Abstract
Background
Identification of the relationship between valgus stress in the medial elbow and ulnar nerve strain during maximum external rotation of the shoulder is pivotal for the prevention and management of ulnar neuropathies. In this observational cross-sectional study, we aimed to determine the changes in ulnar nerve stiffness under valgus stress at different nerve entrapment sites.
Methods
Twenty healthy baseball players participated in the study. The stiffness of the ulnar nerve on the throwing side was assessed at two sites, the arcade of Struthers and the Osborne’s ligament, at 0°, 60°, and 90° flexion by shear wave elastography using a 10-MHz linear transducer. The arcade of Struthers was defined as the proximal site and the Osborne's ligament as the distal site. Valgus stress was applied to the medial elbow at 0, 30, 50, and 70 N using a Telos stress device, and the stiffness caused by valgus stress was measured.
Results
At all elbow flexion angles, the stiffness of the ulnar nerve under 70 N valgus stress was higher than that under 30 N stress. The stiffness of the ulnar nerve at the proximal site was significantly higher than that at the distal site.
Conclusion
Valgus stress increases ulnar nerve stiffness. In addition, the stiffness of the proximal site increases.
Keywords: Nerve entrapment, Nerve stiffness, Ulnar neuropathy, Valgus stress, Throwing elbow
Introduction
Ulnar neuropathy is a throwing injury [1]. The medial elbow is subjected to excessive valgus stress during pitching, especially during maximal external rotation (MER) of the shoulder in the late cocking phase [2]. Therefore, elucidation of the relationship between valgus stress in the medial elbow and ulnar neuropathy during MER is important for the prevention and treatment of ulnar neuropathy.
Studies on cadavers have reported that increased elbow valgus stress and flexion lead to increased ulnar nerve tension [3, 4]. Therefore, ulnar nerve tension is thought to differ during each phase of throwing. During the MER in the throwing motion, the elbow flexes approximately 90°–120° [5, 6], with a valgus stress of approximately 64 Nm at its medial side [7]. However, the ulnar nerve tension created when the medial elbow is subjected to valgus stress, in a position that simulates the MER during pitching, has not been determined using in vivo studies.
The three main ulnar nerve entrapment sites are the arcade of Struthers, cubital tunnel, and Osborne’s ligament [8]. Baseball players with medial elbow pain on the throwing side have been found to have swollen ulnar nerves at three entrapment points compared with the condition of the nerves on the non-throwing side [9, 10]. Baseball players with ulnar neuropathies have significantly swollen ulnar nerves in the cubital tunnel and Osborne’s ligament compared to the nerves in the arcade of Struthers [10]. Dynamic ultrasound imaging of the ulnar nerve is commonly used to evaluate hypermobility, instability, snapping, luxation, and subluxation of the ulnar nerve [11]. Recent studies have reported the use of the shear wave elastography mode of ultrasonography to examine peripheral nerve stiffness [12–15]. Therefore, changes in ulnar nerve stiffness due to variation in valgus stress intensities can be measured in vivo using ultrasonography.
We hypothesized that differences at the entrapment sites of the ulnar nerve during valgus stress may affect ulnar nerve stiffness. In this study, we aimed to determine the changes in ulnar nerve stiffness at the MER position according to the entrapment sites. In addition, we aimed to determine changes in ulnar nerve stiffness caused by valgus stress.
Methods
Participants
Twenty-three healthy baseball players were recruited for this study. The purpose of the study was verbally explained, and signed consent forms were obtained. This study was approved by the ethics committee of our institution (approval number 2020-102). The baseball players included in this study had no medial elbow pain during pitching, abnormalities in the ulnar collateral ligament of the elbow were not detected on ultrasonography, and the results of the moving valgus stress test of the elbow were negative. The moving valgus stress test was performed according to previous study [16]. The baseball players included in this study did not sport-related injuries to the elbow in the past or present. Three players were excluded based on the following exclusion criteria: pain during pitching, the results of the moving valgus stress test of the elbow were positive, and symptoms of thoracic outlet syndrome. Physical examination for thoracic outlet syndrome was performed using the Roos test and the Elvey's test based on previous studies [17, 18]. Baseball players were excluded if they tested positive for one or both tests.
Instruments and procedures
Ulnar nerve stiffness was measured by ultrasonography (Aplio 300; Canon Medical Systems, Tokyo, Japan) with a 10-MHz linear transducer (PLT-1005BT; Canon Co., Ltd., Tokyo, Japan) in B mode. The imaging site was selected as described in a previous study [10, 19]. The proximal site (arcade of Struthers) of the ulnar nerve was imaged along the long axis at a site 5 cm proximal to the medial epicondyle. The distal site (Osborne’s ligament) of the ulnar nerve was imaged along the long axis at a site 3 cm distal to the medial epicondyle (Fig. 1). Subsequently, the ultrasonography setting was changed to shear wave elastography mode, and the shear wave velocity (m/s) was measured (Fig. 2). The tip of the transducer was covered with a layer of ultrasound gel of approximately 5 mm width and placed on the skin without compressing the tissue. The transducer was kept stationary for 3–5 s and the image was stored after the shear wave image was stabilized. Three regions of interest on the ulnar nerve were randomly selected. Shear wave velocity data for the selected circular region of interest (ROI, 2 mm in diameter) were acquired automatically by the ultrasonographic software. The average of data obtained from these regions was used as the representative value (Fig. 3). Our default elastography setting was a side-by-side dual-panel display of color mapping of shear wave velocity and propagation of shear wave velocity. The main purpose of the side-by-side propagation of shear wave velocity display was to allow real-time visualization and stabilization of the target lesion, which often was obscured by the color overlay on the shear wave display. The default quantitative shear wave elastography scale showed the shear wave velocity measurements (expressed as velocity), with the color red indicating hard elasticity, the color blue indicating soft elasticity, and the maximum color scale set at 10 m/s.
Fig. 1.
Sites of ultrasound imaging of the ulnar nerve. Proximal site: 5 cm proximal to the medial epicondyle (MEC). Distal site: 3 cm distal to the MEC
Fig. 2.
Ultrasound images of the ulnar nerve. a Proximal. b Distal
Fig. 3.
Shear wave elastography images of the ulnar nerve. The shear velocity was measured at 3 randomly selected ulnar nerve regions of interest. a Color mapping of shear wave velocity results. b Propagation of shear wave velocity results
Valgus stress was applied to the medial elbow using a Telos stress device (Telos SE; Aimedic MMT, Tokyo, Japan). The basic positions were as follows: head and neck neutral, shoulder abduction at 90°, shoulder external rotation at 90°, and maximum forearm supination. The flexion angles of the elbow were set to 0°, 60°, and 90°, according to a previous study [4] (Fig. 4). Valgus stresses of 0 (rest), 30, 50, and 70 N were applied using the Telos stress device. The ultrasonography measurements were conducted under four conditions.
Fig. 4.
Sonographic measurements obtained at different elbow flexion angles. a Elbow flexion 0°. b Elbow flexion 60°. c Elbow flexion 90°
The imaging tests and measurements were performed by a single examiner. The intrarater reliability of this analytical method was examined in advance. One examiner assessed 10 healthy adults using the method described above.
Statistics
Intrarater reliability was defined as poor (< 0.5), moderate (0.5–0.75), good (0.75–0.9), excellent (> 0.9), and absolute [20]. The standard error of measurement (SEM) and minimal detectable change with 95% confidence (MDC 95) were calculated.
The difference in the stiffness at 0 N (rest) relative to the stiffness under different degrees of valgus stress was defined as the amount of change. Comparisons of the amount of change in values for the entrapment sites under valgus stress were performed using a two-way analysis of variance. Subsequently, the Tukey–Kramer test for multiple comparisons was conducted after a two-way analysis of variance. Statistical significance was set at p < 0.05. Statistical analyses were performed by the same examiner using SPSS statistics version 27.
Results
Participants’ characteristics
Twenty healthy baseball players and 20 elbows that met the inclusion criteria were included in this study (Table 1).
Table 1.
Demographic profile of healthy baseball players
| Age | 20.1 ± 1.1 |
| Height (cm) | 171.0 ± 5.8 |
| Weight (kg) | 65.8 ± 9.3 |
| Position |
Pitcher 4 Catcher 4 Fielder 12 |
Intrarater reliability of stiffness changes detected by ultrasonography
Ten healthy adults (age, 21.4 ± 2.1 years; height, 175.3 ± 5 cm; weight, 73.8 ± 9.6 kg) were included. The intraclass correlation coefficients (ICC 1,2) and 95% confidence intervals (CI) for the ulnar nerve stiffness in the proximal site were 0.89 (0.55–0.97) at rest at 60° elbow flexion and 0.89 (0.58–0.97) at 0° elbow flexion under 50 N valgus stress, with good intraexaminer reliability. The other ICC (1,2) ranged from 0.9 to 0.99, with excellent intraexaminer reliability (Table 2).
Table 2.
Intrarater reliability of the proximal part of the ulnar nerve (intraclass correlation coefficient [ICC] 1.2)
| Rest | 30N | 50N | 70N | ||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 0° | 60° | 90° | 0° | 60° | 90° | 0° | 60° | 90° | 0° | 60° | 90° | ||||
| ICC | 0.92 | 0.89 | 0.98 | 0.98 | 0.97 | 0.99 | 0.89 | 0.90 | 0.97 | 0.97 | 0.98 | 0.98 | |||
| 95%CI | 0.69–0.98 | 0.55–0.97 | 0.93–0.99 | 0.95–0.99 | 0.88–0.99 | 0.99–0.99 | 0.58–0.97 | 0.59–0.97 | 0.89–0.99 | 0.88–0.99 | 0.94–0.99 | 0.93–0.99 | |||
| SEM | 0.31 | 0.60 | 0.25 | 0.15 | 0.27 | 0.07 | 0.38 | 0.47 | 0.22 | 0.18 | 0.13 | 0.08 | |||
| MDC95 | 0.87 | 1.66 | 0.69 | 0.43 | 0.76 | 0.20 | 1.07 | 1.32 | 0.63 | 0.50 | 0.38 | 0.23 | |||
The ICC (1,2) for the stiffness of the ulnar nerve in the distal site was 0.89 at 0° elbow flexion under 30 N valgus stress, with good intraexaminer reliability. The other ICC (1,2) ranged from 0.9–0.99, with excellent intrarater reliability (Table 3).
Table 3.
Intrarater reliability of the distal part of the ulnar nerve (ICC 1.2)
| Rest | 30N | 50N | 70N | ||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 0° | 60° | 90° | 0° | 60° | 90° | 0° | 60° | 90° | 0° | 60° | 90° | ||||
| ICC | 0.97 | 0.95 | 0.99 | 0.87 | 0.97 | 0.98 | 0.99 | 0.98 | 0.99 | 0.95 | 0.98 | 0.98 | |||
| 95%CI | 0.88–0.99 | 0.83–0.99 | 0.96–0.99 | 0.49–0.97 | 0.90–0.99 | 0.92–0.99 | 0.96–0.99 | 0.95–0.99 | 0.97–0.99 | 0.79–0.98 | 0.92–0.99 | 0.94–0.99 | |||
| SEM | 0.16 | 0.31 | 0.19 | 0.37 | 0.27 | 0.15 | 0.17 | 0.13 | 0.15 | 0.33 | 0.24 | 0.18 | |||
| MDC95 | 0.45 | 0.87 | 0.54 | 1.03 | 0.76 | 0.42 | 0.48 | 0.38 | 0.44 | 0.92 | 0.68 | 0.52 | |||
Comparison of stiffness at different elbow flexion angles under valgus stress
Valgus stress had a significant effect at 0° elbow flexion (p = 0.001). The values observed at different sites were significantly different (p = 0.009). No interaction between the valgus stress and entrapment site (p = 0.72) was observed. The results of the post hoc test showed that the stiffness of the ulnar nerve increased significantly under 70 N stress compared to that under 30 N valgus stress, both at the proximal and distal sites. In addition, the stiffness of the ulnar nerve in the proximal site was significantly higher under 70 N valgus stress than that in the distal site (Fig. 5a).
Fig. 5.
Comparison of ulnar nerve stiffness at different entrapment sites and under varying intensities of valgus stress. **Significantly different (p < 0.01). *Significantly different (p < 0.05). a Elbow flexion 0°. b Elbow flexion 60°. c Elbow flexion 90°
Valgus stress had a significant effect at 60° elbow flexion (p = 0.001). The values observed at different sites were significantly different (p = 0.003). No interaction between the valgus stress and entrapment site (p = 0.63) was observed. Both the proximal and distal ulnar nerve stiffness values increased significantly under 70 N stress compared to that under 30 N valgus stress. The stiffness of the proximal site was significantly higher than that of the distal site under all valgus stress intensities applied (Fig. 5b).
Valgus stress exerted a significant effect at 90° elbow flexion (p < 0.001). The values observed at different sites were significantly different (p = 0.001). No interaction between the valgus stress and entrapment site (p = 0.46) was observed. Both the proximal and distal ulnar nerve stiffness values increased significantly under 70 N stress compared to that under 30 N valgus stress. The stiffness of the proximal and distal sites of the ulnar nerve significantly increased under 70 N stress compared with that under 50 N stress. The stiffness of the proximal ulnar nerve was significantly higher than that of the distal ulnar nerve under 50 and 70 N valgus stress intensities (Fig. 5c).
Discussion
At all elbow flexion angles, the stiffness of the ulnar nerve under 70 N valgus stress was higher than that under 30 N stress. At 90° elbow flexion, the stiffness of the ulnar nerve at 70 N valgus stress increased compared to that under 50 N stress. Overall, the stiffness of the ulnar nerve increased with an increase in the valgus stress. The stiffness of the proximal ulnar nerve was significantly higher than that of the distal ulnar nerve.
Regarding ulnar nerve stiffness under valgus stress on the medial elbow, anatomical studies have reported that the strain on the ulnar nerve increases during valgus loading compared with that observed during rest [4]. However, in previous study was investigated using cadavers. Thus, the in vivo changes in strain on the ulnar nerve that occur with change in the valgus stress were unclear. In this study, these previous findings were confirmed in vivo using the shear wave elastography mode of ultrasonography. Consistent with these reports, in this study, the stiffness of the ulnar nerve increased with an increase in valgus stress in vivo, and the proximal nerve stiffness was significantly higher than the distal nerve stiffness under valgus stress in vivo.
Moreover, a previous study reported that the strain on the ulnar nerve at the proximal site increased compared to that at the distal site during elbow flexion [21]. However, in these studies, the changes in strain with changes in the elbow flexion angles were investigated using cadavers. The difference in ulnar nerve tension at the proximal and distal sites produced when the medial elbow is subjected to valgus stress in a position simulating the MER during pitching has not been determined using in vivo studies. In this study, the stiffness of the ulnar nerve increases with the valgus stress in vivo, and its proximal stiffness was significantly increased compared to its distal one under valgus stress in vivo. It has been reported that when nerves are stretched, the nerve load on adjacent joints increases, resulting in tension from more proximal locations [22]. During joint movement, nerve motion shifts from laxity to sliding to tension [23]. The strain on the ulnar nerve increases during valgus loading compared with that observed during rest [4]. In addition, the strain on the ulnar nerve at the proximal site increased compared to that at the distal site during elbow flexion [21]. In this study, the stiffness of the proximal site increased more than the distal site when the elbow valgus stress was increased. Under these conditions, the ulnar nerve was pulled proximally, resulting in increased ulnar nerve stiffness on the proximal site rather than the distal site.
Peripheral neuropathy was evaluated using ultrasonography to measure the cross-sectional area and stiffness of the nerve. In a previous study on the cross-sectional area of the ulnar nerve in baseball players with ulnar neuropathy, the ulnar nerve was significantly swollen at the cubital tunnel and Osborne’s ligament sites compared to that in the arcade of Struthers [10]. In this study, the stiffness at the proximal site increased, resulting in swelling at different sites, as reported previously. These findings suggest that nerve swelling due to entrapment neuropathy may be caused by a mechanism other than the increased stiffness of the nerve that is caused by the throwing motion.
This study has several limitations. First, only healthy baseball players were included in the study. The strain on the ulnar nerve at the distal site is reported to be higher than that at the proximal site in cases of ulnar nerve entrapment in the cubital tunnel [21]. Therefore, changes in nerve stiffness may differ among players with valgus instability and those with ulnar neuropathies caused by ulnar collateral ligament injuries. In the future, studies should be conducted to validate these findings in patients with ulnar collateral ligament injuries and ulnar neuropathies. Second, a long-axis image of the ulnar nerve at the cubital tunnel site could not be obtained. Therefore, the changes in nerve stiffness within the cubital tunnel could not be determined. Third, because this was a cross-sectional study, the prognosis regarding the expected changes in ulnar nerve stiffness could not be assessed. In the future, prospective studies are warranted to confirm these findings. Fourth, the shoulder could not be imaged in the MER position. This study was based on analysis of the limb in the MER position during the late cocking phase. However, valgus stress using a Telos stress device cannot be applied to the limb in the MER position. Fifth, an increase in the ulnar nerve stiffness may be related to both the nerve fascicles and the connective scaffold of the nerve. Ricci et al. suggested that in the acute phase, the increased stiffness may be related to the intradural edema of the fascicles [24]. In the chronic phase, stiffness may be related to the thickening of the intraneural connective tissue (neural fibrosis) [24]. Therefore, the data obtained from the shear wave elastography should be always matched with the B-mode sonographic findings.
Conclusion
The stiffness of the ulnar nerve increased significantly under 70 N valgus stress compared to that under 30 N stress. An increase in the valgus load during pitching may increase the stretching stress on the ulnar nerve. A comparison of nerve stiffness at different sites showed that the stiffness of the proximal ulnar nerve was significantly higher than that of the distal nerve.
Acknowledgements
The authors acknowledge Soichiro Kitayama and Ashiya orthopedics sports clinic for assistance with this project. We would like to thank Editage (www.editage.com) for English language editing.
Abbreviations
- MER
Maximal external rotation
- proximal site
Arcade of struthers
- distal site
Osborne’s ligament
- SEM
Standard error of measurement
- MDC 95
Minimal detectable change with 95% confidence
Author contribution
Shintarou Kudo and Issei Noda researched literature and conceived the study. Shintarou Kudo, Issei Noda, Masahiro Tsutsumi and Kengo kawanishi were involved in protocol development, gaining ethical approval, patient recruitment and data analysis. Issei Noda, Rio Goto and Shunpei Yamashita collected the data. Issei Noda wrote the first draft of the manuscript. All authors reviewed and edited the manuscript and approved the final version of the manuscript.
Funding
This author, their immediate family, and any research foundation with which they are affiliated did not receive any financial payments or other benefits from any commercial entity related to the subject of this article.
Declarations
Competing interests
This author, their immediate family, and any research foundation with which they are affiliated did not receive any financial payments or other benefits from any commercial entity related to the subject of this article.
Ethical approval
This study was approved by the Ethics Review Committee of Morinomiya University of medical sciences (approval number 2020-102).
Consent to Participate
Written informed consent was obtained from the patients for their anonymized information to be published in this article.
Consent to Publish
Written informed consent was obtained from the patients for their anonymized information to be published in this article.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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