Shear-Wave Elastography Assessments of Quadriceps Stiffness Changes prior to, during and after Prolonged Exercise: A Longitudinal Study during an Extreme Mountain Ultra-Marathon

Abstract

In sports medicine, there is increasing interest in quantifying the elastic properties of skeletal muscle, especially during extreme muscular stimulation, to improve our understanding of the impact of alterations in skeletal muscle stiffness on resulting pain or injuries, as well as the mechanisms underlying the relationships between these parameters. Our main objective was to determine whether real-time shear-wave elastography (SWE) can monitor changes in quadriceps muscle elasticity during an extreme mountain ultra-marathon, a powerful mechanical stress model. Our study involved 50 volunteers participating in an extreme mountain marathon (distance: 330 km, elevation: +24,000 m). Quantitative SWE velocity and shear modulus measurements were performed in most superficial quadriceps muscle heads at the following 4 time points: before the race, halfway through the race, upon finishing the race and after recovery (+48 h). Blood biomarker levels were also measured. A significant decrease in the quadriceps shear modulus was observed upon finishing the race (3.31±0.61 kPa) (p<0.001) compared to baseline (3.56±0.63 kPa), followed by a partial recovery +48 h after the race (3.45±0.6 kPa) (p = 0.002) across all muscle heads, as well as for each of the following three muscle heads: the rectus femoris (p = 0.003), the vastus medialis (p = 0.033) and the vastus lateralis (p = 0.001). Our study is the first to assess changes in muscle stiffness during prolonged extreme physical endurance exercises based on shear modulus measurements using non-invasive SWE. We concluded that decreases in stiffness, which may have resulted from quadriceps overuse in the setting of supra-physiological stress caused by the extreme distance and unique elevation of the race, may have been responsible for the development of inflammation and muscle swelling. SWE may hence represent a promising tool for monitoring physiologic or pathological variations in muscle stiffness and may be useful for diagnosing and monitoring muscle changes.

Fig 1

a) US image obtained in axial plane showing the different areas of interest within the quadriceps muscle: the RF, rectus femoris (red); the VL, vastus lateralis (pink); and the VM, vastus medialis (green). b) Elastographic data collection: 5 circular 5 mm-diameter ROIs (Q boxes) were manually placed within each squared SWE box by the same radiologist, who was experienced in performing musculoskeletal ultrasound. For example, this picture shows the positions of the Q boxes for the RF. The operator was blinded to the quantitative shear modulus data. c), d), E) and f) are in-plane fiber-aligned US images of the RF, VM, VL, respectively. The orange-dotted square ROIs correspond to the three sequential positions of the SWE-boxes used for the SWE measurements. Thus, at each investigation time, 9 SWE boxes were saved (3 for the RF, 3 for the VM and 3 for the VL). Note the absence of gas bubbles within the thick gel layer. The X- and Y-scales are, respectively, the in-plane and depth distances in centimeters.

Fig 2. Measurement protocol and subject positioning.

An articulated arm ensures that no contact occurs between the transducer and the thigh. Acoustic coupling is ensured using a home-designed silicon pool conforming to the shape of the leg that is filled with bubble-free acoustic gel. All subjects were placed in the supine position using a feet holder to ensure that the quadriceps femoris muscle remained at rest. To maximize inter-day reliability and hasten re-positioning, 4 indelible skin lines were traced during the Pre session (with a waterproof marker). The first line extended across the thigh and was drawn 15 cm above the upper edge of the patella, perpendicular to the patella-ASIS (anterior superior iliac spine) axis. The remaining three lines were drawn parallel to the longitudinal axis of the center of each of the three muscle heads (RF, VM, VL). Per the PLOS ONE policy regarding papers including identifying or potentially identifying, information, each subject was informed of the terms of the PLOS open-access (CC-BY) license and provided permission for the publication of these details under the terms of the license.

Fig 3. Change in muscle head stiffness (shear modulus).

Changes observed in the three muscle heads (RF, VM and VL) at the three measurement times (Mid, Finish, and Recovery) are expressed as percentages of their baseline values, or their Pre values. The error bars denote the 95% confidence interval, and the boxes denote the 25^th–75^th percentiles with the median. The asterisks indicate that the changes from baseline are significant based on the statistical analysis of the raw data, which is presented in the Results section.

Fig 4. Edematous and architectural thigh muscle changes at the Finish assessment.

US images of the quadriceps femoris muscle, which were obtained in the axial plane during the Pre session (a) and the Finish session (b). Note the edematous thickening of the skin and the muscle fascia in the image obtained during the Finish session.