The development of an occlusion is the result of the

ONLINE ONLY Tongue movements in patients with skeletal Class II malocclusion evaluated with real-time balanced turbo field echo cine magnetic resonance imaging Fatih Yılmaz, a Deniz Sagdıç, b Şeniz Karaçay, c Erol Akin, d and Nail Bulakbası e Ankara and Istanbul, Turkey Introduction: The aim of this study was to evaluate the deglutitive tongue movements in patients with skeletal Class II malocclusion. Methods: Fifty-nine patients (26 male, 33 female) with skeletal Class II relationship were divided into 3 groups according to cephalometric analysis. Group 1 (n 5 19) had mandibular retrognathism, group 2 (n 5 20) had maxillary prognathism, and group 3 (n 5 20) had both mandibular retrognathism and maxillary prognathism. Twenty-two skeletal Class I patients (10 male, 12 female) were also included as the controls. Results: In the mandibular retrusion group, the posterior portion of the dorsal tongue moved downward at stage 2 and upward at stage 3; the root of the dorsal tongue was in an inferior and anterior position at stage 2. In patients with both mandibular retrognathism and maxillary prognathism, the middle portion of the dorsal tongue was positioned superiorly at stage 3 relative to stage 1; the tongue tip was retruded at stage 3 relative to stages 1 and 2. In the control group, the middle portion of dorsal tongue was positioned superiorly at stage 3 relative to stages 1 and 2; the posterior portion of the tongue moved upward at stage 2 and downward at stage 3, and tongue-tip retrusion was observed at stage 2 relative to stage 1. Contact of the anterior portion of the tongue with the rugae area of the hard palate decreased in the Class II malocclusion groups relative to the control group. The middle portion of the dorsal tongue was positioned more superiorly in patients with Class II malocclusion during all stages of deglutition. The root of the tongue was more inferior and anterior, and the tongue tip was retruded in patients with Class II malocclusion compared with the control group. The posterior portion of the dorsal tongue was more inferiorly positioned in patients with mandibular retrusion than in the other Class II groups or the controls. In the third stage of deglutition, this portion of the tongue had a superior position in groups 2 and 3 relative to the control group. Conclusions: Dentofacial morphology affects the position and movements of the tongue during deglutition, and adaptive changes occur in the tip, dorsum, and root of the tongue. Deglutitive tongue movements in patients with a skeletal Class II relationship are different from those with a skeletal Class I relationship. (Am J Orthod Dentofacial Orthop 2011;139:e415-e425) The development of an occlusion is the result of the interactions among the genetically developmental factors and a number of environmental factors, including the orofacial functions. 1 The environment of the a Associate professor, Department of Orthodontics, Center of Dental Sciences, Gulhane Military Medical Academy, Ankara, Turkey. b Professor, Department of Orthodontics, Center of Dental Sciences, Gulhane Military Medical Academy, Ankara, Turkey. c Associate professor, Dental Service, Haydarpasha Education Hospital, Gulhane Military Medical Academy, Istanbul, Turkey. d Associate professor, Medicana Dental Hospital, Istanbul, Turkey. e Associate professor, Department of Radiology, Gulhane Military Medical Academy, Ankara, Turkey. The authors report no commercial, proprietary, or financial interest in the products or companies described in this article. Reprint requests to: Şeniz Karaçay, Tıbbiye Caddesi, GATA Haydarpaşa Egitim Hastanesi, Diş Servisi, Ortodonti B ol um u, _Istanbul, Turkey; e-mail, kseniz@ yahoo.com. Submitted, November 2009; revised, January 2010; accepted, February 2010. 0889-5406/$36.00 Copyright Ó 2011 by the American Association of Orthodontists. doi:10.1016/j.ajodo.2010.02.031 teeth and alveolar bone includes conflicting forces and pressures, especially from muscular functions, which in part determine tooth positions. 1,2 The tongue is an organ that occupies a large portion of the oral cavity and performs complex movements during mastication, deglutition, and speech. It also plays important roles in the transport of bolus from the anterior oral cavity to the pharynx. There is debate over the role of the tongue in the development and morphology of the dental arches and dentofacial forms. 3-6 Many investigators have tried to find the relationship between size, posture, and function of the tongue with the surrounding oral cavity and dentofacial morphology. 6-9 The frequency of swallowing, the magnitude of the force exerted on the teeth, the counteraction of these forces by other muscular structures such as lips, the resistance of dentoalveolar structures to displacement, and the resting posture of the tongue when no e415

e416 Yılmaz et al swallowing is occurring are the important factors that might affect the relationship between tongue function and dentofacial form. 9 Melsen et al, 6 who evaluated the relationship between swallowing pattern and different malocclusion traits, reported that malocclusion frequency was higher among children swallowing without tooth contact, and the malocclusion traits most affected by the swallowing pattern were the sagittal discrepancies. They suggested 2 swallowing patterns and reported that a high position of the tongue favored spacing in the maxilla and increased overjet, whereas low tongue position favored spacing in the mandible and decreased overjet, creating a Class III tendency. In recent years, it has been suggested that there are correlations between deglutitive (swallowing) tongue movements and certain features of maxillofacial morphology. Ichiada et al, 10 who evaluated the relationship between the lingual-palatal contact duration associated with swallowing and maxillofacial morphology, reported that the patients with prolonged contact had tendencies for inclination of the maxillary incisors toward the lip, opening of the mandibular and occlusal planes, and posterior rotation of the mandible. Cheng et al 9 also showed significant correlations between the tongue movements during swallowing and dentofacial morphology. They reported that the movements of the tongue during swallowing are related to dentofacial morphology, especially in the motion magnitude of the early final phase. Fujiki et al 11 showed that patients with open bite had tonguetip protrusion, slower movement of the rear part of the dorsal tongue, and earlier closure of the nasopharynx during deglutition. In their subsequent study, they found significant correlations between mandibular plane angle, ramus height, or anteroposterior dimension of the maxilla and movement of the front part of the dorsal tongue during deglutition in the patients with anterior open bite. 12 Akin et al 13 also reported compensatory tongue functions in patients with anterior open bites. Gorgulu et al, 14 who evaluated the deglutitive tongue movements in patients with skeletal Class III malocclusion, reported a decreased contact of the anterior portion of the tongue with the rugae area of the hard palate in those with Class III malocclusions. They also showed that the posterior portion of the dorsal tongue was positioned more inferiorly, the root of the tongue was positioned more inferiorly and anteriorly, and the tongue tip was also positioned more anteriorly in patients with Class III malocclusions. Differences were also observed in the manner of bolus transfer. Linear motion of the tongue was observed in patients with Class III malocclusion, whereas a fluctuation motion of the tongue occurred in patients with Class I malocclusion. 14 As mentioned above, there have been many studies to determine the relationship among oral structures, types of malocclusion, and deglutition. These studies showed that the characteristic tongue movements during deglutition were closely related to the morphologic features of the subjects. The purpose of our study was to investigate tongue posture and tongue movements during 3 stages of deglutition in subjects with Class II malocclusion. Cinematic (cine) images of the tongue were obtained by using real-time balanced turbo field echo cine-magnetic resonance imaging (MRI), which was successfully used in our previous studies to observe deglutitive tongue movements. 13-17 To our knowledge, this technique has not been used before in the evaluation of swallowing patterns of patients with skeletal Class II malocclusion. MATERIAL AND METHODS This prospective study was carried out after institutional approval from the Ethics Committee of Gulhane Military Medical Academy in Ankara, Turkey. Eighty-one patients (45 male, 36 female) were included in the study, and informed consents were obtained from all participants. They were divided into 4 groups according to their skeletal relationships. Skeletal classification was made by the evaluation of the sagittal components of the jaws on the cephalometric radiographs, and it was based on the SNA, SNB, and ANB angles, and N vertical-a and N vertical-pg linear measurements. Nineteen skeletal Class II patients (5 boys, 14 girls; mean age, 14.05 6 1.87 years) with mandibular retrognathism (ANB,.4 ; SNB, \78 ; N vertical- Pg, \ 6 mm) were included in the first group. In the second group, there were 20 skeletal Class II patients (9 boys, 11 girls; mean age, 14.20 6 1.39 years) with maxillary prognathism (ANB,.4 ; SNA,.84 ; N vertical-a,.2 mm). The third group comprised 20 skeletal Class II patients (12 boys, 8 girls; mean age, 14.15 6 2.05 years) with both mandibular retrognathism and maxillary prognathism (ANB,.4 ; SNA,.84 ; SNB, \78 ; N vertical-a,.2 mm; N vertical-pg, \ 6 mm). Finally, 22 subjects (10 male, 12 female; mean age 18.26 6 5.22 years) with skeletal Class I relationship (ANB, 2 6 2 ; SNA, 82 6 2 ; SNB, 80 6 2 ;N vertical-a, 0 6 1 mm; N vertical-pg, 6 6 1 mm) composed the control group. The values of the measured cephalometric parameters and the mean ages of the groups are given in Table I. All patients were examined with a 1.5-T super conducting magnetic resonance scanner with a quad H coil and version 9 software (New Intera Nova, Philips Medical Systems, Best, The Netherlands). Real-time balanced turbo field echo images (shortest TR/TE:2.1/1.09 ms) May 2011 Vol 139 Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics

Yılmaz et al e417 Table I. ages of the groups and the measured cephalometric parameters age (y) SNA ( ) SNB ( ) ANB ( ) N vertical-a (mm) N vertical-pg (mm) SD SD SD SD SD SD Group 1 14.05 1.87 78.42 2.54 72.21 2.55 6.21 0.41 4.18 2.46 12.10 4.62 Group 2 14.20 1.39 86.45 1.39 79.85 1.18 6.60 0.99 4.35 1.30 5.00 1.62 Group 3 14.15 2.05 84.45 0.99 76.70 1.45 7.75 1.25 3.30 1.08 9.55 1.70 All Class II groups 14.13 1.77 83.10 1.64 76.25 1.72 6.85 0.88 1.15 1.61 8.88 2.64 Group 4 18.26 5.22 81.27 1.01 79.36 1.12 1.91 0.83 0.10 1.30 6.73 2.05 Fig 1. A, The oral stage begins when the contact of the tongue s dorsum with the soft palate is lost (1). Tongue (white arrowhead), oropharynx (black arrow), and soft palate (white arrow) are shown. B, The pharyngeal stage begins when the water head passes across the posterior or inferior margin of the ramus (2). Pharyngeal wall (thin, white arrowhead), closure of larynx (bold white arrow), elevation of hyoid (thin white arrow), and opening of esophagus (white triangle) are marked. C, The esophageal stage begins when the water head passes through the opening of the esophagus (3). Opening of the upper esophageal sphincter is shown (white arrow). were taken with a 50 flip angle in the midsagittal plane, 10 mm thickness, 350 3 350 mm field of view dimensions, and 96 3 96 matrix width during the patient swater swallowing. A hundred dynamic scans were captured in 11 seconds. The images were obtained while the subjects were swallowing 10 ml of water that was taken with a syringe just before imaging. For each patient, images matching the following 3 stages were determined by a consensus of 3 specialists and printed out on a radiograph: stage 1 (oral): loss of contact of the dorsal tongue with the soft palate (Fig 1, A); stage 2 (pharyngeal): passage of the bolus head across the posterior or inferior margin of the ramus of the mandible (Fig 1, B); and stage 3 (esophageal): passage of the bolus head through the opening of the esophagus (Fig 1, C). Linear measurements defined by Fujiki et al 11 were made on these radiographs for each stage by 1 author (F.Y.) to prevent interobserver variability. Reference points and planes are shown in Table II. Since AM-E and AM-PM are distances on the palatal mucosa, they were curved lines. A ligature wire was used for the measurement of these parameters. MM-MT, MM-MS, PM-PT, PM-PS, C1-D, C1-Me, and PS-I are straight distances. P 0 -Ti is the shortest distance from a line crossing at a right angle to the NF plane through PNS to Ti (Fig 2). Magnetic resonance analyses of the groups are presented in Table III. The points and measurements of 25 patients were reevaluated 1 month later, and the method error was determined by using Dahlberg s formula: method qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi P error 5 d 2 =2n, where n is the number of subjects and d is the between the 2 measurements of a pair. 18 The method error did not exceed 0.135 mm. All statistical analyses of the groups were performed with the Statistical Package for Social Sciences for Windows software (version 15, SPSS, Chicago, Ill). The American Journal of Orthodontics and Dentofacial Orthopedics May 2011 Vol 139 Issue 5

e418 Yılmaz et al Table II. Reference points and planes used in study ANS Most anterior point of the maxilla at the level of the palate PNS Most posterior point on the bony hard palate Me Lowest point on the symphyseal outline of the chin I Edge point of the maxillary incisor C1 Front-most point of the atlas NF Plane through both ANS and PNS SP Plane passing the edge of the maxillary incisor and parallel to the palatal plane AM Boundary point between the maxillary central incisor and the palatal mucosa E Point nearest the tongue base in the contact region between the tongue and the palatal mucosa MM Point at which the line crossing at a right angle to NF through the middle point between ANS and PNS intersects the palatal mucosa MT Point at which the line crossing at a right angle to NF through the middle point between ANS and PNS intersects the dorsum of the tongue MS Point at which the line crossing at a right angle to NF through the middle point between ANS and PNS intersects SP PM Point at which the line crossing at a right angle to NF through PNS intersects the palatal mucosa PT Point at which the line crossing at a right angle to NF through PNS intersects the dorsum of tongue PS Point at which the line crossing at a right angle to NF through PNS intersects SP D Point at which the line through Me and C1 intersects the dorsum of the tongue Ti Tongue tip Fig 2. Linear measurements on MRI: (a), contact of tongue and palate (distances on the palatal mucosa) (AM-E/AM-PM); (b) middle portion of the dorsal tongue (straight distance) (MM-MT/MM-MS); (c) posterior portion of the dorsal tongue (straight distance) (PM-PT/PM-PS); (d) root of the dorsal tongue (straight distance) (C1-D/C1-Me); (e), tongue tip (shortest distance from the line crossing at a right angle to the NF plane through PNS to Ti) (P 0 -Ti/P 0 -I). 11,12 s between repeated measurements were evaluated by analysis of variance (ANOVA) for repeated measurements. Bonferroni tests were used as post-hoc tests. To analyze the s within the groups, the paired sample t test was used, and P #0.05 was accepted as the level of significant. In the comparison of the Class II groups with the control group, the Dunnett test was used. RESULTS The stages were compared within the groups. In the mandibular retrusion group (group 1) (Table IV), evaluation of the posterior portion of the dorsal tongue (PM- PT/PM-PS) showed a statistically significant increase between stages 1 and 2 (P\0.01) and a statistically significant decrease between stages 2 and 3 (P \0.01). These alterations showed that this portion of the tongue moved downward at stage 2 and upward at stage 3. The root of the dorsal tongue (C1-D/C1-Me) showed a significant increase between stages 1 and 2 (P\0.05) because of the inferior and anterior position of the root of the tongue at stage 2 relative to stage 1. Alterations in the contact of the anterior part of the tongue (AM-E/AM-PM) and the movements of the middle portion of the dorsal tongue (MM-MT/MM-MS) and the tongue tip (P 0 -Ti/P 0 -I) were statistically insignificant. In the maxillary protrusion group (group 2) (Table V), no parameter showed a statistically significant alteration. In the mandibular retrognathism and maxillary prognathism group (group 3) (Table VI), the distance between the middle portion of the dorsal tongue and the palatal mucosa (MM-MT/MM-MS) was significantly smaller at May 2011 Vol 139 Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics

Yılmaz et al e419 Table III. Magnetic resonance measurements of the groups Group 1 Group 2 Group 3 Group 4 (mm/mm) SD (mm/mm) SD (mm/mm) SD (mm/mm) SD Stage 1 Anterior contact 0.158 0.155 0.095 0.082 0.095 0.055 0.266 0.057 Middle part 0.365 0.188 0.301 0.169 0.358 0.147 0.607 0.157 Posterior part 0.299 0.106 0.263 0.183 0.348 0.146 0.308 0.080 Root of tongue 0.385 0.061 0.407 0.056 0.402 0.039 0.215 0.060 Tip of tongue 0.708 0.139 0.775 0.127 0.675 0.207 0.945 0.120 Stage 2 Anterior contact 0.123 0.136 0.078 0.063 0.137 0.141 0.297 0.070 Middle part 0.337 0.153 0.222 0.106 0.323 0.184 0.663 0.153 Posterior part 0.473 0.163 0.276 0.138 0.340 0.169 0.239 0.100 Root of tongue 0.445 0.087 0.419 0.104 0.423 0.042 0.186 0.053 Tip of tongue 0.780 0.142 0.753 0.197 0.755 0.094 0.850 0.125 Stage 3 Anterior contact 0.086 0.039 0.084 0.062 0.081 0.045 0.271 0.051 Middle part 0.275 0.092 0.227 0.140 0.225 0.073 0.403 0.219 Posterior part 0.295 0.167 0.200 0.102 0.256 0.073 0.382 0.153 Root of tongue 0.437 0.070 0.432 0.041 0.428 0.041 0.223 0.073 Tip of tongue 0.773 0.077 0.773 0.068 0.799 0.093 0.904 0.147 Table IV. Comparison of the stages in group 1 Group 1 Stages Anterior contact 1-2 0.035 0.039 1.000 1-3 0.072 0.039 0.216 2-3 0.037 0.039 1.000 Middle part 1-2 0.028 0.049 1.000 1-3 0.089 0.049 0.214 2-3 0.062 0.049 0.632 Posterior part 1-2 0.174 0.048 0.002 y 1-3 0.004 0.048 1.000 2-3 0.177 0.048 0.002 y Root of tongue 1-2 0.060 0.024 0.045* 1-3 0.053 0.024 0.096 2-3 0.007 0.024 1.000 Tip of tongue 1-2 0.071 0.040 0.242 1-3 0.065 0.040 0.331 2-3 0.006 0.040 1.000 Table V. Comparison of the stages in group 2 Group 2 Stages Anterior contact 1-2 0.017 0.022 1.000 1-3 0.011 0.022 1.000 2-3 0.006 0.022 1.000 Middle part 1-2 0.079 0.044 0.243 1-3 0.074 0.044 0.311 2-3 0.005 0.044 1.000 Posterior part 1-2 0.014 0.046 1.000 1-3 0.063 0.046 0.521 2-3 0.077 0.046 0.299 Root of tongue 1-2 0.012 0.023 1.000 1-3 0.025 0.023 0.830 2-3 0.013 0.023 1.000 Tip of tongue 1-2 0.023 0.045 1.000 1-3 0.002 0.045 1.000 2-3 0.021 0.045 1.000 *P \0.05; y P \0.01. stage 3 than at stage 1 (P\0.05), showing that this portion of the tongue was positioned superiorly at stage 3 relative to stage 1. Evaluation of the tongue tip (P 0 -Ti/ P 0 -I) showed that it was retruded at stage 3 relative to stages 1 and 2 (P \0.001). Alterations in the contact of the anterior part of the tongue (AM-E/AM-PM) and the movements of the posterior portion (PM-PT/PM-PS) and the root of the dorsal tongue (C1-D/C1-Me) were statistically insignificant. In the control group (group 4) (Table VII), the distance between the middle portion of the dorsal tongue and the palatal mucosa (MM-MT/MM-MS) was significantly smaller at stage 3 than at stages 1 and 2 (P \0.001), showing that this portion of the tongue was positioned superiorly in stage 3 relative to stages 1 and 2. In the evaluation of the posterior portion of the dorsal tongue (PM-PT/PM-PS), a statistically significant increase was determined at stage 2 relative to stage 1 (P\0.05), and a statistically significant decrease was determined at stage 3 relative to stage 2 (P\0.001). These alterations showed that the posterior portion of the tongue moved upward at stage 2 and downward at stage 3. Evaluation of the tongue tip (P 0 -Ti/P 0 -I) showed a statistically significant decrease at stage 2 relative to stage 1 American Journal of Orthodontics and Dentofacial Orthopedics May 2011 Vol 139 Issue 5

e420 Yılmaz et al Table VI. Comparison of the stages in group 3 Group 3 Stages Anterior contact 1-2 0.042 0.029 0.451 1-3 0.014 0.029 1.000 2-3 0.056 0.029 0.171 Middle part 1-2 0.035 0.045 1.000 1-3 0.133 0.045 0.014* 2-3 0.098 0.045 0.104 Posterior part 1-2 0.008 0.043 1.000 1-3 0.092 0.043 0.109 2-3 0.084 0.043 0.166 Root of tongue 1-2 0.021 0.013 0.317 1-3 0.026 0.013 0.152 2-3 0.005 0.013 1.000 Tip of tongue 1-2 0.080 0.044 0.217 1-3 0.419 0.044 0.000 y 2-3 0.499 0.044 0.000 y Table VIII. Comparison of the groups in stage 1 Stage 1 Groups Anterior contact 1-2 0.0629 0.0302 0.2446 1-3 0.0634 0.0302 0.2354 2-3 0.0005 0.0298 1.0000 Middle part 1-2 0.0642 0.0530 1.0000 1-3 0.0072 0.0530 1.0000 2-3 0.0570 0.0523 1.0000 Posterior part 1-2 0.0364 0.0428 1.0000 1-3 0.0486 0.0428 1.0000 2-3 0.0850 0.0423 0.2874 Root of tongue 1-2 0.0223 0.0175 1.0000 1-3 0.0173 0.0175 1.0000 2-3 0.0050 0.0173 1.0000 Tip of tongue 1-2 0.0666 0.0486 1.0000 1-3 0.0339 0.0486 1.0000 2-3 0.1005 0.0480 0.2368 *P \0.05; y P \0.001. Table VII. Comparison of the stages in group 4 Group 4 Stages Anterior contact 1-2 0.031 0.019 0.120 1-3 0.005 0.018 0.770 2-3 0.026 0.018 0.177 Middle part 1-2 0.056 0.052 0.294 1-3 0.204 0.046 0.000 y 2-3 0.260 0.058 0.000 y Posterior part 1-2 0.069 0.024 0.010* 1-3 0.074 0.037 0.057 2-3 0.142 0.034 0.000 y Root of tongue 1-2 0.029 0.018 0.116 1-3 0.008 0.020 0.698 2-3 0.037 0.018 0.051 Tip of tongue 1-2 0.095 0.035 0.013* 1-3 0.041 0.045 0.371 2-3 0.054 0.045 0.243 *P \0.05; y P \0.001. Table IX. Comparison of the groups in stage 2 Stage 2 Groups Anterior contact 1-2 0.0452 0.0344 1.0000 1-3 0.0133 0.0344 1.0000 2-3 0.0585 0.0340 0.5336 Middle part 1-2 0.1153 0.0486 0.1212 1-3 0.0143 0.0486 1.0000 2-3 0.1010 0.0480 0.2318 Posterior part 1-2 0.1966 0.0461 0.0003 y 1-3 0.1331 0.0461 0.0300* 2-3 0.0635 0.0455 0.9997 Root of tongue 1-2 0.0257 0.0241 1.0000 1-3 0.0217 0.0241 1.0000 2-3 0.0040 0.0238 1.0000 Tip of tongue 1-2 0.0270 0.0462 1.0000 1-3 0.0250 0.0462 1.0000 2-3 0.0020 0.0456 1.0000 *P \0.05; y P \0.001. (P \0.001) because of the retrusion of the tongue tip at stage 2. Alterations in the contact of the anterior part of the tongue (AM-E/AM-PM) and the movements of the root of the dorsal tongue (C1-D/C1-Me) were statistically insignificant. The stages were also compared between the groups. In stage 1 (Tables VIII and XI), no parameter had a statistically significant in the comparison of the Class II groups (groups 1, 2, and 3). However some s were determined in the comparison of the Class II groups with the control group (group 4). When the degree of contact between the anterior portion of the tongue and palate (AM-E/AM-PM) was compared between the groups, it was observed that there was a statistically significant decrease in all Class II groups relative to the control group (P \0.001). In the comparison of the distance between the middle portion of the dorsal tongue and the palatal mucosa (MM-MT/MM-MS), a statistically significant increase was found in all Class II groups relative to the control group (P \0.001). This increase showed the inferior positioning of the middle portion of the tongue in the patients with Class II malocclusion. However, no May 2011 Vol 139 Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics

Yılmaz et al e421 Table X. Comparison of the groups in stage 3 Stage 3 Groups Anterior contact 1-2 0.0018 0.0160 1.0000 1-3 0.0053 0.0160 1.0000 2-3 0.0035 0.0158 1.0000 Middle part 1-2 0.0483 0.0467 1.0000 1-3 0.0503 0.0467 1.0000 2-3 0.0020 0.0461 1.0000 Posterior part 1-2 0.0958 0.0415 0.1416 1-3 0.0398 0.0415 1.0000 2-3 0.0560 0.0409 1.0000 Root of tongue 1-2 0.0054 0.0187 1.0000 1-3 0.0099 0.0187 1.0000 2-3 0.0045 0.0185 1.0000 Tip of tongue 1-2 0.0002 0.0329 1.0000 1-3 0.0258 0.0329 1.0000 2-3 0.0260 0.0325 1.0000 statistically significant alteration was observed in the position of the posterior portion of the dorsal tongue (PM-PT/PM-PS). Evaluation of the root of the dorsal tongue (C1-D/ C1-Me) showed that the distance between the root of the tongue and the front point of the atlas increased significantly in all Class II groups relative to the control group (P \0.001). This increase was due to the inferior and anterior position of the root of the tongue in patients with Class II malocclusion. The tongue-tip (P 0 -Ti/P 0 -I) evaluation showed statistically significant decreases in all Class II groups relative to the control group (P \0.001). This decrease showed the retrusion of the tongue tip in patients with Class II malocclusion. In stage 2 (Tables IX and XI), the degree of contact between the anterior portion of the tongue and palate, and the position of the middle portion and the root of the dorsal tongue showed the same alterations as at stage 1, and these parameters (AM-E/AM-PM, MM-MT/ MM-MS, C1-D/C1-Me) were statistically significant in the comparison of the Class II groups (groups 1, 2, and 3) with the control group (group 4) (P \0.001). When the position of the posterior portion of the dorsal tongue (PM-PT/PM-PS) was compared between the groups, statistically significant increases were determined in the mandibular retrusion group (group 1) relative to group 2 (P \0.001), group 3 (P \0.05), and group 4 (P \0.001). These decreases showed that the posterior portion of the dorsal tongue was positioned more inferiorly in patients with mandibular retrusion. Evaluation of the tongue tip (P 0 -Ti/P 0 -I) showed retrusion in all Class II groups relative to the control group, but, contrary to stage 1, it was not statistically significant at stage 2. Table XI. Comparison of the Class II groups with the control group Groups Stage 1 Anterior contact 1-4 0.11 0.03 0.00 z 2-4 0.17 0.03 0.00 z 3-4 0.17 0.03 0.00 z Middle part 1-4 0.24 0.05 0.00 z 2-4 0.31 0.05 0.00 z 3-4 0.25 0.05 0.00 z Posterior part 1-4 0.01 0.04 0.99 2-4 0.05 0.04 0.56 3-4 0.04 0.04 0.66 Root of tongue 1-4 0.17 0.02 0.00 z 2-4 0.19 0.02 0.00 z 3-4 0.19 0.02 0.00 z Tip of tongue 1-4 0.24 0.05 0.00 z 2-4 0.17 0.05 0.00 z 3-4 0.27 0.05 0.00 z Stage 2 Anterior contact 1-4 0.24 0.05 0.00 z 2-4 0.17 0.05 0.00 z 3-4 0.27 0.05 0.00 z Middle part 1-4 0.33 0.05 0.00 z 2-4 0.44 0.05 0.00 z 3-4 0.34 0.05 0.00 z Posterior part 1-4 0.23 0.05 0.00 z 2-4 0.04 0.04 0.75 3-4 0.10 0.04 0.07 Root of tongue 1-4 0.26 0.02 0.00 z 2-4 0.23 0.02 0.00 z 3-4 0.24 0.02 0.00 z Tip of tongue 1-4 0.07 0.05 0.29 2-4 0.10 0.04 0.08 3-4 0.10 0.04 0.09 Stage 3 Anterior contact 1-4 0.19 0.02 0.00 z 2-4 0.19 0.02 0.00 z 3-4 0.19 0.02 0.00 z Middle part 1-4 0.13 0.05 0.02* 2-4 0.18 0.05 0.00 z 3-4 0.18 0.05 0.00 z Posterior part 1-4 0.09 0.04 0.09 2-4 0.18 0.04 0.00 z 3-4 0.13 0.04 0.01 y Root of tongue 1-4 0.21 0.02 0.00 z 2-4 0.21 0.02 0.00 z 3-4 0.20 0.02 0.00 z Tip of tongue 1-4 0.13 0.03 0.00 z 2-4 0.13 0.03 0.00 z 3-4 0.11 0.03 0.00 z *P \0.05; y P \0.01; z P \0.001. In stage 3 (Tables X and XI), the degree of contact between the anterior portion of the tongue and the palate, the position of the middle portion and the root of the dorsal tongue, and the tongue tip showed the American Journal of Orthodontics and Dentofacial Orthopedics May 2011 Vol 139 Issue 5

e422 Yılmaz et al Fig 3. Graphics showing the anterior contact of tongue and palate (mm/mm). Fig 5. Graphics showing the posterior portion of the dorsal tongue (mm/mm). Fig 4. Graphics showing the middle portion of the dorsal tongue (mm/mm). same alterations as at stage 1, and these parameters (AM-E/AM-PM, MM-MT/MM-MS, C1-D/C1-Me, P 0 -Ti/ P 0 -I) were statistically significant in the comparison of the Class II groups with the control group (group 4). Evaluation of the position of the posterior portion of the dorsal tongue (PM-PT/PM-PS) showed that it was positioned superiorly in groups 2 and 3 in the comparison with the control group (P \0.001 and P \0.01, respectively). The same alteration was also observed at group 1, but it was statistically insignificant. Graphics of all measurements are presented in Figures 3-7. DISCUSSION Deglutition is a complex action involving multiple anatomic structures in the oral cavity, pharynx, larynx, and esophagus. During normal swallowing, the tongue tip rests on the lingual part of the dentoalveolar area, and the middle portion of the tongue elevates from front to back. In recent years, some investigators suggested that there are correlations between deglutitive tongue movements and maxillofacial morphology. 9,10,12 Posture and function of the tongue have been found to be significantly correlated with jaw relationship, abnormality of the dental arch form, and Fig 6. Graphics showing the root of the dorsal tongue. abnormal tooth positions. Tongue movements in deglutition immediately adapt to changes in the local environment. 17 In recent years, the movements of the anatomic structures that participate in deglutition have been investigated by several methods: ultrasonography, 9 electropalatography, 10 cineradiography, 11 electromyography, 19 and electromagnetic articulography. 20 However, all these techniques have various disadvantages, such as radiation exposure, the risk of aspiration of barium, and indirect visualization of the involved structures. 11,12,21 Dynamic MRI is a noninvasive method that has recently become available in the evaluation of deglutition. New developments in MRI techniques made it possible to provide dynamic images in cine- MRI that produces a series of anatomic images with periodic motion. Recently, dynamic MRI has been used to evaluate tongue movements and the anatomic structures involved in deglutition, 13-17 vocal fold motion, 22 pharyngeal airway space, 23,24 and laryngeal and tracheal motion during breathing 25 ; this technique has the advantages of noninvasiveness, absence of ionizing radiation exposure, and the capability of imaging softtissue anatomy during motion. On the other hand, Anagnostara et al 26 reported that this technique has limited utility as a diagnostic tool for deglutition studies under May 2011 Vol 139 Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics

Yılmaz et al e423 Fig 7. Graphics showing the tongue tip (mm/mm). physiologic conditions because the examination is performed while the subjects are in a supine position. However, since all the subjects were in a supine position during the examinations, the comparison of the selected groups is convenient with this technique. 13,14,17 In the studies of Fujiki et al, 11,12 the swallowing events were recorded 3 times, but, in our study, because of the high cost of the technique, only 1 scan was performed. The patients supine position and the high cost of the technique are the disadvantages of cine MRI. Dynamic images of anatomic structures involved in deglutition can be obtained by using fast scan techniques such as echo-planar imaging or fast gradient echo techniques such as fast low-angle shot, fast field echo, or turbo field echo. Anagnostara et al 26 compared these sequences and reported that the turbo field echo sequence provided the best temporal resolution and was optimal for the investigation of swallowing function. In our study, the turbo field echo sequence was performed. In many studies, it has been suggested that tongue movements during deglutition might be related to the maxillofacial morphology of the patients. In our study, the patients with Class II skeletal malocclusion were divided into 3 groups after evaluation of the SNA, SNB, and ANB angles, and N vertical-a and N vertical-pg linear measurements to determine the source of the skeletal malocclusion. Not only the relationship between the maxilla and the mandible, but also the relationship between the jaws and the anterior cranial base were considered while the groups of skeletal Class II malocclusion were being created. Evaluation of the contact between the anterior portion of the tongue and the rugae area of the hard palate showed a significant decrease in all Class II malocclusion groups relative to the control group. Similar results were also found in the patients with Class III malocclusion in our preceding study. 14 Therefore, the results of these 2 studies suggest that increased or decreased overjet decreases the contact between the anterior portion of the tongue and the rugae area of the hard palate because, in both of these conditions, it was difficult to seal off the front of the mouth during swallowing. Lips make contact to provide the seal in the anterior region of the mouth in patients with normal overjet. Nevertheless, this physiologic seal is usually provided by tongue-lipmaxillary incisor contact in subjects with Class II or Class III malocclusion; in this situation, the contact between the anterior portion of the tongue and the rugae area of the hard palate decreases. Supporting our results, Subtelny and Subtelny 27 also reported that subjects with maxillary protrusion, maxillary deficiency, and open bite had difficulties in attaining an anterior seal, and these patients used the anterior portion of their tongue to close the anterior opening. In all Class II malocclusion groups, the middle portion of the dorsal tongue was positioned more superiorly in all deglutition stages relative to the control group. The result conflicted with the results of our previous studies that evaluated tongue movements in patients with open bite and Class III malocclusion. 13,14 In these studies, the middle portion of the dorsal tongue did not show any significant in the comparison with the control group. However, this study showed that Class II malocclusion affected the movements of the middle portion of the tongue during deglutition. In our opinion, it depended on the retrusion of the tongue tip and the decreased contact of the anterior portion of tongue and the rugae area of the hard palate. This contact also decreased in patients with Class III malocclusion, but the position of the middle portion was not affected in these patients, probably depending on the anterior positioning of the tongue tip in patients with a Class III skeletal relationship. 14 Akin et al 13 reported that, in patients with open bite, the contact of the anterior portion of the tongue and the rugae area of the hard palate showed no statistically significant, but the middle portion of the tongue was lower, and the tongue tip moved anteriorly. In the light of these findings, it can be concluded that the position of the tongue tip and the anterior and middle portions of the tongue affected the movements of each other during deglutition. The posterior portion of the dorsal tongue did not show significant s at stage 1, but, at stage 2, it was positioned more inferiorly in patients with mandibular retrusion (group 1) relative to the other 3 groups. At stage 3, this portion was positioned superiorly in patients with Class II malocclusion relative to the control group. However, it was not statistically significant in patients with mandibular retrusion. In this group, inferior positioning of the posterior portion of the dorsal tongue at stage 2 decreased the elevation of this portion American Journal of Orthodontics and Dentofacial Orthopedics May 2011 Vol 139 Issue 5

e424 Yılmaz et al at stage 3. In patients with Class III malocclusion, the posterior portion of the tongue was positioned more inferiorly in all Class III groups relative to the control group. 14 These results show that dentofacial morphology affects the movements of the posterior portion of the tongue during deglutition. In the evaluation of tongue movements relative to the deglutition stages, it was determined that the posterior portion of the dorsal tongue moved inferiorly at stage 2 and superiorly at stage 3 in patients with mandibular retrusion. However, in the control group, it moved superiorly at the second stage and inferiorly at the third stage in the control group. During bolus transfer, a fluctuation motion was determined at the posterior portion of the dorsal tongue in these 2 groups, but the directions of the motions were opposite. The motions in groups 2 and 3 were not significant. Fujiki et al 11 also reported fluctuation movements in patients with open bite and normal overbite. This is a physiologic function of the tongue for the transportation of the bolus. Evaluation of the root of the tongue showed that it was positioned more inferiorly and anteriorly in all Class II groups relative to the control group at all stages. The same finding was also reported for the patients with Class III malocclusion. 14 In the evaluation of the deglutition stages, it was observed that, in the mandibular retrusion group, the root of the tongue moved in an inferior and anterior direction at stage 2. In this group, the posterior portion of the dorsal tongue also moved inferiorly at stage 2. Probably, the movement of the root of the tongue was affected by the movement of the posterior portion of the dorsal tongue. The results of our study showed that the tongue tips were positioned more posteriorly in all Class II groups than in the Class I control group. However, the retrusion of the tongue tip was not statistically significant at stage 2. When the movement of the tongue tip was evaluated according to the stages, it was observed that, in the mandibular retrusion and maxillary protrusion group (group 3), it moved in the posterior direction at stage 3 relative to stages 1 and 2. The reason for not moving in the posterior direction at stage 2 was probably to create an anterior seal to prevent exudation and to help the transportation of the bolus toward the pharyngeal area. However, in the control group, the retrusion was observed at stage 2 relative to stage 1. In the other Class II groups (groups 1 and 2), tongue-tip movements during deglutition were not statistically significant. In some previous studies, it was shown that tongue-tip position was closely related to overbite, overjet, and skeletal morphology. 11,13,14 Gorgulu et al, 14 Subtelny and Subtelny, 27 and Fuhrmann and Diedrich 28 reported that the tongue tip was positioned more anteriorly in patients with Class III malocclusion. Similarly, Fujiki et al 11 and Akin et al 13 showed that the tongue tip was more protrusive during deglutition in patients with open bite. Similar to these results, tongue-tip position was affected by the Class II malocclusion, and it was retruded in these patients. On the other hand, its movements were affected only when both jaws were malpositioned. CONCLUSIONS 1. Dentofacial morphology affects the position of the tongue and its deglutitive movements. 2. In patients with Class II malocclusion, the dorsal tongue is positioned more superiorly, and the tongue tip is positioned more posteriorly than in those with skeletal Class I malocclusion. 3. Further studies are needed to determine the adaptive changes after the correction of Class II malocclusion, and this is the issue of another investigation planned in our department. REFERENCES 1. Proffit WR. Equilibrium theory revisited: factors influencing position of the teeth. Angle Orthod 1978;48:175-86. 2. Proffit WR. Muscle pressures and tooth position: North American whites and Australian aborigines. Angle Orthod 1975;45:1-11. 3. Subtelney JD, Sakuda M. Muscle function, oral malformation, and growth changes. Am J Orthod 1966;52:495-517. 4. Cleall JF. Deglutition: a study of form and function. Am J Orthod 1965;51:566-94. 5. Subtelney JD. Malocclusions, orthodontic corrections and orofacial muscle adaptation. Angle Orthod 1970;40:170-201. 6. Melsen B, Atina L, Santuari M, Atina A. Relationships between swallowing pattern, mode of respiration and development of malocclusion. Angle Orthod 1987;57:113-20. 7. Lowe AA, Johnston WD. Tongue and jaw muscle activity in response to mandibular rotations in a sample of normal and anterior open-bite subjects. Am J Orthod 1979;76:565-76. 8. Alexander S. Genioglossus muscle electrical activity and associated arch dimensional changes in simple tongue thrust swallowing pattern. J Clin Pediatr Dent 1997;21:213-22. 9. Cheng CF, Peng CL, Chiou HY, Tsai CY. Dentofacial morphology and tongue function during swallowing. Am J Orthod Dentofacial Orthop 2002;122:491-9. 10. Ichida T, Takiguchi R, Yamada K. Relationship between the lingual-palatal contact duration associated with swallowing and maxillofacial morphology with the use of electropalatography. Am J Orthod Dentofacial Orthop 1999;116:146-51. 11. Fujiki T, Takano-Yamamoto T, Noguchi H, Yamashiro T, Guan G, Tanimoto K. A cineradiographic study of deglutitive tongue movement and nasopharyngeal closure in patients with anterior open bite. Angle Orthod 2000;70:284-9. 12. Fujiki T, Inoue M, Miyawaki S, Nagasaki T, Tanimoto K, Takano-Yamamoto T. Relationship between maxillofacial morphology and deglutitive tongue movement in patients with anterior open bite. Am J Orthod Dentofacial Orthop 2004;125: 160-7. May 2011 Vol 139 Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics

Yılmaz et al e425 13. Akın E, Sayın M O, Karaçay Ş, Bulakbaşı N. Real-time balanced turbo field echo cine-magnetic resonance imaging evaluation of tongue movements during deglutition in subjects with anterior open bite. Am J Orthod Dentofacial Orthop 2006;129:24-8. 14. G org ul u S, Sagdic D, Akın E, Karacay S, Bulakbaşı N. Evaluation of tongue movements in skeletal Class III malocclusions: a study with real-time balanced turbo field echo cine MRI. Am J Orthod Dentofacial Orthop 2011;139:e405-e414. 15. Karacay S, Akın E, Ortakoglu K, Bengi AO. Dynamic MRI evaluation of tongue posture and deglutitive movements in a surgically corrected open bite. Angle Orthod 2006;76:1057-65. 16. Karaçay Ş,Akın E, Sayın O, Bulakbaşı N. Real time balanced turbo field echo (B-TFE) cine-mri in the analysis of deglutition events and transit times. J Oral Rehabil 2006;33:646-53. 17. Sayın M O, Akin E, Karaçay Ş, Bulakbaşı N. Initial effects of the tongue crib on tongue movements during deglutition. Angle Orthod 2006;76:400-5. 18. Dahlberg G. Statistical methods for medical and biological students. New York: Interscience Publications; 1940. 19. Vaiman M, Eviatar E. Surface electromyography as a screening method for evaluation of dysphagia and odynophagia. Head Face Med 2009;20:5-9. 20. Steele CM, Van Lieshout PH. Use of electromagnetic midsagittal articulography in the study of swallowing. J Speech Lang Hear Res 2004;47:342-52. 21. Furia CL, Carrara-de-Angelis E, Martins NM, Barros AP, Carceiro B, Kowalski LP. Videofluoroscopic evaluation after glossectomy. Arch Otolaryngol Head Neck Surg 2000;126:378-83. 22. Gilbert RJ, Daftary S, Campell TA, Weisskoff RM. Echo-planar magnetic resonance imaging of deglutitive vocal fold closure: normal and pathologic patterns of displacement. Laryngoscope 1996; 106:568-72. 23. Ikeda K, Ogura M, Oshima T, Suzuki H, Higano S, Takahashi S, et al. Quantitative assessment of the pharyngeal airway by dynamic magnetic resonance imaging in obstructive sleep apnea syndrome. Ann Otol Rhinol Laryngol 2001;110:183-9. 24. Faust RA, Remley KB, Fimell FL. Real-time cine magnetic resonance imaging for evaluation of the pediatric airway. Laryngoscope 2001;111:2187-90. 25. Kitano H, Asada Y, Hayashi K, Inoue H, Kitajima K. The evaluation of dysphagia following radical surgery for oral and pharyngeal carcinomas by cine-mri. Dysphagia 2002;17:187-91. 26. Anagnostara A, Stoeckli S, Weber OM, Kollias SS. Evaluation of the anatomical and functional properties of deglutition with various kinetic high-speed MRI sequences. J Magn Reson Imaging 2001; 14:194-9. 27. Subtelny JD, Subtelny JD. Oral habits studies in form, function, and therapy. Angle Orthod 1973;43:349-83. 28. Fuhrmann R, Diedrich P. B-mode ultrasound scanning of the tongue during swallowing. Dentomaxillofac Radiol 1994;23:211-5. American Journal of Orthodontics and Dentofacial Orthopedics May 2011 Vol 139 Issue 5

本文献由 学霸图书馆 - 文献云下载 收集自网络, 仅供学习交流使用 学霸图书馆 (www.xuebalib.com) 是一个 整合众多图书馆数据库资源, 提供一站式文献检索和下载服务 的 24 小时在线不限 IP 图书馆 图书馆致力于便利 促进学习与科研, 提供最强文献下载服务 图书馆导航 : 图书馆首页文献云下载图书馆入口外文数据库大全疑难文献辅助工具