Influence of toe flexor muscle fatigue on stiffness of the intrinsic foot muscles

Abstract

BACKGROUND:

Assessing intrinsic foot muscles (IFM) is important for understanding their role in loading movements. Additionally, knowledge of the impact of IFM following toe flexor muscle fatigue may aid the teaching of IFM exercises.

OBJECTIVE:

To examine the influence of toe flexor muscle fatigue on IFM stiffness using ultrasound shear-wave elastography.

METHODS:

This study included 19 college students. IFM stiffness at 10%, 50%, and 90% body weight was measured using ultrasound-based shear-wave elastography. IFM including the abductor hallucis (AbH), flexor hallucis brevis (FHB), flexor digitorum brevis (FDB), and quadratus plantae (QP) were assessed. The fatigue induction protocol comprised a series of toe flexions at a controlled pace of 40 beats per minute and an amplitude of 75% of the maximum toe flexor strength for a duration of 5 minutes.

RESULTS:

Muscle stiffness significantly increased with increasing load. Toe flexor muscle fatigue significantly increased the stiffness of the FDB.

CONCLUSIONS:

IFM stiffness significantly increased with increasing load, and the stiffness of FDB significantly increased in the toe flexor muscle fatigue condition at DLS and SLS loads. The findings of this study will contribute to the study and clinical setting of IFM exercises.

Keywords

Intrinsic foot muscles stiffness toe flexor muscle body weight load

1. Introduction

The intrinsic foot muscles (IFM) are the main medial longitudinal arch stabilizers and are crucial to the passive, active, and neurological subsystems that make up the core foot musculature [1]. During balancing tasks, IFM stabilize the foot to provide postural stability [2]. During walking, IFM provide dynamic support to the longitudinal arch [3]. Thus, IFM plays an important stabilizing role in loading movements in daily life and sports. Therefore, it is important to assess IFM during loading.

In recent years, ultrasound shear-wave elastography (SWE) has made it possible to measure changes in the stiffness of individual muscles and the properties of the deeper layers of individual muscle tissues beyond the surface [4, 5]. The SWE reliably assesses IFM morphology [4, 6, 7, 8]. Muscle stiffness in both normal and flat feet IFM increases with body weight loading [4, 9]. Thus, although foot morphology affects IFM stiffness, to our knowledge, no studies have examined the effect of IFM after muscle fatigue. When muscles become fatigued, their flexibility and extensibility decrease, while at the same time, muscle stiffness tends to increase. The increase in muscle stiffness during fatigue is primarily attributed to the stiffening of muscle fibers and fascia, decreased control of muscle contractions, accumulation of lactate and other metabolic byproducts within the muscle, and fatigue within the nervous system [10, 11, 12]. As a result, there is a decrease in muscular flexibility and a possible reduction in movement and physical activity performance. Furthermore, IFM is associated with toe flexor muscle strength. Therefore, understanding the effects of toe flexor muscle fatigue on IFM will help in teaching IFM exercises.

This study aimed to examine the influence of toe flexor muscle fatigue and loading conditions on IFM stiffness using ultrasound SWE. We hypothesized that IFM stiffness would be higher in the toe flexor muscle fatigue group than that in the sham group. In addition, it was hypothesized that muscle stiffness would increase with each increase in load.

Figure 1.

The measurement setup.

2. Methods

2.1 Participants

Twenty-one male and female college students agreed to participate in this study. However, two students dropped out of the study during the experimental period for reasons unrelated to the study. Thus, the study included nineteen students (13 men and 6 women) for the final analysis (mean $\pm$ standard deviation; height, 1.67 $\pm$ 0.09 m; body weight, 60.50 $\pm$ 7.46 kg; age, 20.37 $\pm$ 0.98 years). The inclusion criteria were as follows: (1) no ankle or foot joint instability; (2) no history of ligament rupture, fracture, or dislocation in the lower extremities; (3) no neuromuscular illness; (4) no previous history of neuromuscular disorder; (5) no head trauma in the last six months; and, (6) no illnesses or injuries that could affect balance. Participants were excluded from the study if pain occurred in the lower extremities or other body parts during the measurement. G*Power (version 3.1.9.7) was used to determine the sample size. The calculation was based on the F test (Effect size $=$ 0.3, $\alpha$ $=$ 0.05, Power $=$ 0.8), which required a sample size of 19 participants [4]. All participants provided written informed consent, and the Chukyo University Research Ethics Committee (No. 2022-41) approved the study.

2.2 Procedures

The participants reported to the laboratory for two testing sessions that were one week apart. Measurements were obtained under two fatigue conditions: induced toe flexor muscle fatigue and sham. A simple randomization procedure (sequentially numbered draws from containers) was used to allocate the testing sessions.

IFM stiffness: IFM stiffness was measured using an Aixplorer ultrasound system (Supersonic Imagine; Aix-en-Provence, France). Muscle stiffness of the abductor hallucis (AbH), flexor hallucis brevis (FHB), flexor digitorum brevis (FDB), and quadratus plantae (QP) was assessed with participants in three testing positions: seated, both-leg stance, and single-leg stance [6, 7, 8, 13]. Measurements were taken with the foot on the scale, monitoring 10% (sitting stance, SS), 50% (double leg stance, DLS), and 90% of the body weight load (single leg stance, SLS) (Fig. 1) [4]. The measuring positions of the IFM were determined by Kobayashi et al. in their study [4]. Two examiners measured the stiffness of the IFM, and the Young modulus (kPa) was calculated to analyze the quantitative changes in muscle stiffness between fatigue conditions [4].

Figure 2.

The toe flexor muscle fatigue task.

Fatigue-induction protocol: The fatigue-induction protocol comprised a series of toe flexions at a controlled pace (40 beats per minute) and amplitude (75% of maximum toe flexor strength) that lasted for 5 min (Fig. 2). The maximum force of toe flexor strength was assessed before and after the fatigue protocol. The time, pace, and amplitude of the fatigue protocol were determined based on a pilot study with five participants. As a result of the fatigue protocol, the maximum toe flexor strength decreased in all five participants and was therefore adopted for this study. A series of toe flexions were implemented using a toe muscle strength dynamometer (T.K.K.3365b, Takei Scientific Instruments Co., Ltd, Japan). The sham protocol consisted of five minutes of resting in a seated position.

2.3 Statistical analyses

Statistical analyses were performed using SPSS (version 26.0; IBM Corp., Armonk, NY, USA). The normality of all data was analyzed using the Shapiro-Wilk test. Results are expressed as mean $\pm$ standard deviation (SD). Two-way ANOVA (between-participant factor, condition; within-participant factor, load) was used for group comparisons of IFM stiffness. Post-hoc analyses were performed using the Bonferroni method when appropriate. Differences were considered statistically significant at $p<$ 0.05.

Figure 3.

Comparison between muscle stiffness of AbH for each condition and load.

Figure 4.

Comparison between muscle stiffness of FHB for each condition and load.

Figure 5.

Comparison between muscle stiffness of FDB for each condition and load.

Figure 6.

Comparison between muscle stiffness of QP for each condition and load.

Table 1

Muscle stiffness of intrinsic foot muscle variables for each condition and load

Muscle stiffness variables (kPa)	SS	DLS	SLS
	Mean $\pm$ SD	Mean $\pm$ SD	Mean $\pm$ SD
AbH
Fatigue condition	18.03 $\pm$ 12.30	42.12 $\pm$ 21.54	69.71 $\pm$ 30.46
Sham condition	26.42 $\pm$ 16.04	42.72 $\pm$ 31.17	67.45 $\pm$ 37.19
FHB
Fatigue condition	20.38 $\pm$ 10.65	37.92 $\pm$ 19.00	54.01 $\pm$ 30.02
Sham condition	19.03 $\pm$ 11.19	40.82 $\pm$ 23.13	64.67 $\pm$ 37.78
FDB
Fatigue condition	25.67 $\pm$ 9.88	69.03 $\pm$ 29.68	90.38 $\pm$ 36.22
Sham condition	20.12 $\pm$ 12.06	38.31 $\pm$ 22.11	55.72 $\pm$ 23.25
QP
Fatigue condition	21.84 $\pm$ 11.60	55.67 $\pm$ 28.24	78.26 $\pm$ 31.52
Sham condition	17.56 $\pm$ 6.81	28.34 $\pm$ 23.18	46.66 $\pm$ 34.55

SS, sitting stance; DLS, doubleleg stance; SLS, singleleg stance; AbH, abductor hallucis; FHB, flexor hallucis brevis; FDB, flexor digitorum brevis; QP, quadratus plantae.

3. Results

Table 1 shows the means and standard deviations (SD) of all variables. The main effect of load was observed in all the muscles, which showed a significantly greater increase in fatigue in DLS and SLS loads than that in SS loads ( $p<$ 0.001) (Figs 3–6). Furthermore, the stiffness of all muscles significantly increased during the SLS load compared to that during the DLS load ( $p<$ 0.01). An interaction was observed for FDB ( $p=$ 0.004). In both conditions, the stiffness of FDB was significantly higher at the DLS and SLS loads than that at the SS load ( $p<$ 0.01). Furthermore, the stiffness of FDB was significantly higher with the SLS load than that with the DLS load ( $p<$ 0.05). The stiffness of FDB was significantly higher in the toe flexor muscle fatigue condition than that in the sham fatigue condition at the DLS and SLS loads ( $p<$ 0.01).

4. Discussion

This is the first study to examine the influence of toe flexor muscle fatigue on IFM stiffness by using ultrasound SWE. All muscle stiffness values significantly increased with increasing load. Additionally, the stiffness of FDB was significantly higher in the toe flexor muscle fatigue condition than that in the sham fatigue condition under the DLS and SLS loads.

Kobayashi et al. [4] reported the morphological and mechanical characteristics of the soft tissue structures in normal and flat feet subjected to loading; IFM stiffness increased with increasing load in both normal and flat feet. This finding is consistent with that of this study. Muscle stiffness increases with elongation due to passive tension [14, 15]. Therefore, regardless of the fatigue condition, IFM is assumed to be stiff due to loading-associated muscle elongation. However, the increased stiffness of IFM under loading could contributing to muscle contraction. This is an important topic for future research.

The muscle stiffness of the FDB was significantly higher in the toe flexor muscle fatigue condition under DLS and SLS loads. The FDB affects PIP joint flexion and MTP joint slight flexion. In our study, muscle fatigue was due to toe flexion, mainly in the second to fourth toes. Therefore, because the extrinsic foot muscles are connected to the QP, the extrinsic muscles of toe flexion are used in the toe flexor muscle fatigue condition, and the muscle stiffness of the FDB at the surface of the QP is significantly increased. In addition, to consider the safety of the participants, the strength and duration of the muscle fatigue conditions in the present study were set with reference to a preliminary experiment. Therefore, the fatigue task performed in this study may not have reached the intensity required to fatigue the IFM. This issue should be addressed in future studies. Notwithstanding these limitations, this is the first study to observe IFM stiffness after a toe flexor muscle fatigue task. It has been revealed that the IFM plays a crucial role in balance function [16], and strengthening these muscles is believed to be effective in improving balance ability. A previous study also suggests that the IFM stiffness may be related to the performance of the jump performance and landing in adolescent athletes [17]. Our findings contribute to the fact that improving athletic performance requires not only IFM exercises, such as short foot exercises, but also the elimination of foot fatigue.

This study has several limitations. First, the study included both men and women. Because the effects of sex on muscle stiffness of the IFM are unclear [4, 18, 19], future research may need to examine the sexes differently. Secondly, the fatigue tasks in this study were not performed under uniform conditions. Therefore, we cannot exclude the possibility that individual toe flexor muscle strength levels during the measurements may have affected the results.

5. Conclusions

Intrinsic foot muscle stiffness significantly increased with increasing load, and stiffness of the FDB significantly increased in the toe flexor muscle fatigue condition under DLS and SLS loads. The findings of this study will contribute to the study and clinical setting of IFM exercises. Further studies are required to validate the muscle stiffness of IFM after fatigue.

Author contributions

CONCEPTION: Kazushi Yoshida, Junji Shinohara.

PERFORMANCE OF WORK: Kazushi Yoshida,Mikuto Katuya, Shogo Takano, Kazuma Hayashi.

INTERPRETATION OR ANALYSIS OF DATA:Kazushi Yoshida, Mikuto Katuya, Taisei Hakozaki.

PREPARATION OF THE MANUSCRIPT: Kazushi Yoshida.

REVISION FOR IMPORTANT INTELLECTUAL CONTENT: Kazushi Yoshida, Junji Shinohara, Taisei Hakozaki.

SUPERVISION: Kazushi Yoshida, Mikuto Katuya, Junji Shinohara.

Ethical approval

All participants provided written informed consent and approval for the study was obtained from the Chukyo University Research Ethics Committee (approval number: No. 2022-041, dated March 14, 2023).

Funding

The authors report no funding.

Footnotes

Acknowledgments

The authors thank all those who participated in the research. We would like to thank Editage (www.editage. jp) for English language editing.

Conflict of interest

The authors declare no conflicts of interest.

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