Plantar intrinsic foot muscle activity and its relationship with postural sway during single-legged and bipedal tiptoe standing in ballet dancers

doi:10.21203/rs.3.rs-4702997/v1

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Plantar intrinsic foot muscle activity and its relationship with postural sway during single-legged and bipedal tiptoe standing in ballet dancers

https://doi.org/10.21203/rs.3.rs-4702997/v1

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During tiptoe standing, especially with the single-legged support, the foot joints in ballet dancers are heavily loaded. Thus, the activity of the plantar intrinsic foot muscles (PIFMs), which stabilize the foot joints, may be important in reducing postural sway during tiptoe standing. We compared PIFM activity during single-legged and bipedal tiptoe standing and examined its relationship to postural sway in dancers. In 11 female ballet dancers, the electromyography (EMG) amplitudes of PIFMs and the center of pressure (COP) data were recorded during single-legged and bipedal tiptoe standing tasks. The EMG amplitudes were normalized to those during the maximal voluntary contraction, and PIFM activity level and its coefficient of variation over time (EMG-CVtime) during the task were assessed. From the COP data, standard deviations in the anteroposterior (COP-SDAP) and mediolateral (COP-SDML) direction, velocity, and area were calculated. PIFM activity level and COP velocity were 2–2.5-fold higher in the single-legged than bipedal task (p≤0.003). Significant correlations were found between PIFM activity level and COP velocity (r=0.666, p=0.025) and between EMG-CVtime and COP-SDAP or COP-SDML (r≥0.738, p≤0.010) only in the single-legged task. These results suggest that PIFM activity is associated with postural sway, especially during single-legged tiptoe standing in dancers.

Biological sciences/Neuroscience

Health sciences/Anatomy

high-density electromyography

temporal variability

postural sway

center of pressure

foot

Reducing postural sway during tiptoe standing ("demi-pointe" in ballet terminology) is essential for ballet dancers (hereafter referred to as "dancers")^1,2. In particular, single-legged tiptoe standing (STS) is frequently employed in ballet choreography because the unsupported leg can be used for a variety of expression. During STS, dancers are required to maintain a high and stable foot arch structure in the supported leg, which is aesthetically desirable^3,4. The foot arch structure is primarily supported by passive and non-contractile components (e.g., bones, ligaments, plantar fascia, etc.)⁵. However, in situations of high postural demands or heavy foot loading, stabilization of the foot arch structure is achieved by additional muscle-generated forces^6,7. Given that the foot joints of dancers are characterized by hypermobility^8,9, the activity of the muscles involved in the stability of these joints may be important in reducing postural sway during STS.

The plantar intrinsic foot muscles (PIFMs), which originate and insert within the foot, function in the stability or mobility of the foot joints^5,6,10–12. Electromyography (EMG) studies in non-dancers have shown that PIFM activity increases or decreases in response to postural demands or foot loading; PIFM activity level is significantly higher in single-legged standing, bipedal tiptoe standing (BTS), and STS compared to bipedal standing^6,13. Recent studies also suggest that the primary role of PIFMs during standing is to stabilize the foot joint (i.e., indirectly contribute to postural control) due to their short moment arms^5,14,15. Nevertheless, there is little information on how PIFMs activity is associated with postural sway during tiptoe standing performed by dancers. Our previous study showed that dancers had much less postural sway and lower level/variability of PIFM activity during BTS, compared to non-dancers¹⁶. This suggests that BTS is not a high postural demand for dancers and that low and steady PIFM activity is associated with less postural sway. However, no studies have examined PIFM activity during STS and how it relates to postural sway in dancers.

The tiptoe standing that dancers perform in daily practice and on stage requires a large ankle plantar flexion (PF) angle, which is not achievable in non-dancers, and this is even more so during STS^8,9,16. When comparing muscle activity between individuals/conditions and examining its relationship to other parameters such as postural sway, a well-controlled task setting with the specified/same joint angle is appropriate^17,18. In fact, our previous study found that PIFM activity and postural sway during BTS differed among different ankle PF angles, and the relationships between these variables were also different depending on the ankle PF angle¹⁶. Thus, comparing PIFM activity between STS and BTS, as well as examining its relationship with postural sway, at a large and specified ankle PF angle will shed light on dancers’ postural control during tiptoe standing. However, this has never been studied. Some previous studies have used intramuscular EMG to examine PIFM activity^6,7,13, but there are difficulties in using this technique due to its invasive nature, especially considering its potential detrimental effect on the dancers' subsequent performance. This study therefore adopted high-density EMG using a grid with multiple surface electrodes, which can noninvasively record PIFM activity across a large region of the plantar foot^14,16,19.

The objectives of this study were to 1) compare PIFM activity and postural sway between STS and BTS conditions in dancers, and 2) examine the relationship between PIFM activity and postural sway in each condition. We hypothesized that 1) PIFM activity (its level and temporal variability) and postural sway would be significantly higher during STS than during BTS, and 2) PIFM activity would be associated with postural sway during both STS and BTS but especially the former.

Participants

Eleven female ballet dancers (age: 25.1 ± 2.3 y, height: 163.9 ± 6.3 cm, body mass: 47.9 ± 4.9 kg, BMI: 17.8 ± 1.2 kg/m²) were enrolled in this study. The participants were the same as those in our recent publication¹⁶, which compared postural sway and PIFM activity during BTS in dancers versus non-dancers (n = 14 vs 13). This study reports original data for STS that was performed by eleven dancers only, while deriving the data from our previous study for BTS performed by the same eleven dancers. Dancers needed to have an at least 10 years of ballet experience and still receive at least 7.5 hours of ballet training per week. None of the participants had a history of injury or surgery in the ankle and foot joints within the past 3 months or 1 year, respectively. The study protocols complied with the principles of the Declaration of Helsinki and were approved by the Ethics Committee of Ritsumeikan University (BKC-LSMH-2021-048), and all participants provided written informed consent.

Experimental Protocol

The postural control task consisted of BTS for 30 seconds and STS (right leg) for 10 seconds, both at ankle PF 60°^16,20. Electric goniometers (SG110, Biometrics, UK) were applied to measure ankle PF angles during the postural control tasks. The stationary arm of the goniometer was aligned with the long axis of the fibula in the sagittal plane, while the moving arm was aligned with the plantar plane on the side of the little toe (i.e., fifth metatarsal bone) and attached to both feet. Note that the ankle PF angle is the sum of the talocrural joint and several foot joints (Chopart’s joint, Lisfranc’s joint, etc.). The visual feedback of the goniometer data of each foot was provided in real time via two 16-bit A/D converters (PowerLab 2/20; ADInstruments, Australia) and on two PC monitors located at participants’ eye level, approximately 1 m in front of them (Fig. 1A)^16,20. During the STS task, the goniometer on the left (unsupported) leg was removed. Participants initially stood on a force plate (SS-FP40AO-SY, Sports Sensing, Japan). In the BTS task, they began tiptoe standing while holding the bar in front of themselves with their hands, and then removed their hands from the bar after they were able to maintain the PF angles of both feet at the specified angle as much as possible by watching the monitor so that the body mass on both feet was equal. During the BTS task, they kept both feet parallel at a comfortable stance width, with the knees fully extended, and hands relaxed on the sides of the body. In the STS task, participants started the right leg tiptoe standing with both hands holding the bar, and when they were able to maintain the PF angle at the specified angle as much as possible while watching the monitor, they removed their hands from the bar. During the STS task, the right leg was maintained in optimal turnout (i.e., external rotation of the lower limb), the left leg in retiré (i.e., the left small toe on the knee joint of the right leg), and the upper limb in en avant (i.e., the upper limbs in a circular position with both fingertips in front of the trunk) (Fig. 1B). Considering the degree of postural demand, trials were performed in the order of the BTS task and then STS task. Participants performed practice trials to familiarize themselves with the procedure and subsequently performed 3 trials at each task with a rest period of at least 1 minute between trails. The average data from three successful trials were used in the data analysis. A successful trial was defined as one in which the participant was able to maintain the specified angle without grasping the bar or stepping out during the trial.

Data Acquisition

Monopolar surface EMG amplitudes from the PIFMs were acquired with a high-density grid of 64 channels (GR08MM1305, OT Bioelettronica, Italy) consisting of 13 rows and 5 columns (minus one electrode) with an 8 mm inter-electrode distance in both directions (Fig. 2A), in accordance with prior studies^14,16,19. The right plantar skin was lightly rubbed with sandpaper and cleaned with alcohol. After palpation of the heel and metatarsal fat pads, a high-density grid was placed in the center of these areas, aligned with the long axis of the foot (i.e., second metatarsal) (Fig. 2B)^14,16,19. The grid was reinforced with tapes to ensure consistent contact with the sole at any ankle PF angle during the tasks. Reference electrodes were placed around the right knee and left wrist. The acquired amplitudes were amplified using a 16-bit analog-to-digital converter (Quattrocento; OT Bioelectronica, Italy), with a sampling frequency of 2048 Hz and a bandpass filter of 10–500 Hz (Fig. 2C). During the tasks, the COP data were acquired using the force plate and a 16-bit A/D converter (PowerLab/16SP; ADInstruments, Australia) with a sampling frequency of 1000 Hz and a low-pass filter of 5 Hz. Additionally, participants performed 5-s maximum voluntary contractions (MVCs) against manual resistance provided by one researcher twice for each of toe flexion (all toes) and toe abduction (the great and little toes), during which EMG were recorded^13,16,21.

Data Analysis

The EMG amplitude and COP data were synchronized using a trigger from a 16-bit A/D converter (PowerLab/8SP; ADInstruments, Australia). The analysis interval was 20 s excluding the first 5 s from the start of the task in the BTS task and 5 s excluding the first 2.5 s from the start of the task in the ST task. EMG signals recorded from 64 electrodes were visually inspected, and channels showing noise were reconstructed based on the interpolation of the signals from neighboring channels^14,16,19. For each channel, the EMG root-mean-square (RMS) values during the tasks were calculated and normalized to the highest value over a 500-ms time window during the MVC tasks. The normalized EMG values were averaged across 64-channels^14,16,19, and used as a criterion value for PIFM activity level (% MVC). From the EMG amplitude, the coefficient of variation over time (EMG-CV_time) during the tasks was also calculated to evaluate the temporal variability of PIFM activity level. This was calculated by dividing the standard deviation (SD) by the mean of the EMG amplitudes during the analysis interval for each channel and then averaging over all 64 channels^16,22,23. From the COP data, the SD in the anteroposterior and mediolateral directions (COP-SD_AP and COP-SD_ML), average velocity (COP-Velocity), and area of a 95% confidence ellipse encompassing the COP (COP-Area) were further calculated for the analysis interval as indices of postural sway^16,24,25.

Statistical Analysis

For all variables, the Shapiro-Wilk test was applied to assess normality, which was confirmed for all variables except for PIFM activity level and EMG-CV_time in the BTS task, and COP-Area in the STS task. Therefore, between-task comparisons were made by Wilcoxon's signed rank test for these non-normally distributed variables, and by paired t-tests for the other variables. Effect sizes of between-task differences were calculated as Cohen’s d values and were interpreted as trivial < 0.2; small 0.2–0.49; moderate 0.5–0.79; and large ≥ 0.8²⁶. Additionally, their bootstrap 95% confidence interval (5,000 samples, bias-corrected and accelerated) was assessed by using estimation statistics to improve statistical inference²⁷. To evaluate the relationship between COP variables and EMG variables in each task, Pearson's correlation coefficient and Spearman's rank correlation coefficient were calculated for normally and non-normally distributed data, respectively. Values were considered statistically significant at p < 0.05. All data were analyzed using SPSS software (SPSS Statistics 28, IBM, USA) unless otherwise stated.

Compared to the BTS task, the STS task had significantly higher COP-Velocity (BTS vs STS, 2.0 ± 0.3 vs 5.1 ± 0.4 cm/s, p < 0.001, d = 8.77, Fig. 3C) and PIFM activity level (11.4 ± 2.8 vs 25.8 ± 7.8%MVC, p = 0.003, d = 2.47, Fig. 4A). There was no significant difference between tasks in the other variables (p = 0.093–0.941, d = 0.05–0.61, Figs. 3 and 4).

In the STS task, significant correlations were found between PIFM activity level and COP-Velocity (r = 0.666, p = 0.025), between EMG-CV_time and COP-SD_AP (r = 0.846, p = 0.001), and between EMG-CV_time and COP-SD_ML (r = 0.738, p = 0.010) (Table 1). In the BTS task, no correlation was found between any combinations of the variables (r = 0.097–0.559, p = 0.074–0.778, Table 1).

Table 1

Correlation coefficients between COP and EMG variables
		PIFM activity level (%MVC)			EMG-CV_time (%)
COP	Position	r		P	r		p
SD_AP (cm)	BTS	0.174		0.608	0.097		0.778
SD_AP (cm)	STS	0.083		0.808	0.846	**	0.001
SD_ML (cm)	BTS	−0.210		0.536	0.340		0.306
SD_ML (cm)	STS	−0.037		0.913	0.738	**	0.010
Velocity (cm/s)	BTS	0.282		0.400	0.559		0.074
Velocity (cm/s)	STS	0.666	*	0.025	0.499		0.118
Area (cm²)	BTS	0.000		1.000	0.362		0.275
Area (cm²)	STS	−0.191		0.574	0.301		0.368
Significance of Pearson’s correlation coefficient and Spearman's rank correlation coefficient are indicated as follows: p < 0.05, *p < 0.01. COP, center of pressure; SD, standard deviation; AP, anteroposterior; ML, mediolateral; PIFM, plantar intrinsic foot muscle; EMG-CV_time, temporal variability of EMG; BTS, bipedal tiptoe standing; STS, single-legged tiptoe standing.

The main findings of this study are as follows: 1) COP-Velocity and PIFM activity level were higher in the STS than BTS task, and 2) significant correlations were found between COP and EMG variables only in the STS task. These results partially support our hypothesis and suggest that foot loading and postural demands are increased during STS compared to BTS, and that PIFM activity is particularly associated with postural sway during STS in dancers.

In the present study, only COP-Velocity of the four COP variables was significantly higher in the STS than BTS task by 2.6-fold on average. This was consistent for all dancers, as shown by the individual plots in Fig. 3C. COP-Velocity represents the average distance traveled by the COP per second, regardless of the directions, and a higher value is interpreted as greater postural sway^24,25. Postural stability is primarily biomechanically constrained by three conditions where: 1) the base of support is wide, 2) the line of gravity is in the center of the base of support, and 3) the center of gravity is low^28,29. Compared to BTS, STS is particularly disadvantaged in conditions 1 and 2, resulting in generally higher postural demands. The results of this study suggest that this is no exception for dancers accustomed to STS. In contrast, the other three COP variables did not significantly differ between tasks. This is apparently due to inconsistent responses/patterns among dancers during STS compared to BTS, and these inter-individual variabilities suggest that there are large individual differences in their postural control strategies during the tiptoe standing tasks. More specifically, some dancers were higher but others were lower during STS than BTS in COP-SD_AP (Fig. 3A), COP-SD_ML (Fig. 3B), and COP-Area (Fig. 3D), which are all influenced by the directions and degree of variability of the COP trajectory. Overall, these results suggest that COP-Velocity can serve as a representative variable for postural sway, and the other variables can supplement directional information, in studies adopting tiptoe standing in dancers.

PIFM activity level (% MVC) in the STS task was significantly higher than in the BTS task by 2.2-fold on average, and this was also consistent for all dancers (Fig. 4A). Since the body mass load on the foot is simply twice as heavy with the single-legged compared to bipedal support, it makes sense to assume that most of this increase in PIFM activity level is due to the increased foot loading. Furthermore, the correlation analysis showed that PIFM activity level was positively correlated with COP-Velocity (r = 0.666) only in the STS task, indicating that activity level was indeed associated with postural sway particularly during STS. A study examining PIFM activity level in non-dancers reported that it was 1.5 to 1.7-fold higher in STS compared to BTS¹³. However, the tasks in that study were not compared robustly because the participants (all participants during STS and half during BTS) lightly touched a wall or other objects during postural control, and the ankle joint PF angle was not specified¹³. Taken together, the results of this study suggest that PIFM activity, particularly during STS, is dependent on foot loading and postural demands, ensuring the methodological validity of the present study that matched the PF angle during both tasks.

Contrary to our expectations, EMG-CV_time did not significantly differ between tasks (p = 0.142), although STS on average had a 1.2-fold higher value with a borderline small/moderate effect size (d = 0.49) (Fig. 4B). Higher and lower values of EMG-CV_time reflect greater neuromuscular fluctuation and greater steadiness^22,23, respectively, and therefore we expected it to be higher for STS than BTS. However, it is worth mentioning that our previous study¹⁶ also found no significant differences in EMG-CV_time during BTS performed at 20°, 40°, and 60° in dancers, while PIFM activity level was significantly higher for 60° than 20°, which is in line with the EMG findings of this study (i.e. different activity level, similar steadiness). In other words, these results suggest that in dancers, although PIFM activity is higher during STS than BTS, its activity is similarly steady during both STS and BTS at their respective levels. This is likely due to adaptations to dancers’ daily training where they perform STS as steady as possible.

Also, EMG-CV_time showed a strong positive correlation with COP-SD_AP and COP-SD_ML only in the STS task (r = 0.846 and 0.738, Table 1). These suggest that PIFM activity is associated with postural sway in both directions during STS in dancers, and that these indices representing the variability of the EMG and directional COP data are sensitive to each other in the STS condition. A previous study has shown that PIFM activity during single-legged standing (with the heel on the floor) in non-dancers is synchronized with COP sway only in the mediolateral direction⁶. The reason for this discrepancy may be partly attributed to the participants being dancers vs non-dancers, but may also be explained by the combined motion of foot joints and the function of windlass mechanism due to the difference in the limb position. The foot joints have a flexibly shape-changing structure^5,30, and in single-legged standing, each joint responds in a coordinated manner to postural sway, primarily in the frontal plane (i.e., mediolateral direction). For example, eversion of the subtalar joint in the hindfoot causes the combined motion such as inversion of the Chopart's and Lisfranc's joint in the mid/forefoot (and vice versa), resulting in a lowering/collapse of the medial longitudinal arch^12,31,32. In tiptoe standing, on the other hand, the plantar fascia covering the calcaneus to the toes is tensed as the metatarsophalangeal joint is extended, resulting in the windlass mechanism that raises the medial longitudinal arch and increases joint stiffness of the foot; when this mechanism functions, the joints of the foot are unified, thus the aforementioned combined motion is reduced³³. The present findings support recent suggestions that PIFMs are more actively involved in the windlass mechanism than previously considered^10,34–36, and add that their less variable (i.e., steadier) activity is associated with less postural sway during STS in dancers.

This study had a relatively small sample size (n = 11), due to difficulty in recruiting professional/high-level dancers, potentially reducing statistical power. For example, our previous study¹⁶ with a larger sample size (n = 14) found that EMG-CV_time was found to be positively correlated with COP-Velocity in the BTS task, which was not the case in either task in this study. Furthermore, both tasks in this study were compared only at the ankle PF joint angle of 60°, and it is unknown whether the results are generalizable to other PF joint angles. Further investigations addressing these issues are needed in the light of both kinetics and kinematic mechanics to better understand postural control of dancers.

In summary, PIFM activity level and postural sway were higher during single-legged than bipedal tiptoe standing in dancers, likely due to increased foot loading and postural demands. The findings of the correlations between EMG and COP variables provide new evidence that PIFM activity is associated with postural sway during tiptoe standing in dancers, especially performed on a single leg.

Author Contribution

H.F. and S.M.: Investigation, Resources, Writing original drafts. Y.K. and T.I.: Formal analysis, Visualization, Formal analysis. Data curation.

Data Availability

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

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Plantar intrinsic foot muscle activity and its relationship with postural sway during single-legged and bipedal tiptoe standing in ballet dancers

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