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RELATIONSHIP BETWEEN THE ELECTRICAL ACTIVITY OF SUPRAHYOID AND DURING AND CEPHALOMETRY

Relação da atividade elétrica dos músculos supra e infra-hióideos durante a deglutição e cefalometria

Maria Elaine Trevisan(1), Priscila Weber(2), Lilian G.K. Ries(3), Eliane C.R. Corrêa(4)

ABSTRACT

Purpose: to investigate the influence of the habitual head posture, jaw and position on the supra and infrahyoid muscles activity of the muscles during swallowing of different food textures. Method: an observational, cross-sectional study, with women between 19 and 35 years, without myofunctional swallowing disorders. The craniocervical posture, position of the and hyoid bone were evaluated by cephalometry. The electromyographic activity of the supra and infrahyoid muscles was collected during swallowing water, gelatin and cookie. Results: sample of 16 women, mean age 24.19 ± 2.66 years. At rest, there were negative/moderate correlations between the electrical activity of the with NSL/CVT (head position in relation to the cervical vertebrae) and NSL/OPT (head position in relation to the cervical spine) postural variables, and positive/moderate with the CVA angle (position of flexion/extension of the head). During swallowing the cookie, the activity of infrahyoid muscles showed a negative/moderate correlation with NSL/OPT angle. It was found higher electrical activity of the suprahyoid muscles during swallowing of all foods tested, and of the infrahyoid muscles at rest. There was difference on the muscle activity during swallowing of foods with different consistencies, which was higher with cookie compared to water and gelatin. Conclusion: the head hyperextension reflected in lower activity of the suprahyoid muscles at rest and of the infrahyoid muscles during swallowing. The consistency of food influenced the electrical activity of the suprahyoid and infrahyoid muscles, with greater muscle recruitment in swallowing solid food.

KEYWORDS: Posture; Deglutition; Electromyography; Cephalometry

„„ INTRODUCTION (1) Physical Therapist; Professor at Physical Therapy Depart- ment (Master Degree) and doctoral student at Graduate Program of Human Communication Disorders, Federal Uni- The deglutition process is a complex sensory- versity of Santa Maria – UFSM, RS, Brazil. motor mechanism that involves, in a sequence, (2) Physical Therapist; Graduate Program Human Commu- excitation and inhibition of different levels of the nication Disorders (Master Degree), Federal University of 1,2 Santa Maria – UFSM, RS, Brazil. Central Nervous System (CNS) . It is charac- (3) Physical Therapist; Professor at Physical Therapy Depart- terized by three phases: oral, pharyngeal and ment (PhD), University of the Santa Catarina State – esophagic; which demand coordinated movements UDESC , SC, Brazil. of mouth, tongue, and and they (4) Physical Therapist; Professor at Physical Therapy Depart- are independent of each other 1-3. Nevertheless, the ment (PhD) and Graduate Program of Human Communica- tion Disorders, Federal University of Santa Maria – UFSM, generation of the CNS patterns controls the time of RS, Brazil. these events and the peripherical manifestations of Conflict of interest: non-existent these phases that depend on peripherical sensory

Rev. CEFAC. 2013 Jul-Ago; 15(4):895-903 896 Trevisan ME, Weber P, Ries LGK, Corrêa ECR stimulus3. The oral phase of the deglutition is a affect the stomatognathic functions, in particular, voluntary event, while the pharyngeal is involuntary the deglutition. and independent1. However, the deglutition always Recent studies have investigated the supra and occurs in the same sequence, being the pharynx infra-hyoid muscle behavior in different body and and esophagus responses dependent on the food head positioning during the swallowing function7,13-15. bolus properties1-3 Differently, this study aimed to investigate the The complexity of the pharyngeal phase must influence of the usual head posture, mandibular and be pointed out once it requires the concomitance hyoid bone position on the supra and infra-hyoid of a series of events, including the antero-posterior muscles during the swallowing of three different displacement of the hyoid bone and the types of food. cartilage; epiglottis closing; vocal cord closing and superior esophagic sphincter opening. The hyoid „„ METHOD displacement to upward and forward occurs at the moment in which the bolus crosses the pharyngeal The present experiment was approved by the cavity and depends on the tongue basis and the Research Ethics Committee of the local institution, 4-6 supra-hyoid muscle contraction . under protocol CAAE number 0281.0.243.000-08. For an efficient swallowing function, the mandible The volunteers were included in the research after adopts a fix and stable position, by the intercuspal of signing the Consent Term. the occlusal surfaces, immediately before the tongue It consists of a cross-sectional observational 7 impulses the food bolus to the oropharynx . On the study, with quantitative data analysis. The partici- other hand, the mandibular stabilization allows the pants were evaluated by an experienced speech suprahyoid muscle contraction and, consequently, language pathologist in orofacial motricity, according the hyoid bone and larynx antero-superior traction to the Myofunctional Evaluation with Scores Protocol 7,8 assuring a safe deglutition . (AMIOFE)16, prior to participating in the study. There are evidences that the mandibular rest The inclusion criteria were: female gender, age position suffers alterations due to occlusal interfer- from 19 to 35 years old, without myofunctional ences, temporomandibular, stress, nasal obstruction alterations during the masticatory and swallowing and head posture9. Considering the established functions. relations between the craniocervical posture and The exclusion criteria were: facial trauma, craniofacial morphology, body posture changes, craniomandibular or cervical orthopedic surgical especially in the head, tend to modify the activity procedures, musculoskeletal deformities, temporo- of the muscles that take part in the positioning of mandibular disorder (TMD), Angle Class II and III 10 the mandibular rest . Suprahyoid muscles are occlusions, tooth loss, anterior and posterior open directly involved in the mandible stabilization during bite, cross bite, edge-to-edge bite and overbite, as intercuspal and food grinding, as well in the active well as being wearing braces. The TMD presence elevation of the hyoid bone and the larynx during was investigated by only one examiner according swallowing, having close association between the to the Research Criteria for Temporomandibular functions that involve the mandible posture and the Disorder (RDC/TMD)17. The occlusion was evaluated 11 supra and infra-hyoid muscle action . through intra-oral photographies observed by an Forward head posture is a commonly observed Orthodontist. postural change that leads to compensations such The craniocervical posture, mandible and as cranium and upper cervical spine hyperextension hyoid position were evaluated using cephalometric and lower cervical curvature flexion. It also produces analysis. The volunteers have undergone a right alterations in the mandible, hyoid and tongue lateral radiography of the cranium and cervical position, modifying the craniocervicomandibular spine in standing position, without any instruction biomechanical relations and, consequently, the for aligning it. In order to reproduce the natural head mandibular rest position. The mandible in a more position, they were oriented to keep staring at the retruded and elevated position pulls the supra-hyoid reflection of their eyes in a mirror placed at one-meter musculature12. distance18,19. The radiography was performed on the Harmony and balance between form and Orthophos Plus (Siemens, Germany) equipment, function are essential to determine the system with 1.52 m of focus-film distance. stomatognathic health condition. Therefore, under- The angle variables that assess the cranio- standing the relation between the craniocervical cervical posture were: CVT/EVT angle – cervical posture, mandible and hyoid bone position and the curve (figure 1); NSL/OPT and NSL/CVT – cranium supra and infra-hyoid muscle activity may elucidate inclination in relation to C2 and in relation to the the biomechanical changes that, occasionally, cervical spine (C2 –C4), respectively (Figure 2);

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CVA- flexion/extension head position and CPL/ The cephalograms were manually traced, by the Horizontal line – forward head posture (Figure same examiner, on acetate paper with the aid of a 3) 18,20-22. The mandibular and hyoid bone spatial mechanical pencil with 0.3mm tip, tape, soft rubber, position were determined, respectively, by NSL/ML with the radiographs placed on a negatoscope in (cranium basis inclination related to the mandible)18 order to allow a better visualization of the structures. and by the linear distance from the hyoid to mentum A protractor, for the angular measurements, and a (HY/ME), to mandible (HY/ ML) and to third cervical millimeter ruler for the linear measures were used. 4,22 vertebra (HY/C3) (Figure 4) .

CV2tg – the tangent point at the superior posterior extremity sp – anterior nasal spine; pm – posterior nasal spine; O – basi- of the odontoid process of the second cervical vertebra (C2); -occiput; CV2Ap – tangent point to the apex of the C2 dente; CV4ip – the most infero-posterior point on the body of the fourth CV2ia – the most infero-anterior point on the body of the second cervical vertebra; CV6ip – the most infero-posterior point on the cervical vertebra; Ce1 a Ce7 – central points of the vertebral sixth cervical vertebra. bodies from C1 to C7.

Figure 1 – Anatomical points utilized in the Figure 3 – Anatomical points utilized in the cephalometric analysis of the CVT/EVT angle cephalometric analysis of the CVA and CPL angles

N (nasion) – anterior point at fronto-nasal suture; S (Sella) – center of sella turcica CV2tg – the tangent point at the supe- N (nasion) – anterior point at fronto-nasal suture; S (Sella) – cen- rior posterior extremity of the odontoid process of the second ter of sella turcica; H – most anterosuperior point of the Hyoid cervical vertebra (C2); CV2ip – the most infero-posterior point bone; RGn (retrognathion) – the most inferior posterior point at on the body of the second cervical vertebra; CV4ip – the most the ; Me (Mentum) – most inferior point at infero-posterior point on the body of the fourth cervical vertebra. the mandibular symphysis.

Figure 2 – Anatomical points utilized in the Figure 4 – Anatomical points utilized in the cephalometric analysis of the NSL/OPT and cephalometric analysis of the NSL/ML angle and

NSL/CVT angles Hy/ML, Hy/Me and Hy/C3 linear measures

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The craniovertebral angle (CVA) gradually infrahyoid muscle signals were aligned and the t1 classifies the antero-posterior cranium position and t2 points were the same for both muscles. related to the cervical spine: CVA between 96-106 In order to determine the integral of the rectified corresponds to the head natural position, head electromyographic signal (S EMG), 20 Hz high-pass extension < 96, and head flexion > 10620. and 400Hz low-pass filters were used. The S EMG From the CPL angle, the individuals with during the swallowing test were demarcated the measure lower and higher than 80º, that is, between t1 and t2. These S EMG were corrected by presenting more or less forward head posture22. S EMG of base line, being calculated between 50 and For the electromyographic signal (EMG) acqui- 150 ms after the beginning of the data acquisition, sition of the supra and infra-hyoid muscular groups, according to the equation bellow: the individuals were instructed to comfortably seat in a chair, with eyes open and head oriented in the Frankfort Plan position. The signals were acquired at least three times for each of the tests in search of a better signal quality23. The room temperature was maintained at approx- S EMG is the integral of the EMG signal in the imately 25ºC and the possible noises that could time space determined for the water, gelatin and interfere in the EMG acquisition were controlled. cookie swallowing activities less 20 times 100 ms The Miotool 400 (Miotec, Porto Alegre, Brasil) was of the EMG base recorded between 50 and 150 used for the electromyographic evaluation, with ms after the beginning of the acquisition (figure 5). four channels, 14 bit resolution, 2000 Hz sample The S EMG during resting (S EMG) were demarcated frequency per channel, Butterworth filter and band between t1 and t2 comprehending medial time pass with 20-500Hz cutoff frequency. Electrodes spaces of 2000 ms (t1 + 2000ms= t2), according to Ag/AgCl double type (Hal Indústria e Comércio the equation bellow: Ltda) connected to pre-amplifiers active sensors were positioned in the supra and infra-hyoid area. A reference electrode unipolar (Meditrace 100) was placed on the aiming to reduce interference and/or noise during the EMG acquisition24. The EMG data acquisition was carried out during the swallowing of 20ml of water, 20 ml of gelatin The normalized S EMG (S EMG%) of each activity and half cookie (BONO®). The bolus size of the fine was expressed as the maximum value obtained liquids were based on a previous study25 and the from three repetitions of the cookie swallowing, for sequence water, gelatin and cookie was at random each muscle and subject. and maintained for all participants. Depending The participants were characterized by on the food texture/consistency, after chewing, if descriptive statistics (mean, standard-deviation) necessary, the volunteer was instructed to swallow and for each EMG variable, the aritmethic mean the entire volume offered in one single gulp, under of the three repetitions was considered. The data the evaluator verbal command. For each texture/ for normality and homocedasticity were tested by consistency, there were three attempts with Shapiro-Wilk and Levene tests, respectively. one-minute rest intervals between them, totaling The repeated measures variance analysis were nine swallows for each volunteer. carried out to test the effect of the fix factor muscles The signals were analyzed by the Matlab (supra and infrahyoid), the fix factor swallowing software (The MathWorks®, version 5.3). To detect (water, gelatin, cookie) and the interaction of these the onset of the swallowing activity (t1) 20 Hz factors in the quantitative dependent muscular high-pass and 50 Hz low-pass filters were used26. variable. t1 was determined as the point where the supra- In all analysis, Tukey’s HSD post hoc test was hyoid muscle signal amplitude became higher than used. To analyze the difference between the supra three standard-deviations (SD) that were observed and infrahyoid muscle activity at rest, the t test was in the mean amplitude (basal activity) before the used for paired data. swallowing activity of each subject. The end of The relationship between the cephalometric the swallowing activity (t2) was determined after and electromyographic variables was analyzed by 2000 ms from t1 (t1+2000ms = t2). The supra and Pearson´s correlation coefficient. The correlation

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The signal from t1 to t2 (t1+2000ms) was used for the integral EMG calculation.

Figure 5 – EMG signal of the suprahyoid (S-H) and infra-hyoid (I-H) muscles. was considered very low for r < 0.2; low for 0.2 < r NSL/OPT angles, as well as a moderate positive < 0.3; moderate for 0.4 < r < 0.69; high for 0.7 < r < correlation with CVA angle. There was a moderate 0.89 and very high for 0.9 < r < 127. The Statistical negative correlation between infrahyoid muscles Package for the Social Sciences (SPSS) version and NSL/OPT angle during cookie swallow. 17.0 for Windows (SPSS) statistics software was Figure 6 illustrates the results of the supra and used for the analysis and P values <0.05 (bi-tailed) infrahyoid muscle activity during water, gelatin and were considered statistically significant. cookie swallow. The repeated measure variance analysis „ „ RESULTS showed a significant difference between the supra and infrahyoid muscles (F=4.32, p=0.04) during The study group was composed of 16 women swallowing. Additionally, the suprahyoid muscles with 24.19±2.66 years old and CMI of 23.89±4.83 showed a higher activity during all food swallowing. kg/cm2. In contrast, the infrahyoid presented significant The angular cephalometric variables (mean and higher activity (44.28±19.42) than the suprahyoid standard-deviation) related to the head and cervical muscles (14.08±4.67) at rest ( p=0.00). Using spine position were: NSL/CVT (103±5.7°); NSL/OPT Tukey`s HSD test, it was observed differences in (100±6.9°); EVT/CVT (4.4±5.9°); CVA (96.9±7.5°) e CPL (78.2±3.6°). Regarding the spatial position of the cookie swallow compared to the water (p=0.00) and to the gelatin ( p=0.00) . As there was no inter- the hyoid bone, the variables were HY/C3 (43.6±4.3 mm), HY/ML (14.1±5.5) and HY/Me (55.8±7.1 action between the muscles and the swallowing mm). The mean of NSL/ML angle, related to the (F=1.01, p=0.37) it is possible to generalize the mandibular position was 30.9±6.8°. effect of the different food swallowing on both Table 1 shows the correlations between the evaluated muscles. craniocervical and electromigraphic variables. At Therefore, it can be inferred that the cookie rest, it was observed moderate negative correlations swallow demanded higher activity of both muscles between the suprahyoid activity and NSL/CVT and compared to the water and gelatin swallow.

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Table 1 – Correlation between craniocervical posture, mandible and hyoid position and the electromyographic activity of suprahyoid and infrahyoid muscles during resting and swallowing

Suprahyoid Infrahyoid water cookie gelatin Resting water cookie Gelatin Resting NSL/CVT -0.30 -0.03 -0.30 -0.59* 0.06 -0.50 -0.09 0.30 NSL/OPT -0.09 -0.04 -0.25 -0.55* 0.22 -0.55* 0.09 -0.31 EVT/CVT -0.15 0.23 0.38 0.17 -0.23 -0.01 -0.25 -0.11 CVA 0.20 -0.03 0.27 0.57* -0.16 0.34 0.22 -0.36 CPL 0.30 -0.04 0.00 0.46 0.11 0.37 0.35 -0.00 NSLML 0.09 -0.24 -0.34 0.08 -0.09 -0.38 -0.03 -0.07 HyC3 -0.42 -0.09 0.05 -0.40 -0.39 -0.27 -0.40 0.05 HyML -0.23 0.25 -0.40 -0.48 -0.37 -0.39 -0.38 0.03 HyMe -0.21 0.02 0.11 -0.30 0.46 -0.41 0.27 0.42 NSL/OPT; NSL/CVT (cranium inclination in relation to C2 and in relation to the cervical spine); CVT/EVT (cervical curve); CVA (flexion/ extension head position); CPL (forward head posture); NSL/ML (cranium basis inclination related to the mandible); HY/ME (linear dis- tance from the hyoid to mentum); HY/ML (linear distance from the hyoid to mandible) e HY/C3 (linear distance from the hyoid to third cervical vertebra). Results expressed in r (Pearson correlation coefficient),* p<0,05.

„„ DISCUSSION segment as result of the posterior rotation of the head. Due to the interaction between cervical and Considering the inverse relation that the angles craniomandibular systems, the hyperextension of have, biomechanically, between them, it can be the head produces a mandibular plane elevation, stated that: the more the NSL/CVT and NSL/OPT with consequent activation of the masseter muscle angles increase, the less the CVA reduces, charac- in order to keep mouth closed, what may reflect on terizing a posterior cranial tilt on the upper cervical the lower activation of suprahyoid muscles28. 20 spine . The modification of the mandibular positioning In this study, the correlation among the NSL/ interferes in the muscular fiber length, resulting CVT, NSL/OPT and CVA with the electromyographic in electromyographic activity changes in both the activity of the suprahyoid muscles at rest can be masseter and the suprahyoid muscles28. In this attributed to the postural changes in the mandibular condition, a higher activation of the masseter muscle

Figure 6 – Mean and standard-deviation of integral signal % between t1 e t2 (t1+2000ms) of the suprahyoid and infrahyoid muscles during the water, gelatin and cookie swallowing

Rev. CEFAC. 2013 Jul-Ago; 15(4):895-903 Hyoid muscles in swallowing and cefalometry 901 pulls the mandible upward, causing a passive The results of the present study also demon- tension of the suprahyoid muscles, decreasing their strated a significant higher electrical activity of the activation at rest. On the other hand, the infrahyoid suprahyoid muscles during the water, gelatin and muscle tension increases at rest in order to keep cookie swallowing. Such finding is explained by the the hyoid bone stability29. Considering that, the fact that the swallowing act is, essentially, exerted main muscles that displace the hyoid bone upward by the suprahyoid muscles, whose action promotes (milohyoid) and forward (geniohyoid) are originated the forward and upward dislocation of the hyoid in the mandible, its adopted position directly inter- bone7. feres on these muscles due to the length-tension It must be pointed out the importance of such relation5. dislocation of the hyoid bone, since when the The muscular synergism of the craniocervico- suprahyoid muscle action becomes reduced, it may have a smaller opening of the upper esophagic mandibular system has been previously demon- sphincter, penetration and/or aspiration of food, strated. Studies have shown the hyperextension besides the permanence of pharyngeal residues of the head as the most commonly postural alter- post swallowing31. ation that modifies the mandible and hyoid bone Finally, it was evidenced that the cookie positioning12,20,30. swallowing demanded higher muscular activity 22 In a recent study , based on the interpretation of the supra and infrahyoid muscles compared to of the correlation for NSL/OPT, NSL/CVT and water and gelatin. It is known that the viscosity CVA angles with the mandibular and hyoid bone has a considerable effect on the swallowing and, position, it was concluded that the hyperextension bolus with greater viscosity tends to have a lower of the cranium causes the mandible elevation. swallowing velocity due to the higher resistance to Consequently, there is an increase in the hyoid to the movement and therefore with a higher activity mentum distance, placing the suprahyoid muscle at of the muscles responsible for swallowing32. Ishida a disadvantage to exert its function. et al. 33 observed greater upward and forward However, it was not observed significant corre- hyoid excursion during the solid food swallowing lation between the craniocervical posture and the compared to liquid consistencies in young subjects, suprahyoid muscle activity during swallowing. Only confirming the need for higher muscular activity for one inverse and significant correlation was found the solid swallowing. between NSL/OPT angle and the infrahyoid muscle activity during cookie swallow. It is believed that this „„ CONCLUSION result may be due to the small number of subjects in this study, as well as their craniocervical posture, The head hyperextension position reflected on with values close to the normality for the CVA angle. the lower suprahyoid muscle activity at rest and on Based on the repercussion of the cranium hyperex- the infrahyoid muscles during swallowing. The supra- tension on the supra-hyoid action by the cranioman- hyoid muscles were more recruited in relation to the dibular interdependence, the correlation between infrahyoid muscles during this function. Different these structures during the muscular action may not food consistencies influenced the muscular activity, have been evidenced due to the normality condition with greater recruitment of both muscular groups of the craniocervical posture observed in the partici- evaluated during cookie swallowing, compared to pants in this study. water and gelatin.

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RESUMO

Objetivo: investigar a influência da postura habitual da cabeça, da posição mandibular e do osso hióide na atividade dos músculos supra e infra-hióideos durante deglutição de diferentes consistên- cias de alimentos. Método: estudo observacional, transversal, com mulheres entre 19 e 35 anos, sem alterações miofuncionais de deglutição. A postura craniocervical, posição da mandíbula e osso hióide foram avaliados pela cefalometria. A atividade eletromiográfica dos músculos supra e infra-hióideos foi coletada durante a deglutição de água, gelatina e biscoito. Resultados: amostra com 16 mulhe- res, média de idade 24,19±2,66 anos. No repouso, observaram-se correlações negativas/moderadas entre a atividade elétrica dos músculos supra-hióideos com as variáveis posturais NSL/CVT (posição da cabeça em relação às vértebras cervicais) e NSL/OPT (posição da cabeça em relação à coluna cervical) e positiva/moderada com o ângulo CVA (posição de flexão/extensão da cabeça). Durante a deglutição do biscoito, a atividade dos músculos infra-hióideos apresentou correlação negativa/mode- rada com o ângulo NSL/OPT. Constatou-se maior atividade elétrica dos músculos supra-hióideos durante a deglutição de todos os alimentos testados e, dos músculos infra-hióideos, no repouso. Os supra-hióideos foram mais ativos que os infra-hióideos durante a deglutição, entretanto, houve aumento da atividade eletromiográfica em ambos os grupos musculares durante a deglutição do bis- coito, comparado com a deglutição de água e gelatina. Conclusão: a hiperextensão da cabeça reper- cutiu na menor atividade dos músculos supra-hióideos no repouso e, dos músculos infra-hióideos, na deglutição. A consistência do alimento influenciou na atividade elétrica dos músculos supra e infra- -hióideos, havendo maior recrutamento muscular na deglutição de alimento sólido.

DESCRITORES: Postura; Deglutição; Eletromiografia; Cefalometria

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Received on: November 14, 2012 Accepted on: June 17, 2013

Mailing address: Maria Elaine Trevisan Universidade Federal de Santa Maria Avenida Roraima 1000 – Prédio 26, Sala 1308 – Cidade Universitária – Bairro Camobi Santa Maria – RS – Brasil CEP: 97105-900 E-mail: [email protected]

Rev. CEFAC. 2013 Jul-Ago; 15(4):895-903