ATP turnover and heat production in human skeletal muscle during dynamic exercise: higher efficiency of anaerobic than aerobic aTP resynthesis

P. Krustrup, R.A. Ferguson, M. Kjaer, J. Bangsbo

Research output: Contribution to journalArticle

75 Citations (Scopus)

Abstract

The aim of the present study was to simultaneously examine skeletal muscle heat production and ATP turnover in humans during dynamic exercise with marked differences in aerobic metabolism. This was done to test the hypothesis that efficiency is higher in anaerobic than aerobic ATP resynthesis. Six healthy male subjects performed 90 s of low intensity knee-extensor exercise with (OCC) and without thigh occlusion (CON-LI) as well as 90 s of high intensity exercise (CON-HI) that continued from the CON-LI bout. Muscle heat production was determined by continuous measurements of muscle heat accumulation and heat release to the blood. Muscle ATP production was quantified by repeated measurements of thigh oxygen uptake as well as blood and muscle metabolite changes. All temperatures of the thigh were equalized to ≈37 °C prior to exercise by a water-perfused heating cuff. Oxygen uptake accounted for 80 ± 2 and 59 ± 4 %, respectively, of the total ATP resynthesis in CON-LI and CON-HI, whereas it was negligible in OCC. The rise in muscle temperature was lower (P < 0.05) in OCC than CON-LI (0.32 ± 0.04 vs. 0.37 ± 0.03 °C). The mean rate of heat production was also lower (P < 0.05) in OCC than CON-LI (36 ± 4 vs. 57 ± 4 J s−1). Mechanical efficiency was 52 ± 4 % after 15 s of OCC and remained constant, whereas it decreased (P < 0.05) from 56 ± 5 to 32 ± 3 % during CON-LI. During CON-HI, mechanical efficiency transiently increased (P < 0.05) to 47 ± 4 %, after which it decreased (P < 0.05) to 36 ± 3 % at the end of CON-HI. Assuming a fully coupled mitochondrial respiration, the ATP turnover per unit of work was calculated to be unaltered during OCC (≈20 mmol ATP kJ−1), whereas it increased (P < 0.05) from 21 ± 4 to 29 ± 3 mmol ATP kJ−1 during CON-LI and further (P < 0.05) to 37 ± 3 mmol ATP kJ−1 during CON-HI. The present data confirm the hypothesis that heat loss is lower in anaerobic ATP resynthesis than in oxidative phosphorylation and can in part explain the finding that efficiency declines markedly during dynamic exercise. In addition, the rate of ATP turnover apparently increases during constant load low intensity exercise. Alternatively, mitochondrial efficiency is lowered as exercise progresses, since ATP turnover was unaltered during the ischaemic exercise bout.
LanguageEnglish
Pages255-269
Number of pages15
JournalJournal of Physiology
Volume549
DOIs
Publication statusPublished - 2003

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Thermogenesis
Skeletal Muscle
Adenosine Triphosphate
Exercise
Muscles
Thigh
Hot Temperature
Oxygen
Temperature
Oxidative Phosphorylation
Heating
Knee
Healthy Volunteers
Respiration

Keywords

  • aerobic metabolism
  • muscle heat production
  • oxidative phosphorylation

Cite this

@article{1bf9890243ad4c609427de5f5e1d8a6e,
title = "ATP turnover and heat production in human skeletal muscle during dynamic exercise: higher efficiency of anaerobic than aerobic aTP resynthesis",
abstract = "The aim of the present study was to simultaneously examine skeletal muscle heat production and ATP turnover in humans during dynamic exercise with marked differences in aerobic metabolism. This was done to test the hypothesis that efficiency is higher in anaerobic than aerobic ATP resynthesis. Six healthy male subjects performed 90 s of low intensity knee-extensor exercise with (OCC) and without thigh occlusion (CON-LI) as well as 90 s of high intensity exercise (CON-HI) that continued from the CON-LI bout. Muscle heat production was determined by continuous measurements of muscle heat accumulation and heat release to the blood. Muscle ATP production was quantified by repeated measurements of thigh oxygen uptake as well as blood and muscle metabolite changes. All temperatures of the thigh were equalized to ≈37 °C prior to exercise by a water-perfused heating cuff. Oxygen uptake accounted for 80 ± 2 and 59 ± 4 {\%}, respectively, of the total ATP resynthesis in CON-LI and CON-HI, whereas it was negligible in OCC. The rise in muscle temperature was lower (P < 0.05) in OCC than CON-LI (0.32 ± 0.04 vs. 0.37 ± 0.03 °C). The mean rate of heat production was also lower (P < 0.05) in OCC than CON-LI (36 ± 4 vs. 57 ± 4 J s−1). Mechanical efficiency was 52 ± 4 {\%} after 15 s of OCC and remained constant, whereas it decreased (P < 0.05) from 56 ± 5 to 32 ± 3 {\%} during CON-LI. During CON-HI, mechanical efficiency transiently increased (P < 0.05) to 47 ± 4 {\%}, after which it decreased (P < 0.05) to 36 ± 3 {\%} at the end of CON-HI. Assuming a fully coupled mitochondrial respiration, the ATP turnover per unit of work was calculated to be unaltered during OCC (≈20 mmol ATP kJ−1), whereas it increased (P < 0.05) from 21 ± 4 to 29 ± 3 mmol ATP kJ−1 during CON-LI and further (P < 0.05) to 37 ± 3 mmol ATP kJ−1 during CON-HI. The present data confirm the hypothesis that heat loss is lower in anaerobic ATP resynthesis than in oxidative phosphorylation and can in part explain the finding that efficiency declines markedly during dynamic exercise. In addition, the rate of ATP turnover apparently increases during constant load low intensity exercise. Alternatively, mitochondrial efficiency is lowered as exercise progresses, since ATP turnover was unaltered during the ischaemic exercise bout.",
keywords = "aerobic metabolism, muscle heat production , oxidative phosphorylation",
author = "P. Krustrup and R.A. Ferguson and M. Kjaer and J. Bangsbo",
year = "2003",
doi = "10.1113/jphysiol.2002.035089",
language = "English",
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ATP turnover and heat production in human skeletal muscle during dynamic exercise: higher efficiency of anaerobic than aerobic aTP resynthesis. / Krustrup, P.; Ferguson, R.A.; Kjaer, M.; Bangsbo, J.

In: Journal of Physiology, Vol. 549, 2003, p. 255-269.

Research output: Contribution to journalArticle

TY - JOUR

T1 - ATP turnover and heat production in human skeletal muscle during dynamic exercise: higher efficiency of anaerobic than aerobic aTP resynthesis

AU - Krustrup, P.

AU - Ferguson, R.A.

AU - Kjaer, M.

AU - Bangsbo, J.

PY - 2003

Y1 - 2003

N2 - The aim of the present study was to simultaneously examine skeletal muscle heat production and ATP turnover in humans during dynamic exercise with marked differences in aerobic metabolism. This was done to test the hypothesis that efficiency is higher in anaerobic than aerobic ATP resynthesis. Six healthy male subjects performed 90 s of low intensity knee-extensor exercise with (OCC) and without thigh occlusion (CON-LI) as well as 90 s of high intensity exercise (CON-HI) that continued from the CON-LI bout. Muscle heat production was determined by continuous measurements of muscle heat accumulation and heat release to the blood. Muscle ATP production was quantified by repeated measurements of thigh oxygen uptake as well as blood and muscle metabolite changes. All temperatures of the thigh were equalized to ≈37 °C prior to exercise by a water-perfused heating cuff. Oxygen uptake accounted for 80 ± 2 and 59 ± 4 %, respectively, of the total ATP resynthesis in CON-LI and CON-HI, whereas it was negligible in OCC. The rise in muscle temperature was lower (P < 0.05) in OCC than CON-LI (0.32 ± 0.04 vs. 0.37 ± 0.03 °C). The mean rate of heat production was also lower (P < 0.05) in OCC than CON-LI (36 ± 4 vs. 57 ± 4 J s−1). Mechanical efficiency was 52 ± 4 % after 15 s of OCC and remained constant, whereas it decreased (P < 0.05) from 56 ± 5 to 32 ± 3 % during CON-LI. During CON-HI, mechanical efficiency transiently increased (P < 0.05) to 47 ± 4 %, after which it decreased (P < 0.05) to 36 ± 3 % at the end of CON-HI. Assuming a fully coupled mitochondrial respiration, the ATP turnover per unit of work was calculated to be unaltered during OCC (≈20 mmol ATP kJ−1), whereas it increased (P < 0.05) from 21 ± 4 to 29 ± 3 mmol ATP kJ−1 during CON-LI and further (P < 0.05) to 37 ± 3 mmol ATP kJ−1 during CON-HI. The present data confirm the hypothesis that heat loss is lower in anaerobic ATP resynthesis than in oxidative phosphorylation and can in part explain the finding that efficiency declines markedly during dynamic exercise. In addition, the rate of ATP turnover apparently increases during constant load low intensity exercise. Alternatively, mitochondrial efficiency is lowered as exercise progresses, since ATP turnover was unaltered during the ischaemic exercise bout.

AB - The aim of the present study was to simultaneously examine skeletal muscle heat production and ATP turnover in humans during dynamic exercise with marked differences in aerobic metabolism. This was done to test the hypothesis that efficiency is higher in anaerobic than aerobic ATP resynthesis. Six healthy male subjects performed 90 s of low intensity knee-extensor exercise with (OCC) and without thigh occlusion (CON-LI) as well as 90 s of high intensity exercise (CON-HI) that continued from the CON-LI bout. Muscle heat production was determined by continuous measurements of muscle heat accumulation and heat release to the blood. Muscle ATP production was quantified by repeated measurements of thigh oxygen uptake as well as blood and muscle metabolite changes. All temperatures of the thigh were equalized to ≈37 °C prior to exercise by a water-perfused heating cuff. Oxygen uptake accounted for 80 ± 2 and 59 ± 4 %, respectively, of the total ATP resynthesis in CON-LI and CON-HI, whereas it was negligible in OCC. The rise in muscle temperature was lower (P < 0.05) in OCC than CON-LI (0.32 ± 0.04 vs. 0.37 ± 0.03 °C). The mean rate of heat production was also lower (P < 0.05) in OCC than CON-LI (36 ± 4 vs. 57 ± 4 J s−1). Mechanical efficiency was 52 ± 4 % after 15 s of OCC and remained constant, whereas it decreased (P < 0.05) from 56 ± 5 to 32 ± 3 % during CON-LI. During CON-HI, mechanical efficiency transiently increased (P < 0.05) to 47 ± 4 %, after which it decreased (P < 0.05) to 36 ± 3 % at the end of CON-HI. Assuming a fully coupled mitochondrial respiration, the ATP turnover per unit of work was calculated to be unaltered during OCC (≈20 mmol ATP kJ−1), whereas it increased (P < 0.05) from 21 ± 4 to 29 ± 3 mmol ATP kJ−1 during CON-LI and further (P < 0.05) to 37 ± 3 mmol ATP kJ−1 during CON-HI. The present data confirm the hypothesis that heat loss is lower in anaerobic ATP resynthesis than in oxidative phosphorylation and can in part explain the finding that efficiency declines markedly during dynamic exercise. In addition, the rate of ATP turnover apparently increases during constant load low intensity exercise. Alternatively, mitochondrial efficiency is lowered as exercise progresses, since ATP turnover was unaltered during the ischaemic exercise bout.

KW - aerobic metabolism

KW - muscle heat production

KW - oxidative phosphorylation

U2 - 10.1113/jphysiol.2002.035089

DO - 10.1113/jphysiol.2002.035089

M3 - Article

VL - 549

SP - 255

EP - 269

JO - Journal of Physiology

T2 - Journal of Physiology

JF - Journal of Physiology

SN - 0022-3751

ER -