Articles in PresS. J Appl Physiol (February 21, 2003). 10.1152/japplphysiol.01107.2002
Muscle temperature transients before, during and following exercise measured
using an intra-muscular multi-sensor probe
G.P Kenny1, F.D. Reardon1, W. Zaleski2,
M.L. Reardon2, F. Haman3 and M.B. Ducharme1,4.
Address for correspondence and reprint requests:
G.P. Kenny
University of Ottawa
School of Human Kinetics
125 University, Montpetit Hall
Room 372
Ottawa, Ontario, Canada
PO Box 450 Station A
K1N 6N5
(613) 562-5800 ext. 4282
(613) 562-5149 (fax)
e-mail: [email protected]
Running Head: Tissue temperature transients
Copyright (c) 2003 by the American Physiological Society.
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
University of Ottawa, 1 Faculty of Health Sciences, School of
Human Kinetics, 2Faculty of Medicine, and 3Faculty of Sciences,
Ottawa, Canada, K1N 6N5; and, 1,4Defence R&D Canada - Toronto,
Human Protection and Performance, Toronto, Canada, M3M 3B9.
Tissue temperature transients
Kenny et al.
ABSTRACT
Seven subjects (1 female) performed an incremental isotonic test on a KINCOM• isokinetic apparatus to determine their maximal oxygen consumption during
x
bilateral knee extensions ( V O2sp). A multi-sensor thermal probe was inserted into the left
vastus medialis (mid-diaphysis) under ultrasound guidance. The deepest sensor (tip,
Tmu10) was located ~10 mm from the femur and deep femoral artery with additional
sensors located at 15 (Tmu25) and 30 (Tmu40) mm from the tip. Esophageal temperature
(Tes) temperature was measured as an index of core temperature. Subjects rested in an
x
15 min of isolated bilateral knee extensions (60% of V O2sp) on a KIN-COM• followed
by 60 min of recovery. Resting Tes was 36.80qC while Tmu10, Tmu25, and Tmu40 were
36.14, 35.86 and 35.01oC respectively. Exercise resulted in a Tes increase of 0.55oC
above pre-exercise resting while muscle temperature of the exercising leg increased by
2.00, 2.37 and 3.20oC for Tmu10, Tmu25, and Tmu40 respectively. Post-exercise Tes
showed a rapid decrease followed by a prolonged sustained elevation ~0.3qC above
resting. Muscle temperature decreased gradually over the course of recovery with values
remaining significantly elevated by 0.92, 1.05 and 1.77qC for Tmu10, Tmu25 and Tmu40
respectively at end of recovery (P < 0.05). These results suggest that the transfer of
residual heat from previously active musculature may contribute to the sustained
elevation in post-exercise Tes.
Key words: heat load, thermoregulation, hyperthermia, heat content, and heat balance.
2
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
upright seated position for 60 min in an ambient condition of 22oC. They then performed
Tissue temperature transients
Kenny et al.
INTRODUCTION
A number of studies have examined muscle temperature profiles for resting
conditions under different thermal conditions (4, 7, 8, 17, 20-22, 25, 27, 30, 31). The
study by Ducharme and co-workers (8) however, was the only study to present a mean
muscle temperature profile for a group of subjects as opposed to single depth
measurements.
Despite the large number of studies, there is still no consistent
studies that have reported muscle temperature response during exercise (1, 2, 5, 6, 19, 2327) of which the study by Saltin et al. (31) seems to be the only one to examine changes
in muscle temperature profile (i.e., muscle temperature measured at multiple depths).
Although, these experiments were not designed to show the time course change in tissue
temperature gradients, their measurement of individual intra-muscular temperature
response did show large variations in the temperature at the superficial, mid and deep
muscle sites. Further, they showed significant variation in the rates of temperature
change during muscle activity.
There are no studies that have examined changes in muscle temperature during
the post-exercise period.
Several have reported post-exercise muscle temperature
response (1, 23, 24), however none have specifically addressed these responses. In short,
there remains a lack of information regarding the kinetics of heat exchange between
muscle and the core of the body and within a given mass of muscle tissue.
This
information is critical to our understanding of the underlying mechanism responsible for
the sustained, post-exercise elevation in core temperature.
In previous work, core
3
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
description of resting muscle temperature profile. There also have been a number of
Tissue temperature transients
Kenny et al.
temperature has been shown to remain elevated by ~0.4qC for a prolonged period
following cessation of exercise (16, 28) performed in different thermal environments.
However, the actual mechanism responsible for this increase in core temperature remains
unresolved.
Tissue temperature at any given time is ultimately determined by the relative rates
of heat production and heat loss. For example, regional muscle temperature at any point
in time is the result of regional differences in metabolic rate (9), conductive heat loss to
would be expected that both regional temperature profile and the rate of temperature
change would differ during resting, exercise and post-exercise recovery. The following
study was designed to measure intra-muscular temperature profile during rest, exercise
and post-exercise recovery.
In contrast to the findings of previous studies, we
hypothesized that the tissue temperature profile will be consistent between subjects as the
probe position is standardized within the muscle of all subjects. Further, in conjunction
with a post-exercise decrease in heat loss, subsequent to a decrease in skin blood
perfusion, and an attenuation of sudomotor activity during the post-exercise recovery
(14), we hypothesized that convective heat transfer between muscle and core will
significantly influence post-exercise core temperature response.
METHODS
Subjects
Subsequent to approval of the project by the University Human Research Ethics
Committee, 7 healthy subjects (6 males, 1 female) consented to participate in the study.
x
Mean values (r SD) of the subject’s age, height, body mass, V O2sp during bilateral
4
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
adjacent tissue (9, 10) and deep and peripheral convective blood flow (9, 29). As such it
Tissue temperature transients
Kenny et al.
concentric knee extensions and body fat content were 24 r 5 years, 1.8 r 0.5 m, 85.6 r
6.1 kg, 2.1 r 0.9 l.min-1 and 10.9 r 2.3%.
In each trial, esophageal temperature (Tes) was measured using a thermocouple
temperature probe (Mallinckrodt Medical, USA) inserted through a nostril, into the
esophagus to the level of the heart. Regional muscle temperature of the vastus medialis
was measured using a flexible multi-thermocouple temperature probe (Physitemp
Instruments Inc, Clifton, NJ, USA, Model IT-17:3) inserted into the vastus medialis.
subsequently to place the probe at a position 10 mm and equidistant from the deep
femoral artery and the femur. The implant site was approximately midway between and
medial to a line joining the anterior superior iliac spine and the superior aspect of the
center of the patella.
Using aseptic technique and under ultra-sound guidance, the skin, subcutaneous
tissue and muscle were anesthetized to a maximum depth of 50 mm by infiltrating ~2 ml
of 1% lidocaine without epinephrine. The tip of this 25-gauge needle was placed at the
proposed site for the deep temperature probe. Under full ultrasound imaging and using
the anaesthetic needle as a guide an 18-gauge, 50-mm polyethylene catheter (Cathlon,
Critikon, Canada, Markham, Ontario) was then inserted into the anesthetized tract to the
required depth. The anaesthetic needle and the catheter stylet were then withdrawn and
the temperature probe inserted in the catheter shaft. When the probe was fully inserted,
the catheter was carefully withdrawn leaving the tip of the temperature probe ~10 mm
from the femur and deep femoral artery. Once the catheter was withdrawn the final
position of the probe was verified using the ultrasound imaging. The average depth of
5
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
Ultra-sound imaging was used to discern the best perpendicular insertion tract and
Tissue temperature transients
Kenny et al.
the probe from the surface was 47.2 mm and within 11.0 mm of both the deep femoral
artery and femur. The probe assembly was secured to the skin with sterile, waterproof
transparent dressing (3M™ 1622W Tegaderm™ Transparent Dressing) and tape (total
surface coverage ~25 cm2). The Tegaderm™ transparent dressing consists of a thin
polyurethane membrane coated with a layer of an acrylic adhesive. The dressing, which
is permeable to both water vapour and oxygen, is impermeable to micro-organisms and
once in position, it provides an effective barrier to external contamination.
Instruments Inc, Clifton, NJ, USA, Model IT-17:3; thermal constant of 0.25 sec). Each
probe had 3 thermocouples, one positioned at the tip, one at 15 and the third at 30 mm
from the tip. The deepest temperature sensor (tip, Tmu10) was located ~10 mm from the
femur and deep femoral artery with 2 sensors located at 15 (Tmu25) and 30 (Tmu40) mm
from the tip (Table 1). The internal position of the temperature sensor relative to the skin
surface was calculated based on the ratio of the known depth of the probe (r) from the
skin surface measured by ultrasound imaging and the radius of the thigh (rsk). Thus r/rsk
is the relative radius (8). Although it was not possible to verify the final position of the
probe following the completion of the experimental trial, the length of the probe within
the limb tissue was measured during the removal of the probe. The depth of the probe
was verified with the pre-experiment depth as determined by ultrasound imaging.
Skin temperature was monitored at 12 sites using Type T thermocouples
integrated into heat-flow sensors (Concept Engineering, Old Saybrook, CT). The areaweighed mean skin temperature (CTsk) and heat flux ( HFsk) were calculated by assigning
the following regional percentages: head 6%, upper arm 9%, forearm 6%, finger 2%,
6
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
The temperature probe was a sterile Teflon coated multisensor probe (Physitemp
Tissue temperature transients
Kenny et al.
chest 19%, upper back 9.5%, lower back 9.5%, anterior thigh 10%, posterior thigh 10%,
anterior calf 9.5%, posterior calf 9.5% (12).
Temperature and heat flux data were
collected and digitized (Hewlett Packard data acquisition module, model 3497A) at 5-s
intervals, simultaneously displayed and recorded in spreadsheet format on a hard disk
(Hewlett Packard, model PC-312, 9000).
x
Oxygen consumption ( V O2) was determined by open circuit analysis using an
automated gas collection system (Quinton Instrument Co, Seattle, Washington, USA,
laser-Doppler velocimetry (PeriFlux System 5000, Main control unit; PF5010 LDPM,
Operating unit; Perimed AB, Stockholm, Sweden) from the left mid-anterior forearm.
The laser-Doppler flow probes (PR 401 Angled Probe, Perimed AB, Stockholm, Sweden)
were taped to cleaned skin, in an area that superficially, did not appear to be highly
vascular and from where consistent readings were noted (18). Sweat rate was estimated
from a 5.0 cm2 ventilated capsule placed on the upper back. Anhydrous compressed air
was passed through the capsule over the skin surface at a rate of 1 l.min-1. Water content
of the effluent air was measured at known barometric pressure using the readings from an
Omega HX93 humidity and temperature sensor (Omega Engineering, Stamford, CT,
USA). Sweat rate was calculated from the product of the difference in water content
between effluent and influent air, and the flow rate. This value was normalized for the
skin surface area under the capsule and expressed in mg min-1 cm-2.
Subjects performed an incremental isotonic test (constant angular velocity,
increases in force output) on the KIN-COM• isokinetic apparatus to determine their
x
maximal capacity ( V O2sp). The exercise consisted of bilateral, concentric knee extension
7
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
Model Q-Plex 1 Cardio-Pulmonary Exercise System). Skin blood flow was measured by
Tissue temperature transients
Kenny et al.
over a range of 70o from perpendicular with the subject sitting (hip angle between 90o
and 110o) and the long axis of the thigh in the horizontal plane. The force output was
increased by 15 newtons every two minutes until fatigue while the angular velocity was
maintained at 58.3o sec-1 throughout the test. The results of the test were used to establish
the work rate for the experimental trial. The experimental trial was conducted in the
morning following a 24 h period without heavy or prolonged physical activity. Upon
arrival at the laboratory at 0800 h, subjects were appropriately instrumented. Subjects
of which the final 20 minutes were recorded as representative of the baseline resting
values. At 2 minutes prior to exercise, the subjects were secured to the KIN-COM•
isokinetic apparatus at the level of the torso and ankles. Subjects then performed 15 min
of exercise as described above consisting of bilateral, concentric knee extension over a
range of 70o from perpendicular against a dynamic resistance sufficient to elicit a heat
load of 4.78 kJ kg-1. Exercise was followed by 60 min of seated rest.
The total energy (Etotal) expended as a result of exercise, during the period from
onset of exercise until the time at which oxygen consumption returned to pre-exercise
values, was calculated from the sum of the energy expended using the following equation
(expressed in kilojoules):
M
total
¦
x
M
Ex / rest
¦
x
(V O 2
x
ª ( RER 0 . 7 )
e
«¬
c
0 .3
x
(1 RER )
0 .3
x
e
º
)
f »¼
(1)
x
where, M Ex/rest =
rate of energy expenditure during exercise and recovery;
ec = the caloric equivalent in kilojoules per liter of oxygen for
carbohydrates;
8
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
then rested in a semi-recumbent position for 60 min at an ambient temperature of 22 qC
Tissue temperature transients
Kenny et al.
ef =
the caloric equivalent in kilojoules per liter of oxygen
for fat; and,
RER = the respiratory exchange ratio.
The minute values were summed for the entire period as described above.
The mechanical work (W) done during each contraction of the exercise phase was
measured and recorded using the KIN-COM• isokinetic machine. This was calculated
from the force exerted and the angular displacement during the knee extension:
W
7T
(2)
The total work done (Wtotal) was the sum of the work accomplished during each of
the contractions during the 15 minutes of exercise.
Mechanical efficiency (M.E.) was defined as the total work (Wtotal) completed
during the 15 minute exercise period divided by the total energy expended minus the
energy expended under resting (Mrest) conditions (Mtotal – Mrest). Thus:
M .E .
Wtotal
M total M rest
(3)
The total energy expanded at rest (Mrest) was calculated from the average rate of
oxygen consumption during the five minutes preceding the exercise bout. These values
were calculated and expressed in kilojoules using the aforementioned equation.
The total heat load generated by the exercise (HLex) for each subject was calculated by
subtracting the total energy expenditure at rest (Mrest) and the energy equivalent of the
total mechanical work done (Wtotal) from the total energy expenditure (Mtotal). Values are
expressed in kilojoules:
HLex
M total ( M rest Wtotal )
(4)
9
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
where 7is rotational force or torque and T is the angular displacement.
Tissue temperature transients
Kenny et al.
The total dry heat loss by radiation, conduction and convection from the skin
surface (Hsk), during exercise and during recovery was estimated by subtracting the area
weighted mean heat flux ( HFsk) (as above) corrected for body surface area (AD) during
rest from those values recorded during exercise and recovery respectively. Thus:
H SKex
( HFSK ˜ AD ) ex ( HFSK ˜ AD ) rest
(5)
and
H SKrec
(6)
The total dry heat loss during exercise (Hskex) and during recovery (Hskrec) was the total
dry heat lost during the 15 minute exercise and 60 minute recovery periods respectively.
Statistical analyses for Tes, Tmu,CTsk andCHFsk was performed by ANOVA for
repeated measures to compare values for pre-exercise, end-exercise, and at 10 min
intervals during post-exercise recovery. Data are presented as means r SD.
RESULTS
Baseline Tes andCTsk were 36.80 r 0.30oC and 31.66 r 0.89oC respectively.
Resting muscle temperature was significantly lower than esophageal temperature (i.e.,
36.14 r 0.29, 35.86 r 0.31 and 35.01 r 0.33oC for Tmu10, Tmu25, and Tmu40
respectively) (Fig. 1). It should be noted that the increase in muscle tissue temperature
prior to the onset of exercise was likely due to the preparation of the subject for the
exercise portion of the experimental trial.
The muscle temperature profiles expressed as a function of the position of the
placement of the temperature relative to the radius of the thigh (r/rsk) shows a parabolic
10
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
( HFSK ˜ AD ) rec ( HFSK ˜ AD ) rest
Tissue temperature transients
profile for mean resting tissue temperature profile (Fig. 2).
Kenny et al.
This parabolic form of
muscle temperature profile was observed consistently in the data of all seven subjects
(Fig. 3). During resting, the deep (36.14qC) and mid (35.86qC) muscle temperature were
significantly different from superficial (35.01qC) muscle temperature. As depicted in
figure 4, the greatest tissue temperature difference (1.13qC) was between the deep and
superficial section of the muscle with a 0.84oC temperature gradient between the mid and
superficial muscle. Mean tissue temperature difference between deep and mid muscle
0.94 and -1.79qC in relation to Tmu10, Tmu25, and Tmu40 respectively (P < 0.05).
Exercise tissue temperature response
Following the onset of exercise, Tes increased gradually reaching a maximum rate of
increase of 0.05r 0.02oC.min-1 between 6 and 9 min of exercise and subsequently the rate
decreased over the balance of the exercise period (Table 2).
In contrast, muscle
temperature at all measured points increased rapidly during the initial period of exercise
followed by a gradual reduction in the rate over the balance of the exercise period.
Superficial muscle (Tmu40) showed the greatest rate of temperature increase (0.61 r
0.19oC.min-1). This value was significantly higher than the rate measured in deep muscle
(0.22 r 0.09oC.min-1). Following the initial 3 minutes of exercise, the rate of muscle
temperature change decreased gradually and was similar at all three intra-muscular sites
until end of exercise. Exercise resulted in a 0.55qC (end exercise Tes of 37.35qC)
increase in core temperature above baseline resting values.
In contrast, muscle
temperature increased by 2.09, 2.37 and 3.20qC above baseline resting for Tmu10, Tmu25,
11
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
was only 0.28oC. Further, the muscle to core temperature gradient was equal to -0.66, -
Tissue temperature transients
Kenny et al.
and Tmu40 measurement points respectively with end-exercise values similar at all three
measured sites (i.e., 38.23, 38.23 and 38.21qC for Tmu10, Tmu25, and Tmu40
respectively). Mean skin temperature increased continuously during exercise to an endexercise value that was significantly elevated above baseline rest (32.79oC, P < 0.05).
The increase inCTsk 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 Figure 2, the tissue temperature profile evolved from a parabolic
of exercise, muscle temperatures across the radial axis were homogenous. As such the
large temperature gradient between the deep and superficial muscle was rapidly reduced
such that by the end of exercise the temperature at all sites were similar. Furthermore,
the muscle to core temperature gradient was reversed from resting such that muscle
temperatures at all sites were significantly elevated above esophageal temperature by
0.90, 0.90 and 0.89oC for Tmu10, Tmu25, and Tmu40 respectively (P < 0.05).
Post-exercise tissue temperature response
Esophageal temperature decreased rapidly (-0.04 oC.min-1) during the initial
minutes following the cessation of exercise (Table 2) after which there was a rapid
decrease in the rate of temperature decrease to negligible values. At ~5 min of recovery,
Tes reached an elevated value 0.35qC above baseline resting (P < 0.05). For the duration
of recovery, the rate of decrease of Tes remained at ~0.001oC.min-1. Tes decreased to
37.11qC by the end of the 60 min recovery period (~0.3qC above baseline). Muscle
temperature showed a similar high rate of temperature decrease during the initial 5
minutes of exercise recovery although the rates were approximately 2 to 2.7 times greater
12
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
form typical of resting to a linear profile during the early stages of exercise. By the end
Tissue temperature transients
Kenny et al.
then that rate measured for Tes. Unlike the response in Tes, muscle temperature for all
measured sites decreased continuously during the initial 30 minutes of recovery.
However, the rates of muscle temperature decay were reduced for the duration of
recovery.
In the final 15 minutes of recovery, superficial muscle demonstrated an
elevated rate of temperature decrease above deep muscle (P < 0.05). Muscle tissue
temperature at the end of the post-exercise recovery period remained significantly
elevated above baseline resting values by 0.92, 1.05 and 1.77qC for Tmu10, Tmu25, and
decreased to baseline resting values within ~20-25 min of recovery. Similarly, forearm
skin blood flow decreased to baseline resting values within 10 min of the termination of
the exercise. In contrast, both thigh non-evaporative heat loss and thigh skin temperature
remained significantly elevated from pre-exercise values for the duration of the recovery
period (P < 0.05).
The temperature gradient between the different depths of muscle remained
relatively unchanged during the post-exercise recovery period despite a slow decay in
muscle temperature. The muscle to core temperature gradient decreased gradually over
the course of the recovery.
At approximately 25 minutes into recovery, muscle
temperature at all depths achieved similar values to that of esophageal temperature. For
the duration of the recovery period, the muscle to core temperature gradient was
increased with superficial muscle demonstrating the largest temperature gradient by the
end of recovery (~0.3qC; P < 0.05) as compared to that temperature gradient between
deep muscle and core. Of note, the deep muscle-to-core temperature gradient remained
relatively unchanged for the duration of the recovery period (~0.02qC).
13
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
Tmu40 respectively (P <0.05) (Fig. 1). CTsk and whole-body non-evaporative heat loss
Tissue temperature transients
Kenny et al.
Heat load and heat loss response
The workload resistance was adjusted for each subject according to the individual
heat load and mechanical efficiency of the leg extension exercise. The mechanical
efficiency varied from 5.98 to 15.96% while the average for the group was 9.93 ± 1.32%.
The average actual workload was one at which the heat production was 4.78 ± 0.38 kJ.kg1
. The total energy expenditure and total work done were 585.87 ± 53.72 kJ and 41.48 ±
4.68 kJ respectively. Thus the average heat load generated as a result of the exercise was
5.98 kJ while during the 60 minutes of post-exercise recovery this value was 37.90 ±
18.80 kJ.
The kinetics of heat load generation at rest, over the 15 minutes of exercise and
over the first 10 minutes of recovery is presented in figure 5. As well the corresponding
evolution of dry heat loss is also shown. Thus during the 5 minutes preceding exercise the
dry heat loss defined relative to heat load, that is minus the resting levels, were
essentially zero. During exercise, the dry heat loss increased at a rate of 0.14 kJ.min-1 to a
maximal level of 2.19 kJ.min-1 after 15 minutes of exercise. At cessation of exercise the
sensitive heat loss dropped exponentially to a level approximately 1.0 kJ.min-1 above
initial resting values and remained elevated for the next ten minutes. The heat production
on the other hand increased to17.08 kJ.min-1 after 2 minutes of exercise and continued to
rise at a rate of approximately 0.78 kJ.min-1 for the next 13 minutes to a maximum heat
production of 27.71 kJ.min-1. Immediately post-exercise the heat load returned
exponentially to resting levels within 5 minutes.
14
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
391.73 ± 38.93 kJ. The average total dry heat loss during the exercise period was 15.93 ±
Tissue temperature transients
Kenny et al.
DISCUSSION
In this study an attempt was made to specifically evaluate the kinetics of heat
exchange in muscle tissue during and following exercise using a multi-sensor thermal
probe positioned at a pre-determined internal marker. In contrast to previous studies, we
observed similar individual and group muscle temperature profiles during resting,
exercise and subsequent resting recovery.
Furthermore, we observed a sustained
elevation of core temperature for the duration of the recovery period that is consistent
decrease in the first minutes of exercise recovery followed by a prolonged sustained
elevation of ~0.3qC. Of particular importance, was the observation that deep muscle
temperature decreased during the early stages of exercise recovery to values equal to that
of esophageal temperature. Subsequently deep muscle temperature remained relatively
unchanged from esophageal temperature for the duration of recovery. This supports the
hypothesis that the post-exercise recovery of core temperature may be to a large degree,
influenced by the residual heat load of muscle.
Tissue temperature response - Resting
Different shapes of limb temperature profile have been reported for resting
conditions during different thermal stresses between individuals whereas we noted a
consistent parabolic profile of muscle temperature in all subjects (4, 7, 8, 17, 20-22, 25,
27, 31). This could arise from inconsistency in the specific placement of the internal
probe in the muscle. There is a wide variation in recorded muscle tissue temperature due
to the proximity of the probe to the surface and to such structures as large arteries and
bone (10). This could have been a source of significant variation in the recorded internal
15
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
with previous findings (16, 28). Specifically, esophageal temperature showed a rapid
Tissue temperature transients
Kenny et al.
temperature. The differences in the specific heat of these tissues, as well as the differing
blood flow and hence the convective effect within these structures influence the rates of
temperature change in adjacent regions of the muscle. Therefore, consistent placement of
the probe is critical. Thus an attempt was made to minimize the variation in temperature
recording resulting from individual anatomical differences.
Muscle temperature response - Exercise
From the onset of exercise until the late phases of exercise there is a gradual
zero gradient or homogenous temperature profile across the muscle. As shown in figure
4, the large temperature gradient that existed between the deep and mid portions of the
muscle and the superficial muscle was rapidly eliminated during the first 5 minutes of
exercise. By the end of exercise the gradient between the different muscle depths was
non-existent as temperatures across the radial axis of the muscle became homogenous.
This effect was not observed earlier by Saltin et al. (25). In that case, it was noted that
both mid and superficial muscle temperature remained generally lower than deep muscle
temperature. Similarly superficial muscle temperature remained lower than mid muscle
temperature while the temperature gradient between mid and deep muscle seemed to
remain relatively constant throughout exercise. The gradient between the superficial
muscle increased relative to both mid and deep muscle. The different response to that
observed in our study may be attributed to a number of factors which may include: 1)
differences in the measurement site (i.e., vastus lateralis); 2) differences in the muscle
mass implicated in the exercise activity; 3) differences in ambient conditions; and 4)
difference in work intensity. For example, it would be expected that the temperature
16
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
change in the muscle temperature profile from one parabolic in form seen at rest, to a
Tissue temperature transients
Kenny et al.
profile of the vastus lateralis would be different from that of the medialis as it is less
affected by the circulation in the femoral artery and vein. The relative influence of
convective heat exchange would be considerably different between these muscles.
The high rate of muscle temperature increase in the early stages of exercise is
consistent with previous studies (1, 3, 24, 25). Aulick et al. (3) showed at the beginning
of exercise, heat gained by the leg (local metabolic heat production plus vascular heat
delivery from the viscera) exceeded heat loss, and femoral vein blood temperature rose
of muscle temperature increase (0.53qC.min-1) that was 1.4 and 1.6 times the rate of
temperature increase for the deep and mid muscle respectively. On the other hand, based
on visual observation of the work by Saltin and co-workers it would seem that the rate of
temperature increase was greater in deep muscle as compared to superficial muscle (25).
During the course of exercise, the muscle-to-core temperature gradient increased
progressively (Fig. 4), from -1.15qC at rest to +0.90qC by the end of exercise. As well,
despite the rapid increase in muscle heat content (as represented by increased muscle
temperature) to values exceeding that for core, the rate of temperature increase of core
remained consistently lower than muscle. Therefore, this would suggest that the rate of
heat accumulation within the core region is attenuated to a large degree by an increase in
the rate of whole-body heat loss (i.e., evaporative and non-evaporative heat loss). For
example, Aulick et al. (3) previously noted that as limb sweat rate, cutaneous blood flow,
and muscle-to-skin temperature differences increased during exercise, the active leg
became a more effective vehicle for heat dissipation, and that femoral venous
temperature eventually reached a plateau during steady state.
Further, Gisolfi and
17
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
rapidly. In this study the superficial regions of the muscle demonstrated the largest rate
Tissue temperature transients
Kenny et al.
Robinson (11) showed that much of the heat produced by active leg muscles is rapidly
transported to surface veins and that this muscle heat is potentially lost across the leg
surface. In this study, muscle-to-skin temperature gradient remained elevated during the
course of the exercise by ~5.2qC and skin blood flow and sweat rate increased gradually
during the course of the exercise. Furthermore, it has previously been shown that during
leg work the inactive upper limbs also acts as an avenue for vascular heat loss from the
central circulation (15) which would further attenuate the increase in core temperature.
Few studies have graphically presented muscle tissue temperature response during
the post-exercise period and even so, no specific discussion was presented in regards to
these data (1, 23, 24). It is clear in this study that during the transition from exercise to
post-exercise resting recovery the muscle temperature profile across the radial axis of the
muscle remains constant (i.e., linear profile, see figure 2 and 3). During the course of the
60 min recovery, all three sites showed a similar rate of temperature change, although
superficial muscle showed a significantly greater rate of temperature decrease towards
the later stages of recovery (P < 0.05).
Deep muscle temperature decreased during the early stages of exercise recovery
to values equal to that of esophageal temperature after which deep muscle temperature
remained relatively unchanged from esophageal temperature for the duration of recovery
with the deep muscle-to-core temperature gradient been no greater than ~0.02qC. The
lack of a difference in temperature gradient between muscle and core suggest
equilibration of heat distribution within the body. Thus, changes in surface heat loss (i.e.,
evaporative and non-evaporative heat loss) will change the rate of whole-body cooling.
18
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
Muscle temperature response – Post-exercise
Tissue temperature transients
Kenny et al.
Therefore, the rate of core temperature decay is limited by the rate at which heat is lost at
the skin/air interface.
All muscle temperatures remained significantly elevated above baseline resting at
the end of recovery.
That was paralleled by a significant increase in esophageal
temperature of ~0.3qC (P < 0.05). Aikas et al. (1) have shown a similar post-exercise
increase in muscle temperature of the previously active muscle, although esophageal
temperature showed a rapid decrease to values below baseline rest within a short period
believes that the convective arterial flow plays a major role in muscle cooling postexercise. Our results are more consistent with Saltin et al. (24) who on the other hand did
observe a sustained increase in post-exercise esophageal temperature while muscle
temperature remained significantly elevated above baseline resting.
Thoden et al. (28) previously showed a prolonged post-exercise elevation (0.40.5qC) in esophageal temperature following dynamic exercise.
It was subsequently
shown that an increase in the post-exercise hypotensive response, induced by exercise of
increasing intensity, was paralleled by an increase (~0.4qC) in the magnitude of the postexercise elevation in esophageal temperature (13). It was suggested that the post-exercise
esophageal temperature response may be defined to a large degree by the gradient
between the periphery and core and that the convective transfer of residual heat from
previously active musculature may contribute to the sustained elevation in post-exercise
esophageal temperature. Our observation of a prolonged elevation in muscle temperature
at values elevated above esophageal provides further evidence to support this conclusion.
Thus, in the absence of a post-exercise increase in heat loss response (14), esophageal
19
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
(~15 min) following cessation of exercise. This is more difficult to explain if one
Tissue temperature transients
Kenny et al.
temperature would remain elevated as long as: 1) the heat content of muscle remains
higher or equal to that of core; 2) the post-exercise hypotensive effect persists; or 3) a
combination of the two.
Summary
In the present study exercise was performed such that the dynamic resistance
during the bilateral knee extension exercise was sufficient to elicit a heat load of 4.78 kJ
kg-1. Thus it can be assumed that the rate of heat production and accumulation in muscle
observed between the transition from rest to exercise and exercise to resting recovery was
not only the result of the change in metabolic heat production but also the result of
changes in the convective heat transfer between blood and muscle and conductive heat
transfer within the muscle and skin surface. Further, as with previous studies that have
shown that tissue heat content and compartmental heat exchange is significantly
influenced by convective heat exchange during rest (9) and exercise (15), our findings
suggest that post-exercise core temperature response (and the rate of temperature decay)
is significantly influenced by convective heat transfer between muscle and core.
20
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
was comparable between subjects. Thus, the variation in muscle temperature profile
Tissue temperature transients
Kenny et al.
ACKNOWLEDGMENTS
This research was supported by the Natural Science and Engineering Research Council of
Canada. We would also like to acknowledge the technical support of Ms. Carolyn
Proulx, and Mr. Normand Boulé.
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
21
Tissue temperature transients
Kenny et al.
REFERENCES
1.
Aikas, E., M. J. Karvonen, P. Piironen, and R. Ruosteenoja. Intramuscular, rectal
and oesophageal temperature during exercise. Acta Physiol Scand 54: 366-370, 1962.
2.
Asmussen, E., and O. Boje. Body temperature and capacity for work. Acta
Physiol Scand 10: 1-22, 1945.
3.
Aulick, L. H., S. Robinson, and S. P. Tzankoff. Arm and leg intravascular
temperatures of men during submaximal exercise. J Appl Physiol 51: 1092-7., 1981.
Bazett, H. C., and B. McGlone. Temperature gradients in the tissues in man. Am J
Physiol 82: 415-451, 1927.
5.
Beelen, A., and A. J. Sargeant. Effect of lowered muscle temperature on the
physiological response to exercise in men. Eur J Appl Physiol Occup Physiol 63: 387-92,
1991.
6.
Blomstrand, E., U. Bergh, B. Essen-Gustavsson, and B. Ekblom. Influence of low
muscle temperature on muscle metabolism during intense dynamic exercise. Acta Physiol
Scand 120: 229-36., 1984.
7.
Clarke, R. S. J., R. F. Hellon, and A. R. Lind. The duration of sustained
contractions of the human forearm at different muscle temperatures. J Physiol 143: 454473, 1958.
8.
Ducharme, M. B., and P. Tikuisis. Forearm temperature profile during the
transient phase of thermal stress. Eur J Appl Physiol Occup Physiol 64: 395-401, 1992.
9.
Ducharme, M. B., and P. Tikuisis. Role of blood as heat source or sink in human
limbs during local cooling and heating. J Appl Physiol 76: 2084-94., 1994.
22
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
4.
Tissue temperature transients
10.
Kenny et al.
Ducharme, M. B., W. P. VanHelder, and M. W. Radomski. Tissue temperature
profile in the human forearm during thermal stress at thermal stability. J Appl Physiol 71:
1973-8., 1991.
11.
Gisolfi, C., and S. Robinson. Venous blood distribution in the legs during
intermittent treadmill work. J Appl Physiol 29: 368-73., 1970.
12.
Hardy, J. D., and E. F. Dubois. The technique of measuring radiation and
convection. J Nutr 15: 461-475, 1938.
Kenny, G. P., and P. C. Niedre. The effect of exercise intensity on the post-
exercise esophageal temperature response. Eur J Appl Physiol 86: 342-6., 2002.
14.
Kenny, G. P., C. E. Proulx, P. M. Denis, and G. G. Giesbrecht. Moderate exercise
increases the post exercise resting warm thermoregulatory response thresholds. Aviat
Space Environ Med 71: 914-9., 2000.
15.
Kenny, G. P., F. D. Reardon, M. B. Ducharme, M. L. Reardon, and W. Zaleski.
Tissue temperature transients in resting contra-lateral leg muscle tissue during isolated
knee extension. Can J Appl Physiol 27: 535-50., 2002.
16.
Kenny, G. P., F. D. Reardon, G. G. Giesbrecht, M. Jette, and J. S. Thoden. The
effect of ambient temperature and exercise intensity on post- exercise thermal
homeostasis. Eur J Appl Physiol Occup Physiol 76: 109-15, 1997.
17.
Kuehn, L. A., S. D. Livingstone, and E. D. Topliff. Tissue temperature gradients
in the African guinea hog. Can J Physiol Pharmacol 48: 28-34., 1970.
18.
Mack, G. W. Assessment of cutaneous blood flow by using topographical
perfusion mapping techniques. J Appl Physiol 85: 353-9., 1998.
23
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
13.
Tissue temperature transients
19.
Kenny et al.
Nadel, E. R., U. Bergh, and B. Saltin. Body temperatures during negative work
exercise. J Appl Physiol 33: 553-8., 1972.
20.
Pennes, H. P. Analysis of tissue and arterial blood temperatures in the resting
human forearm. J Appl Physiol 1: 93-122, 1948.
21.
Petrofski, J. S., and A. R. Lind. The relationship of body fat content to deep
muscle temperature and isometric endurance in man. Clin Sci Mol Med 48: 405-412,
1975.
Reader, S. R., and H. M. White. Tissue temperature gradients. J Appl Physiol 4:
396-402, 1951.
23.
Saltin, B., A. P. Gagge, U. Bergh, and J. A. Stolwijk. Body temperatures and
sweating during exhaustive exercise. J Appl Physiol 32: 635-43., 1972.
24.
Saltin, B., A. P. Gagge, and J. A. Stolwijk. Body temperatures and sweating
during thermal transients caused by exercise. J Appl Physiol 28: 318-27., 1970.
25.
Saltin, B., A. P. Gagge, and J. A. Stolwijk. Muscle temperature during
submaximal exercise in man. J Appl Physiol 25: 679-88., 1968.
26.
Saltin, B., and L. Hermansen. Esophageal, rectal, and muscle temperature during
exercise. J Appl Physiol 21: 1757-62., 1966.
27.
Sargeant, A. J. Effect of muscle temperature on leg extension force and short-term
power output in humans. Eur J Appl Physiol Occup Physiol 56: 693-8, 1987.
28.
Thoden, J., G. Kenny, F. Reardon, M. Jette, and S. Livingstone. Disturbance of
thermal homeostasis during post-exercise hyperthermia. Eur J Appl Physiol Occup
Physiol 68: 170-6, 1994.
24
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
22.
Tissue temperature transients
29.
Kenny et al.
Veicsteinas, A., G. Ferretti, and D. W. Rennie. Superficial shell insulation in
resting and exercising men in cold water. J Appl Physiol 52: 1557-64., 1982.
30.
Webb, P. Temperatures of skin, subcutaneous tissue, muscle and core in resting
men in cold, comfortable and hot conditions. Eur J Appl Physiol Occup Physiol 64: 4716, 1992.
31.Williams, D. B., and R. C. Karl. Measurement of deep muscle temperature in ischemic
limbs. Am J Surg 139: 503-7., 1980.
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
25
Tissue temperature transients
Kenny et al.
TABLE LEGENDS
Table 1. Mean (rSD) and individual data relating to the placement of the intra-muscular
multi-sensor thermal probe of the upper leg.
Table 2. Mean (rSD) rate of change of esophageal and muscle (Tmu10, Tmu25 and
Tmu40) temperatures during exercise and post-exercise recovery.
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
26
Tissue temperature transients
Kenny et al.
FIGURE LEGENDS
Figure 1. Mean (rSE) muscle (R,Tmu10; P, Tmu25; and V, Tmu40) and esophageal
(‘) temperature response during rest, exercise (Ex) and post-exercise recovery. The
vertical dot lines represent the start (time = 0 min) and end (time = 15 min) of exercise.
*, indicates values significant different from baseline resting values (P < 0.05). 1, value
for esophageal temperature not significantly elevated from baseline.
(Ex, R), end-exercise (End Ex, Q) and post-exercise recovery (Post-Ex, U) at selected
periods as a function of the placement of the temperature sensors relative to the radius of
the thigh. r is the radius (cm), rsk is the radius of the thigh (cm), and r/rsk is the relative
radius.
Figure 3. Mean (rSE) (O) and individual muscle temperature profiles during resting (A,
top), end-exercise (B, middle), and at 60 min post-exercise resting (C, bottom). r is the
radius (cm), rsk is the radius of the thigh (cm), and r/rsk is the relative radius. Note:
individual subjects are represented by different symbols and these symbols are the same
for each time period in graphs A through C. §, indicates values significantly different
from superficial muscle (P < 0.05).
Figure 4. Mean (rSE) core to muscle temperature gradient (P, deep muscle to core; R,
mid muscle to core; U, superficial muscle to core; A, top) and intra-muscular
27
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
Figure 2. Mean (rSE) muscle temperature profile during baseline resting (O), exercise
Tissue temperature transients
Kenny et al.
temperature gradients (Â, deep muscle to mid muscle; ‘, deep muscle to superficial
muscle and; V, mid muscle to superficial muscle; B, bottom). The vertical dot lines
represent the start (time = 0 min) and end (time = 15 min) of exercise. ‡, indicates values
significantly different from the deep to mid muscle temperature gradient (P < 0.05). §,
indicates values significantly different from baseline resting (P < 0.05). *, indicates
values for the superficial to core temperature gradient significantly from the deep to core
temperature gradient.
resting, exercise and post-exercise recovery. The vertical dot lines represent the start
(time = 0 min) and end (time = 15 min) of exercise.
28
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
Figure 5. Mean (rSD) heat load () and dry heat loss (’) responses during baseline
Tissue temperature transients
Kenny et al.
Table 1. Mean (rSD) and individual data relating to the placement of the intra-muscular multi-sensor thermal probe
of the upper leg.
Subject
1
2
3
4
5
6
7
Thigh
length
2
(cm)
(cm)
(cm)
58
55
65
56
56
67
61
52
47
48
46
47
44
45
24
22
21
20
23
21
22
Inguinal
crease
2
Base
of
femur
3
Medial
deviation
(cm)
(cm)
28
25
27
26
24
23
25
5.5
5.4
5.9
5.1
6.1
5.7
5.8
4
Insertion depth from
skin surface
Tmu10
Tmu25
Tmu40
4.7
4.8
5.0
4.4
4.7
5.3
5.0
3.2
3.3
3.5
2.9
3.2
3.8
3.5
1.7
1.8
2.0
1.4
1.7
2.3
2.0
(cm)
4
Probe
tip to
femoral
artery
4
Probe
tip to
femur
(cm)
(cm)
0.9
1.0
1.2
1.3
1.0
1.3
1.1
1.0
1.0
1.0
0.9
1.3
1.3
1.2
60
47
22
25
5.6
4.8
3.3
1.8
1.1
1.1
8
4
1
2
0.2
0.3
0.3
0.3
0.2
0.1
1
2
Values represent the circumference of thigh at level of probe insertion. Values represent the distance to probe
insertion in relation to long axis of the thigh. 3 Medial deviation from the thigh long axis. 4 Values determined by
ultra-sound imaging.
SD
29
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
CX
1
Thigh
circum.
Tissue temperature transients
Kenny et al.
Table 2. Mean (rSD) rate of change of esophageal and muscle (Tmu10, Tmu25 and Tmu40)
temperatures during exercise and post-exercise recovery.
Esophageal
Temperature
Tmu10
Muscle Temperature
Tmu25
(qC.min-1)
Tmu40
(qC.min-1)
Exercise
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)
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)*
Post-exercise
*, indicates significant difference from deep muscle, Tmu10 (P <0.05).
30
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
0-3 min
Tissue temperature transients
Kenny et al.
31
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
Figure 1. Mean (rSE) muscle (R,Tmu10; P, Tmu25; and V, Tmu40) and esophageal (‘) temperature
response during rest, exercise (Ex) and post-exercise recovery. The vertical dot lines represent the start
(time = 0 min) and end (time = 15 min) of exercise. *, indicates values significant different from baseline
resting values (P < 0.05). 1, value for esophageal temperature not significantly elevated from baseline.
Tissue temperature transients
Kenny et al.
32
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
Figure 2. Mean (rSE) muscle temperature profile during baseline resting (O), exercise (Ex, R), endexercise (End Ex, Q) and post-exercise recovery (Post-Ex, U) at selected periods as a function of the
placement of the temperature sensors relative to the radius of the thigh. r is the radius (cm), rsk is the radius
of the thigh (cm), and r/rsk is the relative radius.
Tissue temperature transients
Kenny et al.
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
Figure 3. Mean (rSE) (O) and individual muscle temperature profiles during resting (A, top), end-exercise (B, middle), and
at 60 min post-exercise resting (C, bottom). r is the radius (cm), rsk is the radius of the thigh (cm), and r/rsk is the relative
radius. Note: individual subjects are represented by different symbols and these symbols are the same for each time period in
graphs A through C. §, indicates values significantly different from superficial muscle (P < 0.05).
33
Tissue temperature transients
Kenny et al.
34
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
Figure 4. Mean (rSE) core to muscle temperature gradient (P, deep muscle to core; R, mid muscle to core;
U, superficial muscle to core; A, top) and intra-muscular temperature gradients (Â, deep muscle to mid
muscle; ‘, deep muscle to superficial muscle and; V, mid muscle to superficial muscle; B, bottom). The
vertical dot lines represent the start (time = 0 min) and end (time = 15 min) of exercise. ‡, indicates values
significantly different from the deep to mid muscle temperature gradient (P < 0.05). §, indicates values
significantly different from baseline resting (P < 0.05). *, indicates values for the superficial to core
temperature gradient significantly from the deep to core temperature gradient.
Tissue temperature transients
Kenny et al.
35
Downloaded from http://jap.physiology.org/ by 10.220.33.5 on June 14, 2017
Figure 5. Mean (rSD) heat load () and dry heat loss (’) responses during baseline resting, exercise and
post-exercise recovery. The vertical dot lines represent the start (time = 0 min) and end (time = 15 min) of
exercise.