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      Neuromuscular Consequences of an Extreme Mountain Ultra-Marathon

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          Abstract

          We investigated the physiological consequences of one of the most extreme exercises realized by humans in race conditions: a 166-km mountain ultra-marathon (MUM) with 9500 m of positive and negative elevation change. For this purpose, (i) the fatigue induced by the MUM and (ii) the recovery processes over two weeks were assessed. Evaluation of neuromuscular function (NMF) and blood markers of muscle damage and inflammation were performed before and immediately following (n = 22), and 2, 5, 9 and 16 days after the MUM (n = 11) in experienced ultra-marathon runners. Large maximal voluntary contraction decreases occurred after MUM (−35% [95% CI: −28 to −42%] and −39% [95% CI: −32 to −46%] for KE and PF, respectively), with alteration of maximal voluntary activation, mainly for KE (−19% [95% CI: −7 to −32%]). Significant modifications in markers of muscle damage and inflammation were observed after the MUM as suggested by the large changes in creatine kinase (from 144±94 to 13,633±12,626 UI L −1), myoglobin (from 32±22 to 1,432±1,209 µg L −1), and C-Reactive Protein (from <2.0 to 37.7±26.5 mg L −1). Moderate to large reductions in maximal compound muscle action potential amplitude, high-frequency doublet force, and low frequency fatigue (index of excitation-contraction coupling alteration) were also observed for both muscle groups. Sixteen days after MUM, NMF had returned to initial values, with most of the recovery process occurring within 9 days of the race. These findings suggest that the large alterations in NMF after an ultra-marathon race are multi-factorial, including failure of excitation-contraction coupling, which has never been described after prolonged running. It is also concluded that as early as two weeks after such an extreme running exercise, maximal force capacities have returned to baseline.

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          Most cited references36

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          Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans.

          We investigated the role of somatosensory feedback from locomotor muscles on central motor drive (CMD) and the development of peripheral fatigue during high-intensity endurance exercise. In a double-blind, placebo-controlled design, eight cyclists randomly performed three 5 km time trials: control, interspinous ligament injection of saline (5K(Plac), L3-L4) or intrathecal fentanyl (5K(Fent), L3-L4) to impair cortical projection of opioid-mediated muscle afferents. Peripheral quadriceps fatigue was assessed via changes in force output pre- versus postexercise in response to supramaximal magnetic femoral nerve stimulation (DeltaQ(tw)). The CMD during the time trials was estimated via quadriceps electromyogram (iEMG). Fentanyl had no effect on quadriceps strength. Impairment of neural feedback from the locomotor muscles increased iEMG during the first 2.5 km of 5K(Fent) versus 5K(Plac) by 12 +/- 3% (P < 0.05); during the second 2.5 km, iEMG was similar between trials. Power output was also 6 +/- 2% higher during the first and 11 +/- 2% lower during the second 2.5 km of 5K(Fent) versus 5K(Plac) (both P < 0.05). Capillary blood lactate was higher (16.3 +/- 0.5 versus 12.6 +/- 1.0%) and arterial haemoglobin O(2) saturation was lower (89 +/- 1 versus 94 +/- 1%) during 5K(Fent) versus 5K(Plac). Exercise-induced DeltaQ(tw) was greater following 5K(Fent) versus 5K(Plac) (-46 +/- 2 versus -33 +/- 2%, P < 0.001). Our results emphasize the critical role of somatosensory feedback from working muscles on the centrally mediated determination of CMD. Attenuated afferent feedback from exercising locomotor muscles results in an overshoot in CMD and power output normally chosen by the athlete, thereby causing a greater rate of accumulation of muscle metabolites and excessive development of peripheral muscle fatigue.
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            A trauma-like elevation of plasma cytokines in humans in response to treadmill running.

            1. Elevated levels of cytokines, especially interleukin (IL)-6 and IL-1ra, can be measured in the plasma of athletes after exhaustive long term exercise. 2. The present study investigates the kinetics of several cytokines and chemokines in ten male athletes before, during and after 2.5 h of treadmill running at 75 % of maximal oxygen consumption (VO2,max). Blood was sampled before, every half-hour during running and every hour in the following 6 h recovery period. 3. The plasma concentration of IL-6 increased after 30 min of running, and peaked at the end of running with a 25-fold increase compared with the pre-exercise value. IL-1ra increased only after running, and peaked after 2 h of rest with an 18-fold increase compared with the pre-exercise value. No changes were found in the concentrations of IL-1beta, tumour necrosis factor (TNF)alpha, IL-15 and macrophage inflammatory protein (MIP)-1beta, and the concentrations of IL-8 and MIP-1alpha were below detection limits. 4. The results suggest that very early events in exercise trigger the release of IL-6, and that the cytokine response to exercise has similarities to that observed after trauma.
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              Evidence for a supraspinal contribution to human muscle fatigue.

              1. Muscle fatigue can be defined as any exercise-induced loss of ability to produce force with a muscle or muscle group. It involves processes at all levels of the motor pathway between the brain and the muscle. Central fatigue represents the failure of the nervous system to drive the muscle maximally. It is defined as a progressive exercise-induced reduction in voluntary activation or neural drive to the muscle. Supraspinal fatigue is a component of central fatigue. It can be defined as an exercise-induced decline in force caused by suboptimal output from the motor cortex. 2. When stimulus intensity is set appropriately, transcranial magnetic stimulation (TMS) over the motor cortex during an isometric maximal voluntary contraction (MVC) of the elbow flexors commonly evokes a small twitch-like increment in flexion force. This increment indicates that, despite the subject's maximal effort, motor cortical output at the moment of stimulation was not maximal and was not sufficient to drive the motoneurons to produce maximal force from the muscle. An exercise-induced increase in this increment demonstrates supraspinal fatigue. 3. Supraspinal fatigue has been demonstrated during fatiguing sustained and intermittent maximal and submaximal contractions of the elbow flexors where it accounts for about one-quarter of the loss of force of fatigue. It is linked to activity and the development of fatigue in the tested muscles and is little influenced by exercise performed by other muscles. 4. The mechanisms of supraspinal fatigue are unclear. Although changes in the behaviour of cortical neurons and spinal motoneurons occur during fatigue, they can be dissociated from supraspinal fatigue. One factor that may contribute to supraspinal fatigue is the firing of fatigue-sensitive muscle afferents that may act to impair voluntary descending drive.

                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                22 February 2011
                : 6
                : 2
                : e17059
                Affiliations
                [1 ]Université de Lyon, F-42023, Saint-Etienne, France and Exercise Physiology Laboratory, Jean Monnet University, Saint-Etienne, France
                [2 ]HP2 Laboratory (INSERM), Joseph Fourier University and Exercise Research Unit, University Hospital, Grenoble, France
                [3 ]Laboratory of Biochemistry, University Hospital Center Lyon-Sud, Hospices Civils of Lyon, Lyon, France
                [4 ]Université de Lyon, F-42023, Saint-Etienne, France and Department of Anesthesiology and Intensive Care, University Hospital Center, Saint-Etienne, France
                [5 ]Laboratory of Exercise Biology, Blaise Pascal University, Clermont-Ferrand, France
                McMaster University, Canada
                Author notes

                Conceived and designed the experiments: GM LF. Performed the experiments: GM KT SV CV LF VM. Analyzed the data: GM KT RCB. Contributed reagents/materials/analysis tools: RB RCB LG. Wrote the paper: GM. Critical review of the manuscript: KT SV CV RCB LG VM.

                Article
                PONE-D-10-04257
                10.1371/journal.pone.0017059
                3043077
                21364944
                0f6feb84-a444-4282-b894-9b9034373c46
                Millet et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 3 November 2010
                : 19 January 2011
                Page count
                Pages: 14
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Musculoskeletal System
                Muscle
                Muscle Functions
                Electrophysiology
                Biochemistry
                Blood Chemistry
                Medicine
                Anatomy and Physiology
                Musculoskeletal System
                Muscle
                Muscle Functions
                Electrophysiology
                Integrative Physiology
                Sports and Exercise Medicine

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                Uncategorized

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