Accurate work-rate measurements during in vivo MRS studies of exercising human quadriceps

Bringard²,

et al. 2010

NMR in Biomedicine

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Muscle energetics has been largely and quantitatively investigated using (31)P MRS. Various methods have been used to estimate the corresponding rate of oxidative ATP synthesis (ATP(ox)); however, potential differences among methods have not been investigated. In this study, we aimed to compare the rates of ATP production and energy cost in two groups of subjects with different training status using four different methods: indirect method (method 1), ADP control model (method 2) and phosphate potential control model (method 3). Method 4 was a modified version of method 3 with the introduction of a correction factor allowing for similar values to be obtained for the end-exercise oxidative ATP synthesis rate inferred from exercise measurements and the initial recovery phosphocreatine resynthesis rate. Seven sedentary and seven endurance-trained subjects performed a dynamic standardised rest-exercise-recovery protocol. We quantified the rates of ATP(ox) and anaerobic ATP synthesis (ATP(ana)) using (31)P MRS data recorded at 1.5 T. The rates of ATP(ox) over the entire exercise session were independent of the method used, except for method 4 which provided significantly higher values in both groups (p < 0.01). In addition, methods 1-3 were cross-correlated, thereby confirming their statistical agreement. The rate of ATP(ana) was significantly higher with method 1 (p < 0.01) and lower with method 4 (p < 0.01). As a result of the higher rate of ATP(ox), EC (method 4) calculated over the entire exercise session was higher and initial EC (method 1) was lower in both groups compared with the other methods. We showed in this study that the rate of ATP(ox) was independent of the calculation method, as long as no corrections (method 4) were performed. In contrast, results related to the rates of ATP(ana) were strongly affected by the calculation method and, more exactly, by the estimation of protons generated by ATP(ox). Although the absolute EC values differed between the methods, within- or between-subject comparisons are still valid given the tight relationships between them.

Section: Experimental Protocolmentioning

confidence: 99%

Comparative determination of energy production rates and mitochondrial function using different ³¹P MRS quantitative methods in sedentary and trained subjects

Bringard²,

et al. 2010

NMR in Biomedicine

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“…The two-leg knee extension exercise test has been described in details elsewhere, together with the details related to the ergometer (30). Briefly, the subject lay prone within the 1.5T Siemens Vision Plus system (Siemens AG, Erlangen, Germany).…”

Section: Experimental Protocolmentioning

confidence: 99%

Reproducibility assessment of metabolic variables characterizing muscle energetics in Vivo: A ³¹P‐MRS study

Bringard²,

Magnetic Resonance in Med

et al. 2009

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The purpose of the present study was to assess the reliability of metabolic parameters measured using 31 P magnetic resonance spectroscopy ( 31 P MRS) during two standardized rest-exerciserecovery protocols. Twelve healthy subjects performed the standardized protocols at two different intensities; i.e., a moderate intensity (MOD) repeated over a two-month period and heavy intensity (HEAVY) repeated over a year's time. Test-retest reliability was analyzed using coefficient of variation ( Key words: magnetic resonance spectroscopy; reliability; oxidative capacity; PCr kinetics; exercise Phosphorus-31 nuclear magnetic resonance spectroscopy ( 31 P-MRS) is now widely accepted as the "gold standard" method for noninvasive measurements of energy metabolism in exercising muscle. The analysis of changes in phosphorylated compounds concentrations and intracellular pH during rest-exercise-recovery protocols has provided significant advance in the understanding of underlying mechanisms of muscle energy production (1-4). Given the noninvasiveness of the method, 31 P-MRS enables repeated measurements and has been successfully used in a wide range of situations such as the assessment of therapeutic interventions in patients with metabolic disorders (5-7) and the characterization of training-induced metabolic changes (8 -11). More recently, the dynamics of phosphocreatine (PCr) has been used to evaluate the control of mitochondrial respiration in skeletal muscle (12) or the mechanism underlying the V O 2p slow component (13) typically observed during a high-intensity exercise; i.e., above the lactate threshold. In addition, the rate constant of postexercise recovery kinetics of [PCr] has been used as an index of mitochondrial function (14 -17). In addition to these traditional variables, more sophisticated analyses have been put forth in order to quantify the contribution of oxidative and anaerobic pathways to energy production in exercising muscle (2,18,19).Despite the widespread use of 31 P MRS for muscle energetics investigation, the reproducibility of the corresponding variables has been scarcely investigated. It has actually been investigated through repeated measurements performed 1 week (5) and 4 weeks apart (20). Bendahan et al. (5) reported a good reliability in metabolic parameters when investigated using analysis of variance (ANOVA). However, detection of systematic bias might have been affected by large random error between tests as suggested previously (21). observed large test-retest variability in metabolic parameters measured during steady state phases of moderate isometric plantar flexion exercise. However, kinetics parameters of recovery exhibited a small coefficient of variation (CV Ͻ 9%). In this line, van den Broek et al. (22) reported a low variability (CV Ͻ 11.5%) for the parameters describing the recovery kinetics of PCr and adenosine diphosphate (ADP) in a single subject who repeated the same exercise protocol 10 times. Based on a visual inspection of the kinetics of phosphorylated compounds and pH i...

“…Despite the use of a relatively standardized (fixed-weight) exercise (40), it is interesting to note that a small, but significant, increase in mean power output resulted from an augmented displacement of the weight throughout the exercise. Indeed, we previously documented that our setup exhibits an inherent variability (ϳ15%) in the power output produced because of the subjects' difficulty with fine control of the range of motion throughout a 6-min exercise (39).…”

Section: Methodological Considerationmentioning

confidence: 99%

“…After a familiarization session, voluntary maximum isometric force [maximal voluntary contraction (MVC)] was determined during three repeated isometric leg extensions of each leg using a dedicated dynamometric ergometer (40). Subjects lay prone with the knee flexed at ϳ40°.…”

Section: Experimental Protocolmentioning

confidence: 99%

“…On separate days, subjects performed constant-load submaximal double-leg alternate knee extension-flexion at ϳ25% of MVC (rate of 1 Hz) in normoxia (FI O 2 ϭ 0.21) or hyperoxia (FIO 2 ϭ 1.0) in the Vision Plus whole body 1.5-T MRI system (Siemens, Erlangen, Germany), as previously described (40). Specifically, after 3 min of rest, subjects exercised for 6 min and then were allowed to recover for 6 min.…”

Section: Experimental Protocolmentioning

confidence: 99%

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Opposite effects of hyperoxia on mitochondrial and contractile efficiency in human quadriceps muscles

Bringard

American Journal of Physiology-Regulatory, Integrative and Comp

et al. 2015

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-Exercise efficiency is an important determinant of exercise capacity. However, little is known about the physiological factors that can modulate muscle efficiency during exercise. We examined whether improved O 2 availability would 1) impair mitochondrial efficiency and shift the energy production toward aerobic ATP synthesis and 2) reduce the ATP cost of dynamic contraction owing to an improved neuromuscular efficiency, such that 3) whole body O 2 cost would remain unchanged. We used 31 P-magnetic resonance spectroscopy, surface electromyography, and pulmonary O 2 consumption (V O2p) measurements in eight active subjects during 6 min of dynamic knee-extension exercise under different fractions of inspired O 2 (FIO 2 , 0.21 in normoxia and 1.0 in hyperoxia). V O2p (755 Ϯ 111 ml/min in normoxia and 799 Ϯ 188 ml/min in hyperoxia, P Ͼ 0.05) and O 2 cost (P Ͼ 0.05) were not significantly different between normoxia and hyperoxia. In contrast, the total ATP synthesis rate and the ATP cost of dynamic contraction were significantly lower in hyperoxia than normoxia (P Ͻ 0.05). As a result, the ratio of the rate of oxidative ATP synthesis from the quadriceps to V O2p was lower in hyperoxia than normoxia but did not reach statistical significance (16 Ϯ 3 mM/ml in normoxia and 12 Ϯ 5 mM/ml in hyperoxia, P ϭ 0.07). Together, these findings reveal dynamic and independent regulations of mitochondrial and contractile efficiency as a consequence of O 2 availability in young active individuals. Furthermore, muscle efficiency appears to be already optimized in normoxia and is unlikely to contribute to the well-established improvement in exercise capacity induced by hyperoxia.31 P-magnetic resonance spectroscopy; mitochondria; muscle efficiency; muscle energetics; O 2 availability EXERCISE EFFICIENCY, defined as the ratio of mechanical work performed to energy expended (65), plays a key role in exercise tolerance, since even a small improvement in efficiency brings about major increases in exercise capacity (22). Conversely, lower muscle efficiency significantly contributes to the reduced mobility and exercise intolerance associated with some debilitating disorders (30,43,51,67). Conceptually, muscle efficiency is determined to a similar extent by mitochondrial (conversion of chemical energy to ATP) and contractile (conversion of ATP to mechanical work, i.e., the cost of muscle contraction) efficiency (65). While the latter is commonly quantified using 31 P-magnetic resonance (MR) spectroscopy (MRS) (26), the measurement of mitochondrial efficiency in vivo is technically more challenging, as it requires the simultaneous measurement of O 2 consumption (V O 2 ) and ATP production. Consequently, it has actually been assayed very rarely in humans and only in resting muscle (1,46). Interestingly, we recently developed an experimental setup allowing the simultaneous measurement of pulmonary V O 2 (V O 2p ) (7) and oxidative ATP synthesis rate during knee-extension exercise (38) that can shed some light on mitochondrial efficiency in exe...