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Bite force of children with repaired unilateral and bilateral cleft lip and palate
Archives of Oral Biology 68 (2016) 83–87
Contents lists available at ScienceDirect
Archives of Oral Biology journal homepage: www.elsevier.com/locate/aob
Bite force of children with repaired unilateral and bilateral cleft lip and palate Michele Alves Garciaa , Daniela Riosb , Heitor Marques Honórioc , Ivy Kiemle Trindade-Suedamd,* a
Department of Biological Sciences, Discipline of Physiology, Hospital for Rehabilitation of Craniofacial Anomalies, University of São Paulo, Bauru, SP, Brazil Department of Pediatric Dentistry, Orthodontics and Community Health, Bauru School of Dentistry, University of São Paulo, Bauru, SP, Brazil Department of Pediatric Dentistry, Orthodontics and Community Health, Bauru School of Dentistry, University of São Paulo, Bauru, SP, Brazil d Department of Biological Sciences, Bauru School of Dentistry and Laboratory of Physiology, Hospital for Rehabilitation of Craniofacial Anomalies, University of São Paulo, Bauru, SP, Brazil b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 31 August 2015 Received in revised form 3 March 2016 Accepted 29 March 2016
Objective: To assess the bite force (BF) of children with repaired cleft lip and palate (CLP). Design: Children aged 6–12 years, with and without CLP, were divided into the following 5 groups: (1) control group (CON): 34 children without CLP (17 female, 17 male, mean age 8.2 1.4); (2) cleft lip group (CL): 31 children with cleft lip involving the pre-maxilla (15 female, 16 male, mean age 9.7 1.3); (3) unilateral CLP group (UCLP): 36 children with complete unilateral CLP (11 female, 25 male, mean age 9.4 1.6); (4) bilateral CLP group (BCLP): 32 children with complete bilateral CLP (11 female, 21 male, mean age 9.5 1.7); and 5) cleft palate group (CP): 17 children with complete cleft palate (9 female, 8 male, mean age 9.4 1.6). Briefly, in this clinical trial, BF was assessed before alveolar bone grafting with a gnathodynamometer (IDDK, Kratos, Cotia, SP, Brazil). For CON, BCLP, CL and CP groups, BF was obtained in the anterior and posterior region of the maxilla. For the UCLP group, BF was assessed in the anterior and posterior regions of both segments. Differences among groups were evaluated by ANOVA test, and Tukey’s test was used to assess any correlations among variables (P < 0.05). Results: Unexpectedly, no differences of BF were observed among CON and any of the cleft groups. However, a stronger BF was observed in the CL group when compared to the UCLP and BCLP groups. Next, no differences were observed between the cleft side and the noncleft side in the UCLP group. Lastly, in all groups, BFs from the anterior region of the maxilla were less when compared to the posterior regions. Conclusion: The BF of children with CLP is no different from children without CLP. ã 2016 Elsevier Ltd. All rights reserved.
Keywords: Cleft lip Cleft palate Bite force Child
1. Introduction Cleft lip and palate (CLP) is the most prevalent congenital malformation that affects the stomatognathic system and is characterized by a complete segmentation of the maxilla, leading to maxillary hypoplasia and sagittal and transverse maxillomandibular discrepancies. It is speculated that these changes have a negative effect on the stomatognathic system of such individuals (Trindade-Suedam et al., 2012). Among the main parameters indicative of the stomatognathic system functionality is the quantification of bite force (BF), an
* Corresponding author. Hospital for Rehabilitation of Craniofacial Anomalies, University of São Paulo, Rua Dr. Silvio Marchione 3-20, 17012-900, Bauru, SP, Brazil. E-mail addresses: [email protected], [email protected] (I.K. Trindade-Suedam) . http://dx.doi.org/10.1016/j.archoralbio.2016.03.019 0003-9969/ ã 2016 Elsevier Ltd. All rights reserved.
important method for measuring the masticatory function, as a quantitative indicator (N) of masticatory performance (van der Bilt, Tekamp, van der Glas, & Abbink, 2008). BF is directly related to certain conditions such as craniofacial morphology, occlusal pattern, gender, age (Sun et al., 2015), periodontal status, number of teeth present or even to the type of dental prosthesis in use (Boven, Raghoebar, Vissink, & Meijer, 2014; Hatch, Shinkai, Sakai, Rugh, & Paunovich, 2001; Suzuki, Taniguchi, & Ohyama, 1995). Clinically, BF is a parameter indicative of therapeutic success in dental rehabilitation procedures such as orthognathic surgery or oral rehabilitation with dental implants (Rismanchian, Bajoghli, Mostajeran, Fazel, & Eshkevari, 2009). For example, when oral rehabilitated patients present similar BFs when compared to healthy individuals, the rehabilitation process can be considered successful. Previous research conducted in our laboratory (Sipert, Sampaio, Trindade, & Trindade, 2009) has shown that BF is significantly
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reduced in male subjects with CLP when compared to noncleft individuals. However, important variables such as age and the execution of the alveolar bone grafting surgery, which unifies the maxilla into one structure, were not controlled. Notably, studies assessing BF in children with CLP, especially in bilateral cases (which represent the most severe type of cleft) were absent in the literature. Considering that the segmentation of the maxilla might be a limiting factor of the stomatognathic system function in subjects with CLP, the objective of this study was to quantify the BF of children with different types of CLP without alveolar bone grafting, from the Hospital for Rehabilitation of Craniofacial Anomalies at the University of São Paulo (HRAC/USP), Bauru, SP, Brazil. It was hypothesized that children with clefts, independent of cleft type, would have lower bite force values when compared to children without clefts. 2. Material and methods This study was approved by the Institutional Ethics Review Board of the HRAC/USP, (process number 768.103), according to Resolution 466/12 of the National Health Council. All participants and their legal guardians were informed about the procedures involved in the study and signed an informed consent form before examinations. Considering an alpha error of 5%, a beta error of 20%, and adopting an expected standard deviation of 3 kgf and significant difference between groups of at least 5 kgf (Palinkas et al., 2010), an estimated sample size of 10 subjects per group was obtained. Inclusion criteria were the following: children without CLP, children with nonsyndromic unilateral or bilateral CLP, unilateral cleft lip, cleft palate, children in the mixed dentition phase, children without tooth decay and periodontal disease, and children having interocclusal molar relation. Exclusion criteria were the following: pain or discomfort during the exam, Angle class II and III malocclusions, presence of large restorations or endodontic treatment, tooth loss, inability to understand orientations during the exam, alveolar bone grafting and children with systemic diseases. Briefly, 150 children, from both genders, aged 6–12 years, with and without CLP, were divided into the following 5 groups: (1) control group (CON): 34 children without CLP (17 female, 17 male, mean age 8.2 1.4); (2) cleft lip group (CL): 31 children with cleft lip involving the pre-maxilla (15 female, 16 male, mean age 9.7 1.3); (3) unilateral CLP group (UCLP): 36 children with complete unilateral CLP (11 female, 25 male, mean age 9.4 1.6); (4) bilateral CLP group (BCLP): 32 children with complete bilateral CLP (11 female, 21 male, mean age 9.5 1.7); and (5) cleft palate group (CP): 17 children with complete cleft palate (9 female, 8 male, mean age 9.4 1.6). Children from the cleft groups were regularly registered at a tertiary hospital specialized in the treatment of cleft lip and palate patients (Hospital for Rehabilitation of Craniofacial Anomalies, University of São Paulo, Brazil). In turn, children from the control group were from the Pediatric Dentistry Clinic, Bauru School of Dentistry, University of São Paulo, Brazil. In this clinical trial, children were submitted to a BF exam using a gnathodynamometer (digital dynamometer, IDDK model, Kratos, Bauru, SP, Brazil) with a capacity of 100 kgf (980 N) (Fig. 1). This gnathodynamometer is composed of a stainless steel cylinder (10 10 mm) which contains a load cell that measures force when deformed. Measurements were performed 3 times with an interval of about 1 min between measurements to avoid fatigue (Roldán, Buschang, Saldarriaga Isaza, & Throckmorton, 2009; Roldán, Restrepo, Isaza, Vélez, & Buschang, 2015), been this lapse of time sufficient to avoid fatigue (Roldán et al., 2009). For the CON, BCLP,
Fig. 1. Gnathodynamometer used to perform the measurements (digital dynamometer, IDDK model, Kratos, Bauru, SP, Brazil).
Fig. 2. Location of measurements for the UCLP group: central incisors (anterior region of the maxilla).
CL and CP groups, BF was obtained in the anterior and posterior region of the maxilla. For the UCLP group, BF was assessed in the anterior (Fig. 2 and 3) and posterior regions of both segments (Fig. 4). The locations of the measurements are illustrated in Fig. 5. Importantly, every child was naïve to the BF exam and was given the same detailed instruction and amount of practice using the apparatus.
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Table 1 Demographic distribution of the study population. GENDER (%)
CON (n = 34) CL (n = 31) UCLP (n = 36) BCLP (n = 32) CP (n = 17)
AGE (mean SD)
F
M
17 (50) 15 (48) 11 (31) 11 (34) 9 (53)
17 (50) 16 (52) 25 (69) 21 (66) 8 (47)
8.2 1.4 9.7 1.3 9.4 1.6 9.5 1.7 9.4 1.6
CON: control group; CL: cleft lip group; UCLP: cleft lip and palate group; BCLP: bilateral cleft lip and palate group; CP: cleft palate group.
3. Results
Fig. 3. Location of measurements for the UCLP group: tooth adjacent to the cleft (anterior region of the maxilla).
The distribution of the study population’s gender and age are shown on Table 1. The mean BF (N) from the 5 groups obtained for the anterior and posterior regions of the maxilla are reported in Table 2. In all groups, the mean BFs in the anterior region of the maxilla were significantly lower when compared to the BFs in the posterior regions. Surprisingly, no significant differences of BF were observed among CON and any of the cleft groups. However, significantly greater values of BF were observed for CL when compared to UCLP and to BCLP. Next, no differences were observed between the cleft side and the noncleft side in the UCLP and between the BF of males and females. A positive correlation was found between BF and age (r = 0.19), as illustrated in Fig. 6. 4. Discussion
Fig. 4. Location of measurements for the UCLP group: posterior region of the maxilla.
BF data was initially submitted to normality (KolmogorovSmirnov test) and homogeneity of variances (Levene’s test) tests and passed in both cases. Considering that BF was normally distributed, the results are expressed as means standard deviation. Significant differences among groups were evaluated using an ANOVA test with repeated measures (STATISTICA 10.0, Stat Soft. Inc., Tulsa, OK., USA). Next, Tukey’s test was used to assess any correlations among variables. Additionally, correlation of age and BF were assessed using a Pearson Correlation test. In all cases P < 0.05 were considered significant.
Surprisingly, the BF of the individuals with CLP was no different from individuals without CLP. Contrary to what was initially expected, the segmented maxilla does not impact BF, even before alveolar bone grafting which unifies the maxillary segments. To the best of our knowledge, there are no previous studies published that have assessed BF of individuals with CLP besides the study of Sipert et al. (2009). This study (Sipert et al., 2009) found that the BF of adults with CLP was significantly decreased when compared to the control group. However, an important variable, alveolar bone grafting, was not considered. Our current study further investigates BF but in children (6 to 12 years old) with unilateral and bilateral cleft lip and/or palate while excluding all individuals with alveolar bone grafting. When comparing only the cleft groups, it was observed that children from the CL group had a significantly stronger BF when compared to UCLP and to BCLP. This result might indicate that the presence of a segmented maxilla (UCLP and BCLP) negatively impacts BF. On the other hand, considering no differences of BF among children without CLP and with CLP were found, independent of the group, the authors attribute this difference between CL and UCLP/BCLP to random variability in the individuals tested. The authors also speculate that individuals from the CON group had
Fig. 5. Location of measurements according to the groups analyzed.
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Table 2 Mean values of bite force, expressed in N, from the control group (CON), cleft lip group (CL), cleft lip and palate group (UCLP), bilateral cleft lip and palate group (BCLP) and cleft palate group (CP), on the anterior and posterior regions of the maxilla. GROUP
Anterior mean (SD)
Posteriora mean (SD)
CONb CLb UCLP
90.2 (50.0) 132.4 (61.8) 87.3 (77.5) 103.0 (58.8) 88.3 (39.2) 103.0 (45.1)
301.1 (90.2) 346.2 (113.8) 259.9 (104.9)a 290.3 (98.1)a 251.2 (57.9)a 285.4 (117.7)
BCLPb CPb
cleft sideb non cleft sideb
Statistical test applied: “Repeated Measures Three Way ANOVA and Tukey’s test”. a indicates a significant difference from the CL group. b indicates a significant difference from anterior and posterior.
little experience with general dental exams whereas many individuals with clefts are accustomed to various clinical tests. Thus, naïve children in the control group might not have performed their absolute maximum BF when facing an unknown and potentially uncomfortable situation, while children in cleft groups, with perhaps more experience, might have used more force. The reasons for this lack of difference between the CON group and the CLP groups needs further elucidation. The BF of the CON group obtained in this study is similar to those presented by Marquezin et al. (2013) who showed BF of 302 N, in Brazilian children without CLP in the same age range. However, BF values of the CON group from the present study are considerably stronger, 301.1 90.2 N, than what was found in the study by Palinkas et al. (2010), 170 14 N, which assessed the BF of Brazilian children without CLP at a similar age range (7–12 years). The lack of consistency between our results and Palinkas’ are unclear and require further investigation. Independent of the groups tested, significantly stronger BF values were found in the posterior region of the maxilla when compared to the anterior region. This expected observation occurs because molars are designed to grind food, requiring a stronger force, while incisors tear, as demonstrated by Regalo et al. (2008). Notably, the acquisition of BF in the anterior region of the maxilla in the BCLP group is more difficult to accomplish when compared to the other regions tested. In particular, the pre-maxilla is a mobile structure linked to base of the cranium only by the volmer bone. Therefore, the exam may generate discomfort or even pain to the individual. Despite this fact, no differences were observed in the BF of the anterior region of the maxilla when comparing the BCLP group with any of the other groups. Also contrary to initial expectations, no significant differences of BF were observed between the cleft and noncleft sides in the
UCLP group, meaning that equivalent BFs are observed on both sides of the segmented maxilla. This contradicts the hypothesis that the side affected by the cleft would present a lower BF (Sipert et al., 2009). The authors believe that the muscles from the cleft side exhibit more intense contractions when compared to the contralateral side (noncleft side) in order to execute the same task force, resulting in equal forces. This mechanism requires further investigation by evaluating muscle activity on both sides of the maxilla (cleft and noncleft sides) with electromyography. Regarding gender, no differences were found in the BF of female and male subjects. It is hypothesized that, since the sample of the present study is composed of young children (6–12 y), factors that may influence force and muscle activity such as testosterone and estrogen are not yet significant factors. The lack of gender differences was also observed by Palinkas et al. (2010) who showed no statistical differences between the maximal BF of male and female children (7–12 y). In fact, these authors observed a difference between genders emerge as children aged. Moreover, groups composed of humans 21–60 y, have male BFs significantly stronger when compared to female BFs. Although not strong, a positive correlation was found between BF and age (r = 0.19). That is, as age increased so did BF regardless of group. The authors attribute two factors to this increase in BF as children get older—first because of the growth process per se (Mountain, Wood, & Toumba, 2011; Toro, Buschang, Throckmorton, & Roldan, 2006) and second because of the gradual alignment of the dental arch that occurs during the orthodontic treatment which allows an optimal dental occlusion for mastication, corrobotating previous studies, witch observed that the severity of malocclusion is related with bite forte magnitude (Araujo, Marquezin, Barbosa, Gavião, & Castelo, 2015). Ongoing orthodontic treatment, which can negatively influence BF, was a variable not controlled for in the present study. This dental procedure often increases oral sensitivity and can even lead to dental pain, reducing BF. Orthodontic treatment was frequently present in the CLP groups due to the malocclusions commonly observed on this population. For future studies, the assessment of muscle activity by means of electromyography is recommended. Using this technique, differences among groups will become evident. The assessment of BF in individuals already submitted to the alveolar bone grafting is another area that needs further investigation. This type of investigation might clarify the impact of maxilla unification on BF in these subjects. Despite the unexpected results, these findings provide a better understanding of the factors involved in the BF of subjects with cleft lip and palate. Finally, this anomaly does not influence BF and,
Fig. 6. Correlation graph between the variables bite force and age.
M.A. Garcia et al. / Archives of Oral Biology 68 (2016) 83–87
consequently, does not bring significant consequences for the ability of this population to properly masticate. 5. Conclusion The results of this study indicate that the bite force of children with cleft lip and palate is no different from the bite force of children without this congenital anomaly. Conflict of interest The authors report no conflict of interest. Financial support Fundação CAPES (Coordination for the Improvement of Higher Education Personnel). References Araujo, D. S., Marquezin, M. C., Barbosa, T. S., Gavião, M. B., & Castelo, P. M. (2015). Evaluation of masticatory parameters in overweight and obese children. European Journal of Orthodontics Dec 14. pii: cjv092. [Epub ahead of print]. Boven, G. C., Raghoebar, G. M., Vissink, A., & Meijer, H. J. (2014). Improving masticatory performance, bite force, nutritional state and patient’s satisfaction with implant overdentures: a systematic review of the literature. Journal of Oral Rehabilitation, 42, 220–233. Hatch, J. P., Shinkai, R. S., Sakai, S., Rugh, J. D., & Paunovich, E. D. (2001). Determinants of masticatory performance in dentate adults. Archives of Oral Biology, 46, 641–648. Marquezin, M. C., Kobayashi, F. Y., Montes, A. B., Gavião, M. B., & Castelo, P. M. (2013). Assessment of masticatory performance, bite force, orthodontic treatment need
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and orofacial dysfunction in children and adolescents. Archives of Oral Biology, 58, 286–292. Mountain, G., Wood, D., & Toumba, J. (2011). Bite force measurement in children with primary dentition. International Journal of Paediatric Dentistry, 21, 112–118. Palinkas, M., Nassar, M. S., Cecílio, F. A., Siéssere, S., Semprini, M., Machado-deSousa, J. P., et al. (2010). Age and gender influence on maximal BF and masticatory muscles thickness. Archives of Oral Biology, 55, 797–802. Regalo, S. C., Santos, C. M., Vitti, M., Regalo, C. A., de Vasconcelos, P. B., & Mestriner, W. Jr. (2008). Evaluation of molar and incisor bite force in indigenous compared with white population in Brazil. Archives of Oral Biology, 53, 282–286. Rismanchian, M., Bajoghli, F., Mostajeran, Z., Fazel, A., & Eshkevari, P. S. (2009). Effect of implants on maximum bite force in edentulous patients. The Journal of Oral Implantology, 35, 196–200. Roldán, S., Buschang, P. H., Saldarriaga Isaza, J. F., & Throckmorton, G. (2009). Reliability of maximum bite force measurements in age-varying populations. Journal of Oral Rehabilitation, 36(11), 801–807. Roldán, S. I., Restrepo, L. G., Isaza, J. F., Vélez, L. G., & Buschang, P. H. (2015). Are maximum bite forces of subjects 7 to 17 years of age related to malocclusion? Angle Orthodontist Sep 8. [Epub ahead of print]. Sipert, C. R., Sampaio, A. C. M., Trindade, I. E. K., & Trindade, A. S. Jr. (2009). Bite force evaluation in subjects with cleft lip and palate. Journal of Applied Oral Science, 17, 136–139. Sun, K. T., Chen, S. C., Li, Y. F., Chiang, H. H., Tsai, H. H., Li, C. Y., et al. (2015). Bite-force difference among obese adolescents in central Taiwan. Journal of the Formosan Medical Association. http://dx.doi.org/10.1016/j.jfma.2015.05.007. Suzuki, R., Taniguchi, H., & Ohyama, T. (1995). Prosthodontic abutment in four patients with unilateral cleft lip and palate. Cleft Palate Craniofacial Journal, 32, 442–447. Toro, A., Buschang, P. H., Throckmorton, G., & Roldan, S. (2006). Masticatory performance in children and adolescents with Class I and II malocclusions. European Journal of Orthodontics, 28, 112–119. Trindade-Suedam, I. K., Gaia, B. F., Cheng, C. K., Trindade, P. A., Bastos, J. C., & Mattos, B. S. (2012). Cleft lip and palate: recommendations for dental anesthetic procedure based on anatomic evidences. Journal of Applied Oral Science, 20, 122– 127. van der Bilt, A., Tekamp, A., van der Glas, H., & Abbink, J. (2008). Bite force and electromyography during maximum unilateral and bilateral clenching. European Journal of Oral Sciencies, 116, 217–222.
Contents lists available at ScienceDirect
Archives of Oral Biology journal homepage: www.elsevier.com/locate/aob
Bite force of children with repaired unilateral and bilateral cleft lip and palate Michele Alves Garciaa , Daniela Riosb , Heitor Marques Honórioc , Ivy Kiemle Trindade-Suedamd,* a
Department of Biological Sciences, Discipline of Physiology, Hospital for Rehabilitation of Craniofacial Anomalies, University of São Paulo, Bauru, SP, Brazil Department of Pediatric Dentistry, Orthodontics and Community Health, Bauru School of Dentistry, University of São Paulo, Bauru, SP, Brazil Department of Pediatric Dentistry, Orthodontics and Community Health, Bauru School of Dentistry, University of São Paulo, Bauru, SP, Brazil d Department of Biological Sciences, Bauru School of Dentistry and Laboratory of Physiology, Hospital for Rehabilitation of Craniofacial Anomalies, University of São Paulo, Bauru, SP, Brazil b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 31 August 2015 Received in revised form 3 March 2016 Accepted 29 March 2016
Objective: To assess the bite force (BF) of children with repaired cleft lip and palate (CLP). Design: Children aged 6–12 years, with and without CLP, were divided into the following 5 groups: (1) control group (CON): 34 children without CLP (17 female, 17 male, mean age 8.2 1.4); (2) cleft lip group (CL): 31 children with cleft lip involving the pre-maxilla (15 female, 16 male, mean age 9.7 1.3); (3) unilateral CLP group (UCLP): 36 children with complete unilateral CLP (11 female, 25 male, mean age 9.4 1.6); (4) bilateral CLP group (BCLP): 32 children with complete bilateral CLP (11 female, 21 male, mean age 9.5 1.7); and 5) cleft palate group (CP): 17 children with complete cleft palate (9 female, 8 male, mean age 9.4 1.6). Briefly, in this clinical trial, BF was assessed before alveolar bone grafting with a gnathodynamometer (IDDK, Kratos, Cotia, SP, Brazil). For CON, BCLP, CL and CP groups, BF was obtained in the anterior and posterior region of the maxilla. For the UCLP group, BF was assessed in the anterior and posterior regions of both segments. Differences among groups were evaluated by ANOVA test, and Tukey’s test was used to assess any correlations among variables (P < 0.05). Results: Unexpectedly, no differences of BF were observed among CON and any of the cleft groups. However, a stronger BF was observed in the CL group when compared to the UCLP and BCLP groups. Next, no differences were observed between the cleft side and the noncleft side in the UCLP group. Lastly, in all groups, BFs from the anterior region of the maxilla were less when compared to the posterior regions. Conclusion: The BF of children with CLP is no different from children without CLP. ã 2016 Elsevier Ltd. All rights reserved.
Keywords: Cleft lip Cleft palate Bite force Child
1. Introduction Cleft lip and palate (CLP) is the most prevalent congenital malformation that affects the stomatognathic system and is characterized by a complete segmentation of the maxilla, leading to maxillary hypoplasia and sagittal and transverse maxillomandibular discrepancies. It is speculated that these changes have a negative effect on the stomatognathic system of such individuals (Trindade-Suedam et al., 2012). Among the main parameters indicative of the stomatognathic system functionality is the quantification of bite force (BF), an
* Corresponding author. Hospital for Rehabilitation of Craniofacial Anomalies, University of São Paulo, Rua Dr. Silvio Marchione 3-20, 17012-900, Bauru, SP, Brazil. E-mail addresses: [email protected], [email protected] (I.K. Trindade-Suedam) . http://dx.doi.org/10.1016/j.archoralbio.2016.03.019 0003-9969/ ã 2016 Elsevier Ltd. All rights reserved.
important method for measuring the masticatory function, as a quantitative indicator (N) of masticatory performance (van der Bilt, Tekamp, van der Glas, & Abbink, 2008). BF is directly related to certain conditions such as craniofacial morphology, occlusal pattern, gender, age (Sun et al., 2015), periodontal status, number of teeth present or even to the type of dental prosthesis in use (Boven, Raghoebar, Vissink, & Meijer, 2014; Hatch, Shinkai, Sakai, Rugh, & Paunovich, 2001; Suzuki, Taniguchi, & Ohyama, 1995). Clinically, BF is a parameter indicative of therapeutic success in dental rehabilitation procedures such as orthognathic surgery or oral rehabilitation with dental implants (Rismanchian, Bajoghli, Mostajeran, Fazel, & Eshkevari, 2009). For example, when oral rehabilitated patients present similar BFs when compared to healthy individuals, the rehabilitation process can be considered successful. Previous research conducted in our laboratory (Sipert, Sampaio, Trindade, & Trindade, 2009) has shown that BF is significantly
84
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reduced in male subjects with CLP when compared to noncleft individuals. However, important variables such as age and the execution of the alveolar bone grafting surgery, which unifies the maxilla into one structure, were not controlled. Notably, studies assessing BF in children with CLP, especially in bilateral cases (which represent the most severe type of cleft) were absent in the literature. Considering that the segmentation of the maxilla might be a limiting factor of the stomatognathic system function in subjects with CLP, the objective of this study was to quantify the BF of children with different types of CLP without alveolar bone grafting, from the Hospital for Rehabilitation of Craniofacial Anomalies at the University of São Paulo (HRAC/USP), Bauru, SP, Brazil. It was hypothesized that children with clefts, independent of cleft type, would have lower bite force values when compared to children without clefts. 2. Material and methods This study was approved by the Institutional Ethics Review Board of the HRAC/USP, (process number 768.103), according to Resolution 466/12 of the National Health Council. All participants and their legal guardians were informed about the procedures involved in the study and signed an informed consent form before examinations. Considering an alpha error of 5%, a beta error of 20%, and adopting an expected standard deviation of 3 kgf and significant difference between groups of at least 5 kgf (Palinkas et al., 2010), an estimated sample size of 10 subjects per group was obtained. Inclusion criteria were the following: children without CLP, children with nonsyndromic unilateral or bilateral CLP, unilateral cleft lip, cleft palate, children in the mixed dentition phase, children without tooth decay and periodontal disease, and children having interocclusal molar relation. Exclusion criteria were the following: pain or discomfort during the exam, Angle class II and III malocclusions, presence of large restorations or endodontic treatment, tooth loss, inability to understand orientations during the exam, alveolar bone grafting and children with systemic diseases. Briefly, 150 children, from both genders, aged 6–12 years, with and without CLP, were divided into the following 5 groups: (1) control group (CON): 34 children without CLP (17 female, 17 male, mean age 8.2 1.4); (2) cleft lip group (CL): 31 children with cleft lip involving the pre-maxilla (15 female, 16 male, mean age 9.7 1.3); (3) unilateral CLP group (UCLP): 36 children with complete unilateral CLP (11 female, 25 male, mean age 9.4 1.6); (4) bilateral CLP group (BCLP): 32 children with complete bilateral CLP (11 female, 21 male, mean age 9.5 1.7); and (5) cleft palate group (CP): 17 children with complete cleft palate (9 female, 8 male, mean age 9.4 1.6). Children from the cleft groups were regularly registered at a tertiary hospital specialized in the treatment of cleft lip and palate patients (Hospital for Rehabilitation of Craniofacial Anomalies, University of São Paulo, Brazil). In turn, children from the control group were from the Pediatric Dentistry Clinic, Bauru School of Dentistry, University of São Paulo, Brazil. In this clinical trial, children were submitted to a BF exam using a gnathodynamometer (digital dynamometer, IDDK model, Kratos, Bauru, SP, Brazil) with a capacity of 100 kgf (980 N) (Fig. 1). This gnathodynamometer is composed of a stainless steel cylinder (10 10 mm) which contains a load cell that measures force when deformed. Measurements were performed 3 times with an interval of about 1 min between measurements to avoid fatigue (Roldán, Buschang, Saldarriaga Isaza, & Throckmorton, 2009; Roldán, Restrepo, Isaza, Vélez, & Buschang, 2015), been this lapse of time sufficient to avoid fatigue (Roldán et al., 2009). For the CON, BCLP,
Fig. 1. Gnathodynamometer used to perform the measurements (digital dynamometer, IDDK model, Kratos, Bauru, SP, Brazil).
Fig. 2. Location of measurements for the UCLP group: central incisors (anterior region of the maxilla).
CL and CP groups, BF was obtained in the anterior and posterior region of the maxilla. For the UCLP group, BF was assessed in the anterior (Fig. 2 and 3) and posterior regions of both segments (Fig. 4). The locations of the measurements are illustrated in Fig. 5. Importantly, every child was naïve to the BF exam and was given the same detailed instruction and amount of practice using the apparatus.
M.A. Garcia et al. / Archives of Oral Biology 68 (2016) 83–87
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Table 1 Demographic distribution of the study population. GENDER (%)
CON (n = 34) CL (n = 31) UCLP (n = 36) BCLP (n = 32) CP (n = 17)
AGE (mean SD)
F
M
17 (50) 15 (48) 11 (31) 11 (34) 9 (53)
17 (50) 16 (52) 25 (69) 21 (66) 8 (47)
8.2 1.4 9.7 1.3 9.4 1.6 9.5 1.7 9.4 1.6
CON: control group; CL: cleft lip group; UCLP: cleft lip and palate group; BCLP: bilateral cleft lip and palate group; CP: cleft palate group.
3. Results
Fig. 3. Location of measurements for the UCLP group: tooth adjacent to the cleft (anterior region of the maxilla).
The distribution of the study population’s gender and age are shown on Table 1. The mean BF (N) from the 5 groups obtained for the anterior and posterior regions of the maxilla are reported in Table 2. In all groups, the mean BFs in the anterior region of the maxilla were significantly lower when compared to the BFs in the posterior regions. Surprisingly, no significant differences of BF were observed among CON and any of the cleft groups. However, significantly greater values of BF were observed for CL when compared to UCLP and to BCLP. Next, no differences were observed between the cleft side and the noncleft side in the UCLP and between the BF of males and females. A positive correlation was found between BF and age (r = 0.19), as illustrated in Fig. 6. 4. Discussion
Fig. 4. Location of measurements for the UCLP group: posterior region of the maxilla.
BF data was initially submitted to normality (KolmogorovSmirnov test) and homogeneity of variances (Levene’s test) tests and passed in both cases. Considering that BF was normally distributed, the results are expressed as means standard deviation. Significant differences among groups were evaluated using an ANOVA test with repeated measures (STATISTICA 10.0, Stat Soft. Inc., Tulsa, OK., USA). Next, Tukey’s test was used to assess any correlations among variables. Additionally, correlation of age and BF were assessed using a Pearson Correlation test. In all cases P < 0.05 were considered significant.
Surprisingly, the BF of the individuals with CLP was no different from individuals without CLP. Contrary to what was initially expected, the segmented maxilla does not impact BF, even before alveolar bone grafting which unifies the maxillary segments. To the best of our knowledge, there are no previous studies published that have assessed BF of individuals with CLP besides the study of Sipert et al. (2009). This study (Sipert et al., 2009) found that the BF of adults with CLP was significantly decreased when compared to the control group. However, an important variable, alveolar bone grafting, was not considered. Our current study further investigates BF but in children (6 to 12 years old) with unilateral and bilateral cleft lip and/or palate while excluding all individuals with alveolar bone grafting. When comparing only the cleft groups, it was observed that children from the CL group had a significantly stronger BF when compared to UCLP and to BCLP. This result might indicate that the presence of a segmented maxilla (UCLP and BCLP) negatively impacts BF. On the other hand, considering no differences of BF among children without CLP and with CLP were found, independent of the group, the authors attribute this difference between CL and UCLP/BCLP to random variability in the individuals tested. The authors also speculate that individuals from the CON group had
Fig. 5. Location of measurements according to the groups analyzed.
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Table 2 Mean values of bite force, expressed in N, from the control group (CON), cleft lip group (CL), cleft lip and palate group (UCLP), bilateral cleft lip and palate group (BCLP) and cleft palate group (CP), on the anterior and posterior regions of the maxilla. GROUP
Anterior mean (SD)
Posteriora mean (SD)
CONb CLb UCLP
90.2 (50.0) 132.4 (61.8) 87.3 (77.5) 103.0 (58.8) 88.3 (39.2) 103.0 (45.1)
301.1 (90.2) 346.2 (113.8) 259.9 (104.9)a 290.3 (98.1)a 251.2 (57.9)a 285.4 (117.7)
BCLPb CPb
cleft sideb non cleft sideb
Statistical test applied: “Repeated Measures Three Way ANOVA and Tukey’s test”. a indicates a significant difference from the CL group. b indicates a significant difference from anterior and posterior.
little experience with general dental exams whereas many individuals with clefts are accustomed to various clinical tests. Thus, naïve children in the control group might not have performed their absolute maximum BF when facing an unknown and potentially uncomfortable situation, while children in cleft groups, with perhaps more experience, might have used more force. The reasons for this lack of difference between the CON group and the CLP groups needs further elucidation. The BF of the CON group obtained in this study is similar to those presented by Marquezin et al. (2013) who showed BF of 302 N, in Brazilian children without CLP in the same age range. However, BF values of the CON group from the present study are considerably stronger, 301.1 90.2 N, than what was found in the study by Palinkas et al. (2010), 170 14 N, which assessed the BF of Brazilian children without CLP at a similar age range (7–12 years). The lack of consistency between our results and Palinkas’ are unclear and require further investigation. Independent of the groups tested, significantly stronger BF values were found in the posterior region of the maxilla when compared to the anterior region. This expected observation occurs because molars are designed to grind food, requiring a stronger force, while incisors tear, as demonstrated by Regalo et al. (2008). Notably, the acquisition of BF in the anterior region of the maxilla in the BCLP group is more difficult to accomplish when compared to the other regions tested. In particular, the pre-maxilla is a mobile structure linked to base of the cranium only by the volmer bone. Therefore, the exam may generate discomfort or even pain to the individual. Despite this fact, no differences were observed in the BF of the anterior region of the maxilla when comparing the BCLP group with any of the other groups. Also contrary to initial expectations, no significant differences of BF were observed between the cleft and noncleft sides in the
UCLP group, meaning that equivalent BFs are observed on both sides of the segmented maxilla. This contradicts the hypothesis that the side affected by the cleft would present a lower BF (Sipert et al., 2009). The authors believe that the muscles from the cleft side exhibit more intense contractions when compared to the contralateral side (noncleft side) in order to execute the same task force, resulting in equal forces. This mechanism requires further investigation by evaluating muscle activity on both sides of the maxilla (cleft and noncleft sides) with electromyography. Regarding gender, no differences were found in the BF of female and male subjects. It is hypothesized that, since the sample of the present study is composed of young children (6–12 y), factors that may influence force and muscle activity such as testosterone and estrogen are not yet significant factors. The lack of gender differences was also observed by Palinkas et al. (2010) who showed no statistical differences between the maximal BF of male and female children (7–12 y). In fact, these authors observed a difference between genders emerge as children aged. Moreover, groups composed of humans 21–60 y, have male BFs significantly stronger when compared to female BFs. Although not strong, a positive correlation was found between BF and age (r = 0.19). That is, as age increased so did BF regardless of group. The authors attribute two factors to this increase in BF as children get older—first because of the growth process per se (Mountain, Wood, & Toumba, 2011; Toro, Buschang, Throckmorton, & Roldan, 2006) and second because of the gradual alignment of the dental arch that occurs during the orthodontic treatment which allows an optimal dental occlusion for mastication, corrobotating previous studies, witch observed that the severity of malocclusion is related with bite forte magnitude (Araujo, Marquezin, Barbosa, Gavião, & Castelo, 2015). Ongoing orthodontic treatment, which can negatively influence BF, was a variable not controlled for in the present study. This dental procedure often increases oral sensitivity and can even lead to dental pain, reducing BF. Orthodontic treatment was frequently present in the CLP groups due to the malocclusions commonly observed on this population. For future studies, the assessment of muscle activity by means of electromyography is recommended. Using this technique, differences among groups will become evident. The assessment of BF in individuals already submitted to the alveolar bone grafting is another area that needs further investigation. This type of investigation might clarify the impact of maxilla unification on BF in these subjects. Despite the unexpected results, these findings provide a better understanding of the factors involved in the BF of subjects with cleft lip and palate. Finally, this anomaly does not influence BF and,
Fig. 6. Correlation graph between the variables bite force and age.
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consequently, does not bring significant consequences for the ability of this population to properly masticate. 5. Conclusion The results of this study indicate that the bite force of children with cleft lip and palate is no different from the bite force of children without this congenital anomaly. Conflict of interest The authors report no conflict of interest. Financial support Fundação CAPES (Coordination for the Improvement of Higher Education Personnel). References Araujo, D. S., Marquezin, M. C., Barbosa, T. S., Gavião, M. B., & Castelo, P. M. (2015). Evaluation of masticatory parameters in overweight and obese children. European Journal of Orthodontics Dec 14. pii: cjv092. [Epub ahead of print]. Boven, G. C., Raghoebar, G. M., Vissink, A., & Meijer, H. J. (2014). Improving masticatory performance, bite force, nutritional state and patient’s satisfaction with implant overdentures: a systematic review of the literature. Journal of Oral Rehabilitation, 42, 220–233. Hatch, J. P., Shinkai, R. S., Sakai, S., Rugh, J. D., & Paunovich, E. D. (2001). Determinants of masticatory performance in dentate adults. Archives of Oral Biology, 46, 641–648. Marquezin, M. C., Kobayashi, F. Y., Montes, A. B., Gavião, M. B., & Castelo, P. M. (2013). Assessment of masticatory performance, bite force, orthodontic treatment need
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