Skeletal muscle phosphocreatine recovery in exercise-trained humans is dependent on O2availability

1999 ◽  
Vol 86 (6) ◽  
pp. 2013-2018 ◽  
Author(s):  
Luke J. Haseler ◽  
Michael C. Hogan ◽  
Russell S. Richardson
Keyword(s):  
Skeletal Muscle ◽  
Oxidative Metabolism ◽  
Gastrocnemius Muscle ◽  
Plantar Flexion ◽  
Oxidative Capacity ◽  
Submaximal Exercise ◽  
Resonance Spectroscopy ◽  
The Relationship ◽  
Male Subjects ◽  
Plantar Flexion Exercise

In skeletal muscle, phosphocreatine (PCr) recovery from submaximal exercise has become a reliable and accepted measure of muscle oxidative capacity. During exercise, O2 availability plays a role in determining maximal oxidative metabolism, but the relationship between O2 availability and oxidative metabolism measured by31P-magnetic resonance spectroscopy (MRS) during recovery from exercise has never been studied. We used 31P-MRS to study exercising human gastrocnemius muscle under conditions of varied fractions of inspired O2 [Formula: see text]) to test the hypothesis that varied O2availability modulates PCr recovery from submaximal exercise. Six male subjects performed three bouts of 5-min steady-state submaximal plantar flexion exercise followed by 5 min of recovery in a 1.5-T magnet while breathing three different[Formula: see text] concentrations (0.10, 0.21, and 1.00). Under each[Formula: see text] treatment, the PCr recovery time constants were significantly different, being longer in hypoxia [33.5 ± 4.1 s (SE)] and shorter in hyperoxia (20.0 ± 1.8 s) than in normoxia (25.0 ± 2.7 s) ( P ≤ 0.05). End-exercise pH was not significantly different among the three treatments (7.08 ± 0.01 for 0.10, 7.04 ± 0.01 for 0.21, and 7.04 ± 0.02 for 1.00). These results demonstrate that PCr recovery is significantly altered by[Formula: see text] and suggest that, after submaximal exercise, PCr recovery, under normoxic conditions, is limited by O2 availability.

Skeletal muscle oxidative metabolism in sedentary humans: 31P-MRS assessment of O2 supply and demand limitations

2004 ◽  
Vol 97 (3) ◽  
pp. 1077-1081 ◽  
Author(s):  
Luke J. Haseler ◽  
Alexander P. Lin ◽  
Russell S. Richardson
Keyword(s):  
Gastrocnemius Muscle ◽  
Supply And Demand ◽  
Plantar Flexion ◽  
Submaximal Exercise ◽  
Resonance Spectroscopy ◽  
O2 Supply ◽  
Sedentary Subjects ◽  
Mitochondrial Capacity ◽  
Oxidative Rate ◽  
Plantar Flexion Exercise

Previously, it was demonstrated in exercise-trained humans that phosphocreatine (PCr) recovery is significantly altered by fraction of inspired O2 (FiO2), suggesting that in this population under normoxic conditions, O2 availability limits maximal oxidative rate. Haseler LJ, Hogan ML, and Richardson RS. J Appl Physiol 86: 2013–2018, 1999. To further elucidate these population-specific limitations to metabolic rate, we used 31P-magnetic resonance spectroscopy to study the exercising human gastrocnemius muscle under conditions of varied FiO2 in sedentary subjects. To test the hypothesis that PCr recovery from submaximal exercise in sedentary subjects is not limited by O2 availability, but rather by their mitochondrial capacity, six sedentary subjects performed three bouts of 6-min steady-state submaximal plantar flexion exercise followed by 5 min of recovery while breathing three different FiO2 (0.10, 0.21, and 1.00). PCr recovery time constants were significantly longer in hypoxia (47.0 ± 3.2 s), but there was no difference between hyperoxia (31.8 ± 1.9 s) and normoxia (30.0 ± 2.1 s) (mean ± SE). End-exercise pH was not significantly different across treatments. These results suggest that the maximal muscle oxidative rate of these sedentary subjects, unlike their exercise-trained counterparts, is limited by mitochondrial capacity and not O2 availability in normoxia. Additionally, the significant elongation of PCr recovery in these subjects in hypoxia illustrates the reliance on O2 supply at the other end of the O2 availability spectrum in both sedentary and active populations.

scholarly journals A cross-validation of near-infrared spectroscopy measurements of skeletal muscle oxidative capacity with phosphorus magnetic resonance spectroscopy

2013 ◽  
Vol 115 (12) ◽  
pp. 1757-1766 ◽  
Author(s):  
Terence E. Ryan ◽  
W. Michael Southern ◽  
Mary Ann Reynolds ◽  
Kevin K. McCully
Keyword(s):  
Skeletal Muscle ◽  
Near Infrared ◽  
Plantar Flexion ◽  
Oxidative Capacity ◽  
Resonance Spectroscopy ◽  
Time Constants ◽  
Muscle Oxidative Capacity ◽  
Muscle Oxygen ◽  
Muscle Oxygen Consumption ◽  
Plantar Flexion Exercise

The purpose of this study was to cross-validate measurements of skeletal muscle oxidative capacity made with near-infrared spectroscopy (NIRS) measurements to those made with phosphorus magnetic resonance spectroscopy (31P-MRS). Sixteen young (age = 22.5 ± 3.0 yr), healthy individuals were tested with both 31P-MRS and NIRS during a single testing session. The recovery rate of phosphocreatine was measured inside the bore of a 3-Tesla MRI scanner, after short-duration (∼10 s) plantar flexion exercise as an index of skeletal muscle oxidative capacity. Using NIRS, the recovery rate of muscle oxygen consumption was also measured using repeated, transient arterial occlusions outside the MRI scanner, after short-duration (∼10 s) plantar flexion exercise as another index of skeletal muscle oxidative capacity. The average recovery time constant was 31.5 ± 8.5 s for phosphocreatine and 31.5 ± 8.9 s for muscle oxygen consumption for all participants ( P = 0.709). 31P-MRS time constants correlated well with NIRS time constants for both channel 1 (Pearson's r = 0.88, P < 0.0001) and channel 2 (Pearson's r = 0.95, P < 0.0001). Furthermore, both 31P-MRS and NIRS exhibit good repeatability between trials (coefficient of variation = 8.1, 6.9, and 7.9% for NIRS channel 1, NIRS channel 2, and 31P-MRS, respectively). The good agreement between NIRS and 31P-MRS indexes of skeletal muscle oxidative capacity suggest that NIRS is a valid method for assessing mitochondrial function, and that direct comparisons between NIRS and 31P-MRS measurements may be possible.

Interrelationship of oxidative metabolism and local perfusion demonstrated by NMR in human skeletal muscle

1996 ◽  
Vol 81 (5) ◽  
pp. 2221-2228 ◽  
Author(s):  
Jean-François Toussaint ◽  
Kenneth K. Kwong ◽  
Fidelis M’Kparu ◽  
Robert M. Weisskoff ◽  
Paul J. Laraia ◽  
...  
Keyword(s):  
Skeletal Muscle ◽  
Magnetic Resonance ◽  
Time Constant ◽  
Oxidative Metabolism ◽  
Human Skeletal Muscle ◽  
Plantar Flexion ◽  
High Energy ◽  
Resonance Spectroscopy ◽  
Mean Flow ◽  
Normal Volunteers

Toussaint, Jean-François, Kenneth K. Kwong, Fidelis M’Kparu, Robert M. Weisskoff, Paul J. LaRaia, and Howard L. Kantor.Interrelationship of oxidative metabolism and local perfusion demonstrated by NMR in human skeletal muscle. J. Appl. Physiol. 81(5): 2221–2228, 1996.—Using nuclear magnetic resonance (NMR), we have examined the relationship of high-energy phosphate metabolism and perfusion in human soleus and gastrocnemius muscles. With31P-NMR spectroscopy, we monitored phosphocreatine (PCr) decay and recovery in eight normal volunteers and four heart failure patients performing ischemic plantar flexion. By using echo-planar imaging, perfusion was independently measured by a local [inversion-recovery (T1-flow)] and a regional technique (NMR-plethysmography). After correction for its pH dependence, PCr recovery time constant is 27.5 ± 8.0 s in normal volunteers, with mean flow 118 ± 75 (soleus and gastrocnemius T1-flow) and 30.2 ± 9.7 ml ⋅ 100 ml−1 ⋅ min−1(NMR-plethysmography-flow). We demonstrate a positive correlation between PCr time constant and local perfusion given by y = 50 − 0.15 x( r 2 = 0.68, P = 0.01) for the 8 normal subjects, and y = 64 − 0.24 x( r 2 = 0.83, P = 0.0001) for the 12 subjects recruited in the study. Regional perfusion techniques also show a significant but weaker correlation. Using this totally noninvasive method, we conclude that aerobic ATP resynthesis is related to the magnitude of perfusion, i.e., O2availability, and demonstrate that magnetic resonance imaging and magnetic resonance spectroscopy together can accurately assess muscle functional status.

scholarly journals THE RELATIONSHIP BETWEEN CYTOCHONDRIA AND MYOFIBRILS IN PIGEON SKELETAL MUSCLE

1953 ◽  
Vol 98 (1) ◽  
pp. 81-98 ◽  
Author(s):  
John W. Harman ◽  
Ursula H. Osborne
Keyword(s):  
Skeletal Muscle ◽  
Oxidative Phosphorylation ◽  
Oxidative Metabolism ◽  
Krebs Cycle ◽  
Oxidative Capacity ◽  
Breast Muscle ◽  
Oxidative Enzymes ◽  
Mitochondrial Oxidative Capacity ◽  
The Relationship ◽  
Oxidative Rate

In pigeon breast muscle the mitochondria are the principal site of oxidative metabolism, whereas the myofibrils are incapable of oxidizing intermediates of the Krebs cycle. The mitochondria contain the oxidative enzymes, and the sarcosomes are associated with a factor which accelerates the mitochondrial oxidative rate. The maintenance of myofibrillar contractility and structure is closely correlated with preservation of mitochondrial oxidative capacity and structure. By use of fluoride and dinitrophenol the connection between mitochondrial metabolism and myofibrillar behavior is shown to occur through the process of oxidative phosphorylation.

The insulin action-fiber type relationship in humans is muscle group specific

1995 ◽  
Vol 269 (1) ◽  
pp. E150-E154 ◽  
Author(s):  
M. S. Hickey ◽  
M. D. Weidner ◽  
K. E. Gavigan ◽  
D. Zheng ◽  
G. L. Tyndall ◽  
...  
Keyword(s):  
Skeletal Muscle ◽  
Insulin Action ◽  
Citrate Synthase ◽  
Fiber Type ◽  
Vastus Lateralis ◽  
Oxidative Capacity ◽  
Muscle Groups ◽  
The Relationship ◽  
Male Subjects

The purpose of the present investigation was to determine the relationship between skeletal muscle characteristics, adiposity, and in vivo insulin action. Percutaneous muscle biopsies of the vastus lateralis (VL) and gastrocnemius (G) muscles were obtained from twenty-two sedentary male subjects. Insulin sensitivity (SI) and glucose effectiveness (SG) were determined from minimal model analysis, and indexes of regional and overall adiposity were obtained. SI was positively related to the citrate synthase activity from the VL (r = 0.50, P < 0.01) but unrelated to the citrate synthase activity from the G (r = 0.28). Similarly, SI was inversely related to the percentage of type IIb fibers in the VL (r = -0.47, P < 0.01) but unrelated to the percentage of type IIb fibers in the G (r = 0.06). SG was unrelated to fiber type, oxidative capacity, or adiposity. These data suggest that oxidative capacity and other characteristics related to VL skeletal muscle fiber type are determinants of in vivo insulin action but that this relationship cannot be extended to all muscle groups. Finally, neither skeletal muscle characteristics nor adiposity appears to be a determinant of SG in sedentary males.

scholarly journals Oxygen delivery and the restoration of the muscle energetic balance following exercise: implications for delayed muscle recovery in patients with COPD

2017 ◽  
Vol 313 (1) ◽  
pp. E94-E104 ◽  
Author(s):  
Gwenael Layec ◽  
Corey R. Hart ◽  
Joel D. Trinity ◽  
Oh-Sung Kwon ◽  
Matthew J. Rossman ◽  
...  
Keyword(s):  
Skeletal Muscle ◽  
Blood Flow ◽  
Time Constant ◽  
Plantar Flexion ◽  
Chronic Obstructive ◽  
Resonance Spectroscopy ◽  
Proton Efflux ◽  
Muscle Recovery ◽  
Delayed Recovery ◽  
Plantar Flexion Exercise

Patients with chronic obstructive pulmonary disease (COPD) experience a delayed recovery from skeletal muscle fatigue following exhaustive exercise that likely contributes to their progressive loss of mobility. As this phenomenon is not well understood, this study sought to examine postexercise peripheral oxygen (O2) transport and muscle metabolism dynamics in patients with COPD, two important determinants of muscle recovery. Twenty-four subjects, 12 nonhypoxemic patients with COPD and 12 healthy subjects with a sedentary lifestyle, performed dynamic plantar flexion exercise at 40% of the maximal work rate (WRmax) with phosphorus magnetic resonance spectroscopy (31P-MRS), near-infrared spectroscopy (NIRS), and vascular Doppler ultrasound assessments. The mean response time of limb blood flow at the offset of exercise was significantly prolonged in patients with COPD (controls: 56 ± 27 s; COPD: 120 ± 87 s; P < 0.05). In contrast, the postexercise time constant for capillary blood flow was not significantly different between groups (controls: 49 ± 23 s; COPD: 51 ± 21 s; P > 0.05). The initial postexercise convective O2 delivery (controls: 0.15 ± 0.06 l/min; COPD: 0.15 ± 0.06 l/min) and the corresponding oxidative adenosine triphosphate (ATP) demand (controls: 14 ± 6 mM/min; COPD: 14 ± 6 mM/min) in the calf were not significantly different between controls and patients with COPD ( P > 0.05). The phosphocreatine resynthesis time constant (controls: 46 ± 20 s; COPD: 49 ± 21 s), peak mitochondrial phosphorylation rate, and initial proton efflux were also not significantly different between groups ( P > 0.05). Therefore, despite perturbed peripheral hemodynamics, intracellular O2 availability, proton efflux, and aerobic metabolism recovery in the skeletal muscle of nonhypoxemic patients with COPD are preserved following plantar flexion exercise and thus are unlikely to contribute to the delayed recovery from exercise in this population.

Octanoate oxidation measured by13C-NMR spectroscopy in rat skeletal muscle, heart, and liver

2003 ◽  
Vol 95 (5) ◽  
pp. 1908-1916 ◽  
Author(s):  
Marlei E. Walton ◽  
Douglas Ebert ◽  
Ronald G. Haller
Keyword(s):  
Skeletal Muscle ◽  
Nmr Spectroscopy ◽  
Oxidative Metabolism ◽  
Gastrocnemius Muscle ◽  
Oxidative Capacity ◽  
Acid Oxidation ◽  
Acetyl Coa ◽  
Inhalation Anesthesia ◽  
Fractional Contribution ◽  
Muscle Types

Contribution of octanoate to the oxidative metabolism of the major sites of fatty acid oxidation (heart, liver, and resting and contracting skeletal muscle) was assessed in the intact rat with13C-NMR spectroscopy. Under inhalation anesthesia, [2,4,6,8-13C4]octanoate was infused into the jugular vein and the sciatic nerve of one limb was stimulated for 1 h. Octanoate was a principal contributor to the acetyl-CoA pool in all tissues examined, with highest oxidation occurring in heart and soleus muscle followed by predominantly red portion of gastrocnemius muscle (RG), liver, and then white portion of gastrocnemius muscle (WG). Fractional contribution of13C-labeled octanoate to the acetyl-CoA pool (Fc2) was 0.563 ± 0.066 for heart and 0.367 ± 0.054 for liver. Significant differences were observed between each of the muscle types during both rest and contraction. In muscle, Fc2 was highest in soleus (0.565 ± 0.089 rested, 0.564 ± 0.096 contracted), followed by RG (0.470 ± 0.092 rested, 0.438 ± 0.072 contracted), and lowest in WG (0.340 ± 0.081 rested, 0.272 ± 0.065 contracted). Our findings demonstrate that the fractional contribution of octanoate to oxidative metabolism correlates with oxidative capacity of the tissue and that octanoate metabolism increases in contracted muscle in proportion to the overall increase in oxidative rate.

scholarly journals Systemic oxidative stress is associated with lower aerobic capacity and impaired skeletal muscle energy metabolism in heart failure patients

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Takashi Yokota ◽  
Shintaro Kinugawa ◽  
Kagami Hirabayashi ◽  
Mayumi Yamato ◽  
Shingo Takada ◽  
...  
Keyword(s):  
Oxidative Stress ◽  
Heart Failure ◽  
Skeletal Muscle ◽  
Energy Metabolism ◽  
Aerobic Capacity ◽  
Plantar Flexion ◽  
Exercise Intolerance ◽  
Whole Body ◽  
Resonance Spectroscopy ◽  
Systemic Oxidative Stress

AbstractOxidative stress plays a role in the progression of chronic heart failure (CHF). We investigated whether systemic oxidative stress is linked to exercise intolerance and skeletal muscle abnormalities in patients with CHF. We recruited 30 males: 17 CHF patients, 13 healthy controls. All participants underwent blood testing, cardiopulmonary exercise testing, and magnetic resonance spectroscopy (MRS). The serum thiobarbituric acid reactive substances (TBARS; lipid peroxides) were significantly higher (5.1 ± 1.1 vs. 3.4 ± 0.7 μmol/L, p < 0.01) and the serum activities of superoxide dismutase (SOD), an antioxidant, were significantly lower (9.2 ± 7.1 vs. 29.4 ± 9.7 units/L, p < 0.01) in the CHF cohort versus the controls. The oxygen uptake (VO2) at both peak exercise and anaerobic threshold was significantly depressed in the CHF patients; the parameters of aerobic capacity were inversely correlated with serum TBARS and positively correlated with serum SOD activity. The phosphocreatine loss during plantar-flexion exercise and intramyocellular lipid content in the participants' leg muscle measured by 31phosphorus- and 1proton-MRS, respectively, were significantly elevated in the CHF patients, indicating abnormal intramuscular energy metabolism. Notably, the skeletal muscle abnormalities were related to the enhanced systemic oxidative stress. Our analyses revealed that systemic oxidative stress is related to lowered whole-body aerobic capacity and skeletal muscle dysfunction in CHF patients.

HIF-1α in endurance training: suppression of oxidative metabolism

2007 ◽  
Vol 293 (5) ◽  
pp. R2059-R2069 ◽  
Author(s):  
Steven D. Mason ◽  
Helene Rundqvist ◽  
Ioanna Papandreou ◽  
Roger Duh ◽  
Wayne J. McNulty ◽  
...  
Keyword(s):  
Skeletal Muscle ◽  
Endurance Training ◽  
Oxidative Metabolism ◽  
Hypoxia Inducible Factor ◽  
Transcriptional Response ◽  
Oxidative Capacity ◽  
Pyruvate Dehydrogenase Kinase ◽  
Amp Activated Protein Kinase ◽  
Training Protocol

During endurance training, exercising skeletal muscle experiences severe and repetitive oxygen stress. The primary transcriptional response factor for acclimation to hypoxic stress is hypoxia-inducible factor-1α (HIF-1α), which upregulates glycolysis and angiogenesis in response to low levels of tissue oxygenation. To examine the role of HIF-1α in endurance training, we have created mice specifically lacking skeletal muscle HIF-1α and subjected them to an endurance training protocol. We found that only wild-type mice improve their oxidative capacity, as measured by the respiratory exchange ratio; surprisingly, we found that HIF-1α null mice have already upregulated this parameter without training. Furthermore, untrained HIF-1α null mice have an increased capillary to fiber ratio and elevated oxidative enzyme activities. These changes correlate with constitutively activated AMP-activated protein kinase in the HIF-1α null muscles. Additionally, HIF-1α null muscles have decreased expression of pyruvate dehydrogenase kinase I, a HIF-1α target that inhibits oxidative metabolism. These data demonstrate that removal of HIF-1α causes an adaptive response in skeletal muscle akin to endurance training and provides evidence for the suppression of mitochondrial biogenesis by HIF-1α in normal tissue.

scholarly journals Evidence that a higher ATP cost of muscular contraction contributes to the lower mechanical efficiency associated with COPD: preliminary findings

2011 ◽  
Vol 300 (5) ◽  
pp. R1142-R1147 ◽  
Author(s):  
Gwenael Layec ◽  
Luke J. Haseler ◽  
Jan Hoff ◽  
Russell S. Richardson
Keyword(s):  
Skeletal Muscle ◽  
Muscle Contraction ◽  
Energy Cost ◽  
Plantar Flexion ◽  
Mechanical Efficiency ◽  
Exercise Intolerance ◽  
Chronic Obstructive ◽  
Small Subset ◽  
Resonance Spectroscopy ◽  
Muscle Energetics

Impaired metabolism in peripheral skeletal muscles potentially contributes to exercise intolerance in chronic obstructive pulmonary disease (COPD). We used 31P-magnetic resonance spectroscopy (31P-MRS) to examine the energy cost and skeletal muscle energetics in six patients with COPD during dynamic plantar flexion exercise compared with six well-matched healthy control subjects. Patients with COPD displayed a higher energy cost of muscle contraction compared with the controls (control: 6.1 ± 3.1% of rest·min−1·W−1, COPD: 13.6 ± 8.3% of rest·min−1·W−1, P = 0.01). Although, the initial phosphocreatine resynthesis rate was also significantly attenuated in patients with COPD compared with controls (control: 74 ± 17% of rest/min, COPD: 52 ± 13% of rest/min, P = 0.04), when scaled to power output, oxidative ATP synthesis was similar between groups (6.5 ± 2.3% of rest·min−1·W−1 in control and 7.8 ± 3.9% of rest·min−1·W−1 in COPD, P = 0.52). Therefore, our results reveal, for the first time that in a small subset of patients with COPD a higher ATP cost of muscle contraction may substantially contribute to the lower mechanical efficiency previously reported in this population. In addition, it appears that some patients with COPD have preserved mitochondrial function and normal energy supply in lower limb skeletal muscle.

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