Elasticity assessment of flexor pronator muscles using shear wave elastography

Abstract

Background

The flexor pronator muscles (FPMs) have been thought as a dynamic stabilizer to protect the ulnar collateral ligament (UCL) from valgus stress during throwing motion. Thus, evaluation of the FPMs is important for preventing UCL injuries. Shear wave ultrasound elastography (SWE) is an imaging modality that quantifies tissue elasticity. The purpose of this study was to measure the tissue elasticities of healthy FPMs using SWE.

Methods

We investigated 22 healthy men (mean age, 29 ± 6 years). The elasticities of the FPMs, including the pronator teres (PT), flexor digitorum superficialis (FDS), and flexor carpi ulnaris (FCU), were measured using SWE for each arm under two conditions: at rest (unloaded) and under valgus stress (loaded). The values obtained under different loading conditions were compared between both elbows.

Results

The mean SWE values of the PT, FDS, and FCU for the dominant elbows were 22.4 ± 3.6, 22.8 ± 2.9, and 22.3 ± 3.4 kPa, respectively. The corresponding mean SWE values for the nondominant elbows were 24.2 ± 4.6, 23.1 ± 3.5, and 23.4 ± 3.5 kPa, respectively. The mean SWE values of the PT, FDS, and FCU at rest (unloaded) were 23.3 ± 4.2, 22.9 ± 3.2, and 22.9 ± 3.5 kPa, respectively. The corresponding mean SWE values under valgus stress (loaded) were 35.0 ± 6.2, 34.7 ± 5.3, and 31.9 ± 4.8 kPa, respectively.

Conclusion

This noninvasive evaluation of the stiffness of the FPMs may provide clinically relevant data for the prevention of UCL injuries.

In baseball pitchers, the increasing frequencies of ulnar collateral ligament (UCL) injuries in the elbow and the required surgeries are of utmost concern.^6,26 The anterior bundle of the UCL is the primary static stabilizer against valgus stress.^4,22 The flexor pronator muscles (FPMs), including the pronator teres (PT), flexor digitorum superficialis (FDS), and flexor carpi ulnaris (FCU), are secondary dynamic stabilizers.^{1,5,8,11,12,14,24,25,30,31} The anterior bundle of the UCL has been recently described as a part of the tendinous complex comprising FPMs.¹⁷ Stiffness and tenderness of FPMs are the most frequently observed clinical signs of UCL injuries in baseball pitchers. Although evaluating the stiffness of FPMs is necessary to determine the pathogenic mechanisms underlying the elbow symptoms, no reliable diagnostic tools are available to do this. This diagnostic tool may prevent UCL ruptures or lesions by determining the degree of stiffness.

Shear wave elastography (SWE) has been used as a quantitative ultrasound (US) technique to assess muscle stiffness by evaluating shear wave propagation speed.^10,20,32 Although SWE has been frequently used for quantitative evaluations of the UCL,^13,21 no studies have used this technique to assess the mechanical stiffness of FPMs.

This preliminary study aimed to evaluate a method for measuring the stiffness of healthy FPMs (including PT, FDS, and FCU) using SWE. We also compared the stiffness of FPMs under two separate conditions: at rest (unloaded) and under valgus stress (loaded). We hypothesized that the stiffness of individual FPMs can be quantified by SWE and may differ between the loaded and unloaded conditions.

Materials and methods

Design

This study used a repeated-measures examination to evaluate changes in SWE under two separate elbow-loading conditions. The dependent variable was SWE, and the independent variables were the loading conditions (unloaded and loaded). The dominant and nondominant elbows of all participants were subjected to both loading conditions. PT, FDS, and FCU were also assessed separately under these conditions.

Participants

Twenty two healthy individuals aged 22-44 (mean, 29 ± 6) years were recruited from our institute between December 2018 and November 2019. Only men were registered in order to simulate the baseline characteristics of adult male baseball players. The exclusion criteria were as follows: (1) present pain or injury of the upper limbs, (2) previous traumatic UCL injury or elbow dislocation, (3) previous surgery of the upper limbs, and (4) prior involvement in overhead sports. Written informed consent was obtained from all participants, and the study was approved by the appropriate institutional review board.

Imaging technique

All US scans were obtained by a well-trained orthopedic surgeon using an Aixplorer (Supersonic Imagine, Aix-en-Provence, France) scanner with a 10-MHz linear transducer; these scans were used to evaluate the material properties of the muscle (along the muscle fiber direction). This device was equipped with SWE technology and enabled the quantification of tissue elasticity without probe compression. Each participant was laid on the bed with the shoulder, elbow, and forearm at 90° abduction, 90° flexion, and a neutral position, respectively (Fig. 1).²⁹ All angles were measured using a goniometer. SWE evaluation in this study allowed two-dimensional SWE, which in turn allowed the measurement of tissue stiffness with a conventional US transducer. SWE values were calculated in a region of interest (ROI) according to a previous report.⁹ ROIs were identified using the tendinous septum (TS) as a landmark. SWE values ranged from 0 to 800 kPa. Each SWE value was measured three times, and the mean value was used.

Figure 1.

Positioning for the ultrasound examination. The participant was laid on the bed with the shoulder, elbow, and forearm at 90° abduction, 90° flexion, and a neutral position, respectively. Ultrasonography images were acquired from the medial elbow.

SWE for individual FPMs across the two conditions

The transducer was placed on the medial elbow to visualize FPMs. First, a short-axis scan was used to identify TS between PT and FDS, as well as TS between FDS and FCU, in accordance with previous studies (Fig. 2, a).^7,17 Second, these TSs were used as landmarks for differentiating between PT, FDS, and FCU. Third, after identifying these muscles in the short-axis views, the transducer was turned 90° to observe the muscles along their long-axis (Fig. 2, b-d). It has been reported that to quantify muscle stiffness by SWE, the US transducer must be oriented parallel to the muscle fibers.¹⁰ Therefore, each muscle was identified along its long-axis during SWE at the level of the sublime tubercle of the ulna.

Figure 2.

Ultrasound images of the flexor pronator muscles. (a) Short-axis image at the level of the sublime tubercle in the ulna. Two tendinous septa, one between PT and FDS (), and one between FDS and FCU (), were identified. (b) Long-axis image of PT of the medial elbow. (c) Long-axis image of FDS of the medial elbow. (d) Long-axis image of FCU of the medial elbow. Ant, anterior; Dist, distal; FCU, flexor carpi ulnaris; FDS, flexor digitorum superficialis; Med, medial; Prox, proximal; PT, pronator teres; UN, ulnar nerve; ST, sublime tubercle.

SWE measurements of the dominant and nondominant elbows were performed under the following conditions: forearm resting on a handstand (unloaded; Fig. 3, a) and forearm held without any support (loaded; Fig. 3, b).³¹ An elbow was randomly selected for SWE measurements of FPMs, which were recorded under the unloaded and loaded conditions. Thereafter, SWE measurements for the opposite elbow were similarly obtained. Changes in SWE values, which reflected the differences in SWE findings between the two conditions, were used for subsequent analyses. None of the participants experienced medial elbow pain during the examinations.

Figure 3.

Ultrasound examination under different loading conditions. (a) Forearm on the handstand (unloaded). (b) Forearm without support (loaded).

Statistical analysis

A paired t-test was used to compare SWE values of PT, FDS, and FCU between the dominant and nondominant elbows and between the two conditions. A two-sided P value of < .05 was considered statistically significant. Power analysis for the detection of differences between the different loading conditions in each elbow was conducted using an α-value of 0.05, an effect size of 0.4 (determined according to the results of a preliminary study), and a power of 0.95. The power analysis suggested that 44 elbows were required to evaluate the two conditions.

Results

In all participants, the muscle fibers of FPMs were identified on B-mode US images (Fig. 2), and muscle stiffness was measured with SWE (Fig. 4). The mean SWE values of PT, FDS, and FCU for the dominant elbows were 22.4 ± 3.6, 22.8 ± 2.9, and 22.3 ± 3.4 kPa, respectively (Table I). The corresponding mean SWE values for the nondominant elbows were 24.2 ± 4.6, 23.1 ± 3.5, and 23.4 ± 3.5 kPa, respectively (Table I). There were no significant differences in SWE values for the muscles between the dominant and nondominant elbows (Table I). The mean SWE values of PT, FDS, and FCU under unloaded conditions were 23.3 ± 4.2, 22.9 ± 3.2, and 22.9 ± 3.5 kPa, respectively (Table II). The corresponding mean SWE values under loaded conditions were 35.0 ± 6.2, 34.7 ± 5.3, and 31.9 ± 4.8 kPa, respectively (Table II). The mean SWE values under the loaded conditions were significantly greater than the SWE values under the unloaded conditions (Table II).

Figure 4.

Shear wave elastography evaluation of the flexor pronator muscles. PT, FDS, and FCU were identified by two tendinous septa, one between PT and FDS (red dotted line) and the other between FDS and FCU (blue dotted line). The colored region represents the shear elasticity map with the scale to the Right of the figure (blue, soft; green to yellow, medium; red, hard). (a) Long-axis image of the flexor pronator muscle under the unloaded condition. (b) Long-axis image of the flexor pronator muscle under the loaded condition. Dist, distal; FCU, flexor carpi ulnaris; FDS, flexor digitorum superficialis; PT, pronator teres; Prox, proximal.

Table I.

Shear wave elastography values of elbows on the dominant and nondominant sides.

	Dominant elbow	Nondominant elbow	P value
SWE value [mean ± SD]
PT	22.4 ± 3.6	24.2 ± 4.6	.07
FDS	22.8 ± 2.9	23.1 ± 3.5	.58
FCU	22.3 ± 3.4	23.4 ± 3.5	.08

SWE, Shear wave elastography; PT, pronator teres; FDS, flexor digitorum superficialis; FCU, flexor carpi ulnaris; SD, standard deviation.

Values are expressed as kPa (mean ± standard deviation).

Table II.

Shear wave elastography values in the unloaded and loaded conditions.

	Rest	Valgus stress	P value
SWE value [mean ± SD]
PT	23.3 ± 4.2	35.0 ± 6.2	<.001
FDS	22.9 ± 3.2	34.7 ± 5.3	<.001
FCU	22.9 ± 3.5	31.9 ± 4.8	<.001

SWE, Shear wave elastography; PT, pronator teres; FDS, flexor digitorum superficialis; FCU, flexor carpi ulnaris; SD, standard deviation.

Values are expressed as kPa (mean ± standard deviation).

Discussion

In this study, PT, FDS, and FCU were identified in the short-axis views of the US by using TS as a landmark. The muscle fibers of all FPMs were then individually identified along their long axis. SWE was used to quantify the stiffness of PT, FDS, and FCU. No significant differences were observed in SWE values between both elbows. SWE values of FPMs under the loaded conditions were greater than those under the unloaded conditions, thereby validating our hypothesis.

We demonstrated a method for the assessment of the elasticity of individual FPMs. To ensure sufficient shear wave propagation, the US transducer must be oriented parallel to the muscle fibers to quantitatively assess muscle stiffness during SWE.¹⁰ Previously, it was difficult to identify FPMs alone in the long-axis scans.⁷ A recent anatomical study revealed two TSs, one between PT and FDS and one between FDS and FCU.¹⁷ Based on these anatomical findings, it was possible to use the two TSs as landmarks for identifying PT, FDS, and FCU in both the long-axis and short-axis views.

Quantitative assessment of the muscle elasticity of FPMs is necessary for managing players with a UCL injury, based on the anatomical finding that the UCL could be a part of the tendinous complex comprising FPMs. US strain elastography allows a semi-quantitative assessment of muscle elasticity through strain ratios.² SWE has been reported to be a more accurate diagnostic tool than conventional strain elastography due to its improved reproducibility and quantification of muscle elasticity.²³ Previous studies have reported the use of SWE in assessing the tissue elasticity of the UCL of the elbow^13,21; however, this modality has rarely been applied to the assessment of FPMs. Therefore, our new method for evaluating the muscle stiffness of FPMs using SWE might contribute to the assessment of baseball players with a UCL injury.

It is unclear how pitching motion affects the stiffness of each FPM because FPMs work differently during the throwing motion. Muscle stiffness has been reported to result from both active tension produced during muscle contraction and passive tension due to muscle extension in the longitudinal direction.^16,18 Some studies have reported that muscle elasticity increases during contraction.^20,27 In addition, a previous elastography study reported that a repetitive throwing motion could lead to muscular stiffness.¹⁹ These previous studies indicate that the stiffness of FPMs may be due to their active contraction and passive extension during the throwing motion. In the current study, US examination is a dynamic method which allows measuring the muscle stiffness under unloaded and loaded conditions during the same examination. In addition, SWE values for FPMs were greater under loaded conditions than under unloaded conditions. Our findings may inform the development of future studies on healthy and injured baseball players.

Some implications could be deduced from the results of this study. First, we hypothesize that the use of SWE in baseball players may facilitate prevention of medial elbow injury. Some studies have reported that UCL injuries correlate with increased elasticity in FPMs.²⁸ In the current study, no significant differences were observed in SWE values of the individual FPMs between the dominant and nondominant elbows. And this technique may be used easily for other examiners with the two TSs as landmarks for identifying each FPM. Therefore, this technique could be used as screening method for symptomatic baseball players to identify pathological stiffness by comparing both elbows.

Second, we hypothesize that the use of SWE in baseball players may facilitate management medial elbow. It has been reported that repeated pitching caused the stiffness of the FPMs.¹⁵ And a delay in the isometric force response time in stiff muscles results in a decrease in dynamic stability against valgus stress.^3,19 Therefore, this quantitative tool for assessing the degree of stiffness before and after pitching may be useful for management of medial elbow.

This study had several limitations. First, the SWE value was measured by one examiner, and the reliability was not assessed. Second, only healthy participants were included in the study. Third, the locations of the ROIs were not standardized. Forth, we used gravity alone to load the elbow, not using other equipment such as weighted ball. Further research on how force variation affects the load on the FPMs may be required. Lastly, not all regions of the ligaments and muscles were evaluated; therefore, the results may not appropriately represent an exact clinical scenario. We believe that this study provides important quantitative data on the stiffness of FPMs with respect to UCL injuries in baseball players.

Conclusion

This study evaluated a method for measuring the stiffness of healthy FPMs (including PT, FDS, and FCU) using SWE. We hypothesized that the stiffness of individual FPMs can be quantified by SWE and would differ between loaded and unloaded conditions. Our results demonstrated that the stiffness of each FPM could be quantified using SWE. No significant differences were observed in SWE values between both elbows. In addition, SWE values in FPMs under the loaded conditions were greater than those under the unloaded conditions. This study indicated that noninvasive evaluation of the stiffness of FPMs using SWE might provide clinically relevant information for preventing UCL injuries in baseball players.

Acknowledgment

The authors are grateful for all volunteers who participated in this study.

Disclaimers:

Funding: This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflicts of interest: The authors, their immediate families, and any research foundation with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.

Patient consent: Written informed consent was obtained from all participants.