, is to compare thermoregulatory responses between upperand lower-body work of same oxygen consumption during bilateral carotid cooling with an ice pack.
2. Materials and methods 2.1. Subjects The subjects were seven healthy and untrained men, and their age: 24.774.2 yr, height: 17073 cm, weight: 68.574.0 kg, body fat percent: 12.772.4%, body surface area: 1.8070.06 m2, peak oxygen uptake (VO2peak): 2.1370.20 l min1 in arm work and 3.0970.19 l min1 in cycle work. There was a significant difference in the VO2peak between arm cranking (AC) and bicycle (BE) exercises. None of the subjects took any medication at the time of the study. After careful oral and written explanations, written consent was obtained from all subjects and all of the experimental protocols were approved by the Ethical Committee of our Institute. The experiments were conducted from 11:00 to 13:00 and the subjects came to the laboratory without breakfast. 2.2. Experimental procedures Two to three days after the preliminary test, the subjects, wearing only trunks, exercised for 40 min AC or BE. In these cases, there was no significant difference in VO2 (BE: 1.2770.09 l min1 and AC: 1 1.2370.04 l min , P40.05). Work rate was 5575 W in the AC and 9575 W in the BE (Po0.05). In the experiment the subjects received bilateral carotid cooling with an ice pack (SoftTouch, PI Medical Ltd, USA, 13 mm 120 mm 520 mm, 500 g) in both exercises. All experiments were carried out in a climatic chamber in which the ambient temperature was controlled at 32.571.4 1C, and relative humidity was maintained at a constant 5071.1%. To minimize the effect of the season (Torii et al., 1996) on thermoregulatory response, the four exercise experiments were performed between last July and August, with the order randomized. 2.3. Measurements Unilateral (right) Tty, rectal (Tre) and skin (Tsk) temperatures, skin blood flow (SkBF), local sweat rate (LSR) oxygen uptake (VO2), and heart rate (HR) were continuously measured. Tty, Tre and Tsk were spontaneously recorded every minute by a thermistor recording system (Hybrid Recorder K380, Technoseven Co., Yokohama, Japan) throughout the experimental period.
Calculations of mean Tsk and mean body temperature (Tb, 0:9T ty þ 0:1T sk and 0:8T re þ 0:2T sk ) were partially described in our previous work (Torii et al., 1996). HR was continuously recorded by an electrocardiography with a telemeter system (Life Scope 6, Nihon Koudn, Tokyo). SkBF was continuously determined by a laser Doppler flowmeter (ALF21, Advance Co., Tokyo, Japan) at rest and during exercise after the beginning of exercise. The location of the censor probe for determining SkBF was on the cervical vertebra aspect of the back, according to Smolander et al. (1991). SkBF was indicated by change of SkBF (DSkBF, %) against resting conditions. Local SR at the location as well as the censor probe for determining SkBF was continuously determined by the ventilated capsule method using a hygrometry (Kenz-Perspiro OSS-100, Suzuken, Nagoya, Japan). Air under the atmosphere was pumped through the sweat capsule (area, 1.0 cm2) at the rate of 0.3 l min1. The humidity of air gas flowing out of the capsules was measured with the hygrometer. The distance between the capsule and the humidity censor was 120 cm, and the time delay for the measurement was 0.2 s. In each experiment, the base line of the humidity (zero-point) throughout Silica Gel, medium granular with blue (Wako Pure Chemical Industries, Ltd., Osaka, Japan) was decided. VO2 was measured via open-circuit spirometry by using an automated metabolic analysis system (Benchmark, 505 Type, P.K. Morgan, UK). Measurements were obtained at rest and during exercise at 1-min intervals, breath by breath. Commercially available microcomputer-based software was used to register the data every minute and to convert the values of VO2 and CO2 production into STPD units. M was estimated by the following equation: M ¼ VO2 5:0 60=A; where VO2=oxygen consumption in l min1; 5.0 (or 4.8)=caloric value produced by consumption of l.0 l oxygen during exercise (or rest) in kcal; A=body surface area in m2. The values of M were converted into watts per m2 of the body surface (W m2). After the onset of the exercise, VO2 rapidly increased which was greater in the AC than in the BE. There was no significant difference in oxygen consumption (BE, n=14: 1.2770.09 l min1 and AC, n=14: 1.2370.04 l min1, P40.05, paired t-test) in the final stage of either exercises with or without the ice pack. Mechanical work efficiency (ME) was defined as the work rate (W) used during the 40-min exercise period divided by the Mex minus the energy expended under resting conditions (Mrest) (MexMrest). Thus, ME=W/ (MexMrest). The Mrest was calculated from the average rate of O2 during the 5 min preceding the exercise bout. These values were calculated and expressed in watts per square meter (W m2) by using the aforementioned equation.
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2.4. Statistical analysis All the data were expressed as mean7SE, and statistically significant difference between mean values were assessed by one-way (control-by-experimental, bilateral carotid cooling, two-way (the cooling-by-work type) analysis of variance (ANOVA) and paired t-test. P value for significance was set at 0.05.
Tty (°C)
37.6
873
Experimental (A) F[1,36]=22.73, P=0.0001 Work type (B) F[1,36]=5.275, P=0.0278 A x B F[1,36]=0.16, P=0.6913 Two-way ANOVA test
37.4 37.2
BE-CONTROL BE-COOLING AC-CONTROL AC-COOLING
37.0 36.8
3. Results (A)
3.1. Effect of ice cooling on T ty during BE and AC
3.2. Effect of ice cooling on LSR during BE and AC As soon as the subjects started, the rise in sweat secretion was observed in all subjects, and cooling experiments in both exercises, too (Fig. 1C). The LSR tended to a greater variance between the subjects, especially in the BE. In the control experiments, LSR in the AC was significantly higher than that in the BE at the final stage (31st min to 40th min). During the BE, LSR decreased with ice cooling in comparison with the control, especially after the medium through experi-
∆Tty (°C)
Experimental (A) F[1,36]=9.572, P=0.0038 Work type (B) F[1,36]=95.75, P=0.0001 A x B F[1,36]=0.005, P=0.943
0.6 Two-way ANOVA test
0.4 0.2 0
(B) 2.5
LSR (mg . cm-2. min-1)
At the end of the rest period, Tty was 36.9470.05 1C (mean7SE, n=14) in the BE and 36.8570.08 1C (n=14) in the AC. In the later period of exercise, Tty increased linearly for both tasks of the control. During the ice cooling, the change of Tty (DTty) began to be suppressed at the 25th–35th min after the beginning of the BE, and the 20th–25th min after the beginning of the AC. Finally, throughout the AC the Tty was constantly higher than in BE (Fig. 1A). Two-way ANOVA revealed a significant difference for work type (F[1,36]=5.275, P=0.0278). Moreover, ANOVA on cooling effect revealed a significant difference between control and experimental (F[1,36]=22.73, P=0.0001). Furthermore, the DTty was significantly different higher in the AC (0.8170.13 1C, mean7SE) than in the BE (0.677 0.11 1C) (two-way ANOVA, experimental (A) F[1,36]= 9.572, P=0.0038, work type (B) F[1,36]=95.75, P=0.0001, and interaction (A B) F[1,36]=0.005, P=0.943)(Fig. 1B). The same tendency was Tb (Tty0.9+Tsk0.1) in comparison with Tty trends in both works. During the AC Tsk was relatively elevated in both tasks. At the end of the AC and BE, it was 35.470.2 1C and 35.870.3 1C, respectively, with cooling (Po0.05, vs. control, respectively). The change of Tsk was slightly greater (NS) during the AC than in the BE with the cooling. No significant differences were finally observed in Tre and mean Tsk, between the AC and the BE. There were no significant differences of final mean Tre without or with the ice cooling in either kind of work.
0.8
2.0
Two-way ANOVA test
1.5
Experimental (A) F[1,36]=147.4 P=0.0001 Work type (B) F[1,36]=121.5, P=0.0001
A x B [1,36]=91.5,
P=0.0001
1.0
0.5 EXERCISE & COOLING
0 -10 -5
(C)
0
5
10
15 20 25
30 35 40
45
TIME (min)
Fig. 1. Tympanic temperature (A, Tty), change of Tty (B, DTty), local sweating rate (C, LSR) during bicycle (BE, squares) and arm crank (AC, circles) exercise with (closed symbols) and without (open symbols) the ice cooling. The data indicate mean values, and omit one standard error of mean (SE). In A the ranges of one SE in the AC and BE are 0.16 and 0.15 1C, respectively. In B the ranges of one SE in the AC and BE are 0.17 and 0.16 1C, respectively. In C the ranges of one SE in the AC and BE are 0.53 and 0.45 mg cm2 min1, respectively. The results of an ANOVA test in the final stage are indicated at the top in the panel.
mental periods (experimental (A), F[1,36]=147.37, P=0.0001, work type (B), F[1,36]=121.54, P=0.0001, and A B F[1,36]=91.507, P=0.0001, by two-way ANOVA). In contrast, no significant difference was
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observed for LSR at the initial stage (exercise start to 10th min) in either of experimental (control vs. cooling) or work type (AC vs. BE). Two-way ANOVA revealed no significant difference of the experimental (A) F[1,36]=3.871, P=0.0568, work type (B), F[1,36]= 0.569, P=0.4556, and interaction between experimental and work type (A B), F[1,36]=0.384, P=0.5395. However, as applied one-way ANOVA in individuals, LSR in the AC- control vs. cooling did not significantly differ at the final stage (F[1,19]=1.88, P=0.186).
initial stage (F[1,19]=30.19, P=0.0001). Finally, mean DSkBF was approximately1.5- and 5.8-fold against that at rest in the BE and AC, respectively. In the control, the final HR was significantly higher (Po0.05, paired t-test) during the AC (15579) than the BE (13778). At the end of the exercise with the cooling it was 15079 and 13477 beats min1 in the AC and the BE, respectively.
3.3. Effect of ice cooling on SkBF during BE and AC (Fig. 2)
VO2 and M during both tasks increased more rapidly in the AC than in the BE at the initial stage. No significant differences were finally observed in VO2 and M. In contrast, ME was significantly higher in the BE than in the AC (Po0.05, paired t-test). No cooling effect resulted in the ME in either type of work (see Table 1). Two-way ANOVA revealed a significant difference for the experimental (A) (F[1,24]=0.116, P=0.736) and work type (B) (F[1,24]=73.17, P=0.0001) and interaction between experimental and work type (A B) (F[1,24]-0.221, P=0.642). As we estimated %VO2peak in each subject, the values of %VO2peak were significantly higher (Po0.05, paired t-test) in the AC (58.573.8%, n=14) than in the BE (40.471.7%, n=14). Table 1 shows a summary of the above data in the present experiments.
Before exercise average SkBF was 0.1670.03 (mean7SE, n=14) and 0.1570.02 (n=14) volts (P40.05, paired t-test) in the BE and AC, respectively. During the control, DSkBFs in the AC were significantly higher than those of the BE (at all stages, Po0.05 paired t-test). DSkBF increased quickly the first min at the onset of the exercise in the both works, especially in the AC, and after it accumulated progressively until the 10th min in the BE, but not in the AC. DSkBF in both the experiments (control and cooling) was reached a steady state in the BE, but DSkBF in the AC increased progressively until the end of the exercise. There were significant differences in DSkBF between the control and the ice cooling in the AC, but no cooling effect was observed in the BE in the final stage, except for the
3.4. Effect of ice cooling on M and ME
Table 1 Summary table on thermophysiological variables at the final stage (31st–40th min) in the BE and AC
600 mean±SE
AC vs. BE 400
Cooling effect AC
BE
=a o
4b oc o 4 4 = 4 4 4
+ + + + +
+ + + + +
*
200
BE-CONTROL BE-COOLING
0
AC-CONTROL AC-COOLING
EXERCISE -5
0
5
10
15
20
25
30
35
40
45
VO2 (M) in final stage (in initial stage and steady stage) % VO2peak WR ME Tty DTty Tsk LSR SkBF HR
TIME (min) Fig. 2. Skin blood flow (DSkBF, % from rest) during bicycle (BE, squares) and arm crank (AC, circles) exercise with (closed symbols) and without (open symbols) the ice cooling. Data represent mean7SE. *Po0.05, significantly different, control vs. cooling in the AC. y Po0.05, significantly different, BE vs. AC in the control. z Po0.05, significantly different, BE vs. AC in the cooling (by paired t-test, all).
+, Effect, and , no effect. VO2=Oxygen uptake, M=Metabolic rate, %VO2peak=% of peak VO2, WR=work rate, ME=mechanical work efficiency, Tty=tympanic temperature, DTty=change of Tty, LSR=local sweating rate, SkBF=skin blood flow. a No significant difference, b higher in the AC, and c higher in the BE.
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4. Discussion
4.2. Cooling vs. no cooling
The present study demonstrates the differential effect of thermoregulatory effecter responses between upperand lower-body works due to same absolute VO2, e.g., Tty, DTty, LSR, HR, and SkBF by a laser Doppler flowmeter. Furthermore, no differences are observed LSE in the AC and SkBF in the BE with bilateral carotid cooling used an ice pack.
Temperature regulation in humans during exercise reflects a control system with effector responses being proportional to afferent input, particularly the temperature of the body core and the skin (Nadel, 1985). The temperature of blood reaching the brain (Tbrain) is regarded as a major afferent stimulus for the intensity of the effector responses of sweating and vasomotor activity. To estimate Tbrain in humans, measurement sites other than the brain have frequently been utilized, including the tympanic membrane. Tty is an index of Tbrain in circulating blood in the brain (Cabanac et al., 1987). We continuously cooled with an ice pack at the bilateral carotid during upper- and lower-body exercise. As soon as our subjects started in both AC and BE, partial cooling was performed using the ice pack at the bilateral carotid (see Fig. 1A and B). Young et al. (1987) have reported that effect of varying the body surface area being cooled by a liquid microclimate system was evaluated during arm crank and locomotor exercises under heat-stress, and concluded that cooling arms during arm crank exercise provided no thermoregulatory advantage, although cooling the thigh surfaces during walking did. We previously reported thermoregulatory effector responses in healthy young men during bicycle exercise for 40 min, with and without an ice pack after 20 min of the exercise initiation (Torii et al., 2004). We tested whether partial body cooling has a positively effective when thermal responses at a given work load (60–70% of their VO2peak) increase at 30 1C and an rh of 40%. After ice cooling, core temperature (Tty) and sweating rate were significantly decreased, and thermal sensation as an index of non-autonomic regulation was significantly increased in comparison with no cooling. We concluded that the effect of bilateral carotid cooling on the action in the thermal regulatory center may be not only a decrease of wet-heat loss due to sweating rate but also a depression of increase in core temperature. Similarly, as shown in the Fig. 1 A and B and Table 1, core and skin temperature decreased with the cooling using an ice pack at the bilateral carotid in the present experiment. It is suggested that the classical hypothesis has been proposed by Robinson (1974), which is ‘‘neuromuscular reflex’’ may take part in thermoregulatory effector response, especially sweating regulation during muscular work. Moreover, Rowell (1986) suggests that central command from the motor cortex systems modulates non-thermal afferent information from peripheral sensors. Moreover, this phenomenon may combine with thermal information from lowered core and skin temperatures with the cooling. As shown in Table 1, no cooling effects were observed in thermoregulatory effector responses, LSR in the BE or SkBF in the AC, in spite of reduced core temperature.
4.1. BE vs. AC There are many results of investigations on the thermoregulation connected with the lower body exercise such as leg work like cycling or running as compared with those from upper body exercise such as arm cranking and wheel chair work, as previous reviewed by Sawka (1986). In this study, the mean values with one SE for Tty and DTty during exercise at two different work types are presented in Fig. 1A and B. After 20 min of the exercise initiation, tympanic temperature in the AC is higher than it is in the BE. In turn, ME in the AC is markedly lower than in the BE, because of Tty increases in the AC as compared with the BE, in spite of the same metabolic intensity. Our results agreed with Sawka et al. (1984). In the present study, when humans exercised with identical metabolic work loads, VO2=1.2 l min1 or physical work load, work rate=5575 W in the AC and 9575 W, in the BE, Tty, DTty, LSR, HR, and SkBF were markedly higher in the AC than in the BE. In contrast, ME was significantly higher in the BE than in the AC. Moreover, thermal responses were induced according to relative metabolic intensity (%VO2peak, 58.573.8% and 40.471.7% in the AC and in the BE, respectively). Thus, thermoregulatory effector responses may be activated in proportion to relative metabolic work intensity (%VO2peak), without regard to upper- and lower-body muscular work. However, as in our previous study, when mild heatstressed humans exercised with same relative work intensity (at 60% of HRmax), Tty and wet-heat loss responses were markedly higher in cycling-work than in arm cranking-work. In this case, work rate was 12575 (mean7SE, n=9) and 5873 (n=8) watts in the BE and AC, respectively. We suggested that thermoregulatory responses might be associated with differential muscle mass (Umeda and Torii, 2003). In circulatory regulation, the characteristics of the upper-body exercise were lower VO2 and higher HR and cardiac output at the same work intensities as for the lower-body exercise (Miles et al., 1984). In our experiment circulatory control has taken part in sympathetic neural control (Rowell, 1986) to effect rapid increase of DSkBF in the initial stage in both the tasks. Similarly, VO2, and HR accumulations also have been sharply enhanced in the upper-body exercise.
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The mechanisms underlying the increase in sympathetic nerve activity to control the activity of eccrine sweat glands and vasoconstriction and vasodilation during exercise are not completely understood. The present results, therefore, indicate that carotid cooling in the absence of a reduced core temperature is effective in reducing thermal strain and increasing the performance in a 40 min-exercise in the hot temperature conditions.
References Cabanac, M., Germain, M., Brinnel, H., 1987. Tympanic temperatures during hemiface cooling. Eur. J. Appl. Physiol. 56, 534–539. Miles, D.S., Sawka, M.N., Hanpeter, D.E., Poster Jr., J.E., Doerr, B.M., Frey, M.A.B., 1984. Central hemodynamics during progressive upper- and lower-body exercise and recovery. J. Appl. Physiol.: Respirat. Envion. Exercise Physiol. 57, 366–370. Nadel, E.R., 1985. Recent advances in temperature regulation during exercise in humans. Fed. Proc. 44, 2286–2292. Robinson, S., 1974. Physiology of muscular exercise. In: Mountcastle, V. (Ed.), Medical Physiology, vol. II. Saint Louis, The C.V. Mosby Comp., pp. 1273–1304. Rowell, L.B., 1986. Human Circulation. Regulation During Physical Stress. Oxford Univ. Press, New York. Sawka, M.N., 1986. Physiology of upper body exercise. Exer. Sprots Sci. Rev. 14, 175–211. Sawka, M.N., Pimental, N.A., Pandolf, K.B., 1984. Thermoregulatory responses to upper body exercise. Eur. J. Appl. Physiol. 52, 230–234.
Smolander, J., Saalo, J., Korhonen, O., 1991. Effect of work load on cutaneous vascular response to exercise. J. Appl. Physiol. 71, 1614–1619. Torii, M., Yamasaki, M., Sasaki, T., 1996. Effect of prewarming in the cold season on thermoregulatory responses during exercise. Br. J. Sports Med. 30 (2), 102–111. Torii, M., Adachi, K., Miyabayashi, M., Arima, T., Iwashita, M., 2004. Effect of bilateral carotid cooling with an ice on thermal responses during bicycle exercise. In: Tochihara, Y. and Ohnaka, T. (Eds.), Environmental Ergonomics: The Ergonomics of Human Comfort, Health and Performance in the Thermal Environment, Elsevier Science, London, UK, in press. Umeda, K., Torii, M., 2003. Thermoregulatory responses during upper and lower body exercise at the same relative work intensity. Proceeding of the 18th Symposium on Biological and Physiological Engineering, 6–8 October 2003, Niigata, pp. 25–28 (in Japanese). Young, A.J., Sawka, M.N., Epstein, Y., Decristofano, B., Pandolf, K.B., 1987. Cooling different body surfaces during upper and lower body exercise. J. Appl. Physiol. 63, 1218–1223.
Further reading Torii, M., Umeda, K., Arima, T., Hirakoba, K., Szygula, Z., Abe, T., 2003. Effect of fanning on evaporative heat loss and tympanic temperature during exercise under heat stress. Proceedings of the XVth Triennial Congress of the International Ergonomics Association, Vol. 4, 20–25 September 2003, Seoul, Korea, pp. 368–371.