Postural stability and the influence of concurrent muscle activation – Beneficial effects of jaw and fist clenching

Postural stability and the influence of concurrent muscle activation – Beneficial effects of jaw and fist clenching

G Model GAIPOS-4558; No. of Pages 3 Gait & Posture xxx (2015) xxx–xxx Contents lists available at ScienceDirect Gait & Posture journal homepage: ww...

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G Model

GAIPOS-4558; No. of Pages 3 Gait & Posture xxx (2015) xxx–xxx

Contents lists available at ScienceDirect

Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost

Short Communication

Postural stability and the influence of concurrent muscle activation – Beneficial effects of jaw and fist clenching Steffen Ringhof a,*, Timo Leibold a, Daniel Hellmann b, Thorsten Stein a a b

BioMotion Center, Institute of Sports and Sports Science, Karlsruhe Institute of Technology (KIT), Karlsruhe, Germany Department of Prosthodontics, Dental School, University of Heidelberg, Heidelberg, Germany

A R T I C L E I N F O

A B S T R A C T

Article history: Received 21 April 2015 Received in revised form 1 September 2015 Accepted 2 September 2015

Recent studies reported on the potential benefits of submaximum clenching of the jaw on human postural control in upright unperturbed stance. However, it remained unclear whether these effects might also be observed among active controls. The purpose of the present study, therefore, was to comparatively examine the influence of concurrent muscle activation in terms of submaximum clenching of the jaw and submaximum clenching of the fists on postural stability. Posturographic analyses were conducted with 17 healthy young adults on firm and foam surfaces while either clenching the jaw (JAW) or clenching the fists (FIST), whereas habitual standing served as the control condition (CON). Both submaximum tasks were performed at 25% maximum voluntary contraction, assessed, and visualized in real time by means of electromyography. Statistical analyses revealed that center of pressure (COP) displacements were significantly reduced during JAW and FIST, but with no differences between both concurrent clenching activities. Further, a significant increase in COP displacements was observed for the foam as compared to the firm condition. The results showed that concurrent muscle activation significantly improved postural stability compared with habitual standing, and thus emphasize the beneficial effects of jaw and fist clenching for static postural control. It is suggested that concurrent activities contribute to the facilitation of human motor excitability, finally increasing the neural drive to the distal muscles. Future studies should evaluate whether elderly or patients with compromised postural control might benefit from these physiological responses, e.g., in the form of a reduced risk of falling. ß 2015 Elsevier B.V. All rights reserved.

Keywords: Postural stability Balance Concurrent muscle activation Jaw clenching Fist clenching

1. Introduction Recently, submaximum clenching of the jaw was reported to significantly improve postural stability and to decrease the sway of cranial body segments in upright unperturbed stance [1–3]. The authors concluded that these improvements were induced by modulation of somatosensory input, particularly of the neck muscles [4], and facilitation of ankle extensor and flexor muscles [5,6], concomitant with attenuated reciprocal Ia inhibition [6]. Neuroanatomical connections and projections of the trigeminal nerve to structures associated with postural control [7–9] are thought to form the basis for these effects. One limitation of the abovementioned studies [1–3], however, is the lack of active controls, as used by Miyahara et al. [5]. The authors reported that soleus H reflex was not only increased by

* Corresponding author at: BioMotion Center, Institute of Sports and Sports Science, Karlsruhe Institute of Technology (KIT), Engler-Bunte-Ring 15, 76131 Karlsruhe, Germany. Tel.: +49 721 608 47485; fax: +49 721 608 44841. E-mail address: [email protected] (S. Ringhof).

voluntary clenching of the teeth, but also by isometric contraction of the wrist extensors or by clenching of the fists. Ringhof et al. [2], hence, suggested that sway reductions might also be observed among active controls. The purpose of this study, therefore, was to comparatively examine postural stability while submaximum clenching of the jaw and the fists. It was hypothesized that both concurrent muscular activities would significantly improve postural stability compared with habitual standing, but with no differences between jaw and fist clenching. Moreover, this study aimed to assess the effects of concurrent muscle activation under more complex conditions, specifically on foam surfaces, i.e., when the proprioceptive system is challenged. 2. Material and methods 2.1. Subjects A total of 17 healthy young adults participated in this study (Table 1). All subjects were naı¨ve to the experimental procedure

http://dx.doi.org/10.1016/j.gaitpost.2015.09.002 0966-6362/ß 2015 Elsevier B.V. All rights reserved.

Please cite this article in press as: Ringhof S, et al. Postural stability and the influence of concurrent muscle activation – Beneficial effects of jaw and fist clenching. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.09.002

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GAIPOS-4558; No. of Pages 3 S. Ringhof et al. / Gait & Posture xxx (2015) xxx–xxx

2 Table 1 Subject characteristics. Subjects [n]

Sex [m/f]

Age [years]

Height [m]

Mass [kg]

BMI [kg/m2]

17

8/9

22.4  1.0

1.70  0.04

67.7  5.3

23.1  0.9

BMI = body mass index.

and had no known muscular or neurological diseases. The test protocol was approved by the Institutional Review Board, and written informed consent was given by all subjects. 2.2. Measurements To specify the impact of force-controlled biting on postural stability, submaximum clenching of the jaw (JAW) was compared to submaximum clenching of the fists (FIST), both performed at muscular activities of 25% maximum voluntary contraction (MVC). To control for this, electromyographic (EMG) activity of the musculus masseter and the musculus flexor carpi radialis was recorded by use of bipolar surface electrodes (Ag/AgCl) and telemetric equipment (Noraxon, 1000 Hz). A visual feedback of the rectified, smoothed (100 points moving median), and MVC-scaled EMG data was presented to the participants in real time. JAW was performed using a fluid self-adjusting intra-oral splint (Aqualizer), enabling an auto-balanced static equilibrium of the craniomandibular system. Simultaneously, the subjects were instructed to keep their fists in a relaxed resting position and vice versa the mandible during FIST. For the assessment of postural stability, time series of the center of pressure (COP) were recorded by use of a force plate (AMTI, 1000 Hz). Data were acquired for 30 s on stable and unstable surfaces. In stable conditions, subjects stood directly on the firm surface of the force plate, whereas in unstable conditions a foam balance pad (Airex) covered the force plate. Irrespective of the support surface, the subjects stood barefoot, on both legs, with the medial sides of the feet touching each other. The subjects were instructed to maintain an upright position, with their arms hanging at their sides, and to remain as stable as possible, focusing the feedback screen. In habitual standing, which served as the control condition (CON), the subjects focused a circular area attached to the wall. Feedback screen and circular area were positioned at eye level 3.0 m in front of the subjects. The sequences of balance tasks and concurrent muscular activities were assigned randomly to the subjects. After familiarization, all subjects completed five trials per test condition.

2.3. Data analysis The raw COP data were processed with MATLAB R2014a. Initially, the COP time series were filtered by use of a fourth-order Butterworth low-pass filter (cutoff frequency 10 Hz). Postural stability was then quantified by the area of the 95% confidence ellipse of the COP (subsequently referred to as sway area), and COP path lengths in anteroposterior (ap) and mediolateral (ml) directions. 2.4. Statistics Statistical tests were performed by use of IBM SPSS Statistics 22.0. Kolmogorov–Smirnov and Mauchly’s tests were conducted to confirm the normality and sphericity of data distribution, respectively. Differences in postural stability between concurrent muscle activation [JAW, FIST, CON] and support surfaces [firm, foam] were investigated by two-way repeated measures ANOVA, adjusted by use of Bonferroni corrections for multiple comparisons. All data are presented as mean values  and  95% confidence intervals (Mean  CI95%). Partial eta squared h2p is indicated to give information about effect sizes [10,11]. The level of significance for all statistical tests was set a priori to p = 0.05.

3. Results Statistical tests revealed significant main effects of concurrent muscle activation [JAW, FIST, CON] for both COP sway area and path lengths in ap and ml directions (Fig. 1). Bonferroni adjustments indicated that each posturographic variable was significantly improved during JAW [sway area: p = 0.044; path length ap: p < 0.001; path length ml: p = 0.003] and FIST [sway area: p = 0.024; path length ap: p < 0.001; path length ml: p = 0.001] as compared to CON, but with no differences between JAW and FIST [sway area: p = 1.000; path length ap: p = 1.000; path length ml: p = 0.802]. Besides, significant main effects of support surfaces [firm, foam] were indicated; with larger sway area and

Fig. 1. COP sway area and COP path lengths in anteroposterior (ap) and mediolateral (ml) directions as functions of concurrent muscle activities (JAW = jaw clenching, FIST = fist clenching, CON = habitual control condition) and support surfaces (firm, foam).

Please cite this article in press as: Ringhof S, et al. Postural stability and the influence of concurrent muscle activation – Beneficial effects of jaw and fist clenching. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.09.002

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GAIPOS-4558; No. of Pages 3 S. Ringhof et al. / Gait & Posture xxx (2015) xxx–xxx

3

Table 2 P-values and effect sizes ðh2p Þ as revealed by two-way repeated measures ANOVA. Concurrent activation

h

p 2

Sway area [mm ] Path length ap [mm] Path length ml [mm]

Support surface

*

0.009 <0.001* <0.001*

2 p

0.32 0.66 0.52

Interaction

h

p *

<0.001 <0.001* <0.001*

2 p

0.85 0.95 0.91

p

h2p

0.076 <0.001* 0.109

0.16 0.45 0.14

ap = anteroposterior, ml = mediolateral. * Statistically significant; small effect: h2p ¼ 0:01; medium effect: h2p ¼ 0:06; large effect: h2p ¼ 0:14 [10,11].

increased path lengths under foam conditions. All p-values and effect sizes are listed in Table 2.

4. Discussion The results showed that concurrent muscle activation, as submaximum jaw and fist clenching, significantly improved postural stability in upright stance on firm and foam surfaces. By this means, the present follow-up study yields some additional findings, which should be highlighted below. First, in Ringhof et al. [2] COP displacements were reported to be less under submaximum biting as compared to a mandibular rest position, i.e., nonbiting. Hence, the question remained whether these effects were the result of submaximum biting, in terms of decreased postural sway, or the result of nonbiting, in terms of increased postural sway. The present study, however, showed that submaximum clenching of the jaw reduced COP displacement compared with a habitual control condition, and thus emphasizes the beneficial effects of jaw clenching. Second, this follow-up study demonstrated that postural stability is not only improved on firm surfaces, but that submaximum jaw clenching also reduced postural sway on foam surfaces, i.e., under more demanding conditions. This reinforces the stabilizing effect of jaw motor activity, and provides additional evidence for the functional coupling of the craniomandibular system and human posture. Finally, statistical analyses revealed that postural stability was not differently affected by submaximum clenching the jaw and submaximum clenching the fist, indicating that concurrent muscle activity of the m. masseter and the m. flexor carpi radialis similarly improved postural stability. It is suggested that these motor activities contribute to the facilitation of human motor system excitability [5,6,12], which increases the neural drive to the distal muscles [13,14] in a manner similar to the Jendrassik manoeuvre [15]. In conclusion, this study emphasizes the stabilizing effects of concurrent muscle activation in terms of submaximum jaw and fist clenching. These physiological responses to isometric activation of different muscle groups suggest that elderly or patients with

compromised postural control might benefit from these concurrent activities, e.g., in the form of a reduced risk of falling. Conflict of interest statement All authors disclose any financial and personal relationships with other people or organizations that could inappropriately have influenced this work. References [1] Hellmann D, Giannakopoulos NN, Blaser R, Eberhard L, Schindler HJ. The effect of various jaw motor tasks on body sway. J Oral Rehabil 2011;38(10):729–36. [2] Ringhof S, Stein T, Potthast W, Schindler H, Hellmann D. Force-controlled biting alters postural control in bipedal and unipedal stance. J Oral Rehabil 2015;42(3):173–84. [3] Hellmann D, Stein T, Potthast W, Rammelsberg P, Schindler HJ, Ringhof S. The effect of force-controlled biting on human posture control. Hum Movement Sci 2015;43:125–37. [4] Abrahams VC. The physiology of neck muscles; their role in head movement and maintenance of posture. Can J Physiol Pharmacol 1977;55(3):332–8. [5] Miyahara T, Hagiya N, Ohyama T, Nakamura Y. Modulation of human soleus H reflex in association with voluntary clenching of the teeth. J Neurophysiol 1996;76(3):2033–41. [6] Takada Y, Miyahara T, Tanaka T, Ohyama T, Nakamura Y. Modulation of H reflex of pretibial muscles and reciprocal Ia inhibition of soleus muscle during voluntary teeth clenching in humans. J Neurophysiol 2000;83(4):2063–70. [7] Buisseret-Delmas C, Compoint C, Delfini C, Buisseret P. Organisation of reciprocal connections between trigeminal and vestibular nuclei in the rat. J Comp Neurol 1999;409(1):153–68. [8] Devoize L, Dome´jean S, Melin C, Raboisson P, Artola A, Dallel R. Organization of projections from the spinal trigeminal subnucleus oralis to the spinal cord in the rat: a neuroanatomical substrate for reciprocal orofacial-cervical interactions. Brain Res 2010;1343:75–82. [9] Ruggiero DA, Ross CA, Reis DJ. Projections from the spinal trigeminal nucleus to the entire length of the spinal cord in the rat. Brain Res 1981;225(2):225–33. [10] Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed, Hillsdale, NJ: L. Erlbaum Associates; 1988. [11] Richardson JT. Eta squared and partial eta squared as measures of effect size in educational research. Educ Res Rev 2011;6(2):135–47. [12] Boroojerdi B, Battaglia F, Muellbacher W, Cohen LG. Voluntary teeth clenching facilitates human motor system excitability. Clin Neurophysiol 2000;111(6):988–93. [13] Ebben WP, Flanagan EP, Jensen RL. Jaw clenching results in concurrent activation potentiation during the countermovement jump. J Strength Cond Res 2008;22(6):1850–4. [14] Ebben WP. A brief review of concurrent activation potentiation: theoretical and practical constructs. J Strength Cond Res 2006;20(4):985–91. [15] Jendrassik E. Zur Untersuchung des Kniepha¨nomens. Neur Zbl 1885;4:412–5.

Please cite this article in press as: Ringhof S, et al. Postural stability and the influence of concurrent muscle activation – Beneficial effects of jaw and fist clenching. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.09.002