Editorial Type:
Article Category: Research Article
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Online Publication Date: 20 Nov 2017

Effects of bone regeneration materials and tooth movement timing on canine experimental orthodontic treatment

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Page Range: 171 – 178
DOI: 10.2319/062017-407
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ABSTRACT

Objectives:

To evaluate the effects of bone regeneration materials and orthodontic tooth movement (OTM) timing on tooth movement through alveolar bone defects treated with guided bone regeneration (GBR) utilizing xenografts (Bio-Oss) and alloplast (β-TCP).

Materials and Methods:

Twenty-four standard alveolar bone defects in six male beagle dogs were treated by GBR using either Bio-Oss or β-TCP (experimental), whereas the control defects were left empty. The defects were further grouped into early or late subgroups, depending on OTM timing after GBR (ie 1 month or 2 months, respectively). Rates of OTM were measured intraorally, while computed tomography scan images were used to assess bone density, alveolar bone height, second premolar displacement, and tipping tendency.

Results:

Generally, the Bio-Oss early and Bio-Oss late subgroups recorded the lowest amount of tooth movement compared with other modes of GBRs assessed. Before OTM, the control group registered significantly lower bone height compared with the Bio-Oss and β-TCP groups (P < .01). The control group was inferior on bone density and bone height compared with Bio-Oss and β-TCP.

Conclusions:

The Bio-Oss group had favorable radiologic features (higher alveolar bone level and bone density with less premolar tipping) but showed slower OTM than the control group. The late OTM subgroup had favorable radiologic features and showed faster tooth movement than the early OTM in the β -TCP group.

Keywords: Bone regeneration; GBR; Orthodontic tooth movement; Bone resorption; Bone density

INTRODUCTION

Bone regeneration has been popular in contemporary dental practice,1 thus any practicing orthodontist is likely to encounter patients who need both bone regeneration and orthodontic treatment

In dentistry, bone regeneration may be indicated for managing bone defects resulting from several conditions, including traumatic bone destruction, tumor excision, bone infection (osteomyelitis and cancrum oris), congenital defects (cleft palate), alveolar bone resorption of periodontal disease origin (periodontitis and peri-implantitis), and alveolar bone resorption due to loss of teeth.1,2

Many types of bone regeneration materials are currently in clinical use. Some bone substitutes undergo almost immediate biodegradation and resorption; others can remain in the implant site for several years.3–5

Long treatment times, difficulties in treating skeletal malocclusions, and root and alveolar bone resorption, along with increased risks of adverse effects for teeth with reduced bone support, are some of the contemporary challenges orthodontists face. This is especially true in the current era, in which there is an increased number of adult orthodontic patients who are more likely to have periodontal diseases.6,7

Little work has been done regarding the application of bone regeneration in orthodontic treatment, despite the close interrelationship between orthodontics and conditions like severe periodontal diseases, cleft palate, and alveolar defects, which call for an interdisciplinary approach for the comprehensive management of patients.1 There continues to be an increase in the number of adult patients who actively seek orthodontic treatment, and it is undeniable that the incidence of periodontal disease increases with age.6,7 So far, there are no reported randomized clinical trials regarding the application of bone regeneration techniques in orthodontics and the consequent rate of orthodontic tooth movement (OTM). Experimental studies have reported conflicting results on OTM timing after bone regeneration and have not compared the use of different bone regeneration materials (BRMs) along with OTM.8,9 The current study evaluated the effects of BRMs and OTM timing on tooth movement through alveolar bone defects treated with GBR utilizing xenografts (Bio-Oss) and alloplast (β-TCP) BRMs.

MATERIALS AND METHODS

Ethical Considerations

The study was approved by the Ethics Committee of Fujian Medical University. All animal handling and surgical procedures were conducted according to the Institutional Review Board guidelines for the use and care of laboratory animals.

Animal Experiments

This animal experimental study used six male beagle dogs aged 18 months with a mean weight of 11.8 kg. Data were collected by intraoral distance measurement and computed tomography (CT) scan image analysis. Twenty-four alveolar bone defects were created by extending the first premolar extraction socket. The experimental defects were treated by guided bone regeneration (GBR) using synthetic β-TCP (Bio-lu Biomaterials Co, Ltd, Shanghai, China) or xenograft Bio-Oss (Geistlich, Wolhusen, Switzerland) regeneration materials, whereas the control defects were left empty. Resorbable collagen membranes Bio-Gide (Geistlich) were used in both experimental and control defects. The regeneration materials were equally allocated to the maxillary right and left (UR and UL) as well as to the mandibular right and left (LR and LL) defects by randomizing three predetermined sets of defect management to the six experimental animals (ie set 1: UR-β-TCP, UL-Bio-Oss, LR-control, and LL-β-TCP; set 2: UR-Bio-Oss, UL-β-TCP, LR-Bio-Oss, and LL control; set 3: UR-control, LR-β-TCP, UL-control, and LL-Bio-Oss). Every set was randomly assigned to two dogs. Consequently, the three GBR modes (β-TCP, Bio-Oss and control) were equally distributed to the right and left of the maxillary and mandibular jaws. The set randomization also allowed for every GBR mode to be assigned to eight defects.

Surgical Procedure

Under general anesthesia, the maxillary and mandibular first premolar extraction sockets were extended mesially from the second premolar using a 2.0-mm diameter cylindrical tungsten bur to create four-walled standardized artificial defects measuring 5-mm deep, 7-mm long (mesial-distal), and 5-mm wide (buccal-lingual) in each quadrant of the animal's jaws (Figure1). Depending on the GBR mode allocation, the defects were filled with β-TCP or Bio-Oss mixed with the animal's blood collected during defect preparation. The mixture was packed into the artificial defects to the natural alveolar height level, whereas the control defects were left empty. The filled experimental and the empty control defects were all covered by Bio-Gide resorbable collagen membranes (Figure1) followed by wound closure using 3/0 nylon sutures, which remained in the site for 2 weeks.

Figure 1. The stepwise display of the GBR surgical procedure. (a) Standard bone defect made by extending the extraction socket. (b) Collagen membrane covering the bone defect.Figure 1. The stepwise display of the GBR surgical procedure. (a) Standard bone defect made by extending the extraction socket. (b) Collagen membrane covering the bone defect.Figure 1. The stepwise display of the GBR surgical procedure. (a) Standard bone defect made by extending the extraction socket. (b) Collagen membrane covering the bone defect.
Figure 1. The stepwise display of the GBR surgical procedure. (a) Standard bone defect made by extending the extraction socket. (b) Collagen membrane covering the bone defect.

Citation: The Angle Orthodontist 88, 2; 10.2319/062017-407

After the GBR procedure, the animals were further subgrouped into early (E) and late (L) categories based on the planned time of OTM commencement. The group allocation was determined by the defect management sets assigned to every dog, so that both early (E) and late (L) subgroups contained one of the three (1, 2, and 3) management sets. According to the experiment protocol, the OTM in the early (E) group was commenced after 1 month of healing time while the late group animals started OTM after 2 months.

Orthodontic Appliance Design and Tooth Movement Assessment

The second premolar was moved mesially by the application of a 150 g force as measured by a tension gauge (Aidebao, Leqing, China) using a NiTi closed coil spring (Ormco, Orange, Calif) (Figure 2). The distance from the mesial-cervix of the second premolar to the distal-cervix of the canine was measured as previously described by Seifi et al.10 using a digital caliper (Guan lu, Guilin, China) with a precision of 0.01 mm. To complement the intraoral measurement, the distance between the second and third premolar cusps was measured on CT images taken before and after OTM. The difference was used to assess the second premolar displacement as the result of OTM.

Figure 2. Pictorial illustration of (a) distance measurement and (b) orthodontic appliance design.Figure 2. Pictorial illustration of (a) distance measurement and (b) orthodontic appliance design.Figure 2. Pictorial illustration of (a) distance measurement and (b) orthodontic appliance design.
Figure 2. Pictorial illustration of (a) distance measurement and (b) orthodontic appliance design.

Citation: The Angle Orthodontist 88, 2; 10.2319/062017-407

Computed Tomography Scan

One day before OTM, all animals were subjected to CT scanning using a cone beam CT machine (DCT Pro; Vatech & EWOO Group, Hwaseong-si, South Korea). The images were used to extract digital information on bone mineral density, alveolar bone height, and the second premolar displacement and tipping tendency as shown in Figure 3a, b using EZ 3D 2009 software (Vatech). The distance between the second and third premolar cusps was measured digitally before and after OTM (Figure 3) to determine the second premolar displacement. The density was assessed by the region of interest function of the EZ-3D software. A 0.50-cm square area was selected in the density measurement option, to determine the bone density 1 mm mesial to the second premolar mesial root and 8.5 mm from an imaginary apical plane (a line connecting the canine and the first molar mesial root apices) (Figure 3). The second premolar mesial angle was measured by the three-point function between the premolar long axis (a line along the second premolar mesial root canal) and the apical plane (Figure 3). The second premolar tipping as a result of OTM was obtained by subtracting the mesial angle after OTM from the angle before OTM. The alveolar bone height was determined by the length of the line drawn perpendicular to the apical plane to the nearest alveolar crest level mesial to the second premolar (Figure 3). All measurements were done on the reconstructed panoramic images of 1 mm slice thickness and 2 mm interval (Figure 3).

Figure 3. CT image variable measurements. (a) Measuring bone density and second premolar mesial angle. (b) Measuring the second premolar displacement and alveolar bone height).Figure 3. CT image variable measurements. (a) Measuring bone density and second premolar mesial angle. (b) Measuring the second premolar displacement and alveolar bone height).Figure 3. CT image variable measurements. (a) Measuring bone density and second premolar mesial angle. (b) Measuring the second premolar displacement and alveolar bone height).
Figure 3. CT image variable measurements. (a) Measuring bone density and second premolar mesial angle. (b) Measuring the second premolar displacement and alveolar bone height).

Citation: The Angle Orthodontist 88, 2; 10.2319/062017-407

The differences between the two data sets (before and after OTM) were calculated to obtain the second premolar displacement and tipping tendency as well as the bone mineral density and alveolar bone height changes as a result of OTM.

Statistical Analysis

The means and standard deviations were calculated for each group. The data showed a normal distribution tendency; hence, parametric statistical analysis was applied with the level of statistical significance set at P < .05. One-way analysis of variance (ANOVA) was used to evaluate the effects of OTM. Factorial repeated-measures ANOVA was used to evaluate the rate of tooth movement of different GBR modes at every experimental time point. The statistical package for social sciences (SPSS) software version 19.0 (IBM SPSS Inc, Chicago, IL, USA) was used.

RESULTS

To evaluate the effects of BRMs on orthodontic treatment, the CT scan image parameters and total orthodontic tooth movement were analyzed by one-way ANOVA. The rate of tooth movement recorded at 2-week intervals during OTM was analyzed by factorial repeated-measures ANOVA: The first analysis stage did not include the OTM timing factor (Table 1, Figure 4), while the second stage took into account the OTM timing factor (Table 2, Figure 5).

Table 1.  Means and (Standard Deviations) of Orthodontic Tooth Movement by Guided Bone Regeneration Modes Measured Intraorally at 2-Week Intervals for 2 Months
Table 1. 
Figure 4. Means plot of the orthodontic tooth movement (recorded at 2-week intervals) according to GBR modes.Figure 4. Means plot of the orthodontic tooth movement (recorded at 2-week intervals) according to GBR modes.Figure 4. Means plot of the orthodontic tooth movement (recorded at 2-week intervals) according to GBR modes.
Figure 4. Means plot of the orthodontic tooth movement (recorded at 2-week intervals) according to GBR modes.

Citation: The Angle Orthodontist 88, 2; 10.2319/062017-407

Table 2. Mean and standard deviation of OTM GBR modes sub-grouped by OTM timing measured intraorally at two weeks interval for two months
Table 2.
Figure 5. Means plot of the orthodontic tooth movement (recorded at 2-week intervals) according to GBR modes subgrouped by OTM timing.Figure 5. Means plot of the orthodontic tooth movement (recorded at 2-week intervals) according to GBR modes subgrouped by OTM timing.Figure 5. Means plot of the orthodontic tooth movement (recorded at 2-week intervals) according to GBR modes subgrouped by OTM timing.
Figure 5. Means plot of the orthodontic tooth movement (recorded at 2-week intervals) according to GBR modes subgrouped by OTM timing.

Citation: The Angle Orthodontist 88, 2; 10.2319/062017-407

Orthodontic Tooth Movement

In the mandible, the cumulative total tooth movement was 4.891 ± 0.620 mm compared with 4.408 ± 0.768 mm for the maxilla (P = .10).

The control group registered a statistically higher rate of tooth movement than the Bio-Oss group (P < .05) during the first 2 weeks of OTM and over the cumulative total tooth movement time (Table 1). The total tooth displacement digitally measured on CT images also showed a difference between the Bio-Oss and control groups (P < .05).

When BRMs were subgrouped according to OTM timing (Table 2), the total tooth movement ranged from 5.137± 0.183 mm (control-E) to 4.084 ± 0.572 (Bio-Oss-E). Details of OTM timing effects are shown in Table 2.

Alveolar Bone Height

The alveolar bone level measured on CT scan images before OTM showed significantly lower bone height in the control group compared with the Bio-Oss and β-TCP groups (P < .01) (Table 3). Table 4 shows the effects of OTM timing on bone height. After OTM, Bio-Oss-L appeared to have the highest bone gain (1.235 ± 1.90 mm), while β-TCP-L recorded no gain and control-E registered a net reduction (bone resorption) after tooth movement (Table 4, Figure 6). The differences however, were not statistically significant.

Table 3.  Means (Standard Deviations) of Alveolar Bone Height, Bone Density, Premolar Displacement and Tipping Measured by CT Image Analysis According to GBR Modes
Table 3. 
Table 4.  Means (Standard Deviations) of Alveolar Bone Height, Bone Density, Premolar Displacement and Tipping by CT Scan Analysis According to GBR Modes Subgrouped by OTM Timing
Table 4. 
Figure 6. Bar chart showing the alveolar bone height changes after OTM according to GBR mode subgroups.Figure 6. Bar chart showing the alveolar bone height changes after OTM according to GBR mode subgroups.Figure 6. Bar chart showing the alveolar bone height changes after OTM according to GBR mode subgroups.
Figure 6. Bar chart showing the alveolar bone height changes after OTM according to GBR mode subgroups.

Citation: The Angle Orthodontist 88, 2; 10.2319/062017-407

Bone Density Evaluation and Second Premolar Tipping Tendency

Bone density measured before OTM revealed the lowest value in the control group compared with the Bio-Oss and β-TCP groups (Table 3). The effects of OTM timing on bone density are shown in Table 4. After OTM, the control group had the highest density reduction (525.65 ± 428.38), while Bio-Oss showed the lowest (324.28 ± 364.92) reduction. The second premolar tipping tendency is shown in Table 3 and Figure 7.

Figure 7. Bar chart displaying the second premolar tipping according to GBR modes and OTM timing.Figure 7. Bar chart displaying the second premolar tipping according to GBR modes and OTM timing.Figure 7. Bar chart displaying the second premolar tipping according to GBR modes and OTM timing.
Figure 7. Bar chart displaying the second premolar tipping according to GBR modes and OTM timing.

Citation: The Angle Orthodontist 88, 2; 10.2319/062017-407

DISCUSSION

The current study revealed that the type of BRM and the timing of OTM both affected the rate of tooth movement at some point during treatment. The Bio-Oss group had slower OTM than the β-TCP and control groups and the late (L) subgroup of β-TCP showed faster tooth movement than the early (E) group. These observations can be attributed to the well-documented information available regarding the biology of orthodontic tooth movement, which emphasizes the importance of cellular components of a healthy periodontium for OTM.11–14 The possible variations in cellular and mineral components of bone regenerated by different bone substitutes along with the varying amount of new bone formation with time are the probable reasons for the differences found between the GBR modes in this study.

According to published reports, OTM is determined by the cellular and mineral components of the periodontium.11,12 Whereas osteoclasts are responsible for bone resorption induced by orthodontic mechanical force on the pressure zone, osteoblasts respond by appositional bony deposition on the tension zone.13,14 These cellular activities are the backbone of OTM that requires a healthy periodontal ligament, gingiva, cementum, and alveolar bone surrounding the roots of teeth under orthodontic treatment.13,15 The study also elicited some differences in radiologic parameters (alveolar bone level, bone density and premolar tipping) based on the type of BRMs and time OTM commenced. The Bio-Oss group had favorable radiologic features (higher alveolar bone level and bone density with less premolar tipping) than the β-TCP and control groups, while the late OTM group led to more favorable radiologic features than the early OTM group. The difference in cellular and mineral components between the BGR modes may have affected the resorption process, resulting in different radiologic characteristics based on BRMs and OTM timing. Apart from the previously mentioned cellular components, the bone mineral component also has significant impact on orthodontic treatment by influencing the rate of remodeling.11,12

Orthodontic Tooth Movement Assessment

The cumulative total tooth movement showed a statistically significant difference between the Bio-Oss and control groups (P < .05). The disparity can be explained by the high bone density and bone height attained by Bio-Oss before OTM compared with the control group. The Bio-Oss group recorded the lowest rate of tooth movement at all points followed by the β-TCP group, whereas the control group recorded the highest rate. The high bone density registered before OTM for the Bio-Oss group may be one of the contributing factors for the slow rate of OTM in the Bio-Oss group. Several studies have attributed slow tooth movement to high bone mineral density.16,17 The limited amount of bone formed before OTM in the control group meant a low physical barrier for tooth movement, which may have been the reason for faster movement than in the Bio-Oss and β-TCP groups.

Timing of Orthodontic Tooth Movement Commencement

The OTM timing had a significant impact on the rate of tooth movement at some points during the 8 weeks of assessment. When BRMs were subgrouped according to OTM timing (Table 2, Figure 4), the total tooth movement ranged from 4.084 ± 0.572 (Bio-Oss-E) to 5.137± 0.183 mm (control-E). The physical resistance by unresorbed Bio-Oss with limited osteoclasts and osteoblasts for the remodeling process in the early OTM group may be the reason for the slower rate compared with the empty control-E group with significantly lower bone formation that could easily allow tipping movement due to the lack of a physical barrier. The reason for the overall slower rate of tooth movement in the Bio-Oss group can be the slower Bio-Oss resorption previously reported by other researchers.18 Previous studies reported a resorption rate difference between Bio-Oss and β-TCP.19,20

Alveolar Bone Height

The alveolar bone level before OTM showed significantly lower bone height in the control group compared with the Bio-Oss and β-TCP groups (P < .01) (Table 3). These findings are consistent with those of previous studies that reported better and faster bone regeneration for defects treated by Bio-Oss and β-TCP than an empty control.5,18 The regeneration materials act as porous scaffolds through which bone forming cells easily deposit bone organic matrices, ultimately resulting in an efficient and desirable outcome. The materials prevent the possible collapse of soft tissues covering the defects, thus keeping the defect space available for new bone formation.

Bone Density

The higher bone density observed in the Bio-Oss and β-TCP groups was likely due to enhanced new bone formation in these groups compared with the control group. The longer time allowed for new bone formation in the late OTM groups may be the likely reason for more bone density being observed (Table 4). This observation is also supported by a previous comparative study by Bayat et al.21 in which a significant difference in the amount of bone density between the two regenerative materials was observed at the 56th day after surgery, even though the researchers reported no differences at 14 and 28 days.

Being an experimental study in animals, the findings cannot be directly applied to an orthodontic clinical situation due to the physiological differences between humans and canines. Because of different bone turnover rates, the time correlating to the observed events can vary in clinical situations, although the pattern of observation may prevail.

CONCLUSIONS

  • The Bio-Oss group had favorable radiologic features (higher alveolar bone level and bone density with less premolar tipping) but showed slower OTM than the control group.

  • The delayed OTM subgroup had favorable radiologic features (higher alveolar bone level and bone density with less premolar tipping) and showed faster tooth movement than early OTM in the Beta-TCP group.

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Copyright: © 2018 by The EH Angle Education and Research Foundation, Inc.
<bold>Figure 1.</bold>
Figure 1.

The stepwise display of the GBR surgical procedure. (a) Standard bone defect made by extending the extraction socket. (b) Collagen membrane covering the bone defect.

<bold>Figure 2.</bold>
Figure 2.

Pictorial illustration of (a) distance measurement and (b) orthodontic appliance design.

<bold>Figure 3.</bold>
Figure 3.

CT image variable measurements. (a) Measuring bone density and second premolar mesial angle. (b) Measuring the second premolar displacement and alveolar bone height).

<bold>Figure 4.</bold>
Figure 4.

Means plot of the orthodontic tooth movement (recorded at 2-week intervals) according to GBR modes.

<bold>Figure 5.</bold>
Figure 5.

Means plot of the orthodontic tooth movement (recorded at 2-week intervals) according to GBR modes subgrouped by OTM timing.

<bold>Figure 6.</bold>
Figure 6.

Bar chart showing the alveolar bone height changes after OTM according to GBR mode subgroups.

<bold>Figure 7.</bold>
Figure 7.

Bar chart displaying the second premolar tipping according to GBR modes and OTM timing.

Contributor Notes

Corresponding author: Dr Dong Wu, Implantology Department, College of Stomatology, Fujian Medical University, Yangquiao Road No 246, Fuzhou City, Fujian Province, People's Republic of China (e-mail: wudong510_5@hotmail.com)
Received: 01 Jun 2017
Accepted: 01 Oct 2017
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