Time‐courses of perfusion and phosphocreatine in rat leg during low‐level exercise and recovery

Marro, Kenneth I.; Olive, Jennifer L.; Hyyti, Outi M.; Kushmerick, Martin J.

doi:10.1002/jmri.20903

Cited by 10 publications

(10 citation statements)

References 46 publications

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“…Although, there are data that suggest PCr recovery rate is linked to PCr depletion (30), in our hands (10) and in older (19) and very recent publications (17) it is more commonly recognized that these variables are independent of each other (especially if pH is relatively unperturbed, as it was in the current study). The Fig.…”

Section: Discussionmentioning

confidence: 42%

Oxygen availability and PCr recovery rate in untrained human calf muscle: evidence of metabolic limitation in normoxia

Haseler¹,

Lin²,

Hoff³

et al. 2007

American Journal of Physiology-Regulatory, Integrative and Comp

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Haseler LJ, Lin A, Hoff J, Richardson RS. Oxygen availability and PCr recovery rate in untrained human calf muscle: evidence of metabolic limitation in normoxia. Am J Physiol Regul Integr Comp Physiol 293: R2046-R2051, 2007. First published August 22, 2007; doi:10.1152/ajpregu.00039.2007.-In contrast to their exercisetrained counterparts, the maximal oxidative rate of skeletal muscle in sedentary humans appears not to benefit from supplemental O 2 availability but is impacted by severe hypoxia, suggesting a metabolic limitation either at or below ambient O2 levels. However, the critical level of O2 availability at which maximal metabolic rate is reduced in sedentary humans is unknown. Using 31 P magnetic resonance spectroscopy and arterial oximetry, phosphocreatine (PCr) recovery kinetics and arterial oxygenation were assessed in six sedentary subjects performing 5-min bouts of plantar flexion exercise followed by 6 min of recovery. Each trial was repeated while breathing one of four different fractions of inspired O2 (FIO 2 ) (0.10, 0.12, 0.15, and 0.21). The PCr recovery rate constant (a marker of oxidative capacity) was unaffected by reductions in FI O 2 , remaining at a value of 1.5 Ϯ 0.2 min Ϫ1 until arterial O2 saturation (Sa O 2 ) fell to less than ϳ92%, the average value reached breathing an FI O 2 of 0.15. Below this SaO 2 , the PCr rate constant fell significantly by 13 and 31% to 1.3 Ϯ 0.2 and 1.0 Ϯ 0.2 min Ϫ1 (P Ͻ 0.05) as SaO 2 was reduced to 82 Ϯ 3 and 77 Ϯ 2%, respectively. In conclusion, this study has revealed that O 2 availability does not impact maximal oxidative rate in sedentary humans until the O 2 level falls well below that of ambient air, indicating a metabolic limitation in normoxia. oxidative capacity; 31 P-magnetic resonance spectroscopy; exercise THE REDUCED OXYGEN AVAILABILITY of severe hypoxia uniformly attenuates human maximal oxidative metabolic rate; however, limitations to maximal oxidative rate in normoxia and the impact of moderate hypoxia appear to be dependent on the exercise training status of the population studied (5,16,24). The clear dependence between O 2 supply and skeletal muscle maximal oxidative rate assessed during maximal exercise in trained human muscle has been previously recognized (24). In fact, these in vivo studies revealed that under hyperoxic conditions the maximal metabolic rate of these well-trained subjects increased beyond ambient levels, revealing O 2 supply limitation in normoxia (24). Phosphocreatine (PCr) recovery measurements, as an index of maximal oxidative rate, have provided further evidence of this O 2 supply limited maximal metabolic rate in normoxia in the muscle of exercise-trained humans but have failed to identify the level of O 2 availability that creates an O 2 surplus as this appears to fall beyond that achieved by delivering 100% O 2 (9). While a similar hyperoxic approach failed to alter the metabolic rate in the untrained muscle (Fig. 1), a unifying result is observed in both trained and untrained human skeletal muscle when seve...

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Section: Discussionmentioning

confidence: 42%

Oxygen availability and PCr recovery rate in untrained human calf muscle: evidence of metabolic limitation in normoxia

Haseler¹,

Lin²,

Hoff³

et al. 2007

American Journal of Physiology-Regulatory, Integrative and Comp

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“…However, the time course for the observed effect (2 to 3 h postconsumption) in the present study makes this an unlikely mechanism for the AO-mediated improvement in PCr recovery. Alternately, there is already evidence supporting the influence of perfusion on muscle energetics from NMR-based studies, with a clear association between O 2 availability and the rate of PCr recovery at the end of exercise in animals (23) and normal, healthy subjects (15,16). Furthermore, while recognizing the limitation of correlation analysis with small sample sizes, a clear relationship (r 2 ϭ 0.84) between metabolism and perfusion was noted in the present study, such that the greatest AO-induced increase in perfusion AUC also yielded the largest improvement in PCr recovery time.…”

Section: Discussionmentioning

confidence: 99%

Antioxidants and aging: NMR-based evidence of improved skeletal muscle perfusion and energetics

Wray

Nishiyama

Wary

et al. 2009

American Journal of Physiology-Heart and Circulatory Physiology

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Wray DW, Nishiyama SK, Monnet A, Wary C, Duteil SS, Carlier PG, Richardson RS. Antioxidants and aging: NMR-based evidence of improved skeletal muscle perfusion and energetics. Am J Physiol Heart Circ Physiol 297: H1870 -H1875, 2009. First published September 18, 2009 doi:10.1152/ajpheart.00709.2009.-We sought to examine the potential role of oxidative stress on skeletal muscle function with advancing age. Nuclear magnetic resonance (NMR) was employed to simultaneously assess muscle perfusion (arterial spin labeling) and energetics ( 31 P NMR spectroscopy) in the lower leg of young (26 Ϯ 5 yr, n ϭ 6) and older (70 Ϯ 5 yr, n ϭ 6) healthy volunteers following the consumption of either placebo (PL) or an oral antioxidant (AO) cocktail (vitamins C and E and ␣-lipoic acid), previously documented to decrease plasma free radical concentration. NMR measurements were made during and after 5 min of moderate intensity (Ϸ5 W) plantar flexion exercise. AO administration significantly improved end-exercise perfusion (AO, 50 Ϯ 5, and PL, 43 Ϯ 4 ml⅐ 100 g Ϫ1 ⅐ min Ϫ1 ) and postexercise perfusion area under the curve (AO, 1,286 Ϯ 236, and PL, 866 Ϯ 144 ml/100 g) in older subjects, whereas AO administration did not alter hemodynamics in the young group. Concomitantly, muscle oxidative capacity (time constant of phosphocreatine recovery, ) was improved following AO in the older (AO, 43 Ϯ 1, and PL, 51 Ϯ 7 s) but not the young (AO, 54 Ϯ 5, and PL, 48 Ϯ 7 s) group. These findings support the concept that oxidative stress may be partially responsible for the age-related decline in skeletal muscle perfusion during physical activity and reveal a muscle metabolic reserve capacity in the elderly that is accessible under conditions of improved perfusion. leg blood flow; oxidative capacity; exercise; nuclear magnetic resonance WITH ADVANCING AGE, structural and functional changes in the peripheral vasculature develop with potentially deleterious consequences, including a diminished perfusion of skeletal muscle both at rest and during exercise (3,7,8,22,25,26,30,36). The detrimental effects of this age-associated decline in muscle perfusion and the associated decrement in O 2 delivery could be closely linked to muscle energetics, as evidenced by the previously demonstrated decline in skeletal muscle oxidative capacity under O 2 supply-limited conditions in young, healthy individuals (15, 16). Despite the potentially negative impact of these age-associated changes, the practical consequence of reduced skeletal muscle blood flow in this cohort remains poorly understood.The paucity of information concerning the effects of reduced perfusion on muscle function with healthy aging may be due in part to the difficulty of simultaneously assessing perfusion and metabolism within skeletal muscle. Using multiparametric nuclear magnetic resonance (NMR) techniques, we have begun to address this issue and have recently documented that the age-related decline in bulk limb blood flow is also evident when perfusion within the skeletal muscle is examined duri...

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“…Upon the cessation of exercise or ischemia, PCr, P i , and pH recover to baseline level. The time constant of PCr recovery in calf muscle is about 25 to 35 s in humans (99,104) and 50 to 90 s in small animals (96,99,102,105). Prolonged PCr recovery is considered to reflect deficits in mitochondrial oxidative metabolism (6,106).…”

Section: P-mrsmentioning

confidence: 99%

“…Continuous acquisition of 31 P spectra during exercise-recovery or ischemia-reperfusion provides the potential to assess mitochondrial oxidative capacity by quantifying the kinetics of PCr depletion and replenishment. Dynamic 31 P-MRS has been applied to assess skeletal muscle bioenergetics under physiological conditions (60,61,87,(96)(97)(98)(99), as well as to evaluate mitochondrial function in skeletal muscle in both diabetic patients and animal models of diabetes (8,(100)(101)(102). Figure 3 shows dynamic 31 P spectra and the changes of phosphate metabolites and pH during muscle contraction and recovery in human skeletal muscle (103).…”

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confidence: 99%

Assessing tissue metabolism by phosphorous-31 magnetic resonance spectroscopy and imaging: a methodology review

Liu

2017

Quant. Imaging Med. Surg.

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Many human diseases are caused by an imbalance between energy production and demand.Magnetic resonance spectroscopy (MRS) and magnetic resonance imaging (MRI) provide the unique opportunity for in vivo assessment of several fundamental events in tissue metabolism without the use of ionizing radiation. Of particular interest, phosphate metabolites that are involved in ATP generation and utilization can be quantified noninvasively by phosphorous-31 ( 31 P) MRS/MRI. Furthermore, 31 P magnetization transfer (MT) techniques allow in vivo measurement of metabolic fluxes via creatine kinase (CK) and ATP synthase. However, a major impediment for the clinical applications of 31 P-MRS/MRI is the prohibitively long acquisition time and/or the low spatial resolution that are necessary to achieve adequate signal-to-noise ratio. P-MRS/MRI techniques. Applications of these techniques to the investigation of a specific physiology/pathology will be discussed without detailed description. Interested readers are referred to recent review articles on the applications of 31 P-MRS/MRI in metabolic characterization of skeletal muscle (10-12), heart (13), brain (14), and liver (11), as well as in diseases such as cancer (15), heart failure (16), and obesity and diabetes (17,18). Historical perspectiveThe use of 31 P-MRS for metabolic investigations dates back to 1960. Cohn and Hughes were the first to obtain a high-resolution 31 P spectrum of a solution of ATP (19). In addition, they also observed a dependence of the chemical shifts of the phosphorus nuclei of ATP on the pH of the solution. In parallel to the early development of MRI methods by Lauterbur (20), the entire 1970s also witnessed the rapid advance of 31 P-MRS in metabolic investigation of a broad range of biological systems. In 1973, Moon and Richards performed the first 31 P-MRS study that measured intracellular pH in human red blood cells (21). In the following year, Henderson and colleagues obtained the first 31 P spectrum of ATP from human red blood cells (22). At the same time, the Oxford team led by Radda performed the first experiment to acquire 31 P spectra from an intact organ, i.e., the excised and superfused muscle of rat hindlimb (23). The first in vivo 31 P-MRS study was performed on mouse brain by Chance et al. (24). Within the short span of one decade, organelles including mitochondria (25,26) and chromaffin granules (27), cells including Escherichia coli (28), yeast (29), and hepatocytes (30), and organs including skeletal muscle (31,32), heart (33-35), brain (36), kidney (37), and liver (38,39) have all been studied using 31 P-MRS.It is worth noting that most of these organ studies were performed on excised organs to avoid the need for spatial localization. Although Lauterbur has demonstrated the feasibility of imaging water protons (20), it was considered impractical for 31 P imaging of living systems because of the low sensitivity and difficulties with spectral resolution.The 1980s began with the publication of two important studies that aimed a...

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Time‐courses of perfusion and phosphocreatine in rat leg during low‐level exercise and recovery

Cited by 10 publications

References 46 publications

Oxygen availability and PCr recovery rate in untrained human calf muscle: evidence of metabolic limitation in normoxia

Oxygen availability and PCr recovery rate in untrained human calf muscle: evidence of metabolic limitation in normoxia

Antioxidants and aging: NMR-based evidence of improved skeletal muscle perfusion and energetics

Assessing tissue metabolism by phosphorous-31 magnetic resonance spectroscopy and imaging: a methodology review

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