Heat production in human skeletal muscle at the onset of intense dynamic exercise

Abstract

1. We hypothesised that heat production of human skeletal muscle at a given high power output would gradually increase as heat liberation per mole of ATP produced rises when energy is derived from oxidation compared to phosphocreatine (PCr) breakdown and glycogenolysis. 2. Five young volunteers performed 180 s of intense dynamic knee-extensor exercise ( approximately 80 W) while estimates of muscle heat production, power output, oxygen uptake, lactate release, lactate accumulation and ATP and PCr hydrolysis were made. Heat production was determined continuously by (i) measuring heat storage in the contracting muscles, (ii) measuring heat removal to the body core by the circulation, and (iii) estimating heat transfer to the skin by convection and conductance as well as to the body core by lymph drainage. 3. The rate of heat storage in knee-extensor muscles was highest during the first 45 s of exercise (70-80 J s-1) and declined gradually to 14 +/- 10 J s-1 at 180 s. 4. The rate of heat removal by blood was negligible during the first 10 s of exercise, rising gradually to 112 +/- 14 J s-1 at 180 s. The estimated rate of heat release to skin and heat removal via lymph flow was < 2 J s-1 during the first 5 s and increased progressively to 24 +/- 1 J s-1 at 180 s. The rate of heat production increased significantly throughout exercise, being 107 % higher at 180 s compared to the initial 5 s, with half of the increase occurring during the first 38 s, while power output remained essentially constant. 5. The contribution of muscle oxygen uptake and net lactate release to total energy turnover increased curvilinearly from 32 % and 2 %, respectively, during the first 30 s to 86 % and 8 %, respectively, during the last 30 s of exercise. The combined energy contribution from net ATP hydrolysis, net PCr hydrolysis and muscle lactate accumulation is estimated to decline from 37 % to 3 % comparing the same time intervals. 6. The magnitude and rate of elevation in heat production by human skeletal muscle during exercise in vivo could be the result of the enhanced heat liberation during ATP production when aerobic metabolism gradually becomes dominant after PCr and glycogenolysis have initially provided most of the energy.

Figure 1. Anatomical compartments of the thigh and quantification of the knee-extensor muscle mass

A, MRI of cross-sections of upper-thigh (a) and mid-thigh (b) with the white line indicating borders of quadriceps femoris muscle, including vastus lateralis (v.l.), vastus intermedius (v.i.), vastus medialis (v.m.), rectus femoris (r.f.) and tendon of quadriceps femoris muscle (t). A cross-section of the distal end is shown in c. It was sometimes difficult to exactly determine the origin of the muscles at the proximal end (a). This was solved by plotting the serial individual cross-sections and determining the origin by extrapolation (see Ba). Mean values ±s.e.m. for all subjects’ serial cross-sections of the thigh are shown in Bb.

Figure 3. Thigh temperature during the thermal equilibration procedure prior to exercise

The tissue temperatures of the thigh are depicted when warming it with a water-perfused wrapping set at 41 °C for ≈70 min to equalise these temperatures with the core temperatures (≈37 °C). Thereafter, the water temperature was adjusted to 37.5 °C for the remainder of the experiment.

Figure 2. Schematic model used for calculation of total energy turnover

T_a and T_v, arterial and venous temperature. T_v-a, venous-arterial temperature difference. ΔT_m, mean increase in temperature of all muscles.

Figure 6. Temperature in various knee-extensor and hamstring muscles as well as subcutaneous tissue during intense knee-extensor exercise

A, mean increases in the two additional experiments when thermistors were placed in vastus intermedius (v.i.) and tensor fasciae latae (t.f.l.) in addition to other knee-extensors. B, data from another additional experiment. Three thermistor probes were placed in different hamstring muscles (biceps femoris, semitendinosus and semimembranosus), and one in the subcutaneous fat (≈5 mm under the skin) next to a thermistor probe placed in the rectus femoris (depth ≈3 cm).

Figure 5. Temperature and thigh blood flow during intense dynamic knee-extensor exercise

A, mean values (n = 5) for temperature increases in the rectus femoris (r.f.; 2 sites), vastus medialis (v.m.; 1 site) and vastus lateralis (v.l.; 2 sites) of the quadriceps muscle and hamstrings muscle (1 site; biceps femoris medial) during dynamic knee-extensor exercise. s.e.m. bars are not included for reasons of clarity (s.e.m. range 0.00-0.10 °C; mean s.e.m. values 0.04-0.07 °C for all muscle portions). B, the mean (±s.e.m.) increases (n = 5) in arterial and venous blood temperatures are given from start to end of the exercise. For comparison mean (±s.e.m.) quadriceps, oesophageal (core) and skin temperature are given as well. C, mean (±s.e.m.) values for thigh blood flow during exercise are presented. The mean elevation (n = 5) observed during the exercise fits the polynomial equation:

Figure 4. Mean quadriceps muscle temperature, arterial and femoral blood temperature (A) and thigh blood flow (B) for all subjects at rest and during passive exercise, dynamic exercise and recovery

Of note is the observation that the decline in muscle temperature during recovery can be accounted for almost completely by the on-going convective heat removal to the body core.

Figure 7. Heat production during dynamic knee-extensor exercise

Mean values (±s.e.m.; n = 5) of total heat production (H_t) are depicted for each 5 s period of the exercise as well as its subdivision in terms of storage in the quadriceps muscle (H_s) and removal by the blood from the thigh (H_r).

Figure 8. Mechanical power output during dynamic knee-extensor exercise

Mean values for mechanical work per kick (A) and the kicking frequency (B) as well as the mean power output over 30 s intervals (C) for n = 5.

Figure 9. Oxygen consumption (A) and lactate release (B) during exercise

Data are means ±s.e.m. for 5 subjects.

Figure 10. Total and aerobic energy turnover during dynamic exercise

Total energy turnover (E_t) vs. aerobic heat liberation (H_VO2) during 180 s of exercise. Note that the difference in heat between E_t and H_VO2 is accounted for by anaerobic heat liberation.