Muscle damage alters the metabolic response to dynamic exercise in humans: a³¹P-MRS study

Abstract

We used ³¹P-magnetic resonance spectroscopy to test the hypothesis that exercise-induced muscle damage (EIMD) alters the muscle metabolic response to dynamic exercise, and that this contributes to the observed reduction in exercise tolerance following EIMD in humans. Ten healthy, physically active men performed incremental knee extensor exercise inside the bore of a whole body 1.5-T superconducting magnet before (pre) and 48 h after (post) performing 100 squats with a load corresponding to 70% of body mass. There were significant changes in all markers of muscle damage [perceived muscle soreness, creatine kinase activity (434% increase at 24 h), and isokinetic peak torque (16% decrease at 24 h)] following eccentric exercise. Muscle phosphocreatine concentration ([PCr]) and pH values during incremental exercise were not different pre- and post-EIMD (P > 0.05). However, resting inorganic phosphate concentration ([P(i)]; pre: 4.7 ± 0.8; post: 6.7 ± 1.7 mM; P < 0.01) and, consequently, [P(i)]/[PCr] values (pre: 0.12 ± 0.02; post: 0.18 ± 0.05; P < 0.01) were significantly elevated following EIMD. These mean differences were maintained during incremental exercise (P < 0.05). Time to exhaustion was significantly reduced following EIMD (519 ± 56 and 459 ± 63 s, pre- and post-EIMD, respectively, P < 0.001). End-exercise pH (pre: 6.75 ± 0.04; post: 6.83 ± 0.04; P < 0.05) and [PCr] (pre: 7.2 ± 1.7; post: 14.5 ± 2.1 mM; P < 0.01) were higher, but end-exercise [P(i)] was not significantly different (pre: 19.7 ± 1.9; post: 21.1 ± 2.6 mM, P > 0.05) following EIMD. The results indicate that alterations in phosphate metabolism, specifically the elevated [P(i)] at rest and throughout exercise, may contribute to the reduced exercise tolerance observed following EIMD.

Time-course of recovery of peak oxygen uptake after exercise-induced muscle damage

“…Blood lactate levels have also been shown to be elevated (Burt et al, 2013;Gleeson et al, 1998Gleeson et al, , 1995 following EIMD-suggesting a greater reliance on anaerobic metabolism may occur in the undamaged muscle fibers. This is further supported by the finding of an increased ratio of inorganic phosphate (P i ) to phosphocreatine (PCr) (Davies et al, 2011a;Foure et al, 2014) in resting muscle. Our finding of a prolonged reduction of GET would be consistent with greater metabolic stress on undamaged fiber and could lead to an earlier onset of lactate accumulation, fatigue, and consequently a reduced V˙ O 2peak .…”

“…The disruption of sarcomere and contractile ultrastructure following EIMD leads to a well characterized sequelae of signs and symptoms including elevated serum creatine kinase (Newham et al, 1983a), inflammation and localized edema (Black et al, 2008;Black and McCully, 2008a), a decreased ability to generate force (Newham et al, 1983b), and heightened pain sensitivity-often termed delayed-onset muscle soreness (DOMS) (Newham et al, 1983b). A growing body of evidence clearly indicates EIMD negatively impacts endurance exercise performance as demonstrated by reductions in time-trial performance (Burt and Twist, 2011;Marcora and Bosio, 2007;Twist and Eston, 2009) and time-toexhaustion (Asp et al, 1998;Carmichael et al, 2006Carmichael et al, , 2010Davies et al, 2011aDavies et al, , 2008Davies et al, , 2009.…”

“…EIMD leads to increases in the ratio of inorganic phosphate (P i ) to phosphocreatine (PCr) (Davies et al, 2011a;Foure et al, 2014) and blood lactate [La] at rest (Asp et al, 1998). Movement economy (oxygen cost per work rate) has also been shown to be reduced following EIMD (Burt et al, 2013;Burt et al, 2014;Chen et al, 2009Chen et al, , 2007.…”

Impaired Mitochondrial Function and Reduced Energy Cost as a Result of Muscle Damage

“…For instance, the typical inflammation response to voluntary EIMD has been associated with an increased metabolic rate at rest (10), which is likely to result from repair and remodeling processes of muscular tissues, thereby requiring energetically demanding protein synthesis (49). 31P magnetic resonance spectroscopy (jI P-MRS) studies have consistently reported a higher resting inorganic phosphate (Pi)/phosphocreatine (PCr) ratio after voluntary eccentric EIMD (9,37,41). This higher [Pi]/[PCr] ratio might account for impaired exercise tolerance (i.e., reduced time to exhaustion) after volun tary eccentric EIMD (9).…”

“…31P magnetic resonance spectroscopy (jI P-MRS) studies have consistently reported a higher resting inorganic phosphate (Pi)/phosphocreatine (PCr) ratio after voluntary eccentric EIMD (9,37,41). This higher [Pi]/[PCr] ratio might account for impaired exercise tolerance (i.e., reduced time to exhaustion) after volun tary eccentric EIMD (9). However, the adenosine diphosphate (ADP) recovery rate was not affected by the voluntary eccen tric EIMD in the latter study, thereby suggesting that mito chondrial alterations previously reported in vitro (13) did not translate into similar changes in vivo.…”