Ultrasonic Elastography of the Rectus Femoris, a Potential Tool to Predict Sarcopenia in Patients With Chronic Obstructive Pulmonary Disease

Abstract

Purpose: Skeletal muscle dysfunction is common in patients with chronic obstructive pulmonary disease (COPD) and is associated with a poor prognosis. Abnormal muscle quantity of the lower limbs is a manifestation of skeletal muscle dysfunction in patients with COPD. Shear wave ultrasound elastography (SWE) is a novel and possible tool to evaluate qualitative muscle parameters. This study explores the feasibility of SWE to measure the stiffness of the rectus femoris and evaluates its value in predicting sarcopenia in patients with COPD. Methods: Ultrasound examination of the rectus femoris was performed to determine the mean elasticity index (SWE_mean), cross-sectional area (RF_csa), and thickness (RF_thick) using grayscale ultrasonography (US) and SWE in 53 patients with COPD and 23 age-matched non-COPD healthy controls. The serum levels of circulating biomarkers (GDF15, resistin, and TNF-α) were measured using ELISA. The definition of sarcopenia followed the guidelines from the Asian Working Group for Sarcopenia. Receiver operating characteristic (ROC) curve analysis of the SWE_mean, RF_thick, and RF_csa was used to evaluate their predictive ability for sarcopenia. Results: The intraobserver and interobserver repeatability of SWE performance was excellent (all correlation coefficients > 0.95; p < 0.05). The SWE_mean of the rectus femoris in patients with COPD (8.98 ± 3.12 kPa) was decreased compared with that in healthy controls (17.00 ± 5.14 kPa) and decreased with advanced global initiative for chronic obstructive lung disease (GOLD) stage. Furthermore, SWE_mean was found to be independent of sex, height, and body mass, and a lower SWE_mean in patients with COPD was positively associated with reduced pulmonary function, worse physical function, poor exercise tolerance, decreased muscle strength, and worse dyspnea index score. The correlation between physical function [five-repetition sit-to-stand test (5STST)], muscle function, and SWE_mean was higher than those of RF_thick and RF_csa. In addition, SWE_mean was negatively correlated with serum GDF15 levels (r = -0.472, p < 0.001), serum resistin levels (r = -0.291, p = 0.035), and serum TNF-α levels (r = -0.433, p = 0.001). Finally, the predictive power of SWE_mean [area under the curve (AUC): 0.863] in the diagnosis of sarcopenia was higher than that of RF_thick (AUC: 0.802) and RF_csa (AUC: 0.816). Conclusion: Compared with grayscale US, SWE was not affected by the patient's height, weight, or BMI and better represented skeletal muscle function and physical function. Furthermore, SWE is a promising potential tool to predict sarcopenia in patients with COPD.

Keywords: COPD; rectus femoris; sarcopenia; skeletal muscle dysfunction; ultrasonic elastography.

Figure 1

Measurements of rectus femoris stiffness using shear wave elastography. (A) The process of shear wave ultrasound elastography assessment; (B) Shear wave ultrasound elastography (SWE) images of the rectus femoris are displayed together with the grayscale ultrasound images. After placing a box (frame) over the rectus femoris, a colored image appears, revealing blue and red areas on an elastogram. Dark blue areas correspond to soft tissues, whereas red areas correspond to stiff tissues.

Figure 2

The difference in the mean elasticity indices of rectus femoris ultrasound elastography in patients with chronic obstructive pulmonary disease (COPD) and healthy controls. (A) Representative SWE images of the rectus femoris and grayscale ultrasound images in healthy controls; (B) Representative SWE images of rectus femoris and grayscale ultrasound images in patients with COPD; (C) Difference in mean elasticity index (SWE_mean) in patients with COPD and healthy controls; and (D) Difference in SWE_mean in patients with global initiative for chronic obstructive lung disease (GOLD) A and GOLD B and in patients with GOLD C and GOLD D. SWE_mean: mean SWE elasticity index. *p<0.05; ***p<0.001.

Figure 3

The relationship between circulating biomarkers and the mean elasticity indices of rectus femoris ultrasound elastography in patients with COPD. (A) The relationship between SWE_mean and serum GDF15 level; (B) The relationship between SWE_mean and serum resistin level; and (C) The relationship between SWE_mean and serum TNF-α level. SWE_mean: mean SWE elasticity index.

Figure 4

The predictive value of SWE_mean. (A) The SWE_mean were differed between patients with sarcopenia and patients without sarcopenia; (B-D) Receiver operating characteristic curve analysis of the mean elasticity indices of rectus femoris ultrasound elastography and thickness and cross-sectional area of the rectus femoris for predicting sarcopenia in patients with COPD. SWE_mean: mean SWE elasticity index; RF_thick: the thickness of rectus femoris; and RF_csa: the cross-sectional area of rectus femoris. ***p<0.001.