Three-dimensional changes in the temporomandibular joint after maxillary protraction in children with skeletal Class III malocclusion

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1 501 Journal of Oral Science, Vol. 58, No. 4, , 2016 Original Three-dimensional changes in the temporomandibular joint after maxillary protraction in children with skeletal Class III malocclusion Hyunju Lee 1), Woo-Sung Son 1), Chun Kwak 2), Eun-Hee Kang 2), Seong-Sik Kim 1), Soo-Byung Park 1), and Yong-Il Kim 1,3,4) 1)Department of Orthodontics, School of Dentistry, Pusan National University, Yangsan, Republic of Korea 2)Dental Clinics, Busan, Republic of Korea 3) Dental Research Institute, Pusan National University Dental Hospital, Yangsan, Republic of Korea 4)Biomedical Research Institute, Pusan National University Hospital, Yangsan, Republic of Korea (Received March 30, 2016; Accepted May 12, 2016) Abstract: We evaluated 3-dimensional changes in the temporomandibular joints of children with skeletal Class III malocclusion and maxillary deficiency after facemask therapy for maxillary protraction. Eighteen children with anterior crossbite and a Class III molar relationship underwent facemask therapy for maxillary protraction, after which they exhibited positive overjet and a Class II molar relationship. Three-dimensional cone-beam computed tomography images of the patients were obtained before (T1) and after (T2) facemask protraction, and the 3-dimensional coordinates of the anatomical landmarks in T1 and T2 images were compared. After facemask therapy, the mandibular condyles of the patients were displaced outside, upward, and backward. Additionally, the anterior and posterior walls of the glenoid fossa had negative values for anteroposterior change. Three-dimensional analysis of the temporomandibular joint showed that facemask therapy resulted in bone apposition (to the anterior wall) and bone resorption (of the posterior wall) in the glenoid fossa. This bone remodeling resulted in upward and backward displacement of the condyle. Correspondence to Dr. Yong-Il Kim, Department of Orthodontics, School of Dentistry, Geumoro 20, Mulgeumeup, Yangsan , Republic of Korea Fax: kimyongil@pusan.ac.kr Color figures can be viewed in the online issue at J-STAGE. doi.org/ /josnusd DN/JST.JSTAGE/josnusd/ (J Oral Sci 58, , 2016) Keywords: CBCT; 3D cephalometry; TMJ; facemask. Introduction Facemasks are increasingly used to treat skeletal Class III malocclusion and maxillary deficiency. Maxillary protraction separates circummaxillary sutures and stimulates forward and downward movement of the maxillary complex, clockwise rotation of the mandible, and linguoversion of lower incisors (1-8). However, because maxillary protraction imparts force posteriorly to the mandible, changes in the mandibular fossa and the positions of the mandible body and condyles are expected. Although conventional 2-dimensional analysis is frequently used to evaluate anteroposterior positional changes in the temporomandibular joint (TMJ), such analysis is less useful for assessing overall changes in the TMJ. Therefore, remodeling of adjacent bones, TMJ, and soft tissue after facemask therapy for maxillary protraction are not well understood, and previous studies have focused mostly on treatment outcomes (9-13). Although facemask therapy sometimes alters the position and shape of the mandible and TMJ, no study has used 3-dimensional (3-D) analysis of the mandibular condyle and glenoid fossa or maxilla and face to evaluate patients after facemask therapy. Advances in 3-D analysis using cone-beam computed tomography (CBCT) superimposition are helpful in evaluating anatomical

2 502 structures undergoing remodeling and displacement and, thus, in identifying skeletal changes (14-18). Therefore, use of CBCT in 3-D analysis of anatomical landmarks in the maxilla, mandible, and TMJ after facemask therapy might improve understanding of the mechanism of action and effectiveness of such treatment. We compared the 3-D coordinates of anatomical landmarks before and after facemask therapy for maxillary protraction and analyzed overall TMJ changes in children with skeletal Class III malocclusion and maxillary deficiency. Materials and Methods We retrospectively analyzed the medical records of 18 children with skeletal Class III malocclusion and maxillary deficiency (mean age, 8.9 ± 1.1 years): 10 girls (mean age, 8.8 ± 0.8 years) and 8 boys (mean age, 9.1 ± 1.4 years). This study was reviewed and approved by the Ethics Committee of Pusan National University Dental Hospital (PNUDH ). Sample All patients had skeletal Class III malocclusion with maxillary deficiency and anterior crossbite and a Class III molar relationship before treatment (T1). All underwent facemask therapy for maxillary protraction and exhibited positive overjet and a Class II molar relationship after treatment (T2). At the time of treatment, the maxillary central incisors, lateral incisors, and first molars were fully erupted. A Delaire-type facemask was used for maxillary protraction, and a protraction force of 450 g was maintained on each side. All patients were instructed to wear the facemask for more than 16 hours per day. The direction of maxillary protraction was 15 to 30 downward and forward relative to the occlusal plane. Facemask therapy was completed when positive anterior overjet and a Class II molar relationship were attained. The average age at the beginning (T1) and end (T2) of treatment was 8.9 ± 1.1 and 10.0 ± 1.1 years, respectively. The average duration of facemask treatment was 10.8 ± 2.4 months (range, months). CBCT assessment Before 3-D analysis of the effect of facemask therapy, 3-D CBCT images (Pax-Zenith 3D; Vatech Co., Seoul, South Korea) were obtained 1 month before (T1) and after (T2) maxillary protraction. To ensure maximum intercuspation, CBCT images were acquired with patients in an upright position. The Frankfort horizontal (FH) plane was adjusted so that it was parallel to the floor. CBCT scanning of maxillofacial regions was conducted by using the following parameters: mm field of view (FOV), 105 kvp tube voltage, 5.7 ma tube current, and 0.6 mm isotropic voxel size. CBCT data were then reformatted and analyzed 3-dimensionally using 3D imaging software (InVivo Dental software; Anatomage, Inc., San Jose, CA, USA) Using the anterior cranial fossa as the registration area, we superimposed images obtained before (T1) and after (T2) treatment to evaluate mandibular and glenoid fossa changes after facemask therapy. For maximal superimposition accuracy, 3-D CBCT superimposition was done as follows. Both point registration and volume registration, in turn, were used. First, point registration began with landmark identification. Then, T1 and T2 images were 3-dimensionally traced with the nasion (N) as (0,0,0), to obtain the 3-D coordinates of the reference points. After that, the images were superimposed with N, frontozygomatic suture_left (FZ_L), frontozygomatic suture_right (FZ_R), and orbitale_right (OR_R) as reference points. Finally, volume registration was performed for more accurate superimposition. After the images were superimposed using point registration, volume registration was performed with a mm target volume (including the anterior cranial fossa), for enhanced accuracy. The 3-D coordinates of anatomical landmarks obtained from superimposition of T1 and T2 images were analyzed and compared to evaluate changes in the maxilla, mandible, and TMJ. Table 1 shows the anatomical landmarks used in this study. In comparing T2 (after treatment) and T1 (before treatment) images, the extent of coordinate change was calculated by subtracting the T2 value from the T1 value. On the X-axis, positive (+) values indicate leftward displacement and negative ( ) values indicate rightward displacement. On the Y-axis, positive (+) values indicate backward displacement and negative ( ) values indicate forward displacement. On the Z-axis, positive (+) values indicate upward displacement and negative ( ) values indicate downward displacement (Fig. 1). Statistical analysis The Wilcoxon signed rank test was used to compare landmarks before (T1) and after (T2) facemask therapy. Spearman correlation analysis was then performed to assess the T2 correlations among the landmarks. The significance value was set at All 3-D measurements were obtained by the same investigator. To assess the reproducibility of the measurements, all landmarks were retraced 3-dimensionally after a 2-week interval, and intraoperator error, in the form of the intraclass correla-

3 503 Table 1 Reference points and anatomical landmarks of interest Landmark Description Mandible Mandibular fossa AMF_R, L Most anterior point of mandibular fossa SMF_R, L Most superior point of mandibular fossa PMF_R, L Most posterior point of mandibular fossa MMF_R, L Most medial point of mandibular fossa Condyle Ar_R, L Most posterior point of condyle Co_R, L Most superior point of condyle CoA_R, L Most anterior point of condyle CoM_R, L Most medial point of condyle CoL_R, L Most lateral point of condyle Coronoid process CP_R, L Most superior and anterior point of coronoid process Chin B B point Pog Pogonion Me Menton MF_R, L Center of mental foramen Ramus Go_R, L Gonion Ag_R, L Antegonion Maxilla Maxillary bone ANS Anterior nasal spine PNS Posterior nasal spine A A point NPC Center of nasopalatine canal tion coefficient (ICC), was calculated. Results The intraoperator reliability of the present study results was good (average ICC, 0.835). Table 2 shows the landmark changes in T1/T2-superimposed images on the X-, Y-, and Z-axes of the maxilla and mandible (including condyle and glenoid fossa) after facemask therapy for the 18 children. Fig. 1 The 3-dimensional coordinate system. On the X-axis, positive (+) values indicate leftward displacement and negative ( ) values rightward displacement; on the Y-axis, positive (+) values indicate backward displacement and negative ( ) values forward displacement; and, on the Z-axis, positive (+) values indicate upward displacement and negative ( ) values downward displacement. Changes in the X-, Y-, and Z-coordinates of anatomical landmarks On the X-axis, among bilateral landmarks the right-side landmarks exhibited negative displacement and left-side landmarks exhibited positive displacement (except the right superior mandibular fossa, right and left posterior mandibular fossae, right and left medial mandibular fossae, and left mental foramen), indicating movement to the outside. Additionally, the bilateral landmarks of the condyle, coronoid process, and ramus showed displacement to the outside and bone absorption at the lateral wall of the anterior mandibular fossa (P < 0.05). On the Y-axis, the displacement values for the mandibular fossa, condyle, coronoid process, chin, ramus, and mandibular teeth were all positive. These findings indicate backward displacement of the mandibular condyle and bone absorption at the posterior wall along with bone apposition to the medial and right anterior walls in the glenoid fossa (P < 0.05). The central point of the lower central incisal edge also exhibited backward displacement (P < 0.05). On the Z-axis, all landmarks of the glenoid fossa, coronoid process, and condyle, except the most medial point of the left condyle, exhibited positive displacement. Bone absorption at the superior wall of the glenoid fossa and upward displacement of the condyle at the posterior and right-superior points were observed (P < 0.05). Furthermore, all landmarks of the chin, ramus, and maxilla exhibited negative displacement, indicating that they had moved downward (P < 0.05). Correlation between maxillary protraction and displacement of anatomical landmarks Table 3 shows the correlations of the forward displacement of the A point after maxillary protraction with the other anatomical landmarks. On the X- and Z-axes, no significant correlations were observed between maxillary protraction and the displacement of the other landmarks. On the Y-axis, there was no significant correlation between maxillary protraction and mandibular anatomical landmarks, although was a strong correlation between maxillary protraction and forward displacement

4 504 Table 2 Mean (SD) change in coordinates at each landmark in superimposed T1 and T2 images Landmark X-coordinates Y-coordinates Z-coordinates Mean SD P value Mean SD P value Mean SD P value Mandible Mandibular fossa AMF_R 0.88** * AMF_L 1.21** SMF_R * SMF_L 0.93** ** PMF_R ** PMF_L * MMF_R ** MMF_L Condyle Ar_R 0.73* ** * Ar_L 0.82** ** * Co_R 1.04** ** ** Co_L 0.96** * CoA_R 1.23** ** CoA_L 0.97* ** CoM_R 0.59** ** CoM_L 0.51** ** CoL_R 1.29** ** CoL_L 1.04** ** Coronoid process CP_R 0.6** * CP_L 0.46** Chin B ** ** Pog ** ** Me ** ** MF_R 0.65** ** ** MF_L ** ** Ramus Go_R 0.69** ** Go_L 0.9** ** Ag_R 1.28** ** * Ag_L 0.74* ** ** Maxilla Maxillary bone ANS ** ** PNS ** A ** * NPC ** ** When comparing T2 (after treatment) with T1 (before treatment) images, the extent of coordinate changes were calculated by subtracting T2 values from T1 values. X-axis: positive (+) values indicate displacement to the left, negative ( ) values indicate displacement to the right; Y-axis: positive (+) values indicate backward displacement, negative ( ) values indicate forward displacement; Z-axis: positive (+) values indicate upward displacement, negative ( ) values indicate downward displacement. P values were derived from the Wilcoxon signed rank test. *P < 0.05, **P < of the center of the nasopalatine canal. Discussion This study investigated 3-D changes in the maxilla, mandible, and TMJ after facemask therapy for maxillary protraction in children with skeletal Class III malocclusion and maxillary deficiency. Treatment outcome was evaluated in relation to dentoalveolar effect, anterior growth of the maxilla, bone remodeling in the glenoid fossa, and changes in the condyle and mandible after growth and treatment. First, facemask therapy that uses teeth for anchorage cannot deliver a protraction force directly to circummaxillary sutures and thus has a dentoalveolar effect (19). However, forward movement at the anterior nasal spine (1.31 mm) and the A point (1.62 mm) during facemask

5 505 Table 3 Spearman correlation coefficients between A point and all other landmarks X-coordinates Y-coordinates Z-coordinates r value P value r value P value r value P value Mandible Mandibular fossa AMF_R AMF_L SMF_R SMF_L PMF_R PMF_L MMF_R MMF_L Condyle Ar_R Ar_L Co_R Co_L CoA_R CoA_L CoM_R CoM_L CoL_R CoL_L Coronoid process CP_R CP_L Chin B Pog Me MF_R MF_L Ramus Go_R Go_L Ag_R Ag_L Maxilla Maxillary bone ANS PNS A NPC *P < 0.05, **P < ** therapy indicated that growth was greater in this study than at the anterior nasal spine (0.96 mm) and A point (1.07 mm) in a similarly aged cohort assessed for 1 year (20). These results suggest that facemask therapy, in addition to its dentoalveolar effect, results in forward movement of the maxilla (Figs. 2-4). Analysis of X-, Y-, and Z-coordinates of anatomical landmarks by superimposition of 3-D images before Fig. 2 Three-dimensional superimposition of T2 over T1 registered images at the anterior cranial base. The T1 model is shown in white; the superimposed T2 model is shown in blue. A B Fig. 3 Superimposition of sagittal T1 and T2 images. T1 images are shown in white; superimposed T2 images are shown in blue. The superimposed images show anterior displacement of the maxilla and downward and backward displacement of the chin. A and B are images from two different patients. Fig. 4 Three-dimensional tracing of superimposed T1 and T2 images. The T1 model is shown in orange; the superimposed T2 model is shown in blue. The coordinates of T2 after superimposition are shown to the right.

6 506 Fig. 5 Horizontal view of superimposition of T1 and T2 images registered on the anterior cranial base; T1 is shown in white and T2 in blue. The images illustrate resorption of the posterior wall of mandibular fossa. A and B are images from two different patients. Fig. 6 Superimposed sagittal T1 and T2 images. The T1 model is shown in white, and the superimposed T2 model is shown in blue. The images illustrate slight posterior displacement of the condyle. and after treatment revealed bone apposition to the right anterior wall of the glenoid fossa and bone resorption of both posterior walls of the glenoid fossa (Fig. 5). These findings indicate that the effects of facemask therapy were not limited to displacement of the mandible; bone remodeling occurred in the glenoid fossa. Possible causes of TMJ change after facemask are the force produced by the facemask, forward movement of the maxilla, posterior displacement of the condyle, and growth. Among these, the force produced by facemask therapy is the main contributing factor. Maxillary protraction force induced maxillary and mandibular displacement, which were associated with remodeling. The growth pattern of the patient should also be considered. Our results are consistent with those of a previous study (21) reporting that the height and depth of the glenoid fossa increased on the sagittal plane after chin cup treatment. They also accord with the findings of a study showing that bone apposition to the front wall of the glenoid fossa and bone absorption at the posterior wall of the glenoid fossa occurred after bone-anchored maxillary protraction (BAMP) treatment (22). Because facemask therapy has pronounced maxillary protraction effects (23), it likely causes bone remodeling in the glenoid fossa, although the difference between facemask therapy and BAMP treatment was only 1 mm (22). A previous study reported superior displacement of the condyle after maxillary protraction treatment with a Delaire-type facemask (24). In the present study, we noted bone absorption at the superior wall of the glenoid fossa and upward displacement of the right condyle. With regard to posterior displacement of the condyle, the most superior point of the right condyle moved 0.98 mm backward, and the right condyle moved 0.64 mm backward, during 9 months of observation (Table 2). In a similarly aged cohort of patients with untreated skeletal Class III malocclusion, the most superior point of the condyle moved backward at a rate of 0.65 mm per year (20). The superimposed T1 and T2 model images in the present study (Fig. 6) revealed greater displacement of the mandibular condyle. These findings suggest that bone remodeling from bone absorption at the superoposterior wall and bone apposition to the anterior wall of glenoid fossa caused superoposterior displacement of the mandibular condyle. Previous studies using lateral cephalography showed that a counterforce is applied to the mandible in reaction to a maxillary protraction force, thus causing clockwise rotation of the mandible (5). The displacements of the mandibular condyle were mm backward and 0.34 mm upward in the right condyle and 0.97 mm backward and 0.25 mm upward in the left condyle; 2.55 mm backward and 2.94 mm downward in the chin; and 2.94 mm backward and 0.48 mm downward on the right side and 2.32 mm backward and 0.82 mm downward on the left side of the ramen. Thus, clockwise rotation of the mandible had occurred during facemask therapy for maxillary protraction. Forward displacements of the B point, pogonion, and menton were 1.14, 1.55, and 1.42 mm per year, respectively, in a previous study of children with untreated skeletal Class III malocclusion (20); the same landmarks in the present study exhibited backward displacements of 2.44, 2.51, and 2.39 mm, respectively, during the 9-month observation period. This discrepancy was almost certainly attributable to the effects of the present facemask therapy.

7 507 In this study, bone resorption and apposition of the glenoid fossa were evaluated at the level of the anterior cranial fossa by superimposition of CBCT images obtained before and after facemask therapy. A limitation of the study is that data were evaluated only for treated children with skeletal Class III malocclusion. Indeed, the present treatment results include both the treatment effect and growth-related changes. A more accurate analysis of the effects of facemask therapy would include a comparison with CBCT images from untreated children with skeletal Class III malocclusion as a control group. Nonetheless, the present analysis of superimposed CBCT images yielded crucial information on the relationship between facemask therapy and bone remodeling of the mandibular condyle and glenoid fossa. The present 3-D analysis of facemask therapy, especially the analysis of correlations between maxillary protraction and the displacements of relevant anatomical landmarks, confirmed maxillary growth and a dentoalveolar effect. Moreover, bone remodeling after facemask therapy for maxillary protraction leads to bone apposition to the anterior wall and bone absorption of the posterior walls of the glenoid fossa. The simultaneity of the displacement of the condyle and the above-noted bone remodeling results indicates that bone remodeling in the glenoid fossa causes upward and backward displacement of the condyle. Acknowledgments This study was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean Government (MSIP) (2015R1C1A1A ) (YI Kim) and by a grant from Busan Gyeongnam Ulsan Branch of the Korean Association of Orthodontists (WS Son). Conflict of interest None declared. References 1. Hata S, Itoh T, Nakagawa M, Kamagashira K, Ichikawa K, Matsumoto M et al. (1987) Biomechanical effects of maxillary protraction on the craniofacial complex. Am J Orthod Dentofacial Orthop 91, Chong YH, Ive JC, Årtun J (1996) Changes following the use of protraction headgear for early correction of Class III malocclusion. Angle Orthod 66, Sung SJ, Baik HS (1998) Assessment of skeletal and dental changes by maxillary protraction. Am J Orthod Dentofacial Orthop 114, Pangrazio-Kulbersh V, Berger J, Kersten G (1998) Effects of protraction mechanics on the midface. Am J Orthod Dentofacial Orthop 114, Macdonald KE, Kapust AJ, Turley PK (1999) Cephalometric changes after the correction of Class III malocclusion with maxillary expansion/facemask therapy. Am J Orthod Dentofacial Orthop 116, Westwood PV, McNamara JA Jr, Baccetti T, Franchi L, Sarver DM (2003) Long-term effects of Class III treatment with rapid maxillary expansion and facemask therapy followed by fixed appliances. Am J Orthod Dentofacial Orthop 123, Vaughn GA, Mason B, Moon HB, Turley PK (2003) The effects of maxillary protraction therapy with or without rapid palatal expansion: a prospective, randomized clinical trial. Am J Orthod Dentofacial Orthop 128, Cha KS (2003) Skeletal changes of maxillary protraction in patients exhibiting skeletal Class III malocclusion: a comparison of three skeletal maturation groups. Angle Orthod 73, Battagel JM, Orton HS (1995) A comparative study of the effects of customized facemask therapy or headgear to the lower arch on the developing Class III face. Eur J Orthod 17, Chong YH, Ive JC, Artun J (1996) Changes following the use of protraction headgear for early correction of Class III malocclusion. Angle Orthod 66, Kiliçoglu H, Kirliç Y (1998) Profile changes in patients with Class III malocclusions after Delaire mask therapy. Am J Orthod Dentofacial Orthop 113, Deguchi T, Kanomi R, Ashizawa Y, Rosenstein SW (1999) Very early face mask therapy in Class III children. Angle Orthod 69, De Toffol L, Pavoni C, Baccetti T, Franchi L, Cozza P (2008) Orthopedic treatment outcomes in Class III malocclusion. A systematic review. Angle Orthod 78, Seren E, Akan H, Toller MO, Akyar S (1994) An evaluation of the condylar position of the temporomandibular joint by computerized tomography in Class III malocclusions: a preliminary study. Am J Orthod Dentofacial Orthop 105, Adams GL, Gansky SA, Miller AJ, Harrell WE Jr, Hatcher DC (2004) Comparison between traditional 2-dimensional cephalometry and a 3-dimensional approach on human dry skulls. Am J Orthod Dentofacial Orthop 126, Cevidanes LH, Styner MA, Proffit WR (2006) Image analysis and superimposition of 3-dimensional cone-beam computed tomography models. Am J Orthod Dentofacial Orthop 129, Ludlow JB, Gubler M, Cevidanes L, Mol L (2009) Precision of cephalometric landmark identification: Cone-beam computed tomography vs conventional cephalometric views. Am J Orthod Dentofacial Orthop 136, 312.e Nguyen T, Cevidanes L, Cornelis MA, Heymann G, de Paula LK, De Clerck H (2011) Three-dimensional assessment of maxillary changes associated with bone anchored maxillary protraction. Am J Orthod Dentofacial Orthop 140, Ngan PW, Hagg U, Yiu C, Wei SH (1997) Treatment response

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