Associations of Masticatory Muscles Asymmetry and Oral Health with Postural Control and Leg Injuries of Elite Junior Soccer Players

There is increasing recognition that postural control is a key to success in soccer and a protective factor against injuries (Hrysomallis, 2011). Postural control is regulated by a complex cybernetic system in which afferent information from the visual, vestibular and proprioceptive systems is transmitted to the central nervous system (CNS) that processes it and sends commands to the muscular system (Ivanenko and Gurfinkel, 2018). Paillard and Noe (2006) found dominance of proprioception in the postural strategy of elite soccer players, possibly because they gained the ability to perform technical maneuvers while visual attention was primarily directed at circumstances. As technical maneuvers like shooting are preferably performed with the dominant (kicking) limb, while the non-dominant (standing) limb provides stability, postural control while standing on the non-dominant leg is well developed in soccer players (Muehlbauer et al., 2019).

The functions of the postural system can be affected by several factors. Amongst others, attention has been placed on the influence of asymmetry between masticatory muscles as this asymmetry can be transmitted by muscle-facial chains to distal musculature and may influence information from the vestibular and oculomotor systems (Cuccia and Caradonna, 2009). Experimental studies have found close functional connections between masticatory, neck and trunk muscles (e.g. Giannakopoulos et al., 2013). Therefore, asymmetry between masticatory muscles may lead to asymmetrical control of the tonic muscles of the neck which may lead to asymmetrical whole-body postural control.

Another connection between the masticatory muscles and muscles activities responsible for postural control, is based on the anatomical connections between afferent neurons associated with masticatory muscles and the mesencephalic nucleus of the trigeminus (MNT). As the MNT has also a neuronal connection to the vestibular nuclei, the information from the masticatory muscles may affect the vestibular nuclei which play an essential role in maintaining postural control (Bieniek et al., 2019; Cuccia and Caradonna, 2009; Dolański et al., 2018; Gangloff and Perrin, 2002; Karimizadeh et al., 2020).

Because of these connections, a negative effect of asymmetry between masticatory muscles on postural control seems plausible, but the empirical evidence is conflicting (Julià-Sánchez et al., 2019). Possible explanations for the contradictory results include differences in the difficulty of postural tasks and in the efficiency of participants’ neurophysiological mechanisms. Our study investigated whether asymmetry between masticatory muscles of well-trained soccer players, who likely had developed effective neurophysiological mechanisms, would have a negative effect on the difficult task of single-leg standing with eyes closed on the, for single-leg standing better trained, non-dominant (standing) leg and on the less trained dominant (shooting) leg.

Gum disease and dental caries may have a negative effect on the frequency of sports injuries because both oral health problems are associated with elevated levels of cytokines, like tumour necrosis factor (TNF-a) and interleukin-6 (IL-6) (Gornowicz et al., 2012), which have an important role in the origin of muscle fatigue during exercise (Ament and Verkerke, 2009; Robson-Ansley et al., 2004). Fatigue is one of the important risk factor for soccer injuries because it deteriorates proprioception and decreases stabilizing muscle activation (Paillard, 2012). Deteriorated proprioception may trigger sports injuries, as, for example, an altered sense of the limb position may lead to the misplacement of the limb (Barrett et al., 2016). Empirical studies have found an association between poor oral health and the frequency of sports injuries of soccer players (Gay Escoda et al., 2011; Solleveld et al., 2015). In this study we tested the hypothesis that oral health problems are associated with higher prevalence of lower limb injuries during a competitive season.

Longitudinal data for this study were gathered by repeating the measurements after one year. The longitudinal data were used to investigate the temporal stability of the study variables across the year between the first (T1) and the second (T2) assessment and to replicate the cross-sectional analyses, using combined values of the first (T1) and the second (T2) assessment of the study variables because combined values are in general more reliable.

Table 1 summarizes the baseline characteristics, including the distribution of the oral health items, of all participants. Participants included in the longitudinal sample (n = 69) were about 11 months younger at T1 (p = 0.006) then the remaining participants (n = 75).

Pearson correlations between the independent variables at both T1 and T2 are presented in Table 2. It may be noted that correlations between TMJ problems and Oral Health problems were significant at T1 only, while correlations between TMJ problems and asymmetry between the masseter and temporalis muscles (measured as the ACP) were significant at T1 and at T2.

No significant differences between the T1 and T2 measures were found with the study variables, except for sway velocity on the non-dominant leg (eyes closed), that showed a significantly lower mean score at T2 (indicating improvement), and for TC (a sEMG indicator) that showed a significantly lower mean score at T2 (indicating a decline). Nevertheless, the temporal stability across one year of most study variables (except age) was poor. As shown in Table 3, fair to good temporal stability was found for Position (kappa = 0.85), Oral Health (kappa = 0.54), sway velocity on the non-dominant leg (ICC (3,1) = 0.51) and POCMM (ICC (3,1) = 0,43).

Pearson and partial correlations between independent variables and sway velocity on each leg at T1 are presented in Table 4. Sway velocity while standing on the non-dominant leg (eyes closed) was significantly associated with age (Pearson r = -0.25, p = 0.003; partial r = -0.28, p = 0.009) and the playing position (Pearson r = 0.26, p = 0.001; partial r = 0.26, p = 0.002). The negative correlation with age indicates better postural control while standing on the non-dominant leg with increasing age, while the positive correlation with the playing position indicates better postural control of field players compared with goalkeepers. Correlations with oral health, TMJ problems and sEMG indices were not significant.

Sway velocity while standing on the dominant (shooting) leg with eyes closed showed negative Pearson and partial correlation coefficients with the APC, one of the sEMG indices (Pearson r = -0.18, p = 0.03; partial r = -0.24, p = 0.004), indicating that soccer players with higher (better) levels of the APC had lower sway velocity (i.e., better postural control) while standing on the dominant leg with eyes closed. Significant Pearson and partial correlations were found with the playing position (Table 4), correlations with age and the remaining variables were not significant.

The results of analyses of the combined T1 & T2 data were in line with the results of the analyses using T1 data. As shown in Table 5, only age was significantly associated with the overall mean sway velocity while standing on the non-dominant leg with eyes closed (Pearson r = -0.43, p < 0.001; partial r = -0.44, p < 0.001) and only the overall mean APC was significantly associated with the overall mean sway velocity while standing on the dominant leg with eyes closed (Pearson r = -0.35, p = 0.003; partial r = -0.40, p = 0.005).

The number of leg injuries in the past competitive season was associated with oral health problems in T1 data and in the combined T1 and T2 data (Table 6). Using T1 data, we found that participants with two or more oral health problems had higher odds of two or more leg injuries than participants with at most one oral health problem (crude odds ratio 1.99, 95% confidence Interval (CI) 1.01–3.94, p = 0.05), even after adjusting for the effects of all other variables (adjusted odds ratio 2.14, 95% CI 1.02–4.46, p = 0.04). The associations of the other study variables with the number of leg injuries were in the expected direction, but non-significant.

Using the combined T1 & T2 data, we found a trend toward higher odds of two or more leg injuries in the year between T1 and T2 among participants with an overall mean of two or more oral health problems (crude odds 2.42, 95% CI - .87–6.75, p = 0.09), but significantly higher odds were found after adjusting for the effects of all other variables (adjusted odds 4.47, 95% CI 1.25– 15.96, p = 0.02). No associations with leg injuries were found for the other variables.

The current study examined the associations of imbalance in the masticatory muscles, oral health and TMJ problems with postural control and with frequency of leg-injuries of elite junior soccer players. In the analyses using T1 data and in the analyses using T1 & T2 data, we found that (1) higher sway velocity while standing on the dominant leg was associated with more asymmetry between the activities of the masseter and temporalis muscles (APC), but not with age, (2) higher sway velocity while standing on the non-dominant leg was associated with lower age, but not with the APC. Poor oral health was associated with a higher frequency of two or more leg injuries throughout a competitive season.

The finding that asymmetry between the masseter and temporalis muscles was differentially correlated with sway velocity of the dominant and the non-dominant leg, indicates that neurophysiological mechanisms that may reduce the influences of this asymmetry on postural control on the dominant leg, are not effective enough while the reverse is true for the non-dominant leg. This difference cannot be explained by differences in postural control between the legs, as nearly identical levels were found in this and previous research (e.g., Gstöttner et al., 2009). Instead, a difference in the efficiency of neurophysiological adaptations may be explained by differences in the volume of balance-training. Soccer players perform more balance training on the non-dominant leg because they use the non-dominant leg as a standing leg in passing, kicking, and landing (Muehlbauer et al., 2019). The finding that age was negatively associated with sway velocity on the non-dominant leg, but not associated with sway velocity on the dominant leg, most likely also reflects the effect of more balance training on the non-dominant leg.

Previous studies have found that balance training may lead to improvement in motor systems controlling muscular output and adaptations in visual, vestibular and proprioception systems that assist postural control (e.g., Fernández-Rio et al., 2019; Hrysomallis, 2011). Taube et al. (2008) found that balance training may lead to highly task-specific neural adaptations at different sites of the central nervous system. Thus, differences in balance training on the dominant and the non-dominant leg may lead to different neural adaptations for the legs.

The importance of balance training for the development of neural adaptations is supported by the results of a study by Maitre and Paillard (2016) on the influence of vestibular manipulation conditions (i.e., transmastoïdal GVS at 0.5 mA and 3 mA) on postural control of (1) a group of sport science students who have practiced sport at (sub) elite level, and (2) a group of individuals who have not practiced any sport activities for at least three years. The vestibular manipulation lowered postural control of the second group, but not of the first one. The authors note that the GVS signal triggers an inappropriate response because it is interpreted by the CNS as a real head rotation. In participants who practiced sports activities the CNS generates adaptive postural adjustments to withstand the erroneous signal. The practice of sport activities might have contributed to the development of adaptation and habituation mechanisms that reduce the effects of the erroneous signal. Also, sport activities may contribute to a better use of other available sensory information (i.e., proprioceptive and cutaneous sensory information).

We found that the APC, but not the other sEMG indices, showed an association with sway velocity on the dominant leg. Previous studies found that the APC was the only sEMG index associated with myogenous TMD (Mapelli et al., 2016). In this study we found associations with self-reported TMJ problems. As Nota et al. (2017) showed that myogenous TMD was associated with higher levels of postural sway, we may tentatively suggest that the association between the APC and sway velocity can also be partly explained by the presence of myogenous TMD.

The association between poor oral health and leg injuries in the cross-sectional and longitudinal analyses is consistent with the results of previous studies (Gay Escoda et al., 2011; Solleveld et al., 2015). Although only a moderate association was found, as elite athletes have a high risk of caries and periodontal disease due to stress and the use of an acidic diet, this finding underlines the importance of oral health in sports.

This study’s findings are subject to several limitations. First, self-report information is common in studies using large samples, but response bias (i.e., denial of vulnerability), recall error, and lack of insight, may have influenced the results. However, good agreement was shown between self-reported and professionally assessed oral health (Gilbert et al., 2003) and in a preliminary study we found good agreement between numbers of self-reported and registered leg injuries. Second, only static postural stability was examined. As the correlation between static and dynamic postural stability is low (Pau et al., 2015), using measures of dynamic postural stability may have resulted in different findings. Third, participants included in this study were elite junior male soccer players, thus, care is needed when generalizing the findings. Finally, the longitudinal analysis is limited by the sample size.

The current study, using cross-sectional and longitudinal data from elite junior male soccer players, found that asymmetry between the masseter and temporalis muscles was associated with higher sway velocity while standing on the dominant leg, but not with sway velocity while standing on the non-dominant (standing) leg. This finding provides evidence for both the association between imbalance in the masticatory muscles and postural control and the modulating influence of neurophysiological adaptations (induced by practice and training) on this association. This study also found that oral health problems were associated with higher numbers of leg injuries in elite junior male soccer players, even after controlling for age, the player’s position, four indices of masticatory asymmetry, self-reported TMJ problems and sway velocity of each leg. These results underline the need for oral health promotion and monitoring strategies in sports.