http://informahealthcare.com/smr ISSN: 0899-0220 (print), 1369-1651 (electronic) Somatosens Mot Res, Early Online: 1–5 ! 2014 Informa UK Ltd. DOI: 10.3109/08990220.2014.969837
ORIGINAL ARTICLE
Effect of chewing on postural stability during quiet standing in healthy young males Ahmad Alghadir1, Hamayun Zafar1,2, S. L. Whitney3, & Zaheen Iqbal1 Somatosens Mot Res Downloaded from informahealthcare.com by Technische Universiteit Eindhoven on 02/12/15 For personal use only.
1
Department of Rehabilitation Sciences, College of Applied Medical Sciences, King Saud University, Riyadh, Saudi Arabia, 2Department of Odontology, Umea University, Umea, Sweden, and 3Department of Physical Therapy and Otolaryngology, University of Pittsburgh, Pittsburgh, PA, USA Abstract
Keywords
Background and aims: There is an important role of the neck sensory motor system in control of body posture and balance, and it is reasonable to believe that the jaw sensory motor system can directly and indirectly influence the modulation of the postural control system. The purpose of this study was to evaluate possible effects of dynamic jaw position while chewing on the postural control system. Materials and methods: We compared the mean center of gravity (COG) velocity during quite standing on a foam surface with eyes closed during three test conditions: (i) with resting jaw position, (ii) with open jaw position, and (iii) while chewing standard bolus of chewing gum. One hundred and sixteen normal healthy male subjects (average age 31.56 ± 8.51 years; height 170.86 ± 7.26 cm) were recruited for the study. Their COG velocity (deg/s) was measured using the NeuroComÕ Balance Master Version 8.5.0 (Clackamas, OR, USA). Statistical analysis: Data was tested by the Friedman test. Results and conclusions. The results show that COG velocity decreased significantly while chewing in comparison to both open and resting jaw position (p50.0001). Our finding corroborates previous studies and suggests that the jaw sensory motor system can modulate postural control mechanisms. Gum chewing activity can enhance the postural stability during upright standing on an unstable surface and in the absence of visual input in healthy young adults. Our results should be taken into consideration in treatment and rehabilitation planning for patients with postural instability.
Balance, COG velocity, chewing, postural stability
Introduction The central nervous system identifies the head’s orientation in space relative to the body through proprioceptive feedback from the neck and the neck reflexes in association with the vestibular system, which aids in head positioning and stabilization in space and in relation to the body (Kogler et al. 2000). It has been shown that neck sensory information is important for postural control (Abrahams 1977). Provocation of the neck position following neck pain and subjective postural stability problems has also been shown to cause imbalance (Alund et al. 1993). Similarly, in cases of neck trauma like whiplash-associated disorders, patients can have symptoms of gait disturbances, dizziness, and balance impairments (Abrahams 1977; Kogler et al. 2000). These point to an important role of the neck sensory motor system, in the control of body posture and balance. A close functional linkage between jaw and neck regions has been reported previously on the basis of anatomical,
Correspondence: Z. Iqbal, Department of Rehabilitation Sciences, King Saud University, Riyadh, Saudi Arabia. E-mail: [email protected]
History Received 19 May 2014 Revised 14 September 2014 Accepted 19 September 2014 Published online 30 October 2014
biomechanical (Brodie 1950), neurological (Chang et al. 1988), and physiological clinical case studies (Abrahams et al. 1993; Ertekin et al. 1996). Co-activation of muscles of the jaw and neck–shoulder complex has been observed during mandibular movements and clenching (Davies 1979; Clark et al. 1993; Widmalm et al. 1988). Head movements during single and rhythmic jaw opening and closing are also reported (Eriksson et al. 2000; Zafar et al. 2000b). These studies show the existence of neural connections between the trigeminal and neck sensory and motor systems (Eriksson et al. 1998; Zafar et al. 2000a), and indicate that the neuromuscular control of the jaw is finely tuned (Zafar et al. 2000b) and invariant in nature (Zafar et al. 2002). It is suggested that integrated activation of jaw and neck muscles is controlled by a common central nervous network (Eriksson et al. 1998; Zafar et al. 2000b). Neck trauma is also shown to derange integrated jaw and neck behavior showing the functional coupling between the jaw and neck motor systems (Eriksson et al. 2004; Haggman-Henrikson and Eriksson 2004). It has also been shown that dental occlusion status contributes to the maintenance of standing postural balance (Hosoda et al. 2007; Milani et al. 2000). Chewing co-activates jaw and neck
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A. Alghadir et al.
muscles leading to coordinated jaw and head–neck movements (Eriksson et al. 2000). Additionally, it has been shown that chewing movements can physiologically improve the cerebral blood flow (Takada and Miyamoto 2004), and are reported to improve cognition, mood, and relieve stress by relieving anxiety (Scholey et al. 2009; Smith 2010). Previous animal studies have reported trigeminovestibular connections (Buisseret-Delmas et al. 1999; Cuccurazzu et al. 2007). A recent study has shown that the vestibular system in humans can also be modulated by the trigeminal system as indicated by induction or modulation of nystagmus by chewing in patients with both peripheral and central vestibulopathies (Park et al. 2014). Taken together, it is reasonable to believe that activation of the jaw sensory motor system can modulate the postural control system either via its connections to the neck sensory motor system or through its possible direct connections to the vestibular system. Thus, it can be hypothesized that activation of the jaw sensory motor system can affect the postural control of standing balance. Therefore, the purpose of this investigation was to study the possible relationship of jaw movements during chewing on standing postural stability in healthy adults. For this purpose, we studied the effect of chewing movements on the velocity of center of gravity (COG) during quite standing. The findings of this study can be helpful to understand postural control mechanisms and to develop clinical and rehabilitation routines for the management and treatment of patients with balance impairments.
Somatosens Mot Res, Early Online: 1–5
duration was measured by the system with eyes closed during three test conditions in random order: (i) with resting jaw position, that is, natural jaw position without any instructions, (ii) with open jaw position, that is, teeth of both jaws slightly apart, and (iii) while chewing three pieces of chewing gum on the preferred side at natural pace. Recording was started 10 s after the subject assumed the test condition. The same size of chewing gum pieces of a local brand were used for all tests and subjects. During the chewing test condition, the measurement of COG velocity was started after about 30 s of continuous chewing. The duration for each test run for all the three test conditions was 10 s. Each test condition was repeated 3 times for each subject, and a rest of about 30 s was allowed between the trials. The COG velocity (deg/s) of the natural sway while trying to stand as still as possible was sampled at a frequency of 100 Hz and the mean for the three trials was used for analyses. Data analysis Data was analyzed using Graph-Pad Instat 3.0 (GraphPad Software, San Diego, CA, USA). Means and SD were used for descriptive statistics. The hypothesis of no difference in COG velocity during the resting jaw position, open jaw position, and chewing test conditions was tested by the Friedman test. The null hypothesis was rejected at the 0.05 level of significance.
Results Materials and methods Subjects One hundred and sixteen healthy male subjects (average age 31.56, SD 8.51 years; height 170.86 cm, SD 7.26 cm) were recruited for the study. All subjects were informed about the aims and procedures of the study and written consent was obtained in accordance with the Declaration of Helsinki. All subjects had Angle Class I or II dentitions. Before the study, subjects were subjectively and objectively assessed for any signs or symptoms of balance, temporomandibular joint disorders, and skeletal anomalies, involving face, neck, and jaw especially, and were excluded if they had any neurological or vestibular impairment. The study fully complied with the ethical standards for human research of King Saud University.
COG velocity during three test conditions The mean COG velocity values during quiet standing on a relatively unstable surface varied between the three test conditions. The mean COG velocity values of 1.58 (SD 0.64), 1.37 (0.75), and 1.19 (0.55) were found for ‘‘resting jaw’’, ‘‘open jaw’’, and ‘‘chewing’’ test conditions, respectively. Comparison between COG velocities during three test conditions As shown in Figure 1, with reference to the mean COG velocity, there were significant differences between the ‘‘resting jaw’’ and ‘‘open jaw’’ test conditions (p50.0001); ‘‘resting jaw’’ and ‘‘chewing’’ test conditions (p50.0001); and ‘‘open jaw’’ and ‘‘chewing’’ test conditions (p50.0001).
COG velocity assessment
Discussion
The COG velocity was assessed using the NeuroComÕ Balance Master version 8.5.0 (Clackamas, OR, USA) which measures force using variable inductance compression load cells. It includes a 46 152 cm2 force platform interfaced to a computer (Chien and Hu 2007; Liston and Brouwer 1996; Newstead and Hinman 2005). The Balance Master was automatically calibrated before each testing session in the automatic mode. The subjects were asked to stand as still as possible on a soft relatively unstable surface (a foam block of 50 cm by 50 cm by 15 cm, provided by the manufacturer) with their feet comfortably together as marked on the force platform with normal angle of 4–7 deg of toe out, eyes closed, and arms by their sides. The COG velocity (deg/s) during test
In this study, the effect of dynamic jaw position (chewing) in comparison to static jaw positions (rest and open) on postural stability during quiet standing was investigated in healthy male adults. Results showed that the COG velocity of postural sway during quiet standing was significantly different during all three studied test conditions, with least mean COG velocity during the ‘‘chewing’’ test condition. For the stability of static posture, as in quiet standing, the neuromuscular system is governed by intricate postural control mechanisms and constantly works to maintain the projection of the body’s COG within the limits of the base of support, that is, the feet. The postural control system is complex and multifactorial and gets a number of
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DOI: 10.3109/08990220.2014.969837
Figure 1. Mean and 95% confidence intervals of COG velocity (deg/s) values of all subjects (n ¼ 116) for quiet standing on a relatively unstable surface with eyes closed during three test conditions. Note significant differences (p ¼ 0.0001) in COG values between the three test conditions and the least mean value for the chewing test condition.
contributions, including inputs from the proprioceptive system and from different vestibular and neck reflexes and the vestibulo-ocular system (Horak 2006). However, there is evidence that the jaw sensory motor system can influence the vestibular (Park et al. 2014), neck (Davies 1979; Ehrlich et al. 1999) as well as ocular systems and thus can also affect the postural control system (Hellmann et al. 2011). Our present results reflect this as there was significant change in COG velocity with changes in static or dynamic positions of the jaw, that is, with reference to the ‘‘resting jaw’’ position the COG velocity values decreased for ‘‘open jaw’’ and ‘‘chewing’’ test conditions, and also with reference to ‘‘open jaw’’ the values decreased for ‘‘chewing’’ test condition. These results indicate that different activation patterns of the jaw sensory motor system can modulate underlying postural control mechanisms. Our findings corroborate a recent study with 12 healthy adults, showing that the postural stability during quiet standing tends to enhance during chewing of gum (Kushiro and Goto 2011). However, in contrast to the test conditions of our study, the subjects were standing with open eyes and on a firm surface. The role of visual input (Redfern et al. 2001) and standing surface (Mohapatra et al. 2014) in postural balance during quiet standing is well documented. It has been shown that standing on a surface like foam, induces a significant challenge to the postural control system as it alters inputs to both joint receptors and cutaneous mechanoreceptors in the sole of the foot (Blackburn et al. 2003; Mohapatra et al. 2014). While standing on an unstable surface like foam, used in our study, feedforward control of posture is characterized by earlier and larger activation magnitude of anterior leg and trunk muscles when compared with standing on a firm surface (Mohapatra et al. 2014). It is interesting to note that despite deprivation of visual input and the more challenging situation of standing on a relatively unstable foam surface, the subjects of our study showed a decrease in COG velocity with changes in static as well as dynamic jaw
Effect of chewing on postural stability during quiet standing
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positions, indicating that the jaw sensory motor system is capable of modulation of the postural control system to stabilize their bodies. During standing corrective muscular action is required to counter the periodic destabilization in the form of postural sway. It has been reported that mastication facilitates H reflex in both the pretibial and soleus muscles (Takahashi et al. 2001) and that with jaw clenching, neck and trunk muscles co-contract with jaw muscles (Ehrlich et al. 1999). This shows the functional integration of the head–neck region into the neuromuscular system of the body (Hellmann et al. 2011) contributing in the feedback control mechanism to control the sway during such dynamic conditions (Peterka and Loughlin 2004). In comparison to the resting jaw position, there was reduction in COG velocity during chewing as well as with the open jaw position in healthy subjects which supports the body stiffening phenomenon, which is a part of the normal posture control mechanism caused by modification of the fusimotor drive and corresponding enhanced muscle tone (Hellmann et al. 2011). Chewing induces head extension due to co-contraction of sternocleidomastoid and trapezius muscles along with jaw muscles (Ehrlich et al. 1999; Eriksson et al. 2000; HaggmanHenrikson and Eriksson 2004; Shimazaki et al. 2006). This results in sway in the anteroposterior direction (Barin et al. 1992; Jackson and Epstein 1991; Kogler et al. 2000). The decrease in COG velocity may be a response to stabilize the posture and reduce the risk of fall (Hellmann et al. 2011). Therefore, chewing movements may indirectly enhance the postural stability by decreasing the COG velocity. Besides visual, vestibular, and proprioceptive components, postural stability is also affected by several neural inputs and cognitive tasks (Dault and Geurts 2001; Rankin and Woollacott 2000); and components like anxiety (Ishida et al. 2010). Mood of the patient is known to affect his or her postural control as anxiety decreases postural stability (Maki and McIlroy 1996; Wada et al. 2001). High stress has been recorded during anxiety. Chewing is known to lower this stress level (Stephens and Tunney 2004), improve mental condition including concentration (Kushiro and Goto 2011), enhance cognitive performance by reducing the reaction time in several cognitive tasks, and alleviate mood (Smith 2010; Wilkinson et al. 2002; Tahara et al. 2007). Hence, chewing of gum may indirectly influence and improve postural stability. It is important to point out that our results are from healthy subjects and our unpublished results of the effect of dental splint on stability of postural sway show that the jaw sensory motor system plays a very conspicuous role in instantaneous reduction in body sway in patients of whiplash-associated disorders than in healthy subjects. It can be postulated that the effect of chewing movements might be different in patients with postural instability. Nevertheless, our results could be taken into consideration in treatment and rehabilitation planning for patients with postural instability. Stress is inevitable in a situation where risk of falling is higher making patient anxious. In such a situation, chewing may come to their rescue by not only decreasing stress and reducing reaction time to an external stimulus but also increasing postural stability by decreasing their COG velocity as shown in our results.
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Conclusions Our findings corroborate previous studies and suggest that the jaw sensory motor system can modulate postural control mechanisms. Gum chewing activity can enhance postural stability during upright standing on an unstable surface and in the absence of visual input in healthy young male adults. Our results could be taken into consideration in treatment and rehabilitation planning for patients with postural instability.
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Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. The authors extend their appreciation to the College of Applied Medical Sciences Research Center and the Deanship of Scientific Research at King Saud University for funding this research.
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Eriksson PO, Zafar H, Nordh E. 1998. Concomitant mandibular and head–neck movements during jaw opening–closing in man. J Oral Rehabil 25:859–870. Ertekin C, Celebisoy N, Uludag B. 1996. Trigemino-cervical reflexes in normal subjects. J Neurol Sci 143:84–90. Haggman-Henrikson B, Eriksson PO. 2004. Head movements during chewing: Relation to size and texture of bolus. J Dent Res 83: 864–868. Hellmann D, Giannakopoulos NN, Blaser R, Eberhard L, Schindler HJ. 2011. The effect of various jaw motor tasks on body sway. J Oral Rehabil 38:729–736. Horak FB. 2006. Postural orientation and equilibrium: What do we need to know about neural control of balance to prevent falls? Age Ageing 35(Suppl. 2):ii7–ii11. Hosoda M, Masuda T, Isozaki K, Takayanagi K, Sakata K, Takakuda K, Nitta O, Morita S. 2007. Effect of occlusion status on the time required for initiation of recovery in response to external disturbances in the standing position. Clin Biomech (Bristol, Avon) 22:369–373. Ishida M, Saitoh J, Wada M, Nagai M. 2010. Effects of anticipatory anxiety and visual input on postural sway in an aversive situation. Neurosci Lett 474:1–4. Jackson RT, Epstein CM. 1991. Effect of head extension on equilibrium in normal subjects. Ann Otol Rhinol Laryngol 100:63–67. Kogler A, Lindfors J, Odkvist LM, Ledin T. 2000. Postural stability using different neck positions in normal subjects and patients with neck trauma. Acta Otolaryngol 120:151–155. Kushiro K, Goto F. 2011. Effect of masticating chewing gum on postural stability during upright standing. Neurosci Lett 487:196–198. Liston RA, Brouwer BJ. 1996. Reliability and validity of measures obtained from stroke patients using the Balance Master. Arch Phys Med Rehabil 77(5):425–430. Maki BE, McIlroy WE. 1996. Influence of arousal and attention on the control of postural sway. J Vestib Res 6:53–59. Milani RS, De Periere DD, Lapeyre L, Pourreyron L. 2000. Relationship between dental occlusion and posture. Cranio 18:127–134. Mohapatra S, Kukkar KK, Aruin AS. 2014. Support surface related changes in feedforward and feedback control of standing posture. J Electromyogr Kinesiol 24:144–152. Newstead AH, Hinman MR. 2005. Reliability of the Berg Balance Scale and balance master limits of stability tests for individuals with brain injury. J Neurol Phys Ther 29(1):18–23. Park SH, Kim HJ, Kim JS, Koo JW, Oh SW, Kim DU, Kim JT, Welgampola M, Deriu F. 2014. Mastication-induced vertigo and nystagmus. J Neurol 261:480–489. Peterka RJ, Loughlin PJ. 2004. Dynamic regulation of sensorimotor integration in human postural control. J Neurophysiol 91:410–423. Rankin JK, Woollacott MH. 2000. Cognitive influence on postural stability: A neuromuscular analysis in young and older adults. J Gerontol A Biol Sci Med Sci 55(3):M112–M119. Redfern MS, Yardley L, Bronstein AM. 2001. Visual influences on balance. J Anxiety Disord 15:81–94. Scholey A, Haskell C, Robertson B, Kennedy D, Milne A, Wetherell M. 2009. Chewing gum alleviates negative mood and reduces cortisol during acute laboratory psychological stress. Physiol Behav 97: 304–312. Shimazaki K, Matsubara N, Hisano M, Soma K. 2006. Functional relationships between the masseter and sternocleidomastoid muscle activities during gum chewing. Angle Orthod 76:452–458. Smith A. 2010. Effects of chewing gum on cognitive function, mood and physiology in stressed and non-stressed volunteers. Nutr Neurosci 13: 7–16. Stephens R, Tunney RJ. 2004. Role of glucose in chewing gum-related facilitation of cognitive function. Appetite 43:211–213. Tahara Y, Sakurai K, Ando T. 2007. Influence of chewing and clenching on salivary cortisol levels as an indicator of stress. J Prosthodont 16: 129–135. Takada T, Miyamoto T. 2004. A fronto-parietal network for chewing of gum: A study on human subjects with functional magnetic resonance imaging. Neurosci Lett 360:137–140. Takahashi T, Ueno T, Taniguchi H, Ohyama T, Nakamura Y. 2001. Modulation of H reflex of pretibial and soleus muscles during mastication in humans. Muscle Nerve 24:1142–1148. Wada M, Sunaga N, Nagai M. 2001. Anxiety affects the postural sway of the antero-posterior axis in college students. Neurosci Lett 302: 157–159.
DOI: 10.3109/08990220.2014.969837
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Widmalm SE, Lillie JH, Ash Jr MM. 1988. Anatomical and electromyographic studies of the digastric muscle. J Oral Rehabil 15:3–21. Wilkinson L, Scholey A, Wesnes K. 2002. Chewing gum selectively improves aspects of memory in healthy volunteers. Appetite 38: 235–236. Zafar H, Eriksson PO, Nordh E, Haggman-Henrikson B. 2000a. Wireless optoelectronic recordings of mandibular and associated head–neck
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movements in man: A methodological study. J Oral Rehabil 27: 227–238. Zafar H, Nordh E, Eriksson PO. 2000b. Temporal coordination between mandibular and head–neck movements during jaw opening–closing tasks in man. Arch Oral Biol 45:675–682. Zafar H, Nordh E, Eriksson PO. 2002. Spatiotemporal consistency of human mandibular and head–neck movement trajectories during jaw opening–closing tasks. Exp Brain Res 146:70–76.
ORIGINAL ARTICLE
Effect of chewing on postural stability during quiet standing in healthy young males Ahmad Alghadir1, Hamayun Zafar1,2, S. L. Whitney3, & Zaheen Iqbal1 Somatosens Mot Res Downloaded from informahealthcare.com by Technische Universiteit Eindhoven on 02/12/15 For personal use only.
1
Department of Rehabilitation Sciences, College of Applied Medical Sciences, King Saud University, Riyadh, Saudi Arabia, 2Department of Odontology, Umea University, Umea, Sweden, and 3Department of Physical Therapy and Otolaryngology, University of Pittsburgh, Pittsburgh, PA, USA Abstract
Keywords
Background and aims: There is an important role of the neck sensory motor system in control of body posture and balance, and it is reasonable to believe that the jaw sensory motor system can directly and indirectly influence the modulation of the postural control system. The purpose of this study was to evaluate possible effects of dynamic jaw position while chewing on the postural control system. Materials and methods: We compared the mean center of gravity (COG) velocity during quite standing on a foam surface with eyes closed during three test conditions: (i) with resting jaw position, (ii) with open jaw position, and (iii) while chewing standard bolus of chewing gum. One hundred and sixteen normal healthy male subjects (average age 31.56 ± 8.51 years; height 170.86 ± 7.26 cm) were recruited for the study. Their COG velocity (deg/s) was measured using the NeuroComÕ Balance Master Version 8.5.0 (Clackamas, OR, USA). Statistical analysis: Data was tested by the Friedman test. Results and conclusions. The results show that COG velocity decreased significantly while chewing in comparison to both open and resting jaw position (p50.0001). Our finding corroborates previous studies and suggests that the jaw sensory motor system can modulate postural control mechanisms. Gum chewing activity can enhance the postural stability during upright standing on an unstable surface and in the absence of visual input in healthy young adults. Our results should be taken into consideration in treatment and rehabilitation planning for patients with postural instability.
Balance, COG velocity, chewing, postural stability
Introduction The central nervous system identifies the head’s orientation in space relative to the body through proprioceptive feedback from the neck and the neck reflexes in association with the vestibular system, which aids in head positioning and stabilization in space and in relation to the body (Kogler et al. 2000). It has been shown that neck sensory information is important for postural control (Abrahams 1977). Provocation of the neck position following neck pain and subjective postural stability problems has also been shown to cause imbalance (Alund et al. 1993). Similarly, in cases of neck trauma like whiplash-associated disorders, patients can have symptoms of gait disturbances, dizziness, and balance impairments (Abrahams 1977; Kogler et al. 2000). These point to an important role of the neck sensory motor system, in the control of body posture and balance. A close functional linkage between jaw and neck regions has been reported previously on the basis of anatomical,
Correspondence: Z. Iqbal, Department of Rehabilitation Sciences, King Saud University, Riyadh, Saudi Arabia. E-mail: [email protected]
History Received 19 May 2014 Revised 14 September 2014 Accepted 19 September 2014 Published online 30 October 2014
biomechanical (Brodie 1950), neurological (Chang et al. 1988), and physiological clinical case studies (Abrahams et al. 1993; Ertekin et al. 1996). Co-activation of muscles of the jaw and neck–shoulder complex has been observed during mandibular movements and clenching (Davies 1979; Clark et al. 1993; Widmalm et al. 1988). Head movements during single and rhythmic jaw opening and closing are also reported (Eriksson et al. 2000; Zafar et al. 2000b). These studies show the existence of neural connections between the trigeminal and neck sensory and motor systems (Eriksson et al. 1998; Zafar et al. 2000a), and indicate that the neuromuscular control of the jaw is finely tuned (Zafar et al. 2000b) and invariant in nature (Zafar et al. 2002). It is suggested that integrated activation of jaw and neck muscles is controlled by a common central nervous network (Eriksson et al. 1998; Zafar et al. 2000b). Neck trauma is also shown to derange integrated jaw and neck behavior showing the functional coupling between the jaw and neck motor systems (Eriksson et al. 2004; Haggman-Henrikson and Eriksson 2004). It has also been shown that dental occlusion status contributes to the maintenance of standing postural balance (Hosoda et al. 2007; Milani et al. 2000). Chewing co-activates jaw and neck
Somatosens Mot Res Downloaded from informahealthcare.com by Technische Universiteit Eindhoven on 02/12/15 For personal use only.
2
A. Alghadir et al.
muscles leading to coordinated jaw and head–neck movements (Eriksson et al. 2000). Additionally, it has been shown that chewing movements can physiologically improve the cerebral blood flow (Takada and Miyamoto 2004), and are reported to improve cognition, mood, and relieve stress by relieving anxiety (Scholey et al. 2009; Smith 2010). Previous animal studies have reported trigeminovestibular connections (Buisseret-Delmas et al. 1999; Cuccurazzu et al. 2007). A recent study has shown that the vestibular system in humans can also be modulated by the trigeminal system as indicated by induction or modulation of nystagmus by chewing in patients with both peripheral and central vestibulopathies (Park et al. 2014). Taken together, it is reasonable to believe that activation of the jaw sensory motor system can modulate the postural control system either via its connections to the neck sensory motor system or through its possible direct connections to the vestibular system. Thus, it can be hypothesized that activation of the jaw sensory motor system can affect the postural control of standing balance. Therefore, the purpose of this investigation was to study the possible relationship of jaw movements during chewing on standing postural stability in healthy adults. For this purpose, we studied the effect of chewing movements on the velocity of center of gravity (COG) during quite standing. The findings of this study can be helpful to understand postural control mechanisms and to develop clinical and rehabilitation routines for the management and treatment of patients with balance impairments.
Somatosens Mot Res, Early Online: 1–5
duration was measured by the system with eyes closed during three test conditions in random order: (i) with resting jaw position, that is, natural jaw position without any instructions, (ii) with open jaw position, that is, teeth of both jaws slightly apart, and (iii) while chewing three pieces of chewing gum on the preferred side at natural pace. Recording was started 10 s after the subject assumed the test condition. The same size of chewing gum pieces of a local brand were used for all tests and subjects. During the chewing test condition, the measurement of COG velocity was started after about 30 s of continuous chewing. The duration for each test run for all the three test conditions was 10 s. Each test condition was repeated 3 times for each subject, and a rest of about 30 s was allowed between the trials. The COG velocity (deg/s) of the natural sway while trying to stand as still as possible was sampled at a frequency of 100 Hz and the mean for the three trials was used for analyses. Data analysis Data was analyzed using Graph-Pad Instat 3.0 (GraphPad Software, San Diego, CA, USA). Means and SD were used for descriptive statistics. The hypothesis of no difference in COG velocity during the resting jaw position, open jaw position, and chewing test conditions was tested by the Friedman test. The null hypothesis was rejected at the 0.05 level of significance.
Results Materials and methods Subjects One hundred and sixteen healthy male subjects (average age 31.56, SD 8.51 years; height 170.86 cm, SD 7.26 cm) were recruited for the study. All subjects were informed about the aims and procedures of the study and written consent was obtained in accordance with the Declaration of Helsinki. All subjects had Angle Class I or II dentitions. Before the study, subjects were subjectively and objectively assessed for any signs or symptoms of balance, temporomandibular joint disorders, and skeletal anomalies, involving face, neck, and jaw especially, and were excluded if they had any neurological or vestibular impairment. The study fully complied with the ethical standards for human research of King Saud University.
COG velocity during three test conditions The mean COG velocity values during quiet standing on a relatively unstable surface varied between the three test conditions. The mean COG velocity values of 1.58 (SD 0.64), 1.37 (0.75), and 1.19 (0.55) were found for ‘‘resting jaw’’, ‘‘open jaw’’, and ‘‘chewing’’ test conditions, respectively. Comparison between COG velocities during three test conditions As shown in Figure 1, with reference to the mean COG velocity, there were significant differences between the ‘‘resting jaw’’ and ‘‘open jaw’’ test conditions (p50.0001); ‘‘resting jaw’’ and ‘‘chewing’’ test conditions (p50.0001); and ‘‘open jaw’’ and ‘‘chewing’’ test conditions (p50.0001).
COG velocity assessment
Discussion
The COG velocity was assessed using the NeuroComÕ Balance Master version 8.5.0 (Clackamas, OR, USA) which measures force using variable inductance compression load cells. It includes a 46 152 cm2 force platform interfaced to a computer (Chien and Hu 2007; Liston and Brouwer 1996; Newstead and Hinman 2005). The Balance Master was automatically calibrated before each testing session in the automatic mode. The subjects were asked to stand as still as possible on a soft relatively unstable surface (a foam block of 50 cm by 50 cm by 15 cm, provided by the manufacturer) with their feet comfortably together as marked on the force platform with normal angle of 4–7 deg of toe out, eyes closed, and arms by their sides. The COG velocity (deg/s) during test
In this study, the effect of dynamic jaw position (chewing) in comparison to static jaw positions (rest and open) on postural stability during quiet standing was investigated in healthy male adults. Results showed that the COG velocity of postural sway during quiet standing was significantly different during all three studied test conditions, with least mean COG velocity during the ‘‘chewing’’ test condition. For the stability of static posture, as in quiet standing, the neuromuscular system is governed by intricate postural control mechanisms and constantly works to maintain the projection of the body’s COG within the limits of the base of support, that is, the feet. The postural control system is complex and multifactorial and gets a number of
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DOI: 10.3109/08990220.2014.969837
Figure 1. Mean and 95% confidence intervals of COG velocity (deg/s) values of all subjects (n ¼ 116) for quiet standing on a relatively unstable surface with eyes closed during three test conditions. Note significant differences (p ¼ 0.0001) in COG values between the three test conditions and the least mean value for the chewing test condition.
contributions, including inputs from the proprioceptive system and from different vestibular and neck reflexes and the vestibulo-ocular system (Horak 2006). However, there is evidence that the jaw sensory motor system can influence the vestibular (Park et al. 2014), neck (Davies 1979; Ehrlich et al. 1999) as well as ocular systems and thus can also affect the postural control system (Hellmann et al. 2011). Our present results reflect this as there was significant change in COG velocity with changes in static or dynamic positions of the jaw, that is, with reference to the ‘‘resting jaw’’ position the COG velocity values decreased for ‘‘open jaw’’ and ‘‘chewing’’ test conditions, and also with reference to ‘‘open jaw’’ the values decreased for ‘‘chewing’’ test condition. These results indicate that different activation patterns of the jaw sensory motor system can modulate underlying postural control mechanisms. Our findings corroborate a recent study with 12 healthy adults, showing that the postural stability during quiet standing tends to enhance during chewing of gum (Kushiro and Goto 2011). However, in contrast to the test conditions of our study, the subjects were standing with open eyes and on a firm surface. The role of visual input (Redfern et al. 2001) and standing surface (Mohapatra et al. 2014) in postural balance during quiet standing is well documented. It has been shown that standing on a surface like foam, induces a significant challenge to the postural control system as it alters inputs to both joint receptors and cutaneous mechanoreceptors in the sole of the foot (Blackburn et al. 2003; Mohapatra et al. 2014). While standing on an unstable surface like foam, used in our study, feedforward control of posture is characterized by earlier and larger activation magnitude of anterior leg and trunk muscles when compared with standing on a firm surface (Mohapatra et al. 2014). It is interesting to note that despite deprivation of visual input and the more challenging situation of standing on a relatively unstable foam surface, the subjects of our study showed a decrease in COG velocity with changes in static as well as dynamic jaw
Effect of chewing on postural stability during quiet standing
3
positions, indicating that the jaw sensory motor system is capable of modulation of the postural control system to stabilize their bodies. During standing corrective muscular action is required to counter the periodic destabilization in the form of postural sway. It has been reported that mastication facilitates H reflex in both the pretibial and soleus muscles (Takahashi et al. 2001) and that with jaw clenching, neck and trunk muscles co-contract with jaw muscles (Ehrlich et al. 1999). This shows the functional integration of the head–neck region into the neuromuscular system of the body (Hellmann et al. 2011) contributing in the feedback control mechanism to control the sway during such dynamic conditions (Peterka and Loughlin 2004). In comparison to the resting jaw position, there was reduction in COG velocity during chewing as well as with the open jaw position in healthy subjects which supports the body stiffening phenomenon, which is a part of the normal posture control mechanism caused by modification of the fusimotor drive and corresponding enhanced muscle tone (Hellmann et al. 2011). Chewing induces head extension due to co-contraction of sternocleidomastoid and trapezius muscles along with jaw muscles (Ehrlich et al. 1999; Eriksson et al. 2000; HaggmanHenrikson and Eriksson 2004; Shimazaki et al. 2006). This results in sway in the anteroposterior direction (Barin et al. 1992; Jackson and Epstein 1991; Kogler et al. 2000). The decrease in COG velocity may be a response to stabilize the posture and reduce the risk of fall (Hellmann et al. 2011). Therefore, chewing movements may indirectly enhance the postural stability by decreasing the COG velocity. Besides visual, vestibular, and proprioceptive components, postural stability is also affected by several neural inputs and cognitive tasks (Dault and Geurts 2001; Rankin and Woollacott 2000); and components like anxiety (Ishida et al. 2010). Mood of the patient is known to affect his or her postural control as anxiety decreases postural stability (Maki and McIlroy 1996; Wada et al. 2001). High stress has been recorded during anxiety. Chewing is known to lower this stress level (Stephens and Tunney 2004), improve mental condition including concentration (Kushiro and Goto 2011), enhance cognitive performance by reducing the reaction time in several cognitive tasks, and alleviate mood (Smith 2010; Wilkinson et al. 2002; Tahara et al. 2007). Hence, chewing of gum may indirectly influence and improve postural stability. It is important to point out that our results are from healthy subjects and our unpublished results of the effect of dental splint on stability of postural sway show that the jaw sensory motor system plays a very conspicuous role in instantaneous reduction in body sway in patients of whiplash-associated disorders than in healthy subjects. It can be postulated that the effect of chewing movements might be different in patients with postural instability. Nevertheless, our results could be taken into consideration in treatment and rehabilitation planning for patients with postural instability. Stress is inevitable in a situation where risk of falling is higher making patient anxious. In such a situation, chewing may come to their rescue by not only decreasing stress and reducing reaction time to an external stimulus but also increasing postural stability by decreasing their COG velocity as shown in our results.
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A. Alghadir et al.
Conclusions Our findings corroborate previous studies and suggest that the jaw sensory motor system can modulate postural control mechanisms. Gum chewing activity can enhance postural stability during upright standing on an unstable surface and in the absence of visual input in healthy young male adults. Our results could be taken into consideration in treatment and rehabilitation planning for patients with postural instability.
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Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. The authors extend their appreciation to the College of Applied Medical Sciences Research Center and the Deanship of Scientific Research at King Saud University for funding this research.
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