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Kenny, G. P., F. D. Reardon, W. Zaleski, M. L. Rear- have been a number of studies that have reported Tmu
don, F. Haman, and M. B. Ducharme. Muscle tempera- response during exercise (1, 2, 5, 6, 19, 23–27), of which
ture transients before, during, and after exercise measured the study by Saltin et al. (25) seems to be the only one
using an intramuscular multisensor probe. J Appl Physiol 94: to examine changes in Tmu profile (i.e., Tmu measured
2350–2357, 2003. First published February 21, 2003; 10.1152/ at multiple depths). Although, these experiments were
Address for reprint requests and other correspondence: G. P. The costs of publication of this article were defrayed in part by the
Kenny, School of Human Kinetics, Univ. of Ottawa, Rm. 372, Mont- payment of page charges. The article must therefore be hereby
petit Hall, P.O. Box 450 Station A, 125 Univ., Ottawa, Ontario, marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734
Canada K1N 6N5 (E-mail: gkenny@uottawa.ca). solely to indicate this fact.
2350 8750-7587/03 $5.00 Copyright © 2003 the American Physiological Society http://www.jap.org
TISSUE TEMPERATURE TRANSIENTS 2351
subjects as the probe position is standardized within final position of the probe was verified by using the ultra-
the muscle of all subjects. Furthermore, in conjunction sound imaging. The average depth of the probe from the
with a postexercise decrease in heat loss, subsequent to surface was 47.2 mm and within 11.0 mm of both the deep
a decrease in skin blood perfusion, and an attenuation femoral artery and femur. The probe assembly was secured
to the skin with sterile, waterproof transparent dressing (3M
of sudomotor activity during the postexercise recovery
1622W Tegaderm transparent dressing) and tape (total sur-
(14), we hypothesized that convective heat transfer face coverage ⬃25 cm2). The Tegaderm transparent dressing
between muscle and core will significantly influence consists of a thin polyurethane membrane coated with a layer
postexercise core temperature response. of an acrylic adhesive. The dressing, which is permeable to
both water vapor and oxygen, is impermeable to microorgan-
METHODS
isms, and, once in position, it provides an effective barrier to
Subjects. Subsequent to approval of the project by the external contamination.
University Human Research Ethics Committee, seven The temperature probe was a sterile Teflon-coated multi-
healthy subjects (6 men, 1 woman) consented to participate sensor probe (model IT-17:3, Physitemp Instruments; ther-
in the study. Mean values (⫾SD) of the subjects’ age, height, mal constant of 0.25 s). Each probe had three thermocouples:
body mass, maximal oxygen consumption during bilateral one positioned at the tip, one at 15 mm, and the third at 30
concentric knee extensions (V̇O2 sp), and body fat content mm from the tip. The deepest temperature sensor (tip) was
were 24 ⫾ 5 yr, 1.8 ⫾ 0.5 m, 85.6 ⫾ 6.1 kg, 2.1 ⫾ 0.9 l/min, located ⬃10 mm from the femur and deep femoral artery
and 10.9 ⫾ 2.3%, respectively. (Tmu 10), with two sensors located at 15 (Tmu 25) and 30 mm
In each trial, esophageal temperature (Tes) was measured (Tmu 40) from the tip (Table 1). The internal position of the
temperature sensor relative to the skin surface was calcu-
Table 1. Mean (⫾SD) and individual data relating to the placement of the intramuscular multisensor thermal
probe of the upper leg
Insertion Depth From Skin
Surface§
Subject Thigh Thigh Inguinal Base of Medial Probe Tip to Probe Tip
No. Circumference* Length Crease† Femur† Deviation‡ Tmu 10 Tmu 25 Tmu 40 Femoral Artery§ to Femur§
laser-Doppler velocimetry (PeriFlux System 5000, main con- The total work done (Wtotal) was the sum of the work
trol unit; PF5010 LDPM, operating unit; Perimed, Stock- accomplished during each of the contractions during the 15
holm, Sweden) from the left midanterior forearm. The laser- min of exercise.
Doppler flow probes (PR 401 angled probe, Perimed) were Mechanical efficiency (ME) was defined as the Wtotal com-
taped to cleaned skin, in an area that superficially did not pleted during the 15-min exercise period divided by the Mtotal
appear to be highly vascular and from where consistent minus the energy expended under resting conditions (Mrest)
readings were noted (18). Sweat rate was estimated from a (Mtotal ⫺ Mrest). Thus
5.0-cm2 ventilated capsule placed on the upper back. Anhy-
drous compressed air was passed through the capsule over W total
ME ⫽ (3)
the skin surface at a rate of 1 l/min. Water content of the M total ⫺ M rest
effluent air was measured at known barometric pressure by
using the readings from an Omega HX93 humidity and The Mrest was calculated from the average rate of V̇O2 during
temperature sensor (Omega Engineering, Stamford, CT). the 5 min preceding the exercise bout. These values were
Sweat rate was calculated from the product of the difference calculated and expressed in kilojoules by using the aforemen-
in water content between effluent and influent air and the tioned equation.
flow rate. This value was normalized for the skin surface area The total heat load generated by the exercise (HLex) for
under the capsule and expressed in milligrams per minute each subject was calculated by subtracting the Mrest and the
per centimeter squared. energy equivalent of the total mechanical work done (Wtotal)
Subjects performed an incremental isotonic test (constant from the Mtotal. Values are expressed in kilojoules
angular velocity, increases in force output) on the Kin-Com HL ex ⫽ M total ⫺ (M rest ⫹ W total) (4)
isokinetic apparatus to determine their V̇O2 sp. The exercise
冊冉 冊册冎
was likely due to the preparation of the subject for the
兺 再 V̇ 冋冉 (RER ⫺ 0.7) (1 ⫺ RER) exercise portion of the experimental trial.
⫽ O 2䡠 ec ⫹ ef (1)
0.3 0.3 The Tmu profiles, expressed as a function of the
where ṀEx/rest is the rate of energy expenditure during exer- position of the placement of the temperature relative to
cise and recovery, RER is the respiratory exchange ratio, ec is the radius of the thigh (r/rsk), show a parabolic profile
the caloric equivalent (in kJ/l O2) for carbohydrates, and ef is for mean resting tissue temperature profile (Fig. 2).
the caloric equivalent (in kJ/l O2) for fat. This parabolic form of Tmu profile was observed consis-
The minute values were summed for the entire period as tently in the data of all seven subjects (Fig. 3). During
described above. resting, the deep (36.14°C) and mid-Tmu (35.86°C) were
The mechanical work (W) done during each contraction of significantly different from superficial (35.01°C) Tmu.
the exercise phase was measured and recorded by using the As depicted in Fig. 4, the greatest tissue temperature
Kin-Com isokinetic machine. This was calculated from the difference (1.13°C) was between the deep and superfi-
force exerted and the angular displacement during the knee
extension
cial sections of the muscle, with a 0.84°C temperature
gradient between the mid- and superficial muscle.
W ⫽ T (2) Mean tissue temperature difference between deep and
where T is rotational force or torque and is the angular midmuscle was only 0.28°C. Furthermore, the muscle-
displacement. to-core temperature gradient was equal to ⫺0.66,
J Appl Physiol • VOL 94 • JUNE 2003 • www.jap.org
TISSUE TEMPERATURE TRANSIENTS 2353
Fig. 5. Mean (⫾SD) heat load (J) and dry heat loss (ß) responses
(i.e., 38.23, 38.23, and 38.21°C for Tmu 10, Tmu 25, and
sk increased continuously during
Tmu 40, respectively). T
exercise to an end-exercise value that was significantly
elevated above baseline rest (32.79°C, P ⬍ 0.05). The
increase in T sk was paralleled by an increase in non-
evaporative heat loss (i.e., Fig. 5). Forearm skin blood
flow increased continuously during the course of the
exercise.
As depicted in Fig. 2, the tissue temperature profile
Fig. 4. Mean (⫾SE) core-to-muscle temperature gradient (E, deep evolved from a parabolic form typical of resting to a
muscle to core; 䊐, midmuscle to core; ‚, superficial muscle to core) (A) linear profile during the early stages of exercise. By the
and intramuscular temperature gradients (✳, deep muscle to mid- end of exercise, Tmu values across the radial axis were
muscle; {, deep muscle to superficial muscle; ƒ, midmuscle to superficial homogenous. As such, the large temperature gradient
muscle) (B). Vertical dotted lines represent the start (time ⫽ 0 min) and
end (time ⫽ 15 min) of exercise. P ⬍ 0.05: ‡significantly different from
between the deep and superficial muscle was rapidly
the deep to midmuscle temperature gradient; §significantly different reduced such that, by the end of exercise, the temper-
from baseline resting; *superficial-to-core temperature gradient signif- ature at all sites was similar. Furthermore, the mus-
icantly different from deep-to-core temperature gradient. cle-to-core temperature gradient was reversed from
Table 2. Mean (⫾SD) rate of change of esophageal and muscle (Tmu 10, Tmu 25, and Tmu 40) temperatures
during exercise and postexercise recovery
Muscle Temperature
Esophageal
Temperature Tmu 10 Tmu 25 Tmu 40
Exercise
0–3 min 0.022 ⫾ 0.008 0.220 ⫾ 0.091 0.331 ⫾ 0.108 0.547 ⫾ 0.195
3–6 min 0.041 ⫾ 0.009 0.134 ⫾ 0.071 0.137 ⫾ 0.084 0.245 ⫾ 0.099
6–9 min 0.051 ⫾ 0.016 0.059 ⫾ 0.017 0.069 ⫾ 0.023 0.068 ⫾ 0.026
9–12 min 0.038 ⫾ 0.011 0.054 ⫾ 0.015 0.046 ⫾ 0.018 0.056 ⫾ 0.020
12–15 min 0.027 ⫾ 0.009 0.042 ⫾ 0.016 0.043 ⫾ 0.020 0.054 ⫾ 0.021
Postexercise
0–5 min ⫺0.035 ⫾ 0.010 ⫺0.107 ⫾ 0.046 ⫺0.085 ⫾ 0.035 ⫺0.093 ⫾ 0.033
5–10 min ⫺0.006 ⫾ 0.002 ⫺0.034 ⫾ 0.012 ⫺0.041 ⫾ 0.017 ⫺0.045 ⫾ 0.029
10–20 min ⫹0.001 ⫾ 0.007 ⫺0.022 ⫾ 0.010 ⫺0.028 ⫾ 0.009 ⫺0.028 ⫾ 0.011
20–30 min ⫹0.001 ⫾ 0.006 ⫺0.014 ⫾ 0.009 ⫺0.017 ⫾ 0.008 ⫺0.018 ⫾ 0.010
30–40 min ⫺0.003 ⫾ 0.007 ⫺0.005 ⫾ 0.003 ⫺0.006 ⫾ 0.008 ⫺0.010 ⫾ 0.009
40–50 min ⫺0.003 ⫾ 0.002 ⫺0.002 ⫾ 0.001 ⫺0.006 ⫾ 0.004 ⫺0.009 ⫾ 0.007*
50–60 min ⫺0.001 ⫾ 0.005 ⫺0.002 ⫾ 0.004 ⫺0.006 ⫾ 0.005 ⫺0.009 ⫾ 0.007*
Values are means ⫾ SD in °C/min. * Significant difference from deep muscle, Tmu 10 (P ⬍ 0.05).
resting, such that Tmu values at all sites were signifi- exercise period was 15.93 ⫾ 5.98 kJ, whereas, during
cantly elevated above Tes by 0.90, 0.90, and 0.89°C for the 60 min of postexercise recovery, this value was
Tmu 10, Tmu 25, and Tmu 40, respectively (P ⬍ 0.05). 37.90 ⫾ 18.80 kJ.
Postexercise tissue temperature response. Tes de- The kinetics of heat load generation at rest, over the
creased rapidly (⫺0.04°C/min) during the initial min- 15 min of exercise, and over the first 10 min of recovery
utes after the cessation of exercise (Table 2), after are presented in Fig. 5. The corresponding evolution of
which there was a rapid decrease in the rate of tem- dry heat loss is also shown. Thus during the 5 min
perature decrease to negligible values. At ⬃5 min of preceding exercise, the dry heat loss defined relative to
recovery, Tes reached an elevated value 0.35°C above heat load, that is, minus the resting levels, was essen-
baseline resting values (P ⬍ 0.05). For the duration of tially zero. During exercise, the dry heat loss increased
recovery, the rate of decrease of Tes remained at at a rate of 0.14 kJ/min to a maximal level of 2.19
⬃0.001°C/min. Tes decreased to 37.11°C by the end of kJ/min after 15 min of exercise. At cessation of exer-
the 60-min recovery period (⬃0.3°C above baseline). cise, the sensitive heat loss dropped exponentially to a
Tmu showed a similar high rate of temperature de- level ⬃1.0 kJ/min above initial resting values and
crease during the initial 5 min of exercise recovery, remained elevated for the next 10 min. The heat pro-
although the rates were ⬃2 to 2.7 times greater than duction, on the other hand, increased to 17.08 kJ/min
the rate measured for Tes. Unlike the response in Tes, after 2 min of exercise and continued to rise at a rate of
Tmu for all measured sites decreased continuously dur- ⬃0.78 kJ/min for the next 13 min to a maximum heat
ing the initial 30 min of recovery. However, the rates of production of 27.71 kJ/min. Immediately postexercise,
Thus an attempt was made to minimize the variation loss). For example, Aulick et al. (3) previously noted
in temperature recording resulting from individual an- that, as limb sweat rate, cutaneous blood flow, and
atomic differences. muscle-to-skin temperature differences increased dur-
Tmu response: exercise. From the onset of exercise ing exercise, the active leg became a more effective
until the late phases of exercise, there is a gradual vehicle for heat dissipation, and that femoral venous
change in the Tmu profile from one parabolic in the temperature eventually reached a plateau during
form seen at rest to a zero gradient or homogenous steady state. Furthermore, Gisolfi and Robinson (11)
temperature profile across the muscle. As shown in showed that much of the heat produced by active leg
Fig. 4, the large temperature gradient that existed muscles is rapidly transported to surface veins and
between the deep and midportions of the muscle and that this muscle heat is potentially lost across the leg
the superficial muscle was rapidly eliminated during surface. In this study, muscle-to-skin temperature gra-
the first 5 min of exercise. By the end of exercise, the dient remained elevated during the course of the exer-
gradient between the different muscle depths was non- cise by ⬃5.2°C, and skin blood flow and sweat rate
existent, as temperatures across the radial axis of the increased gradually during the course of the exercise.
muscle became homogenous. This effect was not ob- Furthermore, it has previously been shown that, dur-
served earlier by Saltin et al. (24). In that case, it was ing leg work, the inactive upper limbs also act as an
noted that both mid- and superficial Tmu remained avenue for vascular heat loss from the central circula-
generally lower than deep Tmu. Similarly, superficial tion (15), which would further attenuate the increase
Tmu remained lower than mid-Tmu, whereas the tem- in core temperature.
in the postexercise hypotensive response, induced by 8. Ducharme MB and Tikuisis P. Forearm temperature profile
exercise of increasing intensity, was paralleled by an during the transient phase of thermal stress. Eur J Appl Physiol
64: 395–401, 1992.
increase (⬃0.4°C) in the magnitude of the postexercise 9. Ducharme MB and Tikuisis P. Role of blood as heat source or
elevation in Tes (13). It was suggested that the postex- sink in human limbs during local cooling and heating. J Appl
ercise Tes response may be defined to a large degree by Physiol 76: 2084–2094, 1994.
the gradient between the periphery and core and that 10. Ducharme MB, VanHelder WP, and Radomski MW. Tissue
the convective transfer of residual heat from previously temperature profile in the human forearm during thermal stress
active musculature may contribute to the sustained at thermal stability. J Appl Physiol 71: 1973–1978, 1991.
11. Gisolfi C and Robinson S. Venous blood distribution in the
elevation in postexercise Tes. Our observation of a legs during intermittent treadmill work. J Appl Physiol 29:
prolonged elevation in Tmu at values elevated above 368–373, 1970.
esophageal provides further evidence to support this 12. Hardy JD and Dubois EF. The technique of measuring radi-
conclusion. Thus, in the absence of a postexercise in- ation and convection. J Nutr 15: 461–475, 1938.
crease in heat loss response (14), Tes would remain 13. Kenny GP and Niedre PC. The effect of exercise intensity on
the post-exercise esophageal temperature response. Eur J Appl
elevated as long as 1) the heat content of muscle
Physiol 86: 342–346, 2002.
remains higher or equal to that of core; 2) the postex- 14. Kenny GP, Proulx CE, Denis PM, and Giesbrecht GG.
ercise hypotensive effect persists; or 3) a combination Moderate exercise increases the post exercise resting warm
of the two. thermoregulatory response thresholds. Aviat Space Environ Med
Summary. In the present study, exercise was per- 71: 914–919, 2000.
formed such that the dynamic resistance during the 15. Kenny GP, Reardon FD, Ducharme MB, Reardon ML, and