Application of conventional ultrasound coupled with shear wave elastography in the assessment of muscle strength in patients with type 2 diabetes

Abstract

Background: In patients with type 2 diabetes mellitus (T2DM), a decrease in muscle function may be related to changes in the biomechanical properties of skeletal muscles. However, the correlations between muscle function and the characteristics of muscle size and stiffness as measured by ultrasound in patients with T2DM are unclear. The aim of this study was to investigate the abilities of conventional ultrasound and shear wave elastography (SWE) to assess muscle properties in patients with T2DM and to correlate the findings with isokinetic muscle testing and functional tests.

Methods: Sixty patients from the Department of Endocrinology in The Third Affiliated Hospital of Southern Medical University diagnosed with T2DM were recruited in this cross-sectional study from September 2021 to September 2022. T2DM was defined based on the American Diabetes Association criteria. The exclusion criteria were a history of injury or operation of the lower limb or clinical signs of neuromuscular disorders, any muscle-induced disease, and the presence of other types of diabetes mellitus. Thirty-five matched healthy volunteers were continuously included in the control group. SWE was used to measure the muscle stiffness of the quadriceps femoris [vastus lateralis (VL), rectus femoris (RF), vastus medialis (VM), vastus intermedius (VI)] and the biceps brachii (BB) in a relaxed position, and the shear wave velocity (SWV) values were recorded. Muscle size was measured using conventional ultrasound. The participants underwent isokinetic knee extension/flexion (60°/sec) to assess muscle strength and functional tests of physical performance, including the short physical performance battery, 30-s chair stand test, timed up-and-go test, and 6-meter walk test. All demographics and measured variables were compared using the independent samples t-test. Interclass correlation coefficient analysis was performed on the measurement data obtained by the two operators, and Pearson correlation coefficients were used to determine the relationships between variables.

Results: Patients with T2DM exhibited worse physical performance (P<0.05) and weaker lower limb muscle strength (P<0.05) than did healthy controls, but their handgrip strength was comparable (P=0.102). Patients with T2DM had significantly decreased muscle thickness [RF thickness: 10.69±3.21 vs. 13.09±2.41 mm, mean difference =-2.40, 95% confidence interval (CI): -3.56 to -1.24, P<0.001; anterior quadriceps thickness: 23.45±7.11 vs. 27.25±5.25 mm, mean difference =-3.80, 95% CI: -6.33 to -1.26, P=0.004] and RF cross-sectional area (3.04±1.10 vs. 4.11±0.95 cm², mean difference =-1.07, 95% CI: -1.49 to -0.64; P<0.001) compared to healthy controls. Smaller muscle size was associated with decreased muscle strength (r=0.44-0.69, all P values <0.001). Except for the BB (3.48±0.38 vs. 3.61±0.61 m/s, mean difference =-0.12, 95% CI: -0.35 to 0.11; P=0.257) and VI (2.59±0.34 vs. 2.52±0.23 m/s, mean difference =0.03, 95% CI: -0.06 to 0.18; P=0.299), the muscle stiffness in patients with T2DM was significantly decreased. For the patients with T2DM and healthy participants, the SWV of the RF was 1.66±0.23 and 1.83±0.18 m/s (mean difference =-0.17, 95% CI: -0.25 to -0.08; P<0.001), respectively; that of the VM was 1.34±0.15 and 1.51±0.16 m/s (mean difference =-0.17, 95% CI: -0.24 to -0.10; P<0.001), respectively; and that of VL was 1.38±0.19 and 1.53±0.19 m/s (mean difference =-0.15, 95% CI: -0.23 to -0.07; P<0.001), respectively. Excellent interobserver reliability of the SWV measurements on the muscle of T2DM patients was observed (all intraclass correlation coefficients >0.75; P<0.001). The SWV showed moderate correlations with muscle strength in the RF, VM, and VL (r=0.30-0.61; all P values <0.05).

Conclusions: Ultrasound technology exhibits good reliability for repeated measurements of muscle size and stiffness. Reduced muscle stiffness as detected by SWE was demonstrated in patients with diabetes and was associated with decreased muscle strength and impaired functional activity.

Keywords: Muscle strength; isokinetic muscle testing; shear wave elastography (SWE); type 2 diabetes mellitus (T2DM); ultrasound.

Figure 1

Measurement of the elastic property of the RF in the longitudinal view. (Left) Image taken with SWE quality control mode showing a uniform off white distribution. (Right) Colored image of the RF elasticity (stiffer areas are coded in red and softer areas in bule), with the circles depicting the region of interest where shear wave velocity (m/s) was measured. (A) The position of SWE assessment in the lower extremity, with the probe moving parallel along the red line perpendicular to the long axis of the limb. (B) SWE example from a patient with diabetes. (C) SWE example from a healthy control. RF, rectus femoris; SWE, shear wave elastography.

Figure 2

Clustered box plot of SWE by participant type. The black dots represent outlier values, and the hollow circles represent mean values. RF, rectus femoris; VI, vastus intermedius; VM, vastus medialis; VL, vastus lateralis; AVER, average of the SWV of each muscle forming the quadriceps femoris (RF, VI, VM and VL); SWV, shear wave velocity; BB, biceps brachii; SWE, shear wave elastography.

Figure 3

Heat map of the correlation between all measured variables. RF, rectus femoris; VI, vastus intermedius; VM, vastus medialis; VL, vastus lateralis; AVER, average of the SWV of each muscle forming the quadriceps femoris (RF, VI, VM and VL); SWV, shear wave velocity; AQ, anterior quadriceps; RF-CSA, rectus femoris cross-sectional area; PT, peak torque; PT/BW, peak torque to body weight ratio; TW, total work; SARC-F, Strength, Assistance with Walking, Rising from a Chair, Climbing Stairs, and Falls; SPPB, short physical performance battery; TUGT, timed up-and-go test; CST, 30-s chair stand test; 6MWT, 6-meter walk test; Corr, correlation coefficient.