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BoneCeramic graft regenerates alveolar defects but slows orthodontic tooth movement with less root resorption
ORIGINAL ARTICLE
BoneCeramic graft regenerates alveolar defects but slows orthodontic tooth movement with less root resorption Nan Ru,a Sean Shih-Yao Liu,b Yuxing Bai,c Song Li,c Yunfeng Liu,d and Xiaoxia Weie Beijing, Hangzhou, and Zhengzhou, China, and Indianapolis, Ind
Introduction: BoneCeramic (Straumann, Basel, Switzerland) can regenerate bone in alveolar defects after tooth extraction, but it is unknown whether it is feasible to move a tooth through BoneCeramic grafting sites. The objective of this study was to investigate 3-dimensional real-time root resorption and bone responses in grafted sites during orthodontic tooth movement. Methods: Sixty 5-week-old rats were randomly assigned to 3 groups to receive BoneCeramic, natural bovine cancellous bone particles (Bio-Oss; Geistlich Pharma, Wolhusen, Switzerland), or no graft, after the extraction of the maxillary left first molar. After 4 weeks, the maxillary left second molar was moved into the extraction site for 28 days. Dynamic bone microstructures and root resorption were evaluated using in-vivo microcomputed tomography. Stress distribution and corresponding tissue responses were examined by the finite element method and histology. Mixed model analysis of variance was performed to compare the differences among time points with Bonferroni post-hoc tests at the significance level of P \0.05. Results: The BoneCeramic group had the least amount of tooth movement and root resorption volumes and craters, and the highest bone volume fraction, trabecular number, and mean trabecular thickness, followed by the Bio-Oss and the control groups. The highest stress accumulated in the cervical region of the mesial roots. Conclusions: BoneCeramic has better osteoconductive potential and induces less root resorption compared with Bio-Oss grafting and naturally recovered extraction sites. (Am J Orthod Dentofacial Orthop 2016;149:523-32)
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oving a tooth orthodontically into the region of an alveolar defect with insufficient buccolingual width can be problematic.1 It often causes root resorption,2 gingival recessions,3 periodontal
a Lecturer, Department of Orthodontics, School of Stomatology, Capital Medical University, Beijing, China. b Associate professor; director, Mineralized Tissues and Histology Research Laboratory; and director, Orthodontic Fellowship Program, Department of Orthodontics and Oral Facial Genetics, Indiana University School of Dentistry, Indianapolis, Ind. c Professor, Department of Orthodontics, School of Stomatology, Capital Medical University, Beijing, China. d Associate professor, Key Laboratory of Equipment & Manufacturing, Zhejiang University of Technology, Hangzhou, China. e Associate professor, Department of Orthodontics, School of Stomatology, Zhengzhou University, Zhengzhou, China. Nan Ru and Sean Shih-Yao Liu are joint first authors and contributed equally to this work. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Supported by a grant from the Natural Science Foundation of China (81400537). Address correspondence to: Yuxing Bai, Department of Orthodontics, School of Stomatology, Capital Medical University, Tiantan Xili 4, Chongwen District, Beijing, China 100050; e-mail, [email protected]. Submitted, December 2014; revised and accepted, September 2015. 0889-5406/$36.00 Copyright Ó 2016 by the American Association of Orthodontists. http://dx.doi.org/10.1016/j.ajodo.2015.09.027
pockets,4 and traumatic injuries to pulp vitality.5 Alveolar defects may appear in patients with cleft lip and palate. If the cleft involves the alveolus, the alveolar ridge defects in these sites impede tooth eruption6 and delay orthodontic tooth movement with prolonged treatment times.7 Alveolar defects may also be secondary to a large piece of buccal plate with the extraction of an impacted tooth, jaw inflammation, or cyst and trauma surgery.1 Similar scenarios can be seen during extensive remodeling of the edentulous alveolus after the extraction of damaged or periodontal-involved first molars. For some adolescent and young adults, once periodontal disease is under control, an effective way to replace a missing molar is to move the adjacent molar into the first molar area.1 However, alveolar bone in extraction sites quickly resorbs, with reduced height and width, primarily changing to dense cortical bone, which impedes the movement of teeth through the bone. Orthodontic tooth movement is not feasible without reestablishment of the alveolar width with bone grafts before movement.8 To alleviate alveolar ridge resorption and regenerate alveolar bone in the defects, bone grafts, such as autogenous bone, allograft,9 or alloplast,10 can be placed in 523
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the extraction sites immediately after tooth extraction.11 Although autogenous bone is recognized as the gold standard for bone grafts because of the viability of transferable osteogenic cells, it requires a second surgery from the donor site. Patients tend to decline this treatment modality because of the additional discomfort.12 Alternatively, deproteinized bovine bone mineral (Bio-Oss; Geistlich Pharma, Wolhusen, Switzerland) can be used as a graft material for augmenting an alveolar ridge defect.13 However, Bio-Oss degrades slowly and induces uncertain immune responses and fibrous encapsulation with healing.14 A new synthetic bone substitute, BoneCeramic (Straumann, Basel, Switzerland), has been used for ridge preservation because it can be rapidly replaced by regenerative bone.15,16 BoneCeramic consists of 60% hydroxyapatite and 40% beta tricalcium phosphate. After grafting, beta tricalcium phosphate is rapidly resorbed and completely replaced by regenerative bone.17 Meanwhile, the hydroxyapatite, resorbed slowly, serves as a good matrix scaffold for ingrowth of new blood vessels and attachment of bone-forming cells.18 Bone can be greatly regenerated because BoneCeramic can be totally resorbed and subsequently replaced by host bone in a shorter time.19 However, whether it will hamper orthodontic tooth movement in an augmented area of alveolar ridge is still unknown. To evaluate whether a tooth can be moved into an extraction site with bone grafts, one should investigate the rate or distance of orthodontic tooth movement with accompanied bone responses or adverse side effects. The aims of this experiment were (1) to evaluate whether it is feasible to move a tooth in an alveolar ridge augmented with BoneCeramic, and (2) to evaluate realtime 3-dimensional (3D) changes in root resorption and bone microarchitectures, and tissue responses when moving teeth into BoneCeramic and Bio-Oss grafts after extractions. Understanding the dynamic responses in bone graft resorption, bone regeneration, and root resorption will help to establish treatment guidelines for patients. MATERIAL AND METHODS
All procedures were approved by the institutional animal care and use committee of the School of Stomatology, Capital Medical University, Beijing, China. After they were acclimated, 60 male Sprague Dawley rats (age, 5 weeks) (specific pathogen free level 3) had the maxillary left first molar extracted under anesthesia by chloral hydrate (2 mL/kg) injected intraperitoneally. A rectangular (3 3 2 3 2 mm) alveolar ridge defect was created in the socket by completely resecting the intraradicular septa between the tooth roots at the extraction
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sites with a low-speed dental handpiece. The animals were randomly assigned to 3 groups (n 5 20 per group) to receive BoneCeramic (60% hydroxyapatite, 40% beta tricalcium phosphate granules), Bio-Oss (natural bovine spongiosa granules, 0.25-1 mm), or no grafting. The mucosa was reflected and sutured to cover the socket to prevent the materials from leaking. Signs of infection, animal weight, and health conditions were monitored. Four weeks after the extractions, a groove was prepared at the cervical third of the incisors under anesthesia. A nickel-titanium coil spring (0.2 mm in diameter; IMD, Shanghai, China) was ligated between the maxillary left second molar and incisors using an 0.08-in ligature wire secured with bonding adhesive (Transbond; 3M Unitek, Monrovia, Calif). The spring was activated for approximately 1 mm to produce 10 g of continuous force to move the molar forward into the extraction site (Fig 1, A). After spring installation, each animal was scanned using an in-vivo microcomputed tomography system (SkyScan1076; Bruker, Kontich, Belgium) on days 0, 7, 14, 21, and 28. The spring was removed for each invivo microcomputed scan and reattached after scanning. The palate was secured at the supine position parallel to the stage in a carbon composite animal holder. The head was scanned through 180 of rotation at a 0.5 increment with 2 seconds per degree with resolution of 18 mm per pixel. Data were further reconstructed to provide axial cross-section images with SkyScan NRecon software (version 1.4.4; Bruker) and converted into 16bit bitmapped TIFF images with a resolution of 1024 3 1024 pixels.20 Tooth movement distance (Di) (mm) was measured 3 times and averaged at each time point (i 5 0, 7, 14, 21, and 28 days). Tooth movement rate (Vi) was then calculated as Vi 5ðDi Di1 Þ=7 (Fig 1, B). The alveolar bone was equally divided into the cervical and apical regions by a selected middle axial slice from the root apex to the furcation. In the apical region, 6 regions of interest (360 mm3) were selected: 500 mm mesial to the mesiobuccal and the mesiolingual roots, 500 mm distal to the distobuccal and the distolingual roots, and the intraradicular septa between the mesiobuccal and distobuccal roots and between the mesiolingual and distolingual roots (Fig 1, C). In the cervical region, 4 regions of interest (360 mm3) were selected: 500 mm mesial to the mesiobuccal and the mesiolingual roots, and distal to the distobuccal and the distolingual roots (Fig 1, D). Three-dimensional microarchitecture parameters for trabecular bone were measured as the following: bone volume fraction (BV/TV), indicating the ratio of bone volume to total volume; mean trabecular thickness
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Fig 1. A, Schematic of orthodontic tooth movement into the bone graft area. Dotted shadow, the alveolar ridge defect was embedded with bone grafts after the maxillary left first molar extraction; the nickeltitanium spring was ligated to move the molar forward into the extraction site. M2, maxillary left second molar. B, Sagittal view of the tooth roots. Tooth movement distance (Di) was calculated as the shortest width between the second and third molar crowns on the sagittal plane along the distal root of the third molar. White squares, regions of interest. C, Horizontal view of the apical region of tooth roots: 1-6 squares represent the selected regions of interest in the alveolar bone adjacent to the apical region of the 4 roots of the maxillary left second molar. D, Horizontal view of the cervical region of the tooth roots: 7-10 squares represent the selected regions of interest in the alveolar bone adjacent to the cervical region of the 4 roots of the maxillary left second molar. E, Tooth movement distances at different time points in the 3 groups. *Significance between the experimental groups and the control (P \0.05). F, Tooth movement rates at different time points in the 3 groups. *Significance between the experimental groups and the control (P \0.05).
(Tb.Th), indicating the local thickness at each voxel representing bone; trabecular number (Tb.N), indicating the average number of trabeculae per unit of length; and trabecular separation (Tb.Sp), indicating the mean distance between trabeculae. After segmenting the roots from the images using Mimics software (version 17.0; Materialise, Leuven, Belgium), the cervical, apical, and total root volumes of each root were measured for each time point.21 The volumes of root resorption in each region on days 7, 14, 21, and 28 were calculated by subtracting the root volume at each time point from the root volume on day 0. After 28 days, the animals were killed, and the maxillae were dissected, fixed, decalcified, and embedded in paraffin and serially sectioned (5 mm) along the mesiodistal axis of the second molar. The sections were stained with hematoxylin and eosin.
A 3D finite element method model of the maxillary second molar (day 0) was constructed with the Mimics software and imported into Ansys software (Ansys, Canonsburg, Pa). The geometry of the model consisted of 50019 isoparametric tetrahedral-node solid elements and 69731 nodes. The width of the periodontal ligament was set at 0.2 mm, and Young's modulus of the tooth, periodontal ligament, and bone were set as 19,600, 0.7, and 13,700 MPa, respectively. The Poisson ratios of the tooth, periodontal ligament, and bone were 0.15, 0.49, and 0.15, respectively.22 A 10-g force was applied in the finite element method model in the same direction as the spring attached intraorally. Movement was suppressed in 6 degrees of freedom for the nodes on the bottom edge of the alveolar bone. Tooth displacement and stress distribution analyses were performed with the Ansys software.
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Fig 2. Microarchitecture parameter schematic of region of interest 1 adjacent to the second molar: bone volume fraction (BV/TV), trabecular number (Tb.N), trabecular separation (Tb.Sp), mean trabecular thickness (Tb.Th), and at different time points in the BoneCeramic, Bio-Oss, and control groups. *Significance between the experimental groups and the control (P \0.05).
Statistical analysis
For each parameter, mixed-model measures analysis of variance was performed to compare the differences among time points and between groups with Bonferroni post hoc tests using the Statistical Package for the Social Sciences (version 11.5; SPSS, Chicago, Ill). The significance level was set at P \0.05. RESULTS
The greatest amount of tooth movement was observed in the control group, followed by the Bio-Oss group and then the BoneCeramic group (Fig 1, E). In all groups, tooth movement rates accelerated from days 0 to 7 and slightly decelerated from days 7 to 14. This similar tooth movement pattern repeated with acceleration from days 14 to 21, followed by deceleration from days 21 to 28 (Fig 1, F). In all regions of interest, the BV/TV, Tb.N, and Tb.Th significantly decreased from days 0 to 7 but increased from days 14 to 28, except for regions of interest 2 and 8 in all groups. Tb.Sp significantly decreased from days 0 to 7 but fluctuated from days 14 to 28 in all groups (Fig 2). The typical changes of BV/TV, Tb.N, Tb.Th, and Tb.Sp in all regions of interest during tooth
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movement were found in regions of interest 1, 2, 7, 8, and 10 (Tables I-III; Fig 2). Regions of interest 3 to 6 and 9 are omitted because of their similar changes to regions of interest 1, 2, 7, 8, and 10. In the BoneCeramic group, BV/TV, Tb.N, and Tb.Th in regions of interest 1, 2, and 7 were significantly higher than in the Bio-Oss and control groups at each time point (Tables I and II; Fig 2). In the Bio-Oss group, BV/ TV and Tb.Th in regions of interest 2, 7, and 8 on days 0, 21, and 28 were significantly higher than in the control group (Tables I and II). Tb.Sp values in the BoneCeramic group from days 7 to 28 were significantly lower than in the other 2 groups in regions of interest 1, 2, and 10 (Tables I and III; Fig 2). However, in regions of interest 1, 2, and 7, there was no difference in Tb.Sp between the Bio-Oss and control groups (Tables I and II; Fig 2). Root volumes reduced in all groups over time. All roots had a smooth surface on day 0. Starting at day 7 through day 28, small isolated lacunae were mainly scattered on the mesial surfaces of the roots, and wide shallow resorption craters were observed mostly on the distal surfaces of the roots (Fig 3). The greatest root resorption volumes were observed in the apical region of the mesiobuccal root in all groups,
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Table I. Descriptive statistics (means and standard deviations) of BV/TV (%), Tb.N (mm
1
), Tb.Sp (mm), and Tb.Th
(mm) in regions of interest (ROI) 1 and 2 ROI 1 Day 0
7
14
21
28
Group A B C A B C A B C A B C A B C
BV/TV 82.98 (7.21)* 58.48 (8.22) 57.38 (8.24) 78.99 (5.21)* 45.24 (4.22) 35.08 (3.09) 45.22 (3.56)* 21.25 (4.63) 22.03 (5.21) 68.90 (4.11)* 58.33 (3.56) 34.58 (3.09) 69.06 (3.41)* 66.70 (3.56) 43.73 (4.11)
Tb.N 5.31 (0.12)* 4.78 (0.22) 5.86 (0.13) 4.96 (0.21)*y 3.12 (0.14)* 2.17 (0.11) 4.76 (0.08)* 3.01 (0.09) 3.12 (0.10) 4.27 (0.11) 4.28 (0.12) 3.21 (0.14)* 4.87 (0.09) 4.90 (0.12) 3.57 (0.15)
ROI 2
Tb.Sp 0.06 (0.01)* 0.10 (0.01) 0.08 (0.01) 0.09 (0.02)* 0.12 (0.01) 0.16 (0.02) 0.09 (0.01)* 0.19 (0.02) 0.11 (0.02) 0.07 (0.01)* 0.10 (0.01) 0.10 (0.01) 0.05 (0.01)* 0.13 (0.02) 0.13 (0.02)
Tb.Th 0.18 (0.02)* 0.10 (0.01) 0.11 (0.01) 0.12 (0.02)* 0.09 (0.01) 0.09 (0.01) 0.09 (0.01) 0.06 (0.01) 0.09 (0.01) 0.16 (0.02)*y 0.11 (0.01)* 0.06 (0.01) 0.17 (0.02)* 0.13 (0.02) 0.08 (0.01)
BV/TV 80.82 (5.12)*y 48.41 (4.12)* 23.78 (5.67) 57.57 (4.23)*y 42.47 (4.67)* 39.43 (5.78) 32.33 (6.79) 29.25 (2.54) 28.33 (2.57) 43.37 (4.12) 42.24 (4.67) 21.37 (3.29)* 42.46 (5.67) 43.33 (4.43) 23.40 (2.47)*
Tb.N 5.22 (0.14)* 4.11 (0.10) 4.08 (0.09) 4.25 (0.14) 4.10 (0.09) 2.47 (0.13)* 4.69 (0.10)*y 3.52 (0.12)* 2.50 (0.13) 5.10 (0.09) 4.29 (0.08) 2.85 (0.13) 5.51 (0.12)*y 4.46 (0.08)* 3.29 (0.13)
Tb.Sp 0.13 (0.01)* 0.14 (0.02) 0.08 (0.01) 0.18 (0.02)* 0.14 (0.01) 0.12 (0.01) 0.11 (0.01)* 0.13 (0.02) 0.12 (0.01) 0.10 (0.01)* 0.11 (0.01) 0.12 (0.01) 0.08 (0.01)* 0.09 (0.01) 0.12 (0.02)
Tb.Th 0.18 (0.01)* 0.11 (0.09) 0.09 (0.01) 0.12 (0.02) 0.11 (0.02) 0.06 (0.01)* 0.12 (0.02) 0.06 (0.02)* 0.11 (0.01) 0.12 (0.02)*y 0.10 (0.02)* 0.0 (0.01) 0.11 (0.02) 0.10 (0.01) 0.07 (0.01)*
Regions of interest 3 and 4 are omitted because of the similar changes in BV/TV, Tb.N, Tb.Th, and Tb.Sp to regions 1 and 2. A, BoneCeramic; B, Bio-Oss; C, control. *Significance between the experimental groups and the control; ysignificance between the 2 experimental groups (P \0.05).
1
), Tb.Sp (mm), and Tb.Th
Table II. Descriptive statistics (means and standard deviations) of BV/TV (%), Tb.N (mm
(mm) in regions of interest (ROI) 7 and 8 ROI 7 Day 0
7
14
21
28
Group A B C A B C A B C A B C A B C
BV/TV 82.72 (5.78)*y 62.25 (4.18)* 53.91 (3.36) 60.25 (5.56)*y 50.21 (2.59)* 36.16 (5.78) 24.15 (3.56) 22.37 (2.54) 17.37 (4.12)* 36.29 (4.16)*y 27.18 (1.38)* 22.74 (2.54) 38.13 (3.56)*y 27.19 (1.19)* 25.21 (2.54)
Tb.N 4.95 (0.14)* 4.54 (0.13) 4.20 (0.12) 4.52 (0.11)*y 3.92 (0.14)* 3.20 (0.08) 4.01 (0.11) 2.48 (0.08) 1.53 (0.12)* 3.75 (0.14)* 2.62 (0.08) 2.62 (0.12) 3.77 (0.12) 3.36 (0.14) 2.96 (0.15)
ROI 8 Tb.Sp 0.17 (0.02) 0.13 (0.01) 0.14 (0.02) 0.15 (0.01) 0.15 (0.02) 0.14 (0.01) 0.23 (0.02) 0.23 (0.02) 0.22 (0.01) 0.17 (0.02) 0.16 (0.02) 0.17 (0.01) 0.15 (0.02) 0.17 (0.02) 0.16 (0.01)
Tb.Th 0.12 (0.02) 0.11 (0.01) 0.10 (0.02) 0.09 (0.02)* 0.07 (0.01) 0.07 (0.02) 0.05 (0.01) 0.05 (0.01) 0.08 (0.01)* 0.06 (0.02)*y 0.08 (0.02)* 0.10 (0.01) 0.08 (0.01) 0.06 (0.01) 0.07 (0.02)
BV/TV 34.60 (3.35) 30.00 (3.11)* 30.45 (3.56) 20.97 (4.12) 18.73 (2.54) 12.28 (1.38)* 21.25 (4.12) 19.27 (1.19) 12.39 (1.38)* 20.15 (2.54) 20.47 (2.01) 17.40 (2.94)* 17.58 (4.12) 17.50 (1.38) 15.57 (2.54)*
Tb.N 3.58 (0.11)*y 3.68 (0.12)* 2.37 (0.11) 2.35 (0.12)* 2.05 (0.08) 2.06 (0.11) 2.42 (0.14) 2.04 (0.08) 1.70 (0.11)* 3.13 (0.14) 2.85 (0.08) 2.69 (0.11)* 3.21 (0.12) 3.07 (0.14) 3.03 (0.12)
Tb.Sp 0.17 (0.01) 0.15 (0.02) 0.13 (0.01)* 0.15 (0.01) 0.14 (0.01) 0.15 (0.02) 0.15 (0.01) 0.14 (0.02) 0.14 (0.01)* 0.15 (0.02)*y 0.18 (0.01)* 0.15 (0.01) 0.15 (0.02) 0.13 (0.01) 0.14 (0.01)
Tb.Th 0.08 (0.01) 0.08 (0.01) 0.08 (0.01) 0.09 (0.02) 0.09 (0.02) 0.08 (0.01) 0.08 (0.02) 0.08 (0.01) 0.06 (0.01)* 0.11 (0.02) 0.08 (0.02) 0.07 (0.01) 0.09 (0.01) 0.09 (0.02) 0.08 (0.01)
Regions of interest 5 and 6 are omitted because of the similar changes in BV/TV, Tb.N, Tb.Th, and Tb.Sp to regions 7 and 8. A, BoneCeramic; B, Bio-Oss; C, control. *Significance between the experimental groups and the control; ysignificance between the 2 experimental groups (P \0.05).
especially in the control group (0.078 6 0.002 mm3; Fig 4). The smallest root resorption volumes occurred in the cervical region of the distobuccal root in all groups, especially in the BoneCeramic group (0.039 6 0.003 mm3; Fig 4). Root resorption crater volumes significantly increased from days 0 to 7 (BoneCeramic, 0.067 6 0.002 mm3; Bio-Oss, 0.069 6 0.002 mm3; control, 0.074 6 0.001 mm3) and plateaued until day
28 in the apical regions in all groups (BoneCeramic, 0.068 6 0.002 mm3; Bio-Oss, 0.070 6 0.002 mm3; control, 0.075 6 0.002 mm3). However, in the cervical regions, root resorption crater volumes significantly increased from days 0 to 14 (BoneCeramic, 0.044 6 0.001 mm3; Bio-Oss, 0.054 6 0.002 mm3; control: 0.062 6 0.002 mm3) and plateaued from days 14 to 28 (BoneCeramic, 0.045 6 0.001 mm3; Bone-Oss,
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Table III. Descriptive statistics (means and standard deviations) of BV/TV (%), Tb.N (mm
1
), Tb.Sp (mm), and Tb.Th
(mm) in region of interest (ROI) 10 ROI 10 Day 0
7
14
21
28
Group A B C A B C A B C A B C A B C
BV/TV 20.02 (3.56) 20.94 (2.06) 21.52 (1.18)* 14.26 (1.26) 15.24 (1.64) 14.48 (2.16) 17.44 (1.19) 16.37 (2.96) 15.36 (1.38) 25.21 (2.51) 23.47 (2.04) 20.24 (2.54) 27.92 (2.21) 26.91 (2.01) 27.28 (2.54)
Tb.N 2.74 (0.09) 3.32 (0.12) 2.65 (0.07) 1.97 (0.08) 2.07 (0.05) 1.75 (0.04) 2.01 (0.06) 2.32 (0.09) 2.06 (0.07) 3.09 (0.08) 2.65 (0.06) 2.59 (0.05) 4.23 (0.12)*y 3.87 (0.08)* 2.13 (0.07)
Tb.Sp 0.16 (0.02) 0.15 (0.01) 0.12 (0.01) 0.20 (0.02) 0.18 (0.02) 0.17 (0.01) 0.12 (0.01)* 0.17 (0.01) 0.15 (0.02) 0.15 (0.02) 0.16 (0.01) 0.15 (0.02) 0.14 (0.02) 0.13 (0.01) 0.14 (0.01)
Tb.Th 0.10 (0.02) 0.09 (0.02) 0.08 (0.01) 0.05 (0.01) 0.08 (0.02) 0.07 (0.02) 0.08 (0.01) 0.08 (0.01) 0.07 (0.02) 0.07 (0.02) 0.06 (0.01) 0.06 (0.01) 0.09 (0.02) 0.08 (0.02) 0.07 (0.01)
Region of interest 9 is omitted because of the similar changes in BV/TV, Tb.N, Tb.Th, and Tb.Sp to region 10. A, BoneCeramic; B, Bio-Oss; C, control. *Significance between the experimental groups and the control; ysignificance between the 2 experimental groups (P \0.05).
Fig 3. Reconstructed 3D images of the mesiobuccal (MB), distobuccal (DB), mesiolingual (ML), and distolingual (DL) roots at different time points in groups A (BoneCeramic), B (Bio-Oss), and C (control). White arrows indicate root lacunae.
0.056 6 0.002 mm3; control, 0.065 6 0.002 mm3; Fig 4). In the histology testing, root resorption was found on the mesial and distal sides of all roots after tooth movement, especially on the mesiobuccal and distobuccal
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roots in all groups. In the BoneCeramic group, root resorption mostly occurred on the distal surfaces of the cervical region of the distobuccal root, with mostly small and shallow craters with clear margins (Fig 5, A). In the Bio-Oss group, root resorption occurred on the mesial
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Fig 4. Schematics of root resorption crater volumes of the mesiolingual (ML), distolingual (DL), mesiobuccal (MB), and distobuccal (DB) root; root resorption crater volumes in the cervical (CML, CDL, CMB, and CDB) and apical (AML, ADL, AMB, and ADB) regions of the roots at different time points in the 3 groups. *Significance between the experimental groups and the control (P \0.05).
Fig 5. Histologic slices depicting damaged root surfaces with hematoxylin and eosin staining in the 3 groups: A, BoneCeramic; B, Bio-Oss; C, control. Black arrows indicate root resorption craters; M and D indicate the mesial and distal surfaces, respectively. D-F, In the visualized finite element models of the tooth roots, different amounts of stress were distributed on the root surfaces. White arrows indicate the loading forces.
surface of the apical regions of the mesiobuccal and distobuccal roots, with wide shallow or deep resorption craters. Multinucleated osteoclasts appeared in the root resorption lacunae with some evident deposition of cellular cementum on resorbed root cavities (Fig 5, B).
In the control group, the largest root resorption crater was found on the distal surface of the mesiobuccal root. It extended from the cervical region to the apical region with massive dentin destruction. Small or wide resorption craters were also observed on the mesial
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and distal surfaces of the mesiobuccal and distobuccal roots (Fig 5, C). When tested with the finite element method, more stress accumulated in the cervical region than in the apical region of the root surface. The highest level of stress accumulated on the mesial side in the cervical region of the mesiolingual root, followed by the mesial side of the cervical region of the mesiobuccal root, and the distal side of the cervical region of the distobuccal and distolingual roots (Fig 5, D-F). DISCUSSION
This study demonstrated that it is feasible to move a tooth into a BoneCeramic grafting extraction site that intends to preserve bone and reduce the potential for alveolar bone loss. Our data showed that the rats' second molars experienced the least tooth movement rate when they traveled through the BoneCeramic grafts, followed by the Bio-Oss grafts and the control extraction sites with no grafts. This result is opposite to that found by Seifi and Ghoraishian,23 who observed an increased tooth movement rate in the group with the alveolar defect filled with demineralized freeze-dried bone allograft. Others reported that a similar tooth movement distance was observed between the group filled with Bio-Oss and the control group.10 However, with the same amount of orthodontic traction force, it is obvious that bone substitutes decrease the tooth movement rate. The rats' extraction site healing process consisted of 3 phases: (1) organization of the blood clot and covering of the extraction socket by epithelium (1-5 days), (2) new bone formation (5-20 days), and (3) new bone maturation and alveolar ridge remodeling (20-60 days).24,25 The alveolar ridge resorbs with significant reductions in height and width; this is more pronounced during the initial phase of wound healing than during later phases. Schropp et al26 stated that in humans approximately two thirds of this reduction occurs within the first 3 months after tooth extraction. The healing process of a rat's extraction site is similar to a human's but 3 times faster, indicating that the alveolar ridge resorbs within 1 month in rats after tooth removal.27 In our study, grafting of bone substitutes immediately after extraction slowed ridge resorption. When the second molars were moved into the alveolar ridge defects 1 month after bone grafting, bone substitutes were not absorbed completely, with new bone forming in the extraction sockets. Measuring the distance of tooth movement, the bone density, and the root resorption provided the means of evaluating the feasibility of moving teeth into the augmented alveolar ridges with or without adverse effects.
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It was evident that the placement of a bone substitute interfered with the processes of bone modeling and remodeling. In regions of interest 1, 2, and 7 of the BoneCeramic group, the highest levels of BV/TV, Tb.N, and Tb.Th, and the lowest level of Tb.Sp indicated the increased new bone formation in the extraction sites. These demonstrated that BoneCeramic stimulates bone growth with increases in both Tb.N and Tb.Th, implying that BoneCeramic has the potential for osteoconduction. These findings agree with those of Mardas et al19 that BoneCeramic completely preserved the height and width of the alveolar ridge and the interproximal bone in the extraction sites. Because of the highest BV/TV in the BoneCeramic group (BoneCeramic, 69.6%; BioOss, 62.3%; control, 52.8%) (Fig 2), the tooth movement distance and the rate decreased. This is supported by others, showing that the tooth movement rate relies on the density of the alveolar bone.28-30 The tooth movement rate depends on removing hyalinized tissue on the compression side of alveolar bone caused by direct or undermining bone resorption.31 From days 0 to 7, stress on the tooth root induced alveolar bone resorption, shown by decreases in BV/TV, Tb.N, and Tb.Th in region of interest 7 (Table II). Meanwhile, the tooth was rapidly moved into the space of the resorbed bone with a significantly increased tooth movement rate. Once the tooth is completely moved into the resorbed space, the roots were again pulled against the alveolar bone and developed hyalinized tissues.32 It is believed that hyalinization of the tissues provides high resistance and slows orthodontic tooth movement as shown from days 7 to 14 in our study. To continue tooth movement, hyalinized tissues need to be removed by undermining bone resorption. Osteoclasts continued to resorb bone as indicated by decreased BV/TV, Tb.N, and Tb.Th. Interestingly, in all groups, Tb.Sp significantly decreased accompanied by increased BV/TV, Tb.N, and Tb.Th from days 14 to 28 (Fig 2), suggesting that bone regeneration in the extraction sites was preserved by BoneCeramic in the later period of orthodontic treatment. In this study, bone density increased more in the regions of BoneCeramic grafting compared with Bio-Oss grafting, and both grafting methods slowed tooth movement. Under clinical conditions, slowing tooth movement by bone graft materials may be good for preventing neighboring teeth from drifting into the space that is to be prepared for the implant. Whether to graft BoneCeramic or Bio-Oss depends on the alveolar ridge defect width and height, and the tooth movement design. The orthodontist should anticipate how the defect will affect tooth movement and consider which bone substitute will preserve the alveolar ridge better.
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Since two thirds of alveolar ridge resorption occurs in the first 3 months after tooth extraction, this resorption becomes stable in 6 months.26 If the extraction space can be closed in 6 months, Bio-Oss could be placed in the extraction site and will not affect tooth movement. However, if the extraction space would take longer than 6 months to close, the patient might be left with a periodontally involved first molar and lack of alveolar bone around the molar. The orthodontic mechanics are to extract the first molar and to mesialize the second molar to replace the missing first molar. It takes a long time to mesialize the molar and needs enough bone to sustain the alveolar ridge width and height. BoneCeramic increases bone density more and preserves the alveolar ridge for a longer time than does Bio-Oss, and there is no difference in tooth movement rates between BoneCeramic and Bio-Oss at the end of the orthodontic loading cycle. Therefore, BoneCeramic should be grafted in the alveolar ridge defect. Accompanied by tooth movement, root resorption increased significantly from days 0 to 7 after grafting with BoneCeramic. This result agreed with our previous experiment that most resorption occurred on the apical third of the root on day 7.20 However, the whole root resorption volume did not increase from days 7 to 28, suggesting that the root resorption craters were stabilized. The mesiolingual and distolingual roots showed great amounts of root resorption and stress on the root surfaces. These findings are supported by those of Chan and Darendeliler33 that more root resorption undergoes a higher level of stress. Interestingly, our reconstructed 3D images and histologic findings of tooth roots showed that wide or deep resorption craters did not concentrate in the regions with the highest accumulated stress, but rather in the distal and apical regions. This was because the tooth was tipped rather than translated forward in parallel. The distal and apical regions were subjected to accumulated stress on the relatively small root surface. The volumetric measurements and finite element method model also confirmed that the apical regions had smaller volumes and underwent higher levels of stress per unit of area. Therefore, more root resorption appeared in the distal and apical regions. The root resorption volumes in the extraction sites preserved by BoneCeramic did not increase significantly compared with the other groups. We deduced that BoneCeramic is safe and therapeutic for alveolar bone formation and orthodontic tooth movement. CONCLUSIONS
It is suggested that although BoneCeramic slows orthodontic tooth movement, it has a better osteoconductive potential and induces less root resorption compared
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with Bio-Oss grafting and naturally recovered extraction sites. REFERENCES 1. Mayer T, Basdra EK, Komposch G, Staehle HJ. Localized alveolar ridge augmentation before orthodontic treatment. A case report. Int J Oral Maxillofac Surg 1994;23:226-8. 2. Sheats RD, Strauss RA, Rubenstein LK. Effect of a resorbable bone graft material on orthodontic tooth movement through surgical defects in the cat mandible. J Oral Maxillofac Surg 1991;49: 1299-304. 3. Re S, Corrente G, Abundo R, Cardaropoli D. Orthodontic treatment in periodontally compromised patients: 12-year report. Int J Periodontics Restorative Dent 2000;20:31-9. 4. Noda K, Yoshii T, Nakamura Y, Kuwahara Y. The assessment of optimal orthodontic force in various tooth movements. Comparisons of tooth movement, root resorption and degenerating tissues in tipping movement. Orthod Waves 2000;59:329-41. 5. Rotundo R, Nieri M, Iachetti G, Mervelt J, Cairo F, Baccetti T, et al. Orthodontic treatment of periodontal defects: a systematic review. Prog Orthod 2010;11:41-4. 6. Wennstrom J, Stokland BL, Nyman S, Thilander B. Periodontal tissue response to orthodontic movement of teeth with infrabony pockets. Am J Orthod Dentofacial Orthop 1993;103:313-9. 7. Klinge B, Alberius P, Isaksson S, Jonssen J. Osseous response to implanted natural bone mineral and synthetic hydroxylapatite ceramic in the repair of experimental skull bone defects. J Oral Maxillofac Surg 1992;50:241-9. 8. Kaminishi R, Davis WH, Hochwald D, Berger R, Davis C. Reconstruction of alveolar width for orthodontic tooth movement: a case report. Am J Orthod 1986;89:342-5. 9. Carmagnola D, Adriaens P, Berglundh T. Healing of human extraction sockets filled with Bio-Oss. Clin Oral Implants Res 2003;14: 137-43. 10. Feinberg SE, Weisbrode SE, Heintschel G. Radiographic and histologic analysis of tooth eruption through calcium phosphate ceramics in the cat. Arch Oral Biol 1989;34:975-84. 11. Oltramari VP, Navarro RL, Henriques FC, Taga R, Cestari TM, Ceolin DS, et al. Orthodontic movement in bone defects filled with xenogenic graft: an experimental study in minipigs. Am J Orthod Dentofacial Orthop 2007;131:302.e10-7. 12. Cardaropoli G, Araujo M, Hayacibara R, Sukekava F, Lindhe J. Healing of extraction sockets and surgically produced— augmented and non-augmented—defects in the alveolar ridge. An experimental study in the dog. J Clin Periodontol 2005; 32:435-40. 13. Norton MR, Odell EW, Thompson ID, Cook RJ. Efficacy of bovine bone mineral for alveolar augmentation: a human histologic study. Clin Oral Implants Res 2003;14:775-83. 14. Artzi Z, Tal H, Dayan D. Porous bovine bone mineral in healing of human extraction sockets. Part 1: histomorphometric evaluations at 9 months. J Periodontol 2000;71:1015-23. 15. Kesmas S, Swasdison S, Yodsanga S, Sessirisombat S, Jansisyanont P. Esthetic alveolar ridge preservation with calcium phosphate and collagen membrane: preliminary report. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;110:e24-36. 16. Kwon S, Jun Y, Hong S, Kim H. Synthesis and dissolution behavior of b-TCP and HA/b-TCP composite powders. J Eur Ceram Soc 2003;23:1039-45. 17. Piattelli A, Scarano A, Mangano C. Clinical and histologic aspects of biphasic calcium phosphate ceramic (BCP) used in connection with implant placement. Biomaterials 1996;17:1767-70.
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18. Cordaro L, Bosshardt DD, Palattella P, Rao W, Serino G, Chiapasco M. Maxillary sinus grafting with Bio-Oss or Straumann Bone Ceramic: histomorphometric results from a randomized controlled multicenter clinical trial. Clin Oral Implants Res 2008;19:796-803. 19. Mardas N, Chadha V, Donos N. Alveolar ridge preservation with guided bone regeneration and asynthetic bone substitute or a bovine-derived xenograft: a randomized, controlled clinical trial. Clin Oral Implants Res 2010;21:688-98. 20. Ru N, Liu SS, Zhuang L, Li S, Bai Y. In vivo microcomputed tomography evaluation of rat alveolar bone and root resorption during orthodontic tooth movement. Angle Orthod 2013;83:402-9. 21. Harris DA, Jones AS, Darendeliler MA. Physical properties of root cementum: part 8. Volumetric analysis of root resorption craters after application of controlled intrusive light and heavy orthodontic forces: a microcomputed tomography scan study. Am J Orthod Dentofacial Orthop 2006;130:639-47. 22. Gonzales C, Hotokezaka H, Arai Y, Ninomiya T, Tominaga J, Jang I, et al. An in vivo 3D micro-CT evaluation of tooth movement after the application of different force magnitudes in rat molar. Angle Orthod 2009;79:703-14. 23. Seifi M, Ghoraishian SA. Determination of orthodontic tooth movement and tissue reaction following demineralized freeze-dried bone allograft grafting intervention. Dent Res J 2012;9:203-8. 24. Bodner L, Kaffe I, Littner MM, Cohen J. Extraction site healing in rats. A radiologic densitometric study. Oral Surg Oral Med Oral Pathol 1993;75:367-72. 25. Pietroknviski J, Massler M. Ridge remodeling after tooth extraction in rats. J Dent Res 1967;46:222-31. 26. Schropp L, Wenzel A, Kostopoulos L, Karring T. Bone healing and soft tissue contour changes following single-tooth extraction: a
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clinical and radiographic 12-month prospective study. Int J Periodontics Restorative Dent 2003;23:313-23. Astrand P, Carlsson G. Change in the alveolar process after extraction in the white rat: a histologic and fluorescence microscopic study. Acta Odontol Scand 1969;27:113-27. Deguchi T, Takano-Yamamoto T, Yabuuchi T, Ando R, Roberts WE, Garetto LP. Histomorphometric evaluation of alveolar bone turnover between the maxilla and the mandible during experimental tooth movement in dogs. Am J Orthod Dentofacial Orthop 2008;133:889-97. Sidiropoulou-Chatzigiannis S, Kourtidou M, Tsalikis L. The effect of osteoporosis on periodontal status, alveolar bone and orthodontic tooth movement. A literature review. J Int Acad Periodontol 2007;9:77-84. Milne TJ, Ichim I, Patel B, McNaughton A, Meikle MC. Induction of osteopenia during experimental tooth movement in the rat: alveolar bone remodelling and the mechanostat theory. Eur J Orthod 2009;31:221-31. Kohno T, Matsumoto Y, Kanno Z, Warita H, Soma K. Experimental tooth movement under light orthodontic forces: rates of tooth movement and changes of the periodontium. J Orthod 2002;29: 129-35. Nakamura Y, Noda K, Shimoda S, Oikawa T, Arai C, Nomura Y, et al. Time-lapse observation of rat periodontal ligament during function and tooth movement, using microcomputed tomography. Eur J Orthod 2008;30:320-6. Chan E, Darendeliler MA. Physical properties of root cementum: part 7. Extent of root resorption under areas of compression and tension. Am J Orthod Dentofacial Orthop 2006;129: 504-10.
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BoneCeramic graft regenerates alveolar defects but slows orthodontic tooth movement with less root resorption Nan Ru,a Sean Shih-Yao Liu,b Yuxing Bai,c Song Li,c Yunfeng Liu,d and Xiaoxia Weie Beijing, Hangzhou, and Zhengzhou, China, and Indianapolis, Ind
Introduction: BoneCeramic (Straumann, Basel, Switzerland) can regenerate bone in alveolar defects after tooth extraction, but it is unknown whether it is feasible to move a tooth through BoneCeramic grafting sites. The objective of this study was to investigate 3-dimensional real-time root resorption and bone responses in grafted sites during orthodontic tooth movement. Methods: Sixty 5-week-old rats were randomly assigned to 3 groups to receive BoneCeramic, natural bovine cancellous bone particles (Bio-Oss; Geistlich Pharma, Wolhusen, Switzerland), or no graft, after the extraction of the maxillary left first molar. After 4 weeks, the maxillary left second molar was moved into the extraction site for 28 days. Dynamic bone microstructures and root resorption were evaluated using in-vivo microcomputed tomography. Stress distribution and corresponding tissue responses were examined by the finite element method and histology. Mixed model analysis of variance was performed to compare the differences among time points with Bonferroni post-hoc tests at the significance level of P \0.05. Results: The BoneCeramic group had the least amount of tooth movement and root resorption volumes and craters, and the highest bone volume fraction, trabecular number, and mean trabecular thickness, followed by the Bio-Oss and the control groups. The highest stress accumulated in the cervical region of the mesial roots. Conclusions: BoneCeramic has better osteoconductive potential and induces less root resorption compared with Bio-Oss grafting and naturally recovered extraction sites. (Am J Orthod Dentofacial Orthop 2016;149:523-32)
M
oving a tooth orthodontically into the region of an alveolar defect with insufficient buccolingual width can be problematic.1 It often causes root resorption,2 gingival recessions,3 periodontal
a Lecturer, Department of Orthodontics, School of Stomatology, Capital Medical University, Beijing, China. b Associate professor; director, Mineralized Tissues and Histology Research Laboratory; and director, Orthodontic Fellowship Program, Department of Orthodontics and Oral Facial Genetics, Indiana University School of Dentistry, Indianapolis, Ind. c Professor, Department of Orthodontics, School of Stomatology, Capital Medical University, Beijing, China. d Associate professor, Key Laboratory of Equipment & Manufacturing, Zhejiang University of Technology, Hangzhou, China. e Associate professor, Department of Orthodontics, School of Stomatology, Zhengzhou University, Zhengzhou, China. Nan Ru and Sean Shih-Yao Liu are joint first authors and contributed equally to this work. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Supported by a grant from the Natural Science Foundation of China (81400537). Address correspondence to: Yuxing Bai, Department of Orthodontics, School of Stomatology, Capital Medical University, Tiantan Xili 4, Chongwen District, Beijing, China 100050; e-mail, [email protected]. Submitted, December 2014; revised and accepted, September 2015. 0889-5406/$36.00 Copyright Ó 2016 by the American Association of Orthodontists. http://dx.doi.org/10.1016/j.ajodo.2015.09.027
pockets,4 and traumatic injuries to pulp vitality.5 Alveolar defects may appear in patients with cleft lip and palate. If the cleft involves the alveolus, the alveolar ridge defects in these sites impede tooth eruption6 and delay orthodontic tooth movement with prolonged treatment times.7 Alveolar defects may also be secondary to a large piece of buccal plate with the extraction of an impacted tooth, jaw inflammation, or cyst and trauma surgery.1 Similar scenarios can be seen during extensive remodeling of the edentulous alveolus after the extraction of damaged or periodontal-involved first molars. For some adolescent and young adults, once periodontal disease is under control, an effective way to replace a missing molar is to move the adjacent molar into the first molar area.1 However, alveolar bone in extraction sites quickly resorbs, with reduced height and width, primarily changing to dense cortical bone, which impedes the movement of teeth through the bone. Orthodontic tooth movement is not feasible without reestablishment of the alveolar width with bone grafts before movement.8 To alleviate alveolar ridge resorption and regenerate alveolar bone in the defects, bone grafts, such as autogenous bone, allograft,9 or alloplast,10 can be placed in 523
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the extraction sites immediately after tooth extraction.11 Although autogenous bone is recognized as the gold standard for bone grafts because of the viability of transferable osteogenic cells, it requires a second surgery from the donor site. Patients tend to decline this treatment modality because of the additional discomfort.12 Alternatively, deproteinized bovine bone mineral (Bio-Oss; Geistlich Pharma, Wolhusen, Switzerland) can be used as a graft material for augmenting an alveolar ridge defect.13 However, Bio-Oss degrades slowly and induces uncertain immune responses and fibrous encapsulation with healing.14 A new synthetic bone substitute, BoneCeramic (Straumann, Basel, Switzerland), has been used for ridge preservation because it can be rapidly replaced by regenerative bone.15,16 BoneCeramic consists of 60% hydroxyapatite and 40% beta tricalcium phosphate. After grafting, beta tricalcium phosphate is rapidly resorbed and completely replaced by regenerative bone.17 Meanwhile, the hydroxyapatite, resorbed slowly, serves as a good matrix scaffold for ingrowth of new blood vessels and attachment of bone-forming cells.18 Bone can be greatly regenerated because BoneCeramic can be totally resorbed and subsequently replaced by host bone in a shorter time.19 However, whether it will hamper orthodontic tooth movement in an augmented area of alveolar ridge is still unknown. To evaluate whether a tooth can be moved into an extraction site with bone grafts, one should investigate the rate or distance of orthodontic tooth movement with accompanied bone responses or adverse side effects. The aims of this experiment were (1) to evaluate whether it is feasible to move a tooth in an alveolar ridge augmented with BoneCeramic, and (2) to evaluate realtime 3-dimensional (3D) changes in root resorption and bone microarchitectures, and tissue responses when moving teeth into BoneCeramic and Bio-Oss grafts after extractions. Understanding the dynamic responses in bone graft resorption, bone regeneration, and root resorption will help to establish treatment guidelines for patients. MATERIAL AND METHODS
All procedures were approved by the institutional animal care and use committee of the School of Stomatology, Capital Medical University, Beijing, China. After they were acclimated, 60 male Sprague Dawley rats (age, 5 weeks) (specific pathogen free level 3) had the maxillary left first molar extracted under anesthesia by chloral hydrate (2 mL/kg) injected intraperitoneally. A rectangular (3 3 2 3 2 mm) alveolar ridge defect was created in the socket by completely resecting the intraradicular septa between the tooth roots at the extraction
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sites with a low-speed dental handpiece. The animals were randomly assigned to 3 groups (n 5 20 per group) to receive BoneCeramic (60% hydroxyapatite, 40% beta tricalcium phosphate granules), Bio-Oss (natural bovine spongiosa granules, 0.25-1 mm), or no grafting. The mucosa was reflected and sutured to cover the socket to prevent the materials from leaking. Signs of infection, animal weight, and health conditions were monitored. Four weeks after the extractions, a groove was prepared at the cervical third of the incisors under anesthesia. A nickel-titanium coil spring (0.2 mm in diameter; IMD, Shanghai, China) was ligated between the maxillary left second molar and incisors using an 0.08-in ligature wire secured with bonding adhesive (Transbond; 3M Unitek, Monrovia, Calif). The spring was activated for approximately 1 mm to produce 10 g of continuous force to move the molar forward into the extraction site (Fig 1, A). After spring installation, each animal was scanned using an in-vivo microcomputed tomography system (SkyScan1076; Bruker, Kontich, Belgium) on days 0, 7, 14, 21, and 28. The spring was removed for each invivo microcomputed scan and reattached after scanning. The palate was secured at the supine position parallel to the stage in a carbon composite animal holder. The head was scanned through 180 of rotation at a 0.5 increment with 2 seconds per degree with resolution of 18 mm per pixel. Data were further reconstructed to provide axial cross-section images with SkyScan NRecon software (version 1.4.4; Bruker) and converted into 16bit bitmapped TIFF images with a resolution of 1024 3 1024 pixels.20 Tooth movement distance (Di) (mm) was measured 3 times and averaged at each time point (i 5 0, 7, 14, 21, and 28 days). Tooth movement rate (Vi) was then calculated as Vi 5ðDi Di1 Þ=7 (Fig 1, B). The alveolar bone was equally divided into the cervical and apical regions by a selected middle axial slice from the root apex to the furcation. In the apical region, 6 regions of interest (360 mm3) were selected: 500 mm mesial to the mesiobuccal and the mesiolingual roots, 500 mm distal to the distobuccal and the distolingual roots, and the intraradicular septa between the mesiobuccal and distobuccal roots and between the mesiolingual and distolingual roots (Fig 1, C). In the cervical region, 4 regions of interest (360 mm3) were selected: 500 mm mesial to the mesiobuccal and the mesiolingual roots, and distal to the distobuccal and the distolingual roots (Fig 1, D). Three-dimensional microarchitecture parameters for trabecular bone were measured as the following: bone volume fraction (BV/TV), indicating the ratio of bone volume to total volume; mean trabecular thickness
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Fig 1. A, Schematic of orthodontic tooth movement into the bone graft area. Dotted shadow, the alveolar ridge defect was embedded with bone grafts after the maxillary left first molar extraction; the nickeltitanium spring was ligated to move the molar forward into the extraction site. M2, maxillary left second molar. B, Sagittal view of the tooth roots. Tooth movement distance (Di) was calculated as the shortest width between the second and third molar crowns on the sagittal plane along the distal root of the third molar. White squares, regions of interest. C, Horizontal view of the apical region of tooth roots: 1-6 squares represent the selected regions of interest in the alveolar bone adjacent to the apical region of the 4 roots of the maxillary left second molar. D, Horizontal view of the cervical region of the tooth roots: 7-10 squares represent the selected regions of interest in the alveolar bone adjacent to the cervical region of the 4 roots of the maxillary left second molar. E, Tooth movement distances at different time points in the 3 groups. *Significance between the experimental groups and the control (P \0.05). F, Tooth movement rates at different time points in the 3 groups. *Significance between the experimental groups and the control (P \0.05).
(Tb.Th), indicating the local thickness at each voxel representing bone; trabecular number (Tb.N), indicating the average number of trabeculae per unit of length; and trabecular separation (Tb.Sp), indicating the mean distance between trabeculae. After segmenting the roots from the images using Mimics software (version 17.0; Materialise, Leuven, Belgium), the cervical, apical, and total root volumes of each root were measured for each time point.21 The volumes of root resorption in each region on days 7, 14, 21, and 28 were calculated by subtracting the root volume at each time point from the root volume on day 0. After 28 days, the animals were killed, and the maxillae were dissected, fixed, decalcified, and embedded in paraffin and serially sectioned (5 mm) along the mesiodistal axis of the second molar. The sections were stained with hematoxylin and eosin.
A 3D finite element method model of the maxillary second molar (day 0) was constructed with the Mimics software and imported into Ansys software (Ansys, Canonsburg, Pa). The geometry of the model consisted of 50019 isoparametric tetrahedral-node solid elements and 69731 nodes. The width of the periodontal ligament was set at 0.2 mm, and Young's modulus of the tooth, periodontal ligament, and bone were set as 19,600, 0.7, and 13,700 MPa, respectively. The Poisson ratios of the tooth, periodontal ligament, and bone were 0.15, 0.49, and 0.15, respectively.22 A 10-g force was applied in the finite element method model in the same direction as the spring attached intraorally. Movement was suppressed in 6 degrees of freedom for the nodes on the bottom edge of the alveolar bone. Tooth displacement and stress distribution analyses were performed with the Ansys software.
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Fig 2. Microarchitecture parameter schematic of region of interest 1 adjacent to the second molar: bone volume fraction (BV/TV), trabecular number (Tb.N), trabecular separation (Tb.Sp), mean trabecular thickness (Tb.Th), and at different time points in the BoneCeramic, Bio-Oss, and control groups. *Significance between the experimental groups and the control (P \0.05).
Statistical analysis
For each parameter, mixed-model measures analysis of variance was performed to compare the differences among time points and between groups with Bonferroni post hoc tests using the Statistical Package for the Social Sciences (version 11.5; SPSS, Chicago, Ill). The significance level was set at P \0.05. RESULTS
The greatest amount of tooth movement was observed in the control group, followed by the Bio-Oss group and then the BoneCeramic group (Fig 1, E). In all groups, tooth movement rates accelerated from days 0 to 7 and slightly decelerated from days 7 to 14. This similar tooth movement pattern repeated with acceleration from days 14 to 21, followed by deceleration from days 21 to 28 (Fig 1, F). In all regions of interest, the BV/TV, Tb.N, and Tb.Th significantly decreased from days 0 to 7 but increased from days 14 to 28, except for regions of interest 2 and 8 in all groups. Tb.Sp significantly decreased from days 0 to 7 but fluctuated from days 14 to 28 in all groups (Fig 2). The typical changes of BV/TV, Tb.N, Tb.Th, and Tb.Sp in all regions of interest during tooth
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movement were found in regions of interest 1, 2, 7, 8, and 10 (Tables I-III; Fig 2). Regions of interest 3 to 6 and 9 are omitted because of their similar changes to regions of interest 1, 2, 7, 8, and 10. In the BoneCeramic group, BV/TV, Tb.N, and Tb.Th in regions of interest 1, 2, and 7 were significantly higher than in the Bio-Oss and control groups at each time point (Tables I and II; Fig 2). In the Bio-Oss group, BV/ TV and Tb.Th in regions of interest 2, 7, and 8 on days 0, 21, and 28 were significantly higher than in the control group (Tables I and II). Tb.Sp values in the BoneCeramic group from days 7 to 28 were significantly lower than in the other 2 groups in regions of interest 1, 2, and 10 (Tables I and III; Fig 2). However, in regions of interest 1, 2, and 7, there was no difference in Tb.Sp between the Bio-Oss and control groups (Tables I and II; Fig 2). Root volumes reduced in all groups over time. All roots had a smooth surface on day 0. Starting at day 7 through day 28, small isolated lacunae were mainly scattered on the mesial surfaces of the roots, and wide shallow resorption craters were observed mostly on the distal surfaces of the roots (Fig 3). The greatest root resorption volumes were observed in the apical region of the mesiobuccal root in all groups,
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Table I. Descriptive statistics (means and standard deviations) of BV/TV (%), Tb.N (mm
1
), Tb.Sp (mm), and Tb.Th
(mm) in regions of interest (ROI) 1 and 2 ROI 1 Day 0
7
14
21
28
Group A B C A B C A B C A B C A B C
BV/TV 82.98 (7.21)* 58.48 (8.22) 57.38 (8.24) 78.99 (5.21)* 45.24 (4.22) 35.08 (3.09) 45.22 (3.56)* 21.25 (4.63) 22.03 (5.21) 68.90 (4.11)* 58.33 (3.56) 34.58 (3.09) 69.06 (3.41)* 66.70 (3.56) 43.73 (4.11)
Tb.N 5.31 (0.12)* 4.78 (0.22) 5.86 (0.13) 4.96 (0.21)*y 3.12 (0.14)* 2.17 (0.11) 4.76 (0.08)* 3.01 (0.09) 3.12 (0.10) 4.27 (0.11) 4.28 (0.12) 3.21 (0.14)* 4.87 (0.09) 4.90 (0.12) 3.57 (0.15)
ROI 2
Tb.Sp 0.06 (0.01)* 0.10 (0.01) 0.08 (0.01) 0.09 (0.02)* 0.12 (0.01) 0.16 (0.02) 0.09 (0.01)* 0.19 (0.02) 0.11 (0.02) 0.07 (0.01)* 0.10 (0.01) 0.10 (0.01) 0.05 (0.01)* 0.13 (0.02) 0.13 (0.02)
Tb.Th 0.18 (0.02)* 0.10 (0.01) 0.11 (0.01) 0.12 (0.02)* 0.09 (0.01) 0.09 (0.01) 0.09 (0.01) 0.06 (0.01) 0.09 (0.01) 0.16 (0.02)*y 0.11 (0.01)* 0.06 (0.01) 0.17 (0.02)* 0.13 (0.02) 0.08 (0.01)
BV/TV 80.82 (5.12)*y 48.41 (4.12)* 23.78 (5.67) 57.57 (4.23)*y 42.47 (4.67)* 39.43 (5.78) 32.33 (6.79) 29.25 (2.54) 28.33 (2.57) 43.37 (4.12) 42.24 (4.67) 21.37 (3.29)* 42.46 (5.67) 43.33 (4.43) 23.40 (2.47)*
Tb.N 5.22 (0.14)* 4.11 (0.10) 4.08 (0.09) 4.25 (0.14) 4.10 (0.09) 2.47 (0.13)* 4.69 (0.10)*y 3.52 (0.12)* 2.50 (0.13) 5.10 (0.09) 4.29 (0.08) 2.85 (0.13) 5.51 (0.12)*y 4.46 (0.08)* 3.29 (0.13)
Tb.Sp 0.13 (0.01)* 0.14 (0.02) 0.08 (0.01) 0.18 (0.02)* 0.14 (0.01) 0.12 (0.01) 0.11 (0.01)* 0.13 (0.02) 0.12 (0.01) 0.10 (0.01)* 0.11 (0.01) 0.12 (0.01) 0.08 (0.01)* 0.09 (0.01) 0.12 (0.02)
Tb.Th 0.18 (0.01)* 0.11 (0.09) 0.09 (0.01) 0.12 (0.02) 0.11 (0.02) 0.06 (0.01)* 0.12 (0.02) 0.06 (0.02)* 0.11 (0.01) 0.12 (0.02)*y 0.10 (0.02)* 0.0 (0.01) 0.11 (0.02) 0.10 (0.01) 0.07 (0.01)*
Regions of interest 3 and 4 are omitted because of the similar changes in BV/TV, Tb.N, Tb.Th, and Tb.Sp to regions 1 and 2. A, BoneCeramic; B, Bio-Oss; C, control. *Significance between the experimental groups and the control; ysignificance between the 2 experimental groups (P \0.05).
1
), Tb.Sp (mm), and Tb.Th
Table II. Descriptive statistics (means and standard deviations) of BV/TV (%), Tb.N (mm
(mm) in regions of interest (ROI) 7 and 8 ROI 7 Day 0
7
14
21
28
Group A B C A B C A B C A B C A B C
BV/TV 82.72 (5.78)*y 62.25 (4.18)* 53.91 (3.36) 60.25 (5.56)*y 50.21 (2.59)* 36.16 (5.78) 24.15 (3.56) 22.37 (2.54) 17.37 (4.12)* 36.29 (4.16)*y 27.18 (1.38)* 22.74 (2.54) 38.13 (3.56)*y 27.19 (1.19)* 25.21 (2.54)
Tb.N 4.95 (0.14)* 4.54 (0.13) 4.20 (0.12) 4.52 (0.11)*y 3.92 (0.14)* 3.20 (0.08) 4.01 (0.11) 2.48 (0.08) 1.53 (0.12)* 3.75 (0.14)* 2.62 (0.08) 2.62 (0.12) 3.77 (0.12) 3.36 (0.14) 2.96 (0.15)
ROI 8 Tb.Sp 0.17 (0.02) 0.13 (0.01) 0.14 (0.02) 0.15 (0.01) 0.15 (0.02) 0.14 (0.01) 0.23 (0.02) 0.23 (0.02) 0.22 (0.01) 0.17 (0.02) 0.16 (0.02) 0.17 (0.01) 0.15 (0.02) 0.17 (0.02) 0.16 (0.01)
Tb.Th 0.12 (0.02) 0.11 (0.01) 0.10 (0.02) 0.09 (0.02)* 0.07 (0.01) 0.07 (0.02) 0.05 (0.01) 0.05 (0.01) 0.08 (0.01)* 0.06 (0.02)*y 0.08 (0.02)* 0.10 (0.01) 0.08 (0.01) 0.06 (0.01) 0.07 (0.02)
BV/TV 34.60 (3.35) 30.00 (3.11)* 30.45 (3.56) 20.97 (4.12) 18.73 (2.54) 12.28 (1.38)* 21.25 (4.12) 19.27 (1.19) 12.39 (1.38)* 20.15 (2.54) 20.47 (2.01) 17.40 (2.94)* 17.58 (4.12) 17.50 (1.38) 15.57 (2.54)*
Tb.N 3.58 (0.11)*y 3.68 (0.12)* 2.37 (0.11) 2.35 (0.12)* 2.05 (0.08) 2.06 (0.11) 2.42 (0.14) 2.04 (0.08) 1.70 (0.11)* 3.13 (0.14) 2.85 (0.08) 2.69 (0.11)* 3.21 (0.12) 3.07 (0.14) 3.03 (0.12)
Tb.Sp 0.17 (0.01) 0.15 (0.02) 0.13 (0.01)* 0.15 (0.01) 0.14 (0.01) 0.15 (0.02) 0.15 (0.01) 0.14 (0.02) 0.14 (0.01)* 0.15 (0.02)*y 0.18 (0.01)* 0.15 (0.01) 0.15 (0.02) 0.13 (0.01) 0.14 (0.01)
Tb.Th 0.08 (0.01) 0.08 (0.01) 0.08 (0.01) 0.09 (0.02) 0.09 (0.02) 0.08 (0.01) 0.08 (0.02) 0.08 (0.01) 0.06 (0.01)* 0.11 (0.02) 0.08 (0.02) 0.07 (0.01) 0.09 (0.01) 0.09 (0.02) 0.08 (0.01)
Regions of interest 5 and 6 are omitted because of the similar changes in BV/TV, Tb.N, Tb.Th, and Tb.Sp to regions 7 and 8. A, BoneCeramic; B, Bio-Oss; C, control. *Significance between the experimental groups and the control; ysignificance between the 2 experimental groups (P \0.05).
especially in the control group (0.078 6 0.002 mm3; Fig 4). The smallest root resorption volumes occurred in the cervical region of the distobuccal root in all groups, especially in the BoneCeramic group (0.039 6 0.003 mm3; Fig 4). Root resorption crater volumes significantly increased from days 0 to 7 (BoneCeramic, 0.067 6 0.002 mm3; Bio-Oss, 0.069 6 0.002 mm3; control, 0.074 6 0.001 mm3) and plateaued until day
28 in the apical regions in all groups (BoneCeramic, 0.068 6 0.002 mm3; Bio-Oss, 0.070 6 0.002 mm3; control, 0.075 6 0.002 mm3). However, in the cervical regions, root resorption crater volumes significantly increased from days 0 to 14 (BoneCeramic, 0.044 6 0.001 mm3; Bio-Oss, 0.054 6 0.002 mm3; control: 0.062 6 0.002 mm3) and plateaued from days 14 to 28 (BoneCeramic, 0.045 6 0.001 mm3; Bone-Oss,
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Table III. Descriptive statistics (means and standard deviations) of BV/TV (%), Tb.N (mm
1
), Tb.Sp (mm), and Tb.Th
(mm) in region of interest (ROI) 10 ROI 10 Day 0
7
14
21
28
Group A B C A B C A B C A B C A B C
BV/TV 20.02 (3.56) 20.94 (2.06) 21.52 (1.18)* 14.26 (1.26) 15.24 (1.64) 14.48 (2.16) 17.44 (1.19) 16.37 (2.96) 15.36 (1.38) 25.21 (2.51) 23.47 (2.04) 20.24 (2.54) 27.92 (2.21) 26.91 (2.01) 27.28 (2.54)
Tb.N 2.74 (0.09) 3.32 (0.12) 2.65 (0.07) 1.97 (0.08) 2.07 (0.05) 1.75 (0.04) 2.01 (0.06) 2.32 (0.09) 2.06 (0.07) 3.09 (0.08) 2.65 (0.06) 2.59 (0.05) 4.23 (0.12)*y 3.87 (0.08)* 2.13 (0.07)
Tb.Sp 0.16 (0.02) 0.15 (0.01) 0.12 (0.01) 0.20 (0.02) 0.18 (0.02) 0.17 (0.01) 0.12 (0.01)* 0.17 (0.01) 0.15 (0.02) 0.15 (0.02) 0.16 (0.01) 0.15 (0.02) 0.14 (0.02) 0.13 (0.01) 0.14 (0.01)
Tb.Th 0.10 (0.02) 0.09 (0.02) 0.08 (0.01) 0.05 (0.01) 0.08 (0.02) 0.07 (0.02) 0.08 (0.01) 0.08 (0.01) 0.07 (0.02) 0.07 (0.02) 0.06 (0.01) 0.06 (0.01) 0.09 (0.02) 0.08 (0.02) 0.07 (0.01)
Region of interest 9 is omitted because of the similar changes in BV/TV, Tb.N, Tb.Th, and Tb.Sp to region 10. A, BoneCeramic; B, Bio-Oss; C, control. *Significance between the experimental groups and the control; ysignificance between the 2 experimental groups (P \0.05).
Fig 3. Reconstructed 3D images of the mesiobuccal (MB), distobuccal (DB), mesiolingual (ML), and distolingual (DL) roots at different time points in groups A (BoneCeramic), B (Bio-Oss), and C (control). White arrows indicate root lacunae.
0.056 6 0.002 mm3; control, 0.065 6 0.002 mm3; Fig 4). In the histology testing, root resorption was found on the mesial and distal sides of all roots after tooth movement, especially on the mesiobuccal and distobuccal
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roots in all groups. In the BoneCeramic group, root resorption mostly occurred on the distal surfaces of the cervical region of the distobuccal root, with mostly small and shallow craters with clear margins (Fig 5, A). In the Bio-Oss group, root resorption occurred on the mesial
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Fig 4. Schematics of root resorption crater volumes of the mesiolingual (ML), distolingual (DL), mesiobuccal (MB), and distobuccal (DB) root; root resorption crater volumes in the cervical (CML, CDL, CMB, and CDB) and apical (AML, ADL, AMB, and ADB) regions of the roots at different time points in the 3 groups. *Significance between the experimental groups and the control (P \0.05).
Fig 5. Histologic slices depicting damaged root surfaces with hematoxylin and eosin staining in the 3 groups: A, BoneCeramic; B, Bio-Oss; C, control. Black arrows indicate root resorption craters; M and D indicate the mesial and distal surfaces, respectively. D-F, In the visualized finite element models of the tooth roots, different amounts of stress were distributed on the root surfaces. White arrows indicate the loading forces.
surface of the apical regions of the mesiobuccal and distobuccal roots, with wide shallow or deep resorption craters. Multinucleated osteoclasts appeared in the root resorption lacunae with some evident deposition of cellular cementum on resorbed root cavities (Fig 5, B).
In the control group, the largest root resorption crater was found on the distal surface of the mesiobuccal root. It extended from the cervical region to the apical region with massive dentin destruction. Small or wide resorption craters were also observed on the mesial
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and distal surfaces of the mesiobuccal and distobuccal roots (Fig 5, C). When tested with the finite element method, more stress accumulated in the cervical region than in the apical region of the root surface. The highest level of stress accumulated on the mesial side in the cervical region of the mesiolingual root, followed by the mesial side of the cervical region of the mesiobuccal root, and the distal side of the cervical region of the distobuccal and distolingual roots (Fig 5, D-F). DISCUSSION
This study demonstrated that it is feasible to move a tooth into a BoneCeramic grafting extraction site that intends to preserve bone and reduce the potential for alveolar bone loss. Our data showed that the rats' second molars experienced the least tooth movement rate when they traveled through the BoneCeramic grafts, followed by the Bio-Oss grafts and the control extraction sites with no grafts. This result is opposite to that found by Seifi and Ghoraishian,23 who observed an increased tooth movement rate in the group with the alveolar defect filled with demineralized freeze-dried bone allograft. Others reported that a similar tooth movement distance was observed between the group filled with Bio-Oss and the control group.10 However, with the same amount of orthodontic traction force, it is obvious that bone substitutes decrease the tooth movement rate. The rats' extraction site healing process consisted of 3 phases: (1) organization of the blood clot and covering of the extraction socket by epithelium (1-5 days), (2) new bone formation (5-20 days), and (3) new bone maturation and alveolar ridge remodeling (20-60 days).24,25 The alveolar ridge resorbs with significant reductions in height and width; this is more pronounced during the initial phase of wound healing than during later phases. Schropp et al26 stated that in humans approximately two thirds of this reduction occurs within the first 3 months after tooth extraction. The healing process of a rat's extraction site is similar to a human's but 3 times faster, indicating that the alveolar ridge resorbs within 1 month in rats after tooth removal.27 In our study, grafting of bone substitutes immediately after extraction slowed ridge resorption. When the second molars were moved into the alveolar ridge defects 1 month after bone grafting, bone substitutes were not absorbed completely, with new bone forming in the extraction sockets. Measuring the distance of tooth movement, the bone density, and the root resorption provided the means of evaluating the feasibility of moving teeth into the augmented alveolar ridges with or without adverse effects.
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It was evident that the placement of a bone substitute interfered with the processes of bone modeling and remodeling. In regions of interest 1, 2, and 7 of the BoneCeramic group, the highest levels of BV/TV, Tb.N, and Tb.Th, and the lowest level of Tb.Sp indicated the increased new bone formation in the extraction sites. These demonstrated that BoneCeramic stimulates bone growth with increases in both Tb.N and Tb.Th, implying that BoneCeramic has the potential for osteoconduction. These findings agree with those of Mardas et al19 that BoneCeramic completely preserved the height and width of the alveolar ridge and the interproximal bone in the extraction sites. Because of the highest BV/TV in the BoneCeramic group (BoneCeramic, 69.6%; BioOss, 62.3%; control, 52.8%) (Fig 2), the tooth movement distance and the rate decreased. This is supported by others, showing that the tooth movement rate relies on the density of the alveolar bone.28-30 The tooth movement rate depends on removing hyalinized tissue on the compression side of alveolar bone caused by direct or undermining bone resorption.31 From days 0 to 7, stress on the tooth root induced alveolar bone resorption, shown by decreases in BV/TV, Tb.N, and Tb.Th in region of interest 7 (Table II). Meanwhile, the tooth was rapidly moved into the space of the resorbed bone with a significantly increased tooth movement rate. Once the tooth is completely moved into the resorbed space, the roots were again pulled against the alveolar bone and developed hyalinized tissues.32 It is believed that hyalinization of the tissues provides high resistance and slows orthodontic tooth movement as shown from days 7 to 14 in our study. To continue tooth movement, hyalinized tissues need to be removed by undermining bone resorption. Osteoclasts continued to resorb bone as indicated by decreased BV/TV, Tb.N, and Tb.Th. Interestingly, in all groups, Tb.Sp significantly decreased accompanied by increased BV/TV, Tb.N, and Tb.Th from days 14 to 28 (Fig 2), suggesting that bone regeneration in the extraction sites was preserved by BoneCeramic in the later period of orthodontic treatment. In this study, bone density increased more in the regions of BoneCeramic grafting compared with Bio-Oss grafting, and both grafting methods slowed tooth movement. Under clinical conditions, slowing tooth movement by bone graft materials may be good for preventing neighboring teeth from drifting into the space that is to be prepared for the implant. Whether to graft BoneCeramic or Bio-Oss depends on the alveolar ridge defect width and height, and the tooth movement design. The orthodontist should anticipate how the defect will affect tooth movement and consider which bone substitute will preserve the alveolar ridge better.
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Since two thirds of alveolar ridge resorption occurs in the first 3 months after tooth extraction, this resorption becomes stable in 6 months.26 If the extraction space can be closed in 6 months, Bio-Oss could be placed in the extraction site and will not affect tooth movement. However, if the extraction space would take longer than 6 months to close, the patient might be left with a periodontally involved first molar and lack of alveolar bone around the molar. The orthodontic mechanics are to extract the first molar and to mesialize the second molar to replace the missing first molar. It takes a long time to mesialize the molar and needs enough bone to sustain the alveolar ridge width and height. BoneCeramic increases bone density more and preserves the alveolar ridge for a longer time than does Bio-Oss, and there is no difference in tooth movement rates between BoneCeramic and Bio-Oss at the end of the orthodontic loading cycle. Therefore, BoneCeramic should be grafted in the alveolar ridge defect. Accompanied by tooth movement, root resorption increased significantly from days 0 to 7 after grafting with BoneCeramic. This result agreed with our previous experiment that most resorption occurred on the apical third of the root on day 7.20 However, the whole root resorption volume did not increase from days 7 to 28, suggesting that the root resorption craters were stabilized. The mesiolingual and distolingual roots showed great amounts of root resorption and stress on the root surfaces. These findings are supported by those of Chan and Darendeliler33 that more root resorption undergoes a higher level of stress. Interestingly, our reconstructed 3D images and histologic findings of tooth roots showed that wide or deep resorption craters did not concentrate in the regions with the highest accumulated stress, but rather in the distal and apical regions. This was because the tooth was tipped rather than translated forward in parallel. The distal and apical regions were subjected to accumulated stress on the relatively small root surface. The volumetric measurements and finite element method model also confirmed that the apical regions had smaller volumes and underwent higher levels of stress per unit of area. Therefore, more root resorption appeared in the distal and apical regions. The root resorption volumes in the extraction sites preserved by BoneCeramic did not increase significantly compared with the other groups. We deduced that BoneCeramic is safe and therapeutic for alveolar bone formation and orthodontic tooth movement. CONCLUSIONS
It is suggested that although BoneCeramic slows orthodontic tooth movement, it has a better osteoconductive potential and induces less root resorption compared
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