1 Correlation between bite force and electromyographic activity in dentate and partially edentulous individuals

Authors: Lner Botrel ROSA, M.S., School of Dentistry, University of So Paulo (USP) Ribeiro Preto Marisa SEMPRINI, D.D.S., Ph.D Professor, School of Dentistry, University of So Paulo (USP) Ribeiro Preto Selma SISSERE D.D.S., Ph.D Assistant Professor, School of Dentistry, University of So Paulo (USP) Ribeiro Preto Jaime Eduardo Cecilio HALLAK, D.D.S., Ph.D Assistant Professor, School of Medicine, University of So Paulo (USP) Ribeiro Preto Valria Oliveira PAGNANO, D.D.S., Assistant Professor, School of Dentistry, University of So Paulo (USP) Ribeiro Preto Simone Cecilio Hallak REGALO, D.D.S., Ph.D Assistant Professor, School of Dentistry, University of So Paulo (USP) Ribeiro Preto

Correspondence: Simone Cecilio Hallak Regalo schregalo@forp.usp.br Department of Morphology, Stomathology and Physiology, Faculty of Dentistry of Ribeiro Preto, University of So Paulo. Avenida do Caf s/n Tel.: 55 16 36024015 Ribeiro Preto, CEP 14096-030, So Paulo, Brazil. Fax: 55 16 36330999

2 Abstract Dental absence interferes in the physiological functioning of the masticatory system, promoting occlusal and functional alterations. The purpose of this study was to verify maximal bite force and maximal bite force correlated with electromyographic activity in 14 partially edentulous and 14 dentate individuals. Bite force in right and left molar and incisor regions were registered using a dynamometer with capacity of up to 1000N, adapted for oral conditions and at the same time electromyography was performed using Myosystem-Br1 with electrodes positioned on right and left masseter and temporalis muscles, and one reference electrode on the frontal bone. The highest value out of three recordings was considered the individuals maximal bite force. Statistical analysis of the bite force data was performed by means of t test and Pearsons bivariate correlation test was used for the analysis between bite and electromyographic activity using SPSS 12.0 software. Dentate individuals showed greater maximal bite force in the three regions. Correlations between electromyographic activity and bite force in the dentate group obtained positive coefficients for every muscle in the right molar region, for the left temporalis in the left molar region, and for every muscle in the incisive region. For the partially edentulous group, only the left temporalis muscle presented a positive correlation in the right molar region, there was positive correlation for the right masseter and right and left temporalis in the left molar region, and, in the incisive region, every muscle presented negative correlation. These data evidence the strong influence of dental loss over the maximal bite force and small correlation between bite force and electromyographic activity. Key words: bite force, electromyography, correlation, tooth loss, masticatory muscles

3 Introduction Dental loss leads to important changes in the masticatory system, which affects the bone, the buccal mucosa and the muscular function. The alveolar bone tends to reabsorb without the occurrence of new bone formation and the mucosa presents a decreased number of receptors, thus diminishing the number of afferent inputs (13). The contact between superior and inferior teeth in different functions is firstly monitored by the mecanoreceptors in the periodontal ligament. The stimulus of the afferent sensorial inputs sends information to synapses, resulting in afferent responses and triggering muscular activity. When a patient loses one or more teeth, there is loss of function, loss of the periodontal ligament and its receptors, and aesthetic impairment (5). Current research is concerned in determining the bite force in healthy human beings as well as in those with diverse alterations, aimed at assessing and understanding the functionality of the masticatory system (7,9,10). Bite force is intimately related to mastication and is determined by the jaw elevator muscles and regulated by the nervous, muscular, skeletal, and dental systems. Thus, the condition of these systems will directly influence the capacity to masticate and bite (18). The determination of maximal bite force levels has been used in dentistry with the aim of understanding biological factors such as the craniomandibular anatomy, neuromuscular mechanisms, masticatory efficiency, and muscular strength (11, 14).

4 The quantitative evaluation of the strength of jaw elevator muscles is a well-known clinical parameter. Significant correlations between bite force and facial morphology have been found and researchers agree that the former is influenced, among other factors, by ones dental condition (4). According to Gibbs et al. (6), in individuals with posterior dental loss, there is an increase in the load transmitted to the remaining teeth, reducing the bite force in order to diminish the stress on these teeth, consequently reducing the muscular strength as well. Maximal occlusal force can provide essential information to help establish appropriate diagnoses concerning the masticatory function (12). Electromyography has been used for analysis of the implications of functional disorders in the masticatory musculature, being both a research instrument employed as an evaluation procedure and a follow-up tool for treatment (16, 17). The assessment of the myoelectric activity in masticatory muscles is becoming increasingly useful for dentists, furthering the knowledge on these muscles performance, on the movements of regulatory reflexes, and on the changes in muscular patterns. Given the importance of the masticatory musculature on the several functions of the stomatognathic system, the proposal of this work was to investigate maximal bite force and its correlation with the electromyographic activity in partially edentulous individuals compared to dentate individuals, identifying to what extent dental loss may influence strength acquisition and electromyographic activity.

5 MATERIAL AND METHOD Participants Twenty-eight subjects of both genders took part in the study, enrolled in two groups. The first, comprising 14 partially edentulous individuals (minimal absence of 10 posterior teeth), recruited at the Removable Partial Prosthesis Clinic of the Ribeiro Preto College of Dentistry of the University of So Paulo, with mean age 35,0 5 years; and the second group consisting of 14 complete dentate individuals with mean age of 30,0 5, selected among the students, employees and faculty of the Ribeiro Preto College of Dentistry, all considered suitable according to the exclusion/inclusion criteria of the research. The volunteers were fully informed about the experiment and agreed to participate providing signed informed consent for Electromiography research according to resolution 196/96 of the National Health Council Brazil, approved by the Ethics Committee of the Ribeiro Preto College of Dentistry of the University of So Paulo, process number 2005.1.432.58.6.

Exclusion Criteria The selection of the sample and the inclusion/exclusion criteria were determined through anamnesis and clinical exams. The anamnesis interview provided information on personal data, medical records, dental history, presence of parafunctional habits, and possible symptoms of temporomandibular dysfunction. The items used as exclusion criteria were the presence of local or

6 systemic-originated disorders which may impair the craniofacial growth or the masticatory system, such as neurological disorders, cerebral palsy, among others; use of medications that can interfere, directly or indirectly, on muscular activity, such as antihistamines, sedatives, cough syrups, homeopathic remedies or other drugs with depressive action on the Central Nervous System; treatments that can interfere on muscular activity, directly or indirectly, during the period of the study, such as orthodontic treatments, phonoaudiological therapy, and otorhinolaryngologic treatment. Seventy-five partially edentulous individuals were evaluated, and 14 were selected. In order to be included in the sample, the subjects had to present absence of the first superior and inferior molars, where the bite force apparatus was placed. Among partially edentulous individuals in the Brazilian population these are the teeth with the highest rates of absence. None of the individuals in the sample were wearing removal partial dentures at the time for not considering that the absence of teeth could impair the function of the stomatognathic system. For the control group, 100 dentate young individuals were evaluated, 14 being randomly selected to compose the dentate control group.

Bite force and Electromyography The electromyographic signals and bite force measures were collected simultaneously, with the volunteers sitting on a comfortable chair (office-like), with the arms extended along the body and the hands lying on their thighs.

7 Bite force records were taken with a digital dynamometer, model IDDK (Kratos, Cotia, So Paulo, Brazil), with a 1000N capacity, adapted to the mouth (Figure 1). The apparatus has a set-zero key, which allows the exact control of the values obtained and also peak registers, that facilitates the record of the maximal force during measures. It has two arms with plastic disks on each end, over which the force to be measured is applied. Its high-precision charge cell and electronic circuit to indicate force, supply precise measures easily viewed on a digital display. The dynamometer was cleaned with alcohol and disposable latex finger cots (Wariper-SP) were positioned on the biting arms as a biosecurity measure. The participants were given detailed instructions and bite tests were performed before the actual recordings were made, in order to ensure the reliability of the procedure. The volunteers were then asked to bite the dynamometer three times with maximal force, with a two-minute rest interval between records. Evaluations were performed in the first molar (left and right) and central incisive regions. For partially edentulous individuals, the shape of the bite force apparatus enabled the adaptation to the missing teeth region. Maximal bite force was measured in N through the peak force record indicated on the screen for subsequent analysis. The highest value out of three records was considered as the individuals maximal bite force. Method error The method error of bite force measurements was performed in five subjects. Recordings were obtained in two different sessions with a 7-day interval. In each session, an average of three bites was considered for each

8 side, and used later to assess the results. Paired measurements were analyzed to identify systematic errors. No differences were found between first and second (one week later) series (2). Electromyography data Electromyography was performed using five channels of the MyosystemBr1 apparatus (DataHomins Ltda.). The electromyographic signals were analogically amplified with a gain of 1000x, filtered by a pass-band of 0.011.5KHz and sampled by a 12 bit A/D converter with a 2KHz sampling rate. The signals were digitally filtered by a pass-band filter of 10 to 500 Hz in the data processing. Surface differential active electrodes (two 10mm-long and 2mm-wide Silver-chloride bars, separated by a distance of 10mm, with input impedance of 10G and common-mode rejection ratio of 130dB at 60 Hz) were used in the study. The skin region where electrodes were placed was cleaned with alcohol and shaved when necessary. The differential active electrodes were positioned in the ventral region of both masseter and in the anterior portion of the left and right temporal muscles. The position of the electrodes was determined by palpation and they were fixated with adhesive bandage tape, with the longest extension of the bars perpendicular to the direction of the muscle fibers. A stainless still circular electrode (three centimeters of diameter) was also used as a reference electrode (ground electrode), fixated on the skin over the frontal bone region.

9 Data Analysis Statistical analyses were accomplished with the SPSS software, version 12.0 (Chicago, IL) and the data on bite force between dentate and edentulous individuals were analyzed using independent t-test. A 5% level of significance (p0.05) was adopted. The analysis of correlation between bite force and electromyographic activity was performed with the Pearson bivariate correlation test.

10 RESULTS

Bite Force In the analysis of maximal bite force between groups, dentate individuals presented greater bite force (p< 0.05) in the molar region. In respect to the incisive region, although dentate individuals presented greater force, the difference was small and non-significant (Table 1).

Correlation between maximal bite force and electromyographic activity The correlation analysis between bite force and electromyographic activity was performed independently in the two groups for the left and right molar and incisive regions. In the dentate group, a positive correlation was found for the Right Molar region, showing that the greater the bite force, the greater the electromyographic activity for the four muscles analyzed. In the partially edentulous individuals, negative correlations were found for the left and right masseter and right temporal muscles. The analysis shows that, in the dentate group, the correlation values for masseter muscles are higher than those for temporal muscles, while the opposite relation is observed in partially edentulous individuals (Table 2). In the dentate group, the correlation for the Left Molar region was only positive with the left masseter muscle and, for partially edentulous individuals, the correlation was positive for the right masseter and left and right temporal muscles. The correlation values were higher for the temporal muscle compared

11 to the masseter in dentate individuals, while the inverse pattern was observed in partially edentulous individuals (Table 3). The analysis shows positive correlations between the four muscles analyzed and the Incisive region in the dentate group, showing that the greater the bite force, the higher the electromyographic activity. On the other hand, negative correlations were found for the four muscles in the partially edentulous group, that is, the greater the bite force, the lower the electromyographic activity in these individuals. Correlation values for the masseter muscles are higher than those for the temporal muscles in the dentate group, the opposite being observed in the partially edentulous individuals (Table 4).

12 DISCUSSION The number of teeth in the oral cavity and the absence of dental contacts are important factors that influence the functioning of the masticatory system (21, 22), since most activities of this system rely on the stability of dental contacts between the maxilla and the jaw (3). The main objective of this research was to compare partially posterior edentulous individuals, with age ranging from 20 to 40 years, and dentate individuals, observing possible alterations caused by dental loss in terms of bite force and the correlation between bite force and electromyographic activity, evidencing the need for posterior buccal rehabilitation, not only due to the aesthetic value of the smile, but mostly in order to maintain the functional balance of the masticatory system. In the present study, the partially edentulous individuals were selected according to the criteria of presenting loss of at least 10 superior or inferior molar or premolar teeth, regardless of their location in the dental arch. The difficulty to standardize the dental loss in partially edentulous individuals caused the posterior dental absence to be diverse within the group, which may have influenced the results obtained in this work. In the maximal bite force evaluation, the individuals of both groups were properly instructed and collaborated with the experiment. The standardization of the methodology and the performance of three repetitions with two-minute intervals between each for the obtention of maximal bite force were accomplished so that errors and interferences were minimized.

13 A digital dynamometer with a capacity of up to 1000N, adapted to the mouth conditions, was used in this study. The device has two arms with plastic disks on each end, over which the force to be measured was applied. Its high precision charge cell and electronic circuit to indicate force, supply precise and easily readable measures on the digital display. The diameter of the arms, together, is of approximately 10mm, adequate for an oral aperture that does not interfere in the force employed, preventing muscular strain (or even suboptimal sarcomere length) and exaggerated displacement of the condyles (2, 1). Gibbs et al. (6), analyzing the effects of dental loss on masticatory force, observed that the greater the posterior dental absence, the lower the bite force and masticatory efficiency of individuals, a result that is similar to those observed in this work, where the analysis of maximal bite force between groups showed significantly greater bite force in the molar region in dentate individuals (p< 0.05). In the analysis of bite force in the incisive region, as dentate and partially edentulous individuals had all the anterior teeth, no significant differences were observed, and the values obtained for the incisive region in the dentate and partially edentulous individuals were, respectively: 110 N (10) e 90 N (10), which prove acceptable and show that the morphological alterations in the dental arches lead to functional alterations, which may result in changes in the masticatory pattern and muscular physiology. The values obtained in this study for the left and right molar regions in the dentate and partially edentulous groups were, respectively: 470 N (45), 110 N (27), 480 N (45), and 80 N (23), which highlights the huge difference between

14 the values obtained when individuals have a complete dentition evidenced in the present study by the statistically significant difference in bite force between the dentate and partially edentulous groups in the molar. The correlation between electromyographic activity and bite force was analyzed with the Pearson correlation test for the masseter and temporal muscles in the two groups, in the left and right molar and incisive regions. The values obtained were not statistically significant. In the present study, the correlations between electromyographic activity and bite force in the dentate group presented positive coefficients for all the muscles in the right molar region, for the left temporal muscle in the left molar region and for all the muscles in the incisive region. In the right molar region of the partially edentulous group, the left temporal muscle was the only to present a positive correlation. In the left molar region, the correlation was positive for the right masseter and right and left temporal muscles. In the incisive region all muscles presenting negative correlations. Positive correlations were found for most regions analyzed in the dentate group, which shows that the greater the bite force, the higher the electromyographic activity for the four muscles studied and, in the partially edentulous group, correlations were negative in most of the regions analyzed. These results suggest the existence of an asymmetry in the contribution of the muscular activity to the bite force in dentate and partially edentulous individuals. To Raadsheer et al. (15), the absence of positive correlations suggests that the analysis of a single comparison (force) may be little appropriate as a

15 parameter, other factors such as mastication and muscular thickness should be analyzed. The correlation between the magnitude of bite force and the number of teeth in contact has been determined in previous studies. The muscular force that results in greater bite force enhances the masticatory function and the occlusal stability, thus enabling a greater number of teeth to be in contact. Besides, the distribution of the muscular force over a broader occlusal area also distributes the pain and increases the positive feedback of periodontal receptors (8, 19). The dental absence interferes in the physiological functioning of the masticatory system, which leads to occlusal and functional changes. In face of such disharmony, a defense mechanism is activated in an attempt to determine a pattern of action which is less traumatic to the other components of the system. However, each individual presents, physiologically, a tolerance for dysfunctions, and depending on the intensity and frequency with which they are repeated, many can not stand the action of time and may develop severe dysfunctional problems. Tallents et al. (20), while studying the relation between the loss of posterior teeth and intra-articular disorders using magnetic resonance, observed that the results indicated a significant increase in the prevalence of symptoms in patients with posterior dental loss, and that the absence of these can accelerate the onset of degenerative articular diseases. The maintenance of a reasonable amount of natural and healthy teeth is the best way to ensure good masticatory efficiency as the patients age increases.

16 This leads us to reflect on the need for future studies to investigate the masticatory activity in partially edentulous individuals, taking into account the alterations found, which prove the presence of functional alterations in the masticatory system in partially edentulous individuals. We conclude from the above that dental loss leads to alterations in the stomatognathic system; maximal bite force is greater in dentate individuals and, in respect to the correlations between bite force and electromyography, it has been shown that, for dentate individuals, the greater the bite force, the higher the electromyographic activity, which was not true for partially edentulous individuals.

17 REFERENCES

1. Castelo, P.M., Gaviao, M.B., Pereira, L.J., Bonjardim, L.R.: Masticatory muscle thickness, bite force, and occlusal contacts in young children with unilateral posterior crossbite. Eur J Orthod 2007;29:149-56. Epub 2007 Feb 22 2. Fernandes, C.P., Glantz, P.O., Svensson, S.A., Bergmark, A.: A novel sensor for bite force determinations. Dent Mater 2003;19:118-26. 3. Ferrario, V.F., Serrao, G., Dellavia, C., Caruso, E., Sforza, C.: Relationship between the number of occlusal contacts and masticatory muscle activity in healthy young adults. J Cran Pract 2002;20:91-98. 4. Ferrario, V.F., Tartaglia, G.M., Maglione, M., Simion, M., Sforza, C.: Neuromuscular coordination of masticatory muscles in subjects with two types of implant-supported prostheses. Clin Oral Impl Res 2004;15:219225. 5. Gartner, J.L., Mushimoto, K., Weber, H.P., Nishimura, I.: Effect of osseointegrated implants on the coordination of masticatory muscles: A pilot study. J Prosthet Dent 2000;84:185-193. 6. Gibbs, C.H., Anusavice, K.J., Young, H.M., Jones, J.S.: Esquivel-Upshaw, J.F. Maximum clenching force of patients with moderate loss of posterior tooth support: a pilot study. J Prosthet Dent 2002;88:498-502. 7. Helkimo, E., Carlsson, G.E., Carmeli, Y.: Bite force in patients with functional disturbance of the masticatory system. J Oral Rehabil 1975;2:397-406.

18 8. Ingervall, B., Minder, C.: Correlation between maximum bite force and facial morphology in children. Angle Orthod 1997;67:415-22. 9. Kiliaridis, S.: Effects of fatigue and chewing training on maximal bite force end endurance. Am J Orthod Dentofac Orthop 1995;107:372-8. 10. Kogawa, E.M., Calderon, P.S., Lauris, J.R.P., Araujo, C.R.P., Conti, P.C.R.: Evaluation of maximal bite force in temporomandibular disorders patients. J Oral Rehabil 2006;33:559565. 11. Linderholm, H., Wennstrm, A.: Isometric bite force and its relation to general muscle force and body build. Acta Odontol Scand 1970;28:67889. 12. Okiyama, S., Ikebe, K., Nokubi, T.: Association between masticatory performance and maximal occlusal force in young men. J Oral Rehabil 2003;30:278-82. 13. Piancino, M.G., Farina, D., Talpone, F., Castroflorio, T., Gassino, G., Margarino, V., Bracco, P.: Surface EMG of jaw-elevator muscles and chewing pattern incomplete denture wearers. J Oral Rehabil 2005;32:863 870. 14. Proffit, W.R., Fields, H.W., Nixon, W.L.: Occlusal forces in normal and long face adults. J Dent Res 1983;62:566-571. 15. Raadsheer, M.C., Van Eijden, T.M., Van Ginkel, F.C., Prahl-Andersen, B.: Contribution of jaw muscle size nd craniofacial morphology to human bite force magnitude. J Dent Res 1999;78:31-42

19 16. Regalo, S.C.H., Vitti, M., Hallak, J.E.C., Semprini, M., Mattos, M.G., Tosello, D.O., Constancio, R.F., Pegoraro, M.E., Lopes, R.A.: EMG analysis of the upper and lower fascicles of the orbicularis oris muscle in deaf individuals. Electromyogr Clin Neurophysiol 2003;43:367-72. 17. Santos, C.M.: Efeitos do uso de overdenture sobre implantes e de prteses totais na atividade eletromiogrfica da musculatura da mastigao. Dissertao de Mestrado, Ribeiro Preto: Faculdade de Odontologia de Ribeiro Preto, Universidade de So Paulo; 2005. 18. Shiau, Y.Y., Wang, J.S.: The effects of dental condition on hand strength and maximum bite force. J Cran Pract 1993;11:49-54. 19. Sonnesen, L., Bakke, M., Solow, B.: Bite force in pre-orthodontic children with unilateral crossbite. Eur J Orthod 2001;23:741-9. 20. Tallents, R.H., Macher, D.J., Kyrkanides, S., Katzberg, R.W., Moss, M.E.: Prevalence of missing posterior teeth and intra-articular temporomandibular disorders. J Prosthet Dent 2002;87:45-50. 21. van der BILT, A.: Human oral function: a review. Braz J Oral Sci 2002;1:718 22. Wilding, R.J.C.: The association between chewing efficiency and occlusal contact area in man. Arch Oral Biol 1993;38:589-96.

20 Tables

Table 1: Maximal Bite Force (N) and standard-error in the molar and incisive teeth regions in each experimental group.

Sample Force Region Group (n) (N)

Standard Sig. error

Right Molar Left Molar Incisives

Partially edentulous Dentate Partially edentulous Dentate Partially edentulous Dentate

14 14 14 14 14 14

110 470 80 480 90 110

27 45 23 45 11 11

0.0005** 0.0005** 0.224

* *indicates statistical significance for p< 0,05

Table 2: Correlation coefficients (r) between electromyographic activity and maximal bite force in the Right Molar region for the dentate and partially edentulous groups.

21

Muscle

r - dentate

Sig. dentate 0.274 0.063 0.317 0.950

r partially edentulous -0.078 -0.038 -0.203 0.173

Sig. Partially edentulous 0.791 0.896 0.487 0.553

Right Masseter Left Masseter Right Temporal Left Temporal

0.314 0.509 0.289 0.019

Table 3: Correlation coefficients (r) between electromyographic activity and maximal bite force in the Left Molar region for the dentate and partially edentulous groups.

Muscle

r - dentate

Sig. dentate 0.803 0.804

r partially edentulous 0.039 -0.202

Sig. Partially edentulous 0.894 0.489

Right Masseter Left Masseter

-0.073 0.073

22 Right Temporal Left Temporal -0.186 -0.081 0.524 0.782 0.114 0.039 0.699 0.894

Table 4: Correlation coefficients (r) between electromyographic activity and maximal bite force in the Incisive region for the dentate and partially edentulous groups.

Muscle

r - dentate

Sig. dentate 0.297 0.164 0.099 0.727

r partially edentulous -0.045 -0.134 -0.126 -0.221

Sig. Partially edentulous 0.879 0.649 0.667 0.448

Right Masseter Left Masseter Right Temporal Left temporal

0.300 0.393 0.458 0.103