New insights on contraction efficiency in patients with Duchenne muscular dystrophy

Abstract

The decrease in muscle strength in patients with Duchenne muscular dystrophy (DMD) is mainly explained by a decrease in the number of active contractile elements. Nevertheless, it is possible that other electrochemical and force transmission processes may contribute. The present study aimed to quantify the effect of DMD on the relative contribution of electrochemical and force transmission components of the electromechanical delay (i.e., time lag between the onset of muscle activation and force production) in humans using very high frame rate ultrasound. Fourteen patients with DMD and thirteen control subjects underwent two electrically evoked contractions of the biceps brachii with the ultrasound probe over the muscle belly. The electromechanical delay was significantly longer in DMD patients compared with controls (18.5 Ϯ 3.9 vs. 12.5 Ϯ 1.4 ms, P Ͻ 0.0001). More precisely, DMD patients exhibited a longer delay between the onset of muscle fascicles motion and force production (13.6 Ϯ 3.1 vs. 7.9 Ϯ 2.0 ms, P Ͻ 0.0001). This delay was correlated to the chronological age of the DMD patients (r ϭ 0.66; P ϭ 0.01), but not of the controls (r ϭ Ϫ0.45; P ϭ 0.10). No significant difference was found for the delay between the onset of muscle stimulation and the onset of muscle fascicle motion. These results highlight the role of the alteration of muscle force transmission (delay between the onset of fascicle motion and force production) in the impairments of the contraction efficiency in patients with DMD. myopathy; force; ultrasound; electromechanical delay DUCHENNE MUSCULAR DYSTROPHY (DMD) is one of the most severe degenerative muscle diseases characterized by a lack of dystrophin (14). Dystrophin is a protein that has a role, with other proteins, to laterally link actin filaments through the sarcolemma to the extracellular matrix (10). It is essential for the transmission of the force generated by contractile proteins (34,35). An absence of dystrophin ultimately leads to contractile tissue wastage (27) and thus to a dramatic decrease in maximal force-generating capacity (21). This is even observed when maximal strength is normalized to muscle contractile cross-sectional area, illustrating an impairment of muscle quality (37). This alteration is mainly explained by a decrease in the number of active contractile elements for a given muscle volume, due to fiber necrosis (1). Still, it is plausible that other electrochemical and mechanical processes might further alter the contraction efficiency.In addition to the main muscle structural consequence of DMD, it has been shown that both muscle (12) and tendon (32) mechanical properties are altered in X-linked muscular dystrophy mice model (mdx). As both structural and mechanical properties may play an important role in force transmission (12,17,32), the efficiency of force transmission from the actomyosin cross bridges to the tendons is presumed to be altered in patients with DMD (24). The alteration of contraction efficiency in DMD patients might also be related to an alter...

Effect of damaging exercise on electromechanical delay

“…demonstrated the influence of small changes in muscle passive tension on the time required to transmit force from muscle to bone. In addition, an increased time delay between the onset of muscle fascicle motion and force production (aponeurosis and tendon delay) has been shown in children with Duchenne muscular dystrophy (+6.7 ms compared with age‐matched healthy participants) . Taken together, these results suggest that the technique used in our study was sufficiently sensitive to detect even small changes in EMD.…”

“…Interestingly, despite altered excitation–contraction coupling suggested in children with Duchenne muscular dystrophy, our previous work also failed to show an effect on duration, further suggesting that efficiency may be affected independently of duration. However, a significant increase in force transmission (aponeurosis and tendon delay) has been reported in children with Duchenne muscular dystrophy compared with healthy, age‐matched participants (+75%), indicating involvement of muscle structural abnormalities. Due to muscle damage, some force transmitters between myofibrils (e.g., desmin) or muscle fibers (e.g., extracellular matrix) are disrupted, as evidenced by the histological myofibril distortion observed .…”

“…The delay between the onset of fascicle motion and the onset of force production has been attributed to force transmission along the series‐elastic components, which can be split into 2 parts (i.e., aponeurosis and tendon) by detecting the onset of myotendinous junction motion . Using ultrafast ultrasound, Lacourpaille et al . showed that patients with Duchenne muscular dystrophy exhibit a longer delay between the onset of muscle fascicle motion and force production compared with healthy, age‐matched participants, suggesting altered muscle force transmission.…”

Electromechanical delay components during skeletal muscle contraction and relaxation in patients with myotonic dystrophy type 1

“…A similar approach, with the use of high frame rate ultrasound, has been recently proposed in patients with Duchenne dystrophy during contraction [30]. A lengthening of the overall delay due to mechanical component expansion was clearly observed.…”

Non‐invasive assessment of muscle stiffness in patients with duchenne muscular dystrophy

“…The local ethics committee approved the study, and all procedures conformed to the Declaration of Helsinki. Data from the biceps brachii have been published elsewhere …”