- Email: [email protected]
Age and gender influence on maximal bite force and masticatory muscles thickness
archives of oral biology 55 (2010) 797–802
available at www.sciencedirect.com
journal homepage: http://www.elsevier.com/locate/aob
Age and gender influence on maximal bite force and masticatory muscles thickness Marcelo Palinkas a, Mariangela Salles Pereira Nassar a, Fla´via Argentato Cecı´lio a, Selma Sie´ssere a,c, Marisa Semprini a,c, Joa˜o Paulo Machado-de-Sousa b,c, Jaime Eduardo Cecilio Hallak b,c, Simone Cecı´lio Hallak Regalo a,c,* a
Department of Morphology, Stomatology, and Physiology of the Ribeira˜o Preto Dental School (RPDS), University of Sa˜o Paulo, Ribeira˜o Preto, Sa˜o Paulo, Brazil b Department of Neurosciences and Behavior of the Ribeira˜o Preto Medical School (RPMS), University of Sa˜o Paulo, Ribeira˜o Preto, Sa˜o Paulo, Brazil c National Science and Technology Institute (INCT) for Translational Medicine, CNPq, Brazil
article info
abstract
Article history:
The present study aimed investigate the age and gender influence on maximal molar bite force
Accepted 29 June 2010
and at outlining the criteria for normal masticatory muscle development in a sample of 177 Brazilian Caucasian dentate individuals aged 7–80 years divided into five age groups: I (7–12
Keywords:
years), II (13–20 years), III (21–40 years), IV (41–60 years), and V (61–80 years). Except for Group V,
Ultrasound
which comprised nine women and eight men, all groups were equally divided in respect to
Human masseter
gender (20 M/20 F). Bite force was recorded with a mouth-adapted 1000 N dynamometer and the
Human temporal
highest out of three records was regarded as the maximal bite force. The data were submitted to
Muscle thickness
multivariate statistical analysis (SPSS 17.0 p < 0.05). Effects of group and gender were found,
Aging
but no interactions between them. The ANOVA showed significant differences between groups bilaterally. Bonferroni’s test showed that group I had significantly lower bite force means at both sides as compared to all groups, except group V. No differences were found between the left and right sides. In all the groups, gender was found to be a significant factor associated with maximal bite force. A global comparison including all the subjects and measures showed that the means of men were approximately 30% higher than those of women. Within-group comparisons yielded similar results in all groups. Muscle thickness was measured with a SonoSite Titan ultrasound tool using a high-resolution real-time 56 mm/10 MHz linear-array transducer. Three ultrasound images were obtained from the bilateral masseter and temporal muscles at rest and at maximal voluntary contraction. The means of the three measures in each clinical condition were analyzed with multivariate statistical analysis (SPSS 17.0 p < 0.05). A gradual increase in thickness of the masseter and temporal muscles was found both at rest and maximal voluntary contraction for groups I to IV, whereas a decrease in muscle thickness was observed in group V. Multivariate analysis showed that in both conditions there was an effect of group and gender. The study of the development of the stomatognathic system in relation to age and gender can provide useful data for the identification of normal and impaired functioning patterns. The results of this study indicate that age and gender are associated with structural and functional alterations in the muscles of the stomatognathic system. # 2010 Elsevier Ltd. All rights reserved.
* Corresponding author at: Avenida do Cafe´, s/n, Bairro, Monte Alegre, 14040-904 Ribeira˜o Preto, SP, Brazil. Tel.: +55 16 36024025; fax: +55 16 36330999. E-mail address: [email protected] (S.C.H. Regalo). 0003–9969/$ – see front matter # 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.archoralbio.2010.06.016
798
1.
archives of oral biology 55 (2010) 797–802
Introduction
Table 1 – Description of the groups. Group
The stomatognathic system is a physiological and functional entity comprising a set of organs and tissues whose biology and physiopathology are fully dependent on each other. The anatomical and functional development of stomatognathic system, and consequently the masticatory function, is dependent upon two important factors: muscle and craniofacial development.1 The knowledge concerning the thickness of masticatory muscles, allied to findings on facial morphology, occlusal factors, and bite force are vital for understanding the complex functioning of the stomatognathic system.2–4 Ultrasound is a tool that enables researchers to analyze the thickness of the skeletal musculature.5–8 Current research has been concerned with determining the bite force in human subjects, seeking to assess and understand the functionality of masticatory system, craniomandibular anatomy, neuromuscular mechanisms, masticatory efficiency, and muscle force.9,10 Bite force is directly related to mastication and is determined by the size of the jaw lifting muscles (especially in their transversal section1) and their interaction with the nervous, muscular, skeletal, and dental systems. The condition of these systems directly interferes with one’s capacity to chew and bite.11 Given the importance of the musculature in the craniofacial development, this study is aimed searching evidence concerning the muscular interaction with craniofacial development over time. The thickness of the masseter and temporal muscles, as well as the maximal bite force in Brazilian Caucasian children, adolescents, adults, and elderly were analyzed in order to provide the basis for the definition of normality criteria and parameters for muscular masticatory development in relation to age and gender. The results of this study will enable the full morphological and functional assessment of the stomatognathic system, facilitating diagnosis and prognosis and at defining normality standards for population.
2.
Methods
2.1.
Sample
Two hundred and fifty individuals were evaluated and 177 were included in the final sample according to the inclusion and exclusion criteria for participation. All volunteers were Brazilian, fully dentate (except for Group I – mixed dentition, caucasian, aged 7–80 years, and divided into five groups: I (7–12 years), II (13–20 years), III (21–40 years), IV (41–60 years), and V (61–80 years)). Except for Group V, which comprised nine women and eight men, all groups were equally divided in respect to gender (20 M/20 F) (Table 1). All subjects were nasal breathers, had normal occlusion, no parafunctional habits and had to be free of signs and symptoms of any dysfunction of the masticatory system. The study was approved by the Local Ethics Committee at the Ribeira˜o Preto School of Dentistry of the University of Sa˜o Paulo (Process no. 2006 1971.58.5). All subjects were informed about the purpose and potential risks of the study and signed
I II III IV V
Age
Men
07–12 13–20 21–40 41–60 61–80
20 20 20 20 8
Women 20 20 20 20 9
an informed consent term, as required by resolution 196/96 issued by the National Health Council. Those responsible for minor participants signed the informed consent for them. The sample was selected by means of anamneses and clinical exams guided by the inclusion/exclusion criteria. The anamneses provided data regarding the participants’ personal information, medical and dental history, any existing parafunctional habits, and possible temporomandibular dysfunction symptoms (RDC/TMD). All subjects were fully dentate and had no periodontal problems. The following items were used as exclusion criteria during the anamnesis interview:
presence of systemic or local disorders that could impair the craniofacial growth or the masticatory system, such as neurological disorders and cerebral palsy; use of any medication that could interfere in muscle activity, such as antihistamines, sedatives, homeopathic remedies or central nervous system depressors; treatments that could directly or indirectly interfere in muscle activity during the period in which the study was performed, such as speech therapy and otorhinolaryngological treatments.
2.2.
Bite force
Bite force measures were collected with the volunteers sitting on a comfortable chair (office-like), with the arms extended along the body and the hands lying on their thighs. The records were taken with a digital dynamometer, model IDDK (Kratos, Cotia, Sa˜o Paulo, Brazil), with a 1000 N capacity, adapted to the mouth. The apparatus has a ‘‘set-zero’’ key, which allows the exact control of the values obtained and also ‘‘peak’’ registers that facilitate 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 highprecision 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, Sa˜o Paulo, Brazil) 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 2-min rest interval between records. Evaluations were performed in the first molar (left and right). 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 individual’s maximal bite force.
799
archives of oral biology 55 (2010) 797–802
Table 2 – Means of maximal bite force in the left and right molar regions in the five age groups (children – I, adolescents – II, young adults – III, adult – IV, and elderly – V). Region
Group I
Group II
Group III
Group IV
Group V
F4,172
Right molar Left molar
177 16 170 14
339 28 344 26
280 24 297 25
263 20 265 23
248 44 275 52
6.0204 6.964
2.3.
Method error
2.5.
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, the mean of three bites was considered for each side and used later to assess the results. Paired measurements were analyzed to identify systematic errors. No differences were found between the first and second (one week later) series.
2.4.
Ultrasound analysis
Muscle thickness analyses were performed with a SonoSite Titan ultrasound tool using a high-resolution real-time 56 mm/ 10 MHz linear-array transducer placed transversally to the muscle fibers. The middle of masseter muscle was considered to be located between 1.5 and 2.0 cm above the jaw angle towards the upper eyelid, and the anterior portion of the temporal muscle between 1.0 and 1.5 cm to the back and above the external palpebral comissure. The muscle location was confirmed by palpation and transducer movement in order to provide optimized imaging. Ultrasound images were obtained from bilateral temporal and masseter muscles at rest and maximal voluntary contraction. During the exam, the participants remained seated, leaning on the backrest with the head unrestrained. Measures were taken directly over the image in the moment of its acquisition, with an approximation of 0.1 mm. Three acquisitions were made in each muscle condition (rest and dental clenching at maximal habitual intercuspidation), with an interval of 2 min between each acquisition for the participants to rest their muscles after dental clenching.
p <0.01 <0.01
Statistical analysis
The maximal molar bite force and muscle thickness measures at both sides were analyzed using Multivariate General Linear Model statistics (SPSS 17.0 for Windows; Chicago, USA) with group and gender as factors, followed by Bonferroni’s post hoc test for multiple comparisons to investigate group differences. In the case of significant effects of group factor, one-way ANOVA was also performed. Gender differences were analyzed using a t test for independent samples. Bite force and age were correlated using Pearson’s correlation coefficient. A level of significance of 5% ( p 0.05) was adopted.
3.
Results
The maximal molar bite force values of the five age groups are presented in Table 2. Effects of group (F8,334 = 4.124; p < 0.01) and gender (F2,166 = 14.704; p < 0.01) were observed, but with no interaction between them (F8,334 = 1.039; p = 0.41) The ANOVA showed significant differences between groups bilaterally (right side: F4,172 = 6.204, p < 0.01; left side: F4,172 = 6.964, p < 0.01). Bonferroni’s test showed that group I had significantly lower bite force means at both sides than all groups except group V. No differences were found between the left and right sides. In all the groups, gender was found to be a significant factor associated with maximal bite force (F2,166 = 14.704; p < 0.01). A global comparison including all the subjects and measures showed that the means of men were approximately 30% higher than those of women (right side: t = 4.803, df = 175; p < 0.01; left side: t = 4.435; df = 175, p < 0.01). Within-group comparisons yielded similar results in all groups (Table 3).
Table 3 – Means of maximal bite force in the left and right molar regions across genders. Groups
Side
Gender bite force M
F
t
df
p
I
Right molar Left molar
184 30 185 30
170 31 156 32
0.428 0.999
38 38
0.67 0.32
II
Right molar Left molar
405 30 404 31
273 31 287 32
2.514** 2.463**
38 38
0.02 0.02
III
Right molar Left molar
339 32 348 30
221 31 247 31
2.608** 2.038**
38 38
0.01 0.05
IV
Right molar Left molar
324 35 322 34
203 31 201 31
3.330** 2.620**
38 38
<0.01 0.01
V
Right molar Left molar
353 48 391 50
153 45 171 47
2.615** 2.356**
38 38
0.02 0.03
df = degree of freedom. Significant p < 0.05.
**
800
archives of oral biology 55 (2010) 797–802
Table 4 – Means and standard error of the thickness (in cm) of the right masseter (RM), left masseter (LM), right temporal (RT), and left temporal (LT) in the five age groups (children – I, adolescents – II, young adults – III, adults – IV, and elderly – V) in relation to gender – male (M) and female (F) – in the clinical condition of rest. Groups
I II III IV V
Gender
M F M F M F M F M F
Muscles RM
LM
RT
0.78 0.04 0.73 0.04 0.94 0.04 0.92 0.04 1.02 0.04 0.82 0.04 1.16 0.04 0.93 0.04 1.10 0.06 0.90 0.06
0.77 0.03 0.73 0.03 0.95 0.03 0.92 0.04 1.06 0.04 0.84 0.04 1.14 0.03 0.94 0.03 1.07 0.06 0.89 0.05
0.51 0.03 0.44 0.03 0.62 0.03 0.65 0.03 0.67 0.03 0.56 0.03 0.74 0.03 0.59 0.03 0.65 0.05 0.47 0.04
The mean thickness values of the masseter and temporal muscles at rest and maximal voluntary contraction in the five age groups are presented in Tables 4 and 5. A gradual increase in the thickness of these muscles was found in the two conditions (rest and maximal contraction) for groups I to IV, whereas a decrease in muscle thickness was observed in group V. Multivariate analysis showed that in both conditions there was an effect of group and gender (Table 6). In respect to the right masseter, Bonferroni’s post hoc test showed that group I had the lowest muscle thickness values in the rest condition than the other groups, and that such values had a gradual increase from group to group until group IV. In the maximal contraction condition, the only significant difference was that group I had the lowest thickness values as compared to the other groups. For the temporal muscles, the only significant difference found was that in both clinical conditions (rest and maximal contraction), group I had the lowest thickness values compared to all the other groups. At rest and during maximal voluntary contraction, the mean muscle thickness values were similar for the left and the right sides, with no significant differences. Gender, however, was found to be related to muscle thickness measures for all muscles (Table 6).
4.
LT 0.49 0.03 0.43 0.03 0.63 0.03 0.63 0.03 0.68 0.03 0.59 0.03 0.71 0.03 0.59 0.03 0.66 0.05 0.46 0.04
Discussion
The world population has reached increasingly advanced ages and the knowledge regarding factors such as the structural behaviour of muscle thickness and maximal bite force over time are important for the understanding of normal, agerelated alterations. Normality standards for Brazilian caucasian population concerning these factors have not been established to date. Defined standards are crucial for clinicians identify alterations and dysfunctions of stomatognathic system, as well as support clinical diagnosis and prognosis. The human body goes through continuous transformation from birth, both in its form and function. As time passes, the physiological systems suffer a decrease in their ability to perform their functions and aging cause general change in body structures. There is evidence of decreased nutrient intake in old people with masticatory difficulties, although there is no consensus that a healthy dentition is able to sustain an adequate nutritional status.7,12 The decrease in muscle mass and strength is a marked process in the loss of functional capacity in the aging individual, expressed by a reduction in the number and size of the muscle fibers13 and understood as a natural process of decrease of the individual’s functional reserves.14
Table 5 – Means and standard error of the thickness (in cm) of the right masseter (RM), left masseter (LM), right temporal (RT), and left temporal (LT) in the five age groups (children – I, adolescents – II, young adults – III, adults – IV, and elderly – V) in relation to gender – male (M) and female (F) – in the clinical condition of maximal voluntary contraction. Group
I II III IV V
Gender
M F M F M F M F M F
Muscles RM
LM
RT
1.00 0.04 0.93 0.04 1.29 0.04 1.19 0.04 1.35 0.04 1.13 0.04 1.48 0.04 1.17 0.04 1.43 0.07 1.12 0.06
0.97 0.04 0.95 0.04 1.27 0.04 1.21 0.04 1.38 0.04 1.12 0.04 1.48 0.04 1.20 0.04 1.39 0.06 1.13 0.06
0.58 0.03 0.51 0.03 0.70 0.03 0.72 0.03 0.76 0.03 0.64 0.03 0.84 0.03 0.67 0.03 0.72 0.05 0.56 0.04
LT 0.57 0.03 0.51 0.03 0.71 0.03 0.69 0.03 0.77 0.03 0.65 0.03 0.82 0.03 0.66 0.03 0.75 0.05 0.57 0.05
801
archives of oral biology 55 (2010) 797–802
Table 6 – Multivariate analysis of variance of the thickness (in cm) of the right masseter (RM), left masseter (LM), right temporal (RT), and left temporal (LT) in the clinical condition of rest and maximal voluntary contraction. Multivariate analysis of variance Group F4,167 REST RM 20.246 LM 17.409 RT 11.382 LT 10.847 Maximal contraction RM 25.637 LM 24.566 RT 12.110 LT 9.943
Gender
Interaction
p
F1,167
p
F4,167
<0.01 <0.01 <0.01 <0.01
34.595 26.103 19.298 15.141
<0.01 <0.01 <0.01 <0.01
3.756 3.158 2.583 2.040
<0.01 0.02 0.04 0.09
<0.01 <0.01 <0.01 <0.01
54.573 35.753 18.919 19.225
<0.01 <0.01 <0.01 <0.01
3.692 4.306 2.531 1.426
<0.01 <0.01 0.04 0.23
Decreases in muscle mass can be caused by its transformation into intramuscular fat, which leads to alterations in tissue elasticity and capacity for compression.1 Previous findings regarding reduced muscle activity in the elderly15 could be explained by the results of the present study, where the thickness of the muscles studied gradually increased over time, decreasing in the elderly. This was true in both clinical conditions (rest and maximal voluntary contraction). Our group comparisons showed that the highest muscle thickness values were found in male components of group IV (41–60 years), both at rest and muscle contraction, which was not true for women, whose highest values at rest were found in group IV (41–60 years), and at contraction in group II (13–20 years). These data are interesting when correlated with those of maximal molar bite force, since the highest values obtained in both sides and for both men and women belonged to group II (13–20 years). Group I (7–12 years) had the lowest muscle thickness values in both males and females, as well as the lowest bite force values. Studies have shown that age and gender are important factors that influence the resistance of jaw lifting muscles in terms of their maximal bite force, which seems to remain constant between 20 and 50 years of age and to differ between men and women.16 Bite force, a well-established clinical parameter, was found to be significantly higher in men bilaterally. The gender factor can influence bite force because muscle mass and size are usually greater in men.17 There exists a significant association of gender and age with the thickness of the masseter muscle, which has been reported to be greater in men and in the elderly.18 This is not in accordance with our findings, where a decrease in the thickness of both the masseter and temporal muscles was found to occur after 60 years of age in men and women. Muscle thickness differences between adults and adolescents have been frequently reported, showing that men have a greater muscular potential as compared to women.19,20 These data are consonant with those of the present study. The increase in muscle mass during puberty, influenced by androgenic steroids, creates the muscle differences between males and females.21 These differences between genders are first seen in puberty.22 In this study, female adolescents between 13 and 20 years of age had greater muscle thickness
p
compared to females of the other age groups. Among men, a gradual increase in muscle thickness was found to occur over time. With the enrollment of a healthy, heterogeneous population aged between 7 and 80 years, our study provides data that may serve as standards for the Brazilian population in terms of bite force and muscle thickness and the interaction between these two factors. The understandings of the functional integrity and changes in the masticatory system over time are crucial for the establishment of sound clinical judgment that will guide proper care and treatment.
Acknowledgements Funding: This study was supported by grant from ‘‘Fundac¸a˜o de Amparo a Pesquisa – FAPESP’’ no. 2006/60965-6. Competing interests: None declared. Ethical approval: This study was approved ethically by the Local Ethics Committee at the Ribeira˜o Preto School of Dentistry of the University of Sa˜o Paulo (Process no. 2006 1971.58.5). All subjects were informed about the purpose and potential risks of the study and signed an informed consent term, as required by resolution 196/96 issued by the National Health Council.
references
1. Orchardson R, Cadden SW. Mastication, in scientific basis of eating. Front Oral Biol 1998;9:76–121. 2. Bakke M, Tuxen A, Vilmann P, Jensen BR, Vilman A, Toft M. Ultrasound image of human masseter muscle related to bite force, electromyography, facial morphology, and occlusal factors. Scand J Dent Res 1992;100:164–71. 3. Raadsheer MC, Kiliards S, Van Eijden TMGJ, Van Eijden FC, Prahl AB. Masseter muscle thickness in growing individuals and its relation to facial morphology. Arch Oral Biol 1996;41:323–32. 4. Bakke M. Mandibular elevator muscles: physiology, action, and effect of dental occlusion. Scand J Dent Res 1993;101: 314–31. 5. Emshoff R, Bertram S, Brandlmaier I, Scheiderbauer G, Rudisch A, Boner G. Ultrasonographic assessment of local
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cross-sectional dimensions of masseter muscle sites: a reproducible technique? J Oral Rehabil 2002;29:1059–62. Bertram S, Brandlmaier I, Rudisch A, Bodner G, Emshoff R. Cross-sectional characteristics of masseter muscle: an ultrasonographic study. Int J Oral Maxillofac Surg 2003;32:64–8. Satiroglu F, Arun T, Isik F. Comparative data on facial morphology and muscle thickness using ultrasonography. Eur J Orthod 2005;27:562–7. Georgiakaki I, Tortopidis D, Garefis P, Kiliaridis S. Ultrasonographic thickness and electromyographic activity of masseter muscle of human females. J Oral Rehabil 2007;34:121–8. Kiliaridis S, Engvall M, Tzakis MG. Ultrasound imaging of the masseter muscle in myotonic dystrophy patients. J Oral Rehabil 1995;22:619–25. Galo R, Vitti M, Santos CM, Hallak JEC, Regalo SCH. The effect of age on the function of the masticatory system–an electromyographical analysis. Gerodontology 2006;23:177–82. Shiau YY, Wang JS. The effects of dental condition on hand strength and maximum bite force. Cranio 1993;11:48–54. Galo R, Vitti M, Mattos M-G, Regalo SC. Masticatory muscular activation in elderly individuals during chewing. Gerodontology 2007;24:244–8. Ikebe K, Nokubi T, Morii K, Kashiwagi J, Furuya M. Association of bite force with ageing and occlusal support in older adults. J Dent 2005;33:131–7.
14. Baltes L, Mailloux-Pririer O. Pessoas idosas: uma abordagem global. Lisboa: Lusodida´tica; 1995. 15. Karlsson S, Carlsson GE. Characteristics of mandibular masticatory movement in young and elderly dentate subjects. J Dent Res 1990;69:473–6. 16. Shiau YY, Peng CC, Wen SC, Lin LD, Wang JS, Lou KL. The effects of masseter muscle pain on biting performance. J Oral Rehabil 2003;30:978–84. 17. Bonakdarchian M, Askari N, Askari M. Effect of face form on maximal molar bite force with natural dentition. Arch Oral Biol 2009;54:201–4. 18. Kiliaridis S, Georgiakaki I, Katsaros C. Masseter muscle thickness and maxillary dental arch width. Eur J Orthod 2003;25:259–63. 19. Newton JP, Yemm R, Abel RW, Menhinick S. Changes in human jaw muscles with age and dental state. Gerodontology 1993;10:16–22. 20. Waltimo A, Kemppainen P, Ko¨no¨nen M. Maximal contraction force and endurance of human jaw closing muscles in isometric clenching. Scand J Dent Res 1993;101:416–21. 21. Falkner F, Tanner JM. Human growth. Part 2. Postnatal growth. New York: Plenum Press; 1978. 273–94;381–12. 22. Garner LD, Kotwal NS. Correlation study of incisive biting forces with age, sex and anterior occlusion. J Dent Res 1973;52:698–702.
available at www.sciencedirect.com
journal homepage: http://www.elsevier.com/locate/aob
Age and gender influence on maximal bite force and masticatory muscles thickness Marcelo Palinkas a, Mariangela Salles Pereira Nassar a, Fla´via Argentato Cecı´lio a, Selma Sie´ssere a,c, Marisa Semprini a,c, Joa˜o Paulo Machado-de-Sousa b,c, Jaime Eduardo Cecilio Hallak b,c, Simone Cecı´lio Hallak Regalo a,c,* a
Department of Morphology, Stomatology, and Physiology of the Ribeira˜o Preto Dental School (RPDS), University of Sa˜o Paulo, Ribeira˜o Preto, Sa˜o Paulo, Brazil b Department of Neurosciences and Behavior of the Ribeira˜o Preto Medical School (RPMS), University of Sa˜o Paulo, Ribeira˜o Preto, Sa˜o Paulo, Brazil c National Science and Technology Institute (INCT) for Translational Medicine, CNPq, Brazil
article info
abstract
Article history:
The present study aimed investigate the age and gender influence on maximal molar bite force
Accepted 29 June 2010
and at outlining the criteria for normal masticatory muscle development in a sample of 177 Brazilian Caucasian dentate individuals aged 7–80 years divided into five age groups: I (7–12
Keywords:
years), II (13–20 years), III (21–40 years), IV (41–60 years), and V (61–80 years). Except for Group V,
Ultrasound
which comprised nine women and eight men, all groups were equally divided in respect to
Human masseter
gender (20 M/20 F). Bite force was recorded with a mouth-adapted 1000 N dynamometer and the
Human temporal
highest out of three records was regarded as the maximal bite force. The data were submitted to
Muscle thickness
multivariate statistical analysis (SPSS 17.0 p < 0.05). Effects of group and gender were found,
Aging
but no interactions between them. The ANOVA showed significant differences between groups bilaterally. Bonferroni’s test showed that group I had significantly lower bite force means at both sides as compared to all groups, except group V. No differences were found between the left and right sides. In all the groups, gender was found to be a significant factor associated with maximal bite force. A global comparison including all the subjects and measures showed that the means of men were approximately 30% higher than those of women. Within-group comparisons yielded similar results in all groups. Muscle thickness was measured with a SonoSite Titan ultrasound tool using a high-resolution real-time 56 mm/10 MHz linear-array transducer. Three ultrasound images were obtained from the bilateral masseter and temporal muscles at rest and at maximal voluntary contraction. The means of the three measures in each clinical condition were analyzed with multivariate statistical analysis (SPSS 17.0 p < 0.05). A gradual increase in thickness of the masseter and temporal muscles was found both at rest and maximal voluntary contraction for groups I to IV, whereas a decrease in muscle thickness was observed in group V. Multivariate analysis showed that in both conditions there was an effect of group and gender. The study of the development of the stomatognathic system in relation to age and gender can provide useful data for the identification of normal and impaired functioning patterns. The results of this study indicate that age and gender are associated with structural and functional alterations in the muscles of the stomatognathic system. # 2010 Elsevier Ltd. All rights reserved.
* Corresponding author at: Avenida do Cafe´, s/n, Bairro, Monte Alegre, 14040-904 Ribeira˜o Preto, SP, Brazil. Tel.: +55 16 36024025; fax: +55 16 36330999. E-mail address: [email protected] (S.C.H. Regalo). 0003–9969/$ – see front matter # 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.archoralbio.2010.06.016
798
1.
archives of oral biology 55 (2010) 797–802
Introduction
Table 1 – Description of the groups. Group
The stomatognathic system is a physiological and functional entity comprising a set of organs and tissues whose biology and physiopathology are fully dependent on each other. The anatomical and functional development of stomatognathic system, and consequently the masticatory function, is dependent upon two important factors: muscle and craniofacial development.1 The knowledge concerning the thickness of masticatory muscles, allied to findings on facial morphology, occlusal factors, and bite force are vital for understanding the complex functioning of the stomatognathic system.2–4 Ultrasound is a tool that enables researchers to analyze the thickness of the skeletal musculature.5–8 Current research has been concerned with determining the bite force in human subjects, seeking to assess and understand the functionality of masticatory system, craniomandibular anatomy, neuromuscular mechanisms, masticatory efficiency, and muscle force.9,10 Bite force is directly related to mastication and is determined by the size of the jaw lifting muscles (especially in their transversal section1) and their interaction with the nervous, muscular, skeletal, and dental systems. The condition of these systems directly interferes with one’s capacity to chew and bite.11 Given the importance of the musculature in the craniofacial development, this study is aimed searching evidence concerning the muscular interaction with craniofacial development over time. The thickness of the masseter and temporal muscles, as well as the maximal bite force in Brazilian Caucasian children, adolescents, adults, and elderly were analyzed in order to provide the basis for the definition of normality criteria and parameters for muscular masticatory development in relation to age and gender. The results of this study will enable the full morphological and functional assessment of the stomatognathic system, facilitating diagnosis and prognosis and at defining normality standards for population.
2.
Methods
2.1.
Sample
Two hundred and fifty individuals were evaluated and 177 were included in the final sample according to the inclusion and exclusion criteria for participation. All volunteers were Brazilian, fully dentate (except for Group I – mixed dentition, caucasian, aged 7–80 years, and divided into five groups: I (7–12 years), II (13–20 years), III (21–40 years), IV (41–60 years), and V (61–80 years)). Except for Group V, which comprised nine women and eight men, all groups were equally divided in respect to gender (20 M/20 F) (Table 1). All subjects were nasal breathers, had normal occlusion, no parafunctional habits and had to be free of signs and symptoms of any dysfunction of the masticatory system. The study was approved by the Local Ethics Committee at the Ribeira˜o Preto School of Dentistry of the University of Sa˜o Paulo (Process no. 2006 1971.58.5). All subjects were informed about the purpose and potential risks of the study and signed
I II III IV V
Age
Men
07–12 13–20 21–40 41–60 61–80
20 20 20 20 8
Women 20 20 20 20 9
an informed consent term, as required by resolution 196/96 issued by the National Health Council. Those responsible for minor participants signed the informed consent for them. The sample was selected by means of anamneses and clinical exams guided by the inclusion/exclusion criteria. The anamneses provided data regarding the participants’ personal information, medical and dental history, any existing parafunctional habits, and possible temporomandibular dysfunction symptoms (RDC/TMD). All subjects were fully dentate and had no periodontal problems. The following items were used as exclusion criteria during the anamnesis interview:
presence of systemic or local disorders that could impair the craniofacial growth or the masticatory system, such as neurological disorders and cerebral palsy; use of any medication that could interfere in muscle activity, such as antihistamines, sedatives, homeopathic remedies or central nervous system depressors; treatments that could directly or indirectly interfere in muscle activity during the period in which the study was performed, such as speech therapy and otorhinolaryngological treatments.
2.2.
Bite force
Bite force measures were collected with the volunteers sitting on a comfortable chair (office-like), with the arms extended along the body and the hands lying on their thighs. The records were taken with a digital dynamometer, model IDDK (Kratos, Cotia, Sa˜o Paulo, Brazil), with a 1000 N capacity, adapted to the mouth. The apparatus has a ‘‘set-zero’’ key, which allows the exact control of the values obtained and also ‘‘peak’’ registers that facilitate 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 highprecision 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, Sa˜o Paulo, Brazil) 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 2-min rest interval between records. Evaluations were performed in the first molar (left and right). 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 individual’s maximal bite force.
799
archives of oral biology 55 (2010) 797–802
Table 2 – Means of maximal bite force in the left and right molar regions in the five age groups (children – I, adolescents – II, young adults – III, adult – IV, and elderly – V). Region
Group I
Group II
Group III
Group IV
Group V
F4,172
Right molar Left molar
177 16 170 14
339 28 344 26
280 24 297 25
263 20 265 23
248 44 275 52
6.0204 6.964
2.3.
Method error
2.5.
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, the mean of three bites was considered for each side and used later to assess the results. Paired measurements were analyzed to identify systematic errors. No differences were found between the first and second (one week later) series.
2.4.
Ultrasound analysis
Muscle thickness analyses were performed with a SonoSite Titan ultrasound tool using a high-resolution real-time 56 mm/ 10 MHz linear-array transducer placed transversally to the muscle fibers. The middle of masseter muscle was considered to be located between 1.5 and 2.0 cm above the jaw angle towards the upper eyelid, and the anterior portion of the temporal muscle between 1.0 and 1.5 cm to the back and above the external palpebral comissure. The muscle location was confirmed by palpation and transducer movement in order to provide optimized imaging. Ultrasound images were obtained from bilateral temporal and masseter muscles at rest and maximal voluntary contraction. During the exam, the participants remained seated, leaning on the backrest with the head unrestrained. Measures were taken directly over the image in the moment of its acquisition, with an approximation of 0.1 mm. Three acquisitions were made in each muscle condition (rest and dental clenching at maximal habitual intercuspidation), with an interval of 2 min between each acquisition for the participants to rest their muscles after dental clenching.
p <0.01 <0.01
Statistical analysis
The maximal molar bite force and muscle thickness measures at both sides were analyzed using Multivariate General Linear Model statistics (SPSS 17.0 for Windows; Chicago, USA) with group and gender as factors, followed by Bonferroni’s post hoc test for multiple comparisons to investigate group differences. In the case of significant effects of group factor, one-way ANOVA was also performed. Gender differences were analyzed using a t test for independent samples. Bite force and age were correlated using Pearson’s correlation coefficient. A level of significance of 5% ( p 0.05) was adopted.
3.
Results
The maximal molar bite force values of the five age groups are presented in Table 2. Effects of group (F8,334 = 4.124; p < 0.01) and gender (F2,166 = 14.704; p < 0.01) were observed, but with no interaction between them (F8,334 = 1.039; p = 0.41) The ANOVA showed significant differences between groups bilaterally (right side: F4,172 = 6.204, p < 0.01; left side: F4,172 = 6.964, p < 0.01). Bonferroni’s test showed that group I had significantly lower bite force means at both sides than all groups except group V. No differences were found between the left and right sides. In all the groups, gender was found to be a significant factor associated with maximal bite force (F2,166 = 14.704; p < 0.01). A global comparison including all the subjects and measures showed that the means of men were approximately 30% higher than those of women (right side: t = 4.803, df = 175; p < 0.01; left side: t = 4.435; df = 175, p < 0.01). Within-group comparisons yielded similar results in all groups (Table 3).
Table 3 – Means of maximal bite force in the left and right molar regions across genders. Groups
Side
Gender bite force M
F
t
df
p
I
Right molar Left molar
184 30 185 30
170 31 156 32
0.428 0.999
38 38
0.67 0.32
II
Right molar Left molar
405 30 404 31
273 31 287 32
2.514** 2.463**
38 38
0.02 0.02
III
Right molar Left molar
339 32 348 30
221 31 247 31
2.608** 2.038**
38 38
0.01 0.05
IV
Right molar Left molar
324 35 322 34
203 31 201 31
3.330** 2.620**
38 38
<0.01 0.01
V
Right molar Left molar
353 48 391 50
153 45 171 47
2.615** 2.356**
38 38
0.02 0.03
df = degree of freedom. Significant p < 0.05.
**
800
archives of oral biology 55 (2010) 797–802
Table 4 – Means and standard error of the thickness (in cm) of the right masseter (RM), left masseter (LM), right temporal (RT), and left temporal (LT) in the five age groups (children – I, adolescents – II, young adults – III, adults – IV, and elderly – V) in relation to gender – male (M) and female (F) – in the clinical condition of rest. Groups
I II III IV V
Gender
M F M F M F M F M F
Muscles RM
LM
RT
0.78 0.04 0.73 0.04 0.94 0.04 0.92 0.04 1.02 0.04 0.82 0.04 1.16 0.04 0.93 0.04 1.10 0.06 0.90 0.06
0.77 0.03 0.73 0.03 0.95 0.03 0.92 0.04 1.06 0.04 0.84 0.04 1.14 0.03 0.94 0.03 1.07 0.06 0.89 0.05
0.51 0.03 0.44 0.03 0.62 0.03 0.65 0.03 0.67 0.03 0.56 0.03 0.74 0.03 0.59 0.03 0.65 0.05 0.47 0.04
The mean thickness values of the masseter and temporal muscles at rest and maximal voluntary contraction in the five age groups are presented in Tables 4 and 5. A gradual increase in the thickness of these muscles was found in the two conditions (rest and maximal contraction) for groups I to IV, whereas a decrease in muscle thickness was observed in group V. Multivariate analysis showed that in both conditions there was an effect of group and gender (Table 6). In respect to the right masseter, Bonferroni’s post hoc test showed that group I had the lowest muscle thickness values in the rest condition than the other groups, and that such values had a gradual increase from group to group until group IV. In the maximal contraction condition, the only significant difference was that group I had the lowest thickness values as compared to the other groups. For the temporal muscles, the only significant difference found was that in both clinical conditions (rest and maximal contraction), group I had the lowest thickness values compared to all the other groups. At rest and during maximal voluntary contraction, the mean muscle thickness values were similar for the left and the right sides, with no significant differences. Gender, however, was found to be related to muscle thickness measures for all muscles (Table 6).
4.
LT 0.49 0.03 0.43 0.03 0.63 0.03 0.63 0.03 0.68 0.03 0.59 0.03 0.71 0.03 0.59 0.03 0.66 0.05 0.46 0.04
Discussion
The world population has reached increasingly advanced ages and the knowledge regarding factors such as the structural behaviour of muscle thickness and maximal bite force over time are important for the understanding of normal, agerelated alterations. Normality standards for Brazilian caucasian population concerning these factors have not been established to date. Defined standards are crucial for clinicians identify alterations and dysfunctions of stomatognathic system, as well as support clinical diagnosis and prognosis. The human body goes through continuous transformation from birth, both in its form and function. As time passes, the physiological systems suffer a decrease in their ability to perform their functions and aging cause general change in body structures. There is evidence of decreased nutrient intake in old people with masticatory difficulties, although there is no consensus that a healthy dentition is able to sustain an adequate nutritional status.7,12 The decrease in muscle mass and strength is a marked process in the loss of functional capacity in the aging individual, expressed by a reduction in the number and size of the muscle fibers13 and understood as a natural process of decrease of the individual’s functional reserves.14
Table 5 – Means and standard error of the thickness (in cm) of the right masseter (RM), left masseter (LM), right temporal (RT), and left temporal (LT) in the five age groups (children – I, adolescents – II, young adults – III, adults – IV, and elderly – V) in relation to gender – male (M) and female (F) – in the clinical condition of maximal voluntary contraction. Group
I II III IV V
Gender
M F M F M F M F M F
Muscles RM
LM
RT
1.00 0.04 0.93 0.04 1.29 0.04 1.19 0.04 1.35 0.04 1.13 0.04 1.48 0.04 1.17 0.04 1.43 0.07 1.12 0.06
0.97 0.04 0.95 0.04 1.27 0.04 1.21 0.04 1.38 0.04 1.12 0.04 1.48 0.04 1.20 0.04 1.39 0.06 1.13 0.06
0.58 0.03 0.51 0.03 0.70 0.03 0.72 0.03 0.76 0.03 0.64 0.03 0.84 0.03 0.67 0.03 0.72 0.05 0.56 0.04
LT 0.57 0.03 0.51 0.03 0.71 0.03 0.69 0.03 0.77 0.03 0.65 0.03 0.82 0.03 0.66 0.03 0.75 0.05 0.57 0.05
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archives of oral biology 55 (2010) 797–802
Table 6 – Multivariate analysis of variance of the thickness (in cm) of the right masseter (RM), left masseter (LM), right temporal (RT), and left temporal (LT) in the clinical condition of rest and maximal voluntary contraction. Multivariate analysis of variance Group F4,167 REST RM 20.246 LM 17.409 RT 11.382 LT 10.847 Maximal contraction RM 25.637 LM 24.566 RT 12.110 LT 9.943
Gender
Interaction
p
F1,167
p
F4,167
<0.01 <0.01 <0.01 <0.01
34.595 26.103 19.298 15.141
<0.01 <0.01 <0.01 <0.01
3.756 3.158 2.583 2.040
<0.01 0.02 0.04 0.09
<0.01 <0.01 <0.01 <0.01
54.573 35.753 18.919 19.225
<0.01 <0.01 <0.01 <0.01
3.692 4.306 2.531 1.426
<0.01 <0.01 0.04 0.23
Decreases in muscle mass can be caused by its transformation into intramuscular fat, which leads to alterations in tissue elasticity and capacity for compression.1 Previous findings regarding reduced muscle activity in the elderly15 could be explained by the results of the present study, where the thickness of the muscles studied gradually increased over time, decreasing in the elderly. This was true in both clinical conditions (rest and maximal voluntary contraction). Our group comparisons showed that the highest muscle thickness values were found in male components of group IV (41–60 years), both at rest and muscle contraction, which was not true for women, whose highest values at rest were found in group IV (41–60 years), and at contraction in group II (13–20 years). These data are interesting when correlated with those of maximal molar bite force, since the highest values obtained in both sides and for both men and women belonged to group II (13–20 years). Group I (7–12 years) had the lowest muscle thickness values in both males and females, as well as the lowest bite force values. Studies have shown that age and gender are important factors that influence the resistance of jaw lifting muscles in terms of their maximal bite force, which seems to remain constant between 20 and 50 years of age and to differ between men and women.16 Bite force, a well-established clinical parameter, was found to be significantly higher in men bilaterally. The gender factor can influence bite force because muscle mass and size are usually greater in men.17 There exists a significant association of gender and age with the thickness of the masseter muscle, which has been reported to be greater in men and in the elderly.18 This is not in accordance with our findings, where a decrease in the thickness of both the masseter and temporal muscles was found to occur after 60 years of age in men and women. Muscle thickness differences between adults and adolescents have been frequently reported, showing that men have a greater muscular potential as compared to women.19,20 These data are consonant with those of the present study. The increase in muscle mass during puberty, influenced by androgenic steroids, creates the muscle differences between males and females.21 These differences between genders are first seen in puberty.22 In this study, female adolescents between 13 and 20 years of age had greater muscle thickness
p
compared to females of the other age groups. Among men, a gradual increase in muscle thickness was found to occur over time. With the enrollment of a healthy, heterogeneous population aged between 7 and 80 years, our study provides data that may serve as standards for the Brazilian population in terms of bite force and muscle thickness and the interaction between these two factors. The understandings of the functional integrity and changes in the masticatory system over time are crucial for the establishment of sound clinical judgment that will guide proper care and treatment.
Acknowledgements Funding: This study was supported by grant from ‘‘Fundac¸a˜o de Amparo a Pesquisa – FAPESP’’ no. 2006/60965-6. Competing interests: None declared. Ethical approval: This study was approved ethically by the Local Ethics Committee at the Ribeira˜o Preto School of Dentistry of the University of Sa˜o Paulo (Process no. 2006 1971.58.5). All subjects were informed about the purpose and potential risks of the study and signed an informed consent term, as required by resolution 196/96 issued by the National Health Council.
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