The effects of alveolar decortications on orthodontic tooth movement and bone remodelling in rats

The effects of alveolar decortications on orthodontic tooth movement and bone remodelling in rats Summary Objectives Alveolar decortication (AD) is a minimally invasive procedure that can be performed in the orthodontic office as an intervention to accelerate tooth movement. There is a gap in the literature evaluating the earlier and delayed responses after AD using lighter orthodontic forces in a rat model. Therefore, the aim of this study was to determine the effects of AD in the amount of orthodontic tooth movement and on alveolar bone remodelling in a rodent model, after 7 or 14 days. Materials and methods A total of 32 15-week-old male Wistar rats were used in four treatment groups: (1) orthodontic spring only (7 days), (2) orthodontic spring only + AD (7 days), (3) orthodontic spring only (14 days), and (4) orthodontic spring only + AD (14 days). A closed coil nickel–titanium spring delivering 8–10 g of force was used to move the molar mesially. Alveolar decortication was done using a high speed, quarter round bur adjacent to the left first maxillary molar, on the palatal alveolar bone. At each endpoint, rats were sacrificed and microfocus computed tomography and histological analysis were performed. Results The spring + AD group presented with a significant increase in the rate of tooth movement when compared with spring only group, 7 and 14 days after the beginning of the experiments. In addition, the spring + AD group had a significant decrease in bone volume and tissue density and a significant increase in the trabecular spacing and the number of osteoclasts at 7 and 14 days. Furthermore, a fibrous tissue was found to replace the alveolar bone in the spring + AD group at day 14. Conclusion Alveolar decortications enhanced bone remodelling around the tooth movement region and could be used as an adjunct surgical procedure to accelerate the rate of tooth movement. Introduction Orthodontic tooth movement occurs due to an inflammatory process, which results in bone modelling and remodelling (1, 2). The comprehensive orthodontic treatment typically requires 24–36 months to complete. Orthodontic treatment after bone maturation (late adolescence and adults) is challenging and requires longer treatment time to achieve the desired results (3, 4). Prolonged duration of treatment is one of the most frequent complaints by orthodontic patients and may lead to side effects such as root resorption, white spot lesions, and patients becoming noncompliant (5, 6). Over the last decade, procedures to accelerate the rate of orthodontic tooth movement have gained momentum. Invasive and non-invasive adjunctive treatment modalities have been introduced to reduce the time taken in different phases of orthodontic treatment or to reduce the overall treatment time. Non-invasive treatments to accelerate orthodontic tooth movement include mechanical vibration, low-level laser, and low-intensity pulsed ultrasound (7). Additionally, surgical interventions associated with orthodontic treatment include less invasive techniques such as alveolar perforations/decortication, piezocision, and corticision, to more traumatic approaches like corticotomy and dental distraction (8, 9). In the contemporary orthodontics, corticotomies are the most popular invasive method used for accelerating the orthodontic tooth movement and have been shown to double the rate of orthodontic tooth movement (10–12). Although corticotomies have successfully been used to accelerate the orthodontic tooth movement, due to their invasive nature, corticotomies may result in pain and other postoperative discomfort for a week (13). In an effort to reduce postsurgical morbidity, Kim et al. injured the buccal cortical bone (corticision) with a surgical blade and mallet, thus eliminating the need for a periosteal flap reflection (14, 15). However, they observed that the surgical blade penetrated almost 10 mm into the cortical bone. Subsequently to limit the injury, Dibart et al. also performed corticotomies without raising the periosteal flap using a peizo-surgery device and they termed this procedure as peizocision (16). All the above procedures require precision and cannot be done by an orthodontist in a busy day-to-day clinical practice. The regional acceleratory phenomenon (RAP) was described by Frost as a biologic reaction to speed bone healing characterized by a transient burst of catabolic bone modelling followed by anabolic bone modelling (17, 18). The idea to include small surgical procedures adjunctive to orthodontic treatment is a strategy to induce a RAP to the surrounding alveolar bone and decrease local resistance to orthodontic tooth movement. There is evidence that adjunctive surgical procedures associated with orthodontic treatment may have a positive effect in accelerating tooth movement; nevertheless, the opinions are still controversial (19–22). Alveolar decortication (AD) is a minimally invasive procedure that does not require raising a flap and could be performed by an orthodontist in day-to-day clinical practice (23). Clinical reports have suggested that AD can increase the rate of tooth movement (23, 24). In addition, studies in experimental rats have shown positive results in terms of acceleration of tooth movement and cellular response after this procedure (25, 26). Tsai et al. showed acceleration of tooth movement with AD; however, they used growing rats as a model, performing osteoperforations in addition to an orthodontic force of 50 g (25). Nevertheless, a force of 50 g could be considered too high for the rodent model (27). Similarly, Cheung et al. also showed that osteoperforation leads to accelerated orthodontic tooth movement; however, they had a small sample size of six rats and utilized the split mouth technique to study the effects of osteoperforations in the rate of tooth movement (26). The major drawbacks of this model were using a high force (25 g) and a split mouth study design, since the RAP, caused by osteoperforation, may lead to systemic modelling and remodelling of bone, and might affect even the contralateral side of the mandible, used as control in that study. Given the potential clinical benefit of osteoperforations on the rate of tooth movement and the gap in the literature evaluating the tissue response after osteoperforations using lighter orthodontic forces, the aim of this study was to evaluate the early and delayed effects of AD associated with orthodontic movement in a rodent model. Our null hypothesis is that there will be no difference in the amount of tooth movement with or without AD. We had two specific aims: (1) to determine the effect of AD on the amount of tooth movement after 7 and 14 days and (2) to determine the effects of AD and orthodontic tooth movement on bone modelling and remodelling using microfocus computed tomography (micro-CT) and histology. Materials and methods The Institutional Animal Care Committee at the University of Connecticut Health Center approved this study. Thirty-two 15-week-old male Wistar rats (Charles River Laboratories, Wilmington, MA) weighing 500–600 g were randomly divided into four groups: (1) Group 1 (eight rats)—orthodontic tooth movement for 7 days, (2) Group 2 (eight rats)—orthodontic tooth movement for 7 days + AD, (3) Group 3 (eight rats)—orthodontic tooth movement for 14 days, and (4) Group 4 (eight rats)—orthodontic tooth movement for 14 days + AD. All the rats were housed in the same room at constant room temperature and a 12 hour light and dark cycle. They were fed a standard diet of hard pellets and water. The animals were allowed at least a week of acclimatization at our health centre for their different origins. Following the experimental procedures in a previous study (28), the animals were placed under general anaesthesia with xylazine (13 mg/kg) and ketamine (87 mg/kg). A custom mouth prop was fabricated from 0.036 inch stainless steel wire and placed between the maxillary and mandibular incisors to hold the mouth open. A 0.008 inch stainless steel ligature wire was passed beneath the contact between the maxillary first and second molars and threaded to the maxillary first molar. Orthodontic force was applied using the two maxillary incisors as anchorage to move the left maxillary molar mesially. A closed coil nickel–titanium spring (Ultimate Wireforms, Bristol, CT) delivering 8–10 g of force was attached to the 0.008 inch stainless steel ligature around the left maxillary first molar, and the other end of the spring was attached to the incisors with 0.008 inch stainless steel wire. To prevent the dislodgement of the closed coil spring from the maxillary molar, self-etching primer (Transbond Plus; 3M Unitek, Monrovia, CA) and light-cure adhesive resin cement (Transbond; 3M Unitek, Monrovia, CA) were applied to the lingual surfaces of the maxillary first molar. Similarly, to prevent the dislodgement of the ligature wire from the incisors, grooves of depth 0.5–1 mm were made on the facial, lingual, and distal surfaces of the maxillary incisors and light-cure adhesive resin was applied. ADs were made using the quarter round bur using high-speed hand piece. Four ADs were made on the palatal alveolar bone adjacent to the maxillary first molar (Figure 1B). After the ADs and spring placement, animals were allowed to recover with an incandescent light for warmth. The rats were only returned to their respective cages once full ambulation and self-cleansing returned. The rats were monitored closely for pain and discomfort and the appliance was checked twice a week. After 7 or 14 days of experimental period, rats were euthanized by inhalation of carbon dioxide followed by cervical dislocation. Figure 1. View largeDownload slide (A) Sagittal reconstructed micro-CT image of the control group; (B) sagittal reconstructed micro-CT image of the AD group. Arrows depict the alveolar decortications. Figure 1. View largeDownload slide (A) Sagittal reconstructed micro-CT image of the control group; (B) sagittal reconstructed micro-CT image of the AD group. Arrows depict the alveolar decortications. After the euthanization, maxilla from each animal was dissected and fixed in 10 per cent formalin for 5 days. The maxilla was dehydrated with a series of alcohol changes. Following fixation and dehydration, micro-CT imaging and analysis was performed on each animal. Bone volume fraction (BVF), tissue density, trabecular spacing, and intermolar distance (IMD) were analysed. Micro-CT imaging was done at 55 kV and 145 mA, collecting 1000 projections per rotation at 300 milliseconds. Three-dimensional images were constructed using standard convolution and back projection algorithms with Shepp and Logan filtering and were rendered within a 12.3 mm field of view at a discrete density of 578704 voxel/mm3 (isometric 12 mm voxels). The serial images were used for quantitative analysis of alveolar bone changes in the region of interest (ROI) on the maxillary first molar. The ROI was defined vertically as the most occlusal point of the furcation to the apex of the maxillary roots. Transversely, it formed a rectangular confirmation, which included the points on the most distal part of the distobuccal root and distopalatal root and the other sides extending to the points of the most distal parts of the mesiobuccal and mesiopalatal roots. Following micro-CT imaging, samples were rehydrated and decalcified using 14 per cent ethylene diamine tetra-acetic acid for 4 weeks at 4°C. Subsequently, samples were processed for standard paraffin embedding and serial sagittal sections 5–7 µm in thickness were obtained. TRAP staining was performed using a leukocyte acid phosphatase (TRAP) kit (386-1 KT; Sigma-Aldrich, St. Louis, MO) according to the manufacturer’s instructions. TRAP positive, multinucleated cells were counted on the alveolar bone surfaces on the mesial sides of the disto-buccal roots. The ROI for osteoclast quantification on the alveolar bone was identified as a square parallel to the sagittal axis of the distobuccal root of the first molar with 200 µm width and with the length extending from the bifurcation to the apex. The osteoclast numbers were counted in three sections from four rats in each group, and the values were then averaged for each animal to run a statistical test. Statistical analysis Descriptive statistics was used to summarize the data. The outcome variables examined were IMD, BVF, tissue density, trabecular number, trabecular spaces, and osteoclast number. Mean, standard deviation, percentile distribution, and confidence interval were computed for all variables. D’Agostino and Pearson omnibus normality test was used to examine the normality of the data distribution. Since osteoclast numbers were not normally distributed, Wilcoxon Signed Rank test was used to compare osteoclast numbers between groups. Because of the sample size, nonparametric tests were used to examine the outcome variables between the treatment groups. Kruskal–Wallis test was used to compare the IMD, BVF, tissue density, trabecular number, and trabecular spaces. All statistical tests were two sided and a P-value of less than 0.05 was deemed to be statistically significant. Statistical analyses were computed using Graph Pad software (La Jolla, CA, USA). Results Alveolar decortication increases the rate of orthodontic tooth movement All rats used in the study remained healthy and had a slight increase in the body weight. We observed a significant increase in the rate of tooth movement for the group of rats that received ADs in addition to orthodontic spring. This was represented by a significant higher IMD in the spring + AD group when compared with spring only group at day 7 (Table 1 and Figure 2B) and day 14 (Table 2 and Figure 2C). Table 1. Distribution of data at 7 days. IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.1635 0.3575 61.45 22.3 1121 997.8 113 84.2 85.2 102.6 1.233 8.826 SD 0.06999 0.08692 11.01 7.931 29.73 24.78 6.083 5.63 9.859 5.595 1.168 2.957 Minimum 0.08 0.269 47.4 10.8 1087 970 108 77 72 96 0.2 5.142 Maximum 0.287 0.491 82.3 33.3 1164 1034 121 91 98 109 2.5 12.33 Percentiles  25 0.106 0.2893 53.3 15.3 1096 977.5 108 78.5 76 97 0.2 5.982  50 0.152 0.3325 59.4 22.55 1114 990 110 86 86 103 1 8.915  75 0.2128 0.4408 68.78 29.18 1150 1022 119.5 89 94 108 2.5 11.58 Lower 95% CI 0.105 0.2663 52.24 13.98 1084 967 105.4 77.21 72.96 95.65 1.66 4.121 Upper 95% CI 0.222 0.4487 70.66 30.62 1158 1029 120.6 91.19 97.44 109.5 4.134 13.53 Spring only versus Spring + AD P < 0.003 P < 0.0007 P < 0.0001 P < 0.0089 P < 0.0079 P < 0.05 IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.1635 0.3575 61.45 22.3 1121 997.8 113 84.2 85.2 102.6 1.233 8.826 SD 0.06999 0.08692 11.01 7.931 29.73 24.78 6.083 5.63 9.859 5.595 1.168 2.957 Minimum 0.08 0.269 47.4 10.8 1087 970 108 77 72 96 0.2 5.142 Maximum 0.287 0.491 82.3 33.3 1164 1034 121 91 98 109 2.5 12.33 Percentiles  25 0.106 0.2893 53.3 15.3 1096 977.5 108 78.5 76 97 0.2 5.982  50 0.152 0.3325 59.4 22.55 1114 990 110 86 86 103 1 8.915  75 0.2128 0.4408 68.78 29.18 1150 1022 119.5 89 94 108 2.5 11.58 Lower 95% CI 0.105 0.2663 52.24 13.98 1084 967 105.4 77.21 72.96 95.65 1.66 4.121 Upper 95% CI 0.222 0.4487 70.66 30.62 1158 1029 120.6 91.19 97.44 109.5 4.134 13.53 Spring only versus Spring + AD P < 0.003 P < 0.0007 P < 0.0001 P < 0.0089 P < 0.0079 P < 0.05 IMD, intermolar distance; BVF, bone volume fraction; TD, tissue density; Tb.Th, trabecular thickness; Tb. Sp, trabecular spacing; OcN: osteoclast number. View Large Table 1. Distribution of data at 7 days. IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.1635 0.3575 61.45 22.3 1121 997.8 113 84.2 85.2 102.6 1.233 8.826 SD 0.06999 0.08692 11.01 7.931 29.73 24.78 6.083 5.63 9.859 5.595 1.168 2.957 Minimum 0.08 0.269 47.4 10.8 1087 970 108 77 72 96 0.2 5.142 Maximum 0.287 0.491 82.3 33.3 1164 1034 121 91 98 109 2.5 12.33 Percentiles  25 0.106 0.2893 53.3 15.3 1096 977.5 108 78.5 76 97 0.2 5.982  50 0.152 0.3325 59.4 22.55 1114 990 110 86 86 103 1 8.915  75 0.2128 0.4408 68.78 29.18 1150 1022 119.5 89 94 108 2.5 11.58 Lower 95% CI 0.105 0.2663 52.24 13.98 1084 967 105.4 77.21 72.96 95.65 1.66 4.121 Upper 95% CI 0.222 0.4487 70.66 30.62 1158 1029 120.6 91.19 97.44 109.5 4.134 13.53 Spring only versus Spring + AD P < 0.003 P < 0.0007 P < 0.0001 P < 0.0089 P < 0.0079 P < 0.05 IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.1635 0.3575 61.45 22.3 1121 997.8 113 84.2 85.2 102.6 1.233 8.826 SD 0.06999 0.08692 11.01 7.931 29.73 24.78 6.083 5.63 9.859 5.595 1.168 2.957 Minimum 0.08 0.269 47.4 10.8 1087 970 108 77 72 96 0.2 5.142 Maximum 0.287 0.491 82.3 33.3 1164 1034 121 91 98 109 2.5 12.33 Percentiles  25 0.106 0.2893 53.3 15.3 1096 977.5 108 78.5 76 97 0.2 5.982  50 0.152 0.3325 59.4 22.55 1114 990 110 86 86 103 1 8.915  75 0.2128 0.4408 68.78 29.18 1150 1022 119.5 89 94 108 2.5 11.58 Lower 95% CI 0.105 0.2663 52.24 13.98 1084 967 105.4 77.21 72.96 95.65 1.66 4.121 Upper 95% CI 0.222 0.4487 70.66 30.62 1158 1029 120.6 91.19 97.44 109.5 4.134 13.53 Spring only versus Spring + AD P < 0.003 P < 0.0007 P < 0.0001 P < 0.0089 P < 0.0079 P < 0.05 IMD, intermolar distance; BVF, bone volume fraction; TD, tissue density; Tb.Th, trabecular thickness; Tb. Sp, trabecular spacing; OcN: osteoclast number. View Large Figure 2. View largeDownload slide (A) Intermolar distance (M1–M2) in the orthodontic spring only and the orthodontic spring + AD groups; (B) histogram showing the significant increase (P < 0.05) in the orthodontic tooth movement with AD at day 7; (C) histogram showing the significant increase (P < 0.05) in the orthodontic tooth movement with AD at day 14. Figure 2. View largeDownload slide (A) Intermolar distance (M1–M2) in the orthodontic spring only and the orthodontic spring + AD groups; (B) histogram showing the significant increase (P < 0.05) in the orthodontic tooth movement with AD at day 7; (C) histogram showing the significant increase (P < 0.05) in the orthodontic tooth movement with AD at day 14. Table 2. Distribution of data at 14 days. IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.4998 0.8827 60.85 30.25 1152 997.8 96.6 64.2 78.8 112 0.3 3.875 SD 0.1953 0.1463 8.333 5.717 32.24 71.06 5.505 9.834 4.658 9.327 0.2646 2.987 Minimum 0.296 0.679 51.3 23.9 1105 935 89 52 73 101 0 0.625 Maximum 0.713 1.053 72.3 37.2 1187 1110 102 76 86 121 0.5 6.5 Percentiles  25 0.3165 0.7668 55.28 24.88 1121 937.5 91 54.5 75.5 102 0 0.625  50 0.495 0.868 57.45 29.95 1164 990 98 65 78 116 0.4 4.5  75 0.6878 1.037 70.58 35.93 1179 1062 101.5 73.5 82.5 120 0.5 6.5 Lower 95% CI 0.189 0.7291 52.1 21.15 1112 909.6 89.77 51.99 73.02 100.4 0.16 2.87 Upper 95% CI 0.8105 1.036 69.6 39.35 1192 1086 103.4 76.41 84.58 123.6 1.43 9.29 Spring only versus spring + AD P < 0.014 P < 0.0095 P < 0.0159 P < 0.0079 P < 0.0079 P < 0.05 IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.4998 0.8827 60.85 30.25 1152 997.8 96.6 64.2 78.8 112 0.3 3.875 SD 0.1953 0.1463 8.333 5.717 32.24 71.06 5.505 9.834 4.658 9.327 0.2646 2.987 Minimum 0.296 0.679 51.3 23.9 1105 935 89 52 73 101 0 0.625 Maximum 0.713 1.053 72.3 37.2 1187 1110 102 76 86 121 0.5 6.5 Percentiles  25 0.3165 0.7668 55.28 24.88 1121 937.5 91 54.5 75.5 102 0 0.625  50 0.495 0.868 57.45 29.95 1164 990 98 65 78 116 0.4 4.5  75 0.6878 1.037 70.58 35.93 1179 1062 101.5 73.5 82.5 120 0.5 6.5 Lower 95% CI 0.189 0.7291 52.1 21.15 1112 909.6 89.77 51.99 73.02 100.4 0.16 2.87 Upper 95% CI 0.8105 1.036 69.6 39.35 1192 1086 103.4 76.41 84.58 123.6 1.43 9.29 Spring only versus spring + AD P < 0.014 P < 0.0095 P < 0.0159 P < 0.0079 P < 0.0079 P < 0.05 IMD, intermolar distance; BVF, bone volume fraction; TD, tissue density; Tb.Th, trabecular thickness; Tb. Sp, trabecular spacing; OcN, osteoclast number. View Large Table 2. Distribution of data at 14 days. IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.4998 0.8827 60.85 30.25 1152 997.8 96.6 64.2 78.8 112 0.3 3.875 SD 0.1953 0.1463 8.333 5.717 32.24 71.06 5.505 9.834 4.658 9.327 0.2646 2.987 Minimum 0.296 0.679 51.3 23.9 1105 935 89 52 73 101 0 0.625 Maximum 0.713 1.053 72.3 37.2 1187 1110 102 76 86 121 0.5 6.5 Percentiles  25 0.3165 0.7668 55.28 24.88 1121 937.5 91 54.5 75.5 102 0 0.625  50 0.495 0.868 57.45 29.95 1164 990 98 65 78 116 0.4 4.5  75 0.6878 1.037 70.58 35.93 1179 1062 101.5 73.5 82.5 120 0.5 6.5 Lower 95% CI 0.189 0.7291 52.1 21.15 1112 909.6 89.77 51.99 73.02 100.4 0.16 2.87 Upper 95% CI 0.8105 1.036 69.6 39.35 1192 1086 103.4 76.41 84.58 123.6 1.43 9.29 Spring only versus spring + AD P < 0.014 P < 0.0095 P < 0.0159 P < 0.0079 P < 0.0079 P < 0.05 IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.4998 0.8827 60.85 30.25 1152 997.8 96.6 64.2 78.8 112 0.3 3.875 SD 0.1953 0.1463 8.333 5.717 32.24 71.06 5.505 9.834 4.658 9.327 0.2646 2.987 Minimum 0.296 0.679 51.3 23.9 1105 935 89 52 73 101 0 0.625 Maximum 0.713 1.053 72.3 37.2 1187 1110 102 76 86 121 0.5 6.5 Percentiles  25 0.3165 0.7668 55.28 24.88 1121 937.5 91 54.5 75.5 102 0 0.625  50 0.495 0.868 57.45 29.95 1164 990 98 65 78 116 0.4 4.5  75 0.6878 1.037 70.58 35.93 1179 1062 101.5 73.5 82.5 120 0.5 6.5 Lower 95% CI 0.189 0.7291 52.1 21.15 1112 909.6 89.77 51.99 73.02 100.4 0.16 2.87 Upper 95% CI 0.8105 1.036 69.6 39.35 1192 1086 103.4 76.41 84.58 123.6 1.43 9.29 Spring only versus spring + AD P < 0.014 P < 0.0095 P < 0.0159 P < 0.0079 P < 0.0079 P < 0.05 IMD, intermolar distance; BVF, bone volume fraction; TD, tissue density; Tb.Th, trabecular thickness; Tb. Sp, trabecular spacing; OcN, osteoclast number. View Large Alveolar decortication decreases alveolar bone volume and density We next evaluated if ADs in combination to orthodontic force would have an effect in bone volume and quality. Our micro-CT analysis showed a significant decrease in BVF in the spring + AD group when compared with spring only at day 7 (Table 1 and Figure 3A, 3B, and 3E) and at day 14 (Table 2 and Figure 3C, 3D, and 3F). Similarly, tissue density was significantly lower in the spring + AD at day 7 (Table 1 and Figure 3A, 3B, and 3G) and at day 14 (Table 2 and Figure 3C, 3D, and 3H). Figure 3. View largeDownload slide Micro-CT data showing BVF, tissue density, and trabecular thickness at day 7 and day 14 in the orthodontic spring only and orthodontic spring + AD group A, coronally reconstructed micro-CT image of orthodontic spring only group at day 7; (B) coronally reconstructed micro-CT image of orthodontic spring + AD group at day 7; (C) coronally reconstructed micro-CT image of orthodontic spring only group at day 14; (D) coronally reconstructed micro-CT image of orthodontic spring + AD group at day 14; (E and F) histogram showing the significant decrease (P < 0.05) in the BVF with alveolar decortication at day 7 and day 14, respectively; (G and H) histogram showing the significant decrease (P < 0.05) in the tissue density with alveolar decortication at day 7 and day 14, respectively; (I and J) histogram showing the significant increase (P < 0.05) in the trabecular spacing with AD at day 7 and day 14, respectively; (K and L) histogram showing the significant decrease (P < 0.05) in the trabecular thickness with AD at day 7 and day 14, respectively. The white shaded rectangle in Figure 4C is the region of interest where the bone parameters (BVF, tissue density, and trabecular thickness were measured). Figure 3. View largeDownload slide Micro-CT data showing BVF, tissue density, and trabecular thickness at day 7 and day 14 in the orthodontic spring only and orthodontic spring + AD group A, coronally reconstructed micro-CT image of orthodontic spring only group at day 7; (B) coronally reconstructed micro-CT image of orthodontic spring + AD group at day 7; (C) coronally reconstructed micro-CT image of orthodontic spring only group at day 14; (D) coronally reconstructed micro-CT image of orthodontic spring + AD group at day 14; (E and F) histogram showing the significant decrease (P < 0.05) in the BVF with alveolar decortication at day 7 and day 14, respectively; (G and H) histogram showing the significant decrease (P < 0.05) in the tissue density with alveolar decortication at day 7 and day 14, respectively; (I and J) histogram showing the significant increase (P < 0.05) in the trabecular spacing with AD at day 7 and day 14, respectively; (K and L) histogram showing the significant decrease (P < 0.05) in the trabecular thickness with AD at day 7 and day 14, respectively. The white shaded rectangle in Figure 4C is the region of interest where the bone parameters (BVF, tissue density, and trabecular thickness were measured). Additionally, there was a significant increase in the trabecular spacing in the spring + AD group at day 7 (Table 1 and Figure 3A, 3B, and 3I) and at day 14 (Table 2 and Figure 3C, 3D, and 3J). However, there was a significant decrease in the trabecular thickness in spring + AD group at day 7 (Table 1 and Figure 3A, 3B, and 3K) and at day 14 (Table 2 and Figure 3C, 3D, and 3L). Alveolar decortication increases the number of osteoclasts at the pressure site Next, we evaluated whether the increased tooth movement rate and decreased bone volume and density associated with ADs were correlated with changes in osteoclast numbers. Our histological analysis revealed a significant increase in the osteoclast numbers at day 7 (Table 1 and Figure 4A–C and I) and at day 14 (Table 2 and Figure 4E–H and J). Furthermore, at day 14, we observed fibrous tissue replacing the alveolar bone in the spring + AD group when compared with the spring only group (Figure 4G–H). Figure 4. View largeDownload slide Histologic examination and quantification of osteoclast number day 7 and day 14 in the orthodontic spring only and orthodontic spring + AD groups. (A and B) TRAP positive cells in orthodontic spring only group at day 7; (C and D) TRAP positive cells in orthodontic spring + AD group at day 7; (E and F) TRAP positive cells in orthodontic spring only group at day 14; (G and H) TRAP positive cells in orthodontic spring + AD group at day 14; (I) histogram showing the significant increase (P < 0.05) in the osteoclast number with alveolar decortication at day 7; (J) histogram showing the significant increase (P < 0.05) in the osteoclast number with alveolar decortication at day 14. Black arrows depict the number of TRAP positive cells. Figure 4. View largeDownload slide Histologic examination and quantification of osteoclast number day 7 and day 14 in the orthodontic spring only and orthodontic spring + AD groups. (A and B) TRAP positive cells in orthodontic spring only group at day 7; (C and D) TRAP positive cells in orthodontic spring + AD group at day 7; (E and F) TRAP positive cells in orthodontic spring only group at day 14; (G and H) TRAP positive cells in orthodontic spring + AD group at day 14; (I) histogram showing the significant increase (P < 0.05) in the osteoclast number with alveolar decortication at day 7; (J) histogram showing the significant increase (P < 0.05) in the osteoclast number with alveolar decortication at day 14. Black arrows depict the number of TRAP positive cells. Discussion Our null hypothesis that there will be no difference in the amount of tooth movement between the control (spring only) and experimental (spring + AD) groups was rejected. With AD, there was a significant increase in the rate of tooth movement at 7 and 14 days after the application of orthodontic force. We selected them to study the effects of ADs on the rate of tooth movement, since this mildly invasive procedure is feasible to be performed by orthodontists in day-to-day clinical practice. It has been shown that alveolar perforations performed after raising a full-thickness flap induced a RAP in the experimental tooth movement region in animal studies (29–31). Likewise, we found increased osteoclastogenesis (by an increased number of TRAP positive cells) and decreased BVF and tissue density when AD was associated with orthodontic tooth movement, 7 and 14 days after the placement of orthodontic springs, in comparison to spring only group (no alveolar decortications). These observations suggest that alveolar decortications with no surgical incision or flap could induce similar acceleratory remodelling effects to the more invasive procedures. In addition, the RAP induced by ADs seemed to persist for at least 2 weeks after the procedure. Similarly to our study, Cheung et al. studied the effects of placing five osteoperforations around the maxillary first molars of rats during experimental tooth movement. The authors found a 1.86-fold increase in the rate of tooth movement in relation to the opposite side (orthodontic spring only) 3 weeks after the placement of springs. In addition, the alveolar bone at the side that received osteoperforations presented with a significant decrease in bone density (26). Although the split mouth study design would avoid interanimal variation, the degree of tooth movement acceleration could not be fully determined because the induction of the RAP does not seem to be restricted locally (18), suggesting that the control side could also be under the effects of RAP. Tsai et al. also found an increased rate of tooth movement when osteoperforations were performed in the adjacent region of tooth movement in rats (25). In this study, three flapless osteoperforations in the palatal region of the first molar of rats were compared with the effects of alveolar corticision in the same region in the tooth movement rate and tissue reaction. An orthodontic force of 50 g was used in the surgical and control groups, and the rate of tooth movement was assessed weekly, whereas the tissue reaction was evaluated after 3 and 6 weeks. However, a force of 50 g in a rodent model could be too high when comparing with ideal clinical forces (27). In our study, an orthodontic force of 8–10 g was used, and the rate of tooth movement and tissue changes were evaluated after 1 and 2 weeks so that the early responses could also be understood. Furthermore, in our study, we made four holes adjacent to the maxillary first molar on the palatal alveolar bone using a high-speed quarter round bur. A decrease in the number of osteoclasts was observed from day 7 to 14 after the application of orthodontic force. Maximum osteoclast recruitment in experimental tooth movement in rodents has been suggested to occur between days 3 and 5, with the number of osteoclast drastically decreasing at day 7 (25). In addition, 14 days is the duration of a remodelling cycle (activation–resorption–formation) in rodents; that is the reason we have examined the orthodontic tooth movement and bone parameters after alveolar decortication at an earlier time point (7 days) and at a later time point (14 days). We observed fibrous tissue replacing the alveolar bone in the spring + AD group at day 14. This finding was also reported by Wang et al., and the authors found fibrous tissue around the dental roots at the tension side 21 days after experimental corticotomy-assisted tooth movement in rats, which was then replaced by bone at day 60 (32). We plan to investigate the effect of AD associated with tooth movement in later time points to further study the temporal changes in bone quality and osteoclast recruitment in response to this small surgical procedure. The only clinical trial studying the effects of osteoperforations in the alveolar bone in orthodontic patients evaluated the rate of canine retraction with or without osteoperforations (split mouth study design). In addition, the effect of osteoperforations in the stimulation of inflammatory markers in the gingival crevicular fluid (GCF) was studied at different time points. Finally, the pain and discomfort reported by patients during the treatment were also evaluated (23). The authors have shown a 2.3-fold increased rate of canine retraction and a significant increase in the expression of inflammatory markers. In addition, patients reported minimal discomfort at the location of the alveolar perforations, suggesting that osteoperforation is an effective and likely acceptable clinical procedure to decrease orthodontic treatment duration. Although our study showed significant increase in the rate of the orthodontic tooth movement, extrapolation of our findings to the clinical situation must be done with caution as there is no osteonal remodelling (secondary remodelling) in rats, unlike in humans. Moreover, a frictionless space closure mechanism was used in this study. Nevertheless, this in vivo study helped us to understand the effect of alveolar decortication on the orthodontic tooth movement and bone modelling and remodelling. Our future research study will focus on the extent and area of the surgical insult (through alveolar decortications) and its effect on the orthodontic tooth movement and bone modelling and remodelling. Our future study will also focus on the long-term effects of alveolar decortication on the rate of the orthodontic tooth movement and alveolar bone remodelling. Moreover, we will also study the correlation, if any, between increase in osteoclast number and root resorption. Conclusions 1. There was a significant increase in the rate of the tooth movement at day 7 and day 14 with alveolar decortication. 2. There was a decrease in BVF and tissue density and increase in trabecular spacing with alveolar decortications. 3. There was an increase in the osteoclast number with alveolar decortications. Conflict of interest None to declare. References 1. Krishnan , V. and Davidovitch , Z . ( 2009 ) On a path to unfolding the biological mechanisms of orthodontic tooth movement . 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( 2017 ) Comparison of the effects of three surgical techniques on the rate of orthodontic tooth movement in a rat model . The Angle Orthodontist , 87 , 717 – 724 . Google Scholar CrossRef Search ADS PubMed 29. Baloul , S.S. , Gerstenfeld , L.C. , Morgan , E.F. , Carvalho , R.S. , Van Dyke , T.E. and Kantarci , A . ( 2011 ) Mechanism of action and morphologic changes in the alveolar bone in response to selective alveolar decortication-facilitated tooth movement . American Journal of Orthodontics and Dentofacial Orthopedics , 139 , S83 – 101 . Google Scholar CrossRef Search ADS PubMed 30. Chen , Y.W. , Wang , H.C. , Gao , L.H. , Liu , C. , Jiang , Y.X. , Qu , H. , Li , C.Y. and Jiang , J.H . ( 2016 ) Osteoclastogenesis in local alveolar bone in early decortication-facilitated orthodontic tooth movement . PloS One , 11 , e0153937 . Google Scholar CrossRef Search ADS PubMed 31. Teixeira , C.C. , Khoo , E. , Tran , J. , Chartres , I. , Liu , Y. , Thant , L.M. , Khabensky , I. , Gart , L.P. , Cisneros , G. and Alikhani , M . ( 2010 ) Cytokine expression and accelerated tooth movement . Journal of Dental Research , 89 , 1135 – 1141 . Google Scholar CrossRef Search ADS PubMed 32. Wang , L. , Lee , W. , Lei , D.L. , Liu , Y.P. , Yamashita , D.D. and Yen , S.L . ( 2009 ) Tisssue responses in corticotomy- and osteotomy-assisted tooth movements in rats: histology and immunostaining . American Journal of Orthodontics and Dentofacial Orthopedics , 136 , 770.e1 – 11 ; discussion 770. © The Author(s) 2017. Published by Oxford University Press on behalf of the European Orthodontic Society. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png The European Journal of Orthodontics Oxford University Press

The effects of alveolar decortications on orthodontic tooth movement and bone remodelling in rats

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Abstract

Summary Objectives Alveolar decortication (AD) is a minimally invasive procedure that can be performed in the orthodontic office as an intervention to accelerate tooth movement. There is a gap in the literature evaluating the earlier and delayed responses after AD using lighter orthodontic forces in a rat model. Therefore, the aim of this study was to determine the effects of AD in the amount of orthodontic tooth movement and on alveolar bone remodelling in a rodent model, after 7 or 14 days. Materials and methods A total of 32 15-week-old male Wistar rats were used in four treatment groups: (1) orthodontic spring only (7 days), (2) orthodontic spring only + AD (7 days), (3) orthodontic spring only (14 days), and (4) orthodontic spring only + AD (14 days). A closed coil nickel–titanium spring delivering 8–10 g of force was used to move the molar mesially. Alveolar decortication was done using a high speed, quarter round bur adjacent to the left first maxillary molar, on the palatal alveolar bone. At each endpoint, rats were sacrificed and microfocus computed tomography and histological analysis were performed. Results The spring + AD group presented with a significant increase in the rate of tooth movement when compared with spring only group, 7 and 14 days after the beginning of the experiments. In addition, the spring + AD group had a significant decrease in bone volume and tissue density and a significant increase in the trabecular spacing and the number of osteoclasts at 7 and 14 days. Furthermore, a fibrous tissue was found to replace the alveolar bone in the spring + AD group at day 14. Conclusion Alveolar decortications enhanced bone remodelling around the tooth movement region and could be used as an adjunct surgical procedure to accelerate the rate of tooth movement. Introduction Orthodontic tooth movement occurs due to an inflammatory process, which results in bone modelling and remodelling (1, 2). The comprehensive orthodontic treatment typically requires 24–36 months to complete. Orthodontic treatment after bone maturation (late adolescence and adults) is challenging and requires longer treatment time to achieve the desired results (3, 4). Prolonged duration of treatment is one of the most frequent complaints by orthodontic patients and may lead to side effects such as root resorption, white spot lesions, and patients becoming noncompliant (5, 6). Over the last decade, procedures to accelerate the rate of orthodontic tooth movement have gained momentum. Invasive and non-invasive adjunctive treatment modalities have been introduced to reduce the time taken in different phases of orthodontic treatment or to reduce the overall treatment time. Non-invasive treatments to accelerate orthodontic tooth movement include mechanical vibration, low-level laser, and low-intensity pulsed ultrasound (7). Additionally, surgical interventions associated with orthodontic treatment include less invasive techniques such as alveolar perforations/decortication, piezocision, and corticision, to more traumatic approaches like corticotomy and dental distraction (8, 9). In the contemporary orthodontics, corticotomies are the most popular invasive method used for accelerating the orthodontic tooth movement and have been shown to double the rate of orthodontic tooth movement (10–12). Although corticotomies have successfully been used to accelerate the orthodontic tooth movement, due to their invasive nature, corticotomies may result in pain and other postoperative discomfort for a week (13). In an effort to reduce postsurgical morbidity, Kim et al. injured the buccal cortical bone (corticision) with a surgical blade and mallet, thus eliminating the need for a periosteal flap reflection (14, 15). However, they observed that the surgical blade penetrated almost 10 mm into the cortical bone. Subsequently to limit the injury, Dibart et al. also performed corticotomies without raising the periosteal flap using a peizo-surgery device and they termed this procedure as peizocision (16). All the above procedures require precision and cannot be done by an orthodontist in a busy day-to-day clinical practice. The regional acceleratory phenomenon (RAP) was described by Frost as a biologic reaction to speed bone healing characterized by a transient burst of catabolic bone modelling followed by anabolic bone modelling (17, 18). The idea to include small surgical procedures adjunctive to orthodontic treatment is a strategy to induce a RAP to the surrounding alveolar bone and decrease local resistance to orthodontic tooth movement. There is evidence that adjunctive surgical procedures associated with orthodontic treatment may have a positive effect in accelerating tooth movement; nevertheless, the opinions are still controversial (19–22). Alveolar decortication (AD) is a minimally invasive procedure that does not require raising a flap and could be performed by an orthodontist in day-to-day clinical practice (23). Clinical reports have suggested that AD can increase the rate of tooth movement (23, 24). In addition, studies in experimental rats have shown positive results in terms of acceleration of tooth movement and cellular response after this procedure (25, 26). Tsai et al. showed acceleration of tooth movement with AD; however, they used growing rats as a model, performing osteoperforations in addition to an orthodontic force of 50 g (25). Nevertheless, a force of 50 g could be considered too high for the rodent model (27). Similarly, Cheung et al. also showed that osteoperforation leads to accelerated orthodontic tooth movement; however, they had a small sample size of six rats and utilized the split mouth technique to study the effects of osteoperforations in the rate of tooth movement (26). The major drawbacks of this model were using a high force (25 g) and a split mouth study design, since the RAP, caused by osteoperforation, may lead to systemic modelling and remodelling of bone, and might affect even the contralateral side of the mandible, used as control in that study. Given the potential clinical benefit of osteoperforations on the rate of tooth movement and the gap in the literature evaluating the tissue response after osteoperforations using lighter orthodontic forces, the aim of this study was to evaluate the early and delayed effects of AD associated with orthodontic movement in a rodent model. Our null hypothesis is that there will be no difference in the amount of tooth movement with or without AD. We had two specific aims: (1) to determine the effect of AD on the amount of tooth movement after 7 and 14 days and (2) to determine the effects of AD and orthodontic tooth movement on bone modelling and remodelling using microfocus computed tomography (micro-CT) and histology. Materials and methods The Institutional Animal Care Committee at the University of Connecticut Health Center approved this study. Thirty-two 15-week-old male Wistar rats (Charles River Laboratories, Wilmington, MA) weighing 500–600 g were randomly divided into four groups: (1) Group 1 (eight rats)—orthodontic tooth movement for 7 days, (2) Group 2 (eight rats)—orthodontic tooth movement for 7 days + AD, (3) Group 3 (eight rats)—orthodontic tooth movement for 14 days, and (4) Group 4 (eight rats)—orthodontic tooth movement for 14 days + AD. All the rats were housed in the same room at constant room temperature and a 12 hour light and dark cycle. They were fed a standard diet of hard pellets and water. The animals were allowed at least a week of acclimatization at our health centre for their different origins. Following the experimental procedures in a previous study (28), the animals were placed under general anaesthesia with xylazine (13 mg/kg) and ketamine (87 mg/kg). A custom mouth prop was fabricated from 0.036 inch stainless steel wire and placed between the maxillary and mandibular incisors to hold the mouth open. A 0.008 inch stainless steel ligature wire was passed beneath the contact between the maxillary first and second molars and threaded to the maxillary first molar. Orthodontic force was applied using the two maxillary incisors as anchorage to move the left maxillary molar mesially. A closed coil nickel–titanium spring (Ultimate Wireforms, Bristol, CT) delivering 8–10 g of force was attached to the 0.008 inch stainless steel ligature around the left maxillary first molar, and the other end of the spring was attached to the incisors with 0.008 inch stainless steel wire. To prevent the dislodgement of the closed coil spring from the maxillary molar, self-etching primer (Transbond Plus; 3M Unitek, Monrovia, CA) and light-cure adhesive resin cement (Transbond; 3M Unitek, Monrovia, CA) were applied to the lingual surfaces of the maxillary first molar. Similarly, to prevent the dislodgement of the ligature wire from the incisors, grooves of depth 0.5–1 mm were made on the facial, lingual, and distal surfaces of the maxillary incisors and light-cure adhesive resin was applied. ADs were made using the quarter round bur using high-speed hand piece. Four ADs were made on the palatal alveolar bone adjacent to the maxillary first molar (Figure 1B). After the ADs and spring placement, animals were allowed to recover with an incandescent light for warmth. The rats were only returned to their respective cages once full ambulation and self-cleansing returned. The rats were monitored closely for pain and discomfort and the appliance was checked twice a week. After 7 or 14 days of experimental period, rats were euthanized by inhalation of carbon dioxide followed by cervical dislocation. Figure 1. View largeDownload slide (A) Sagittal reconstructed micro-CT image of the control group; (B) sagittal reconstructed micro-CT image of the AD group. Arrows depict the alveolar decortications. Figure 1. View largeDownload slide (A) Sagittal reconstructed micro-CT image of the control group; (B) sagittal reconstructed micro-CT image of the AD group. Arrows depict the alveolar decortications. After the euthanization, maxilla from each animal was dissected and fixed in 10 per cent formalin for 5 days. The maxilla was dehydrated with a series of alcohol changes. Following fixation and dehydration, micro-CT imaging and analysis was performed on each animal. Bone volume fraction (BVF), tissue density, trabecular spacing, and intermolar distance (IMD) were analysed. Micro-CT imaging was done at 55 kV and 145 mA, collecting 1000 projections per rotation at 300 milliseconds. Three-dimensional images were constructed using standard convolution and back projection algorithms with Shepp and Logan filtering and were rendered within a 12.3 mm field of view at a discrete density of 578704 voxel/mm3 (isometric 12 mm voxels). The serial images were used for quantitative analysis of alveolar bone changes in the region of interest (ROI) on the maxillary first molar. The ROI was defined vertically as the most occlusal point of the furcation to the apex of the maxillary roots. Transversely, it formed a rectangular confirmation, which included the points on the most distal part of the distobuccal root and distopalatal root and the other sides extending to the points of the most distal parts of the mesiobuccal and mesiopalatal roots. Following micro-CT imaging, samples were rehydrated and decalcified using 14 per cent ethylene diamine tetra-acetic acid for 4 weeks at 4°C. Subsequently, samples were processed for standard paraffin embedding and serial sagittal sections 5–7 µm in thickness were obtained. TRAP staining was performed using a leukocyte acid phosphatase (TRAP) kit (386-1 KT; Sigma-Aldrich, St. Louis, MO) according to the manufacturer’s instructions. TRAP positive, multinucleated cells were counted on the alveolar bone surfaces on the mesial sides of the disto-buccal roots. The ROI for osteoclast quantification on the alveolar bone was identified as a square parallel to the sagittal axis of the distobuccal root of the first molar with 200 µm width and with the length extending from the bifurcation to the apex. The osteoclast numbers were counted in three sections from four rats in each group, and the values were then averaged for each animal to run a statistical test. Statistical analysis Descriptive statistics was used to summarize the data. The outcome variables examined were IMD, BVF, tissue density, trabecular number, trabecular spaces, and osteoclast number. Mean, standard deviation, percentile distribution, and confidence interval were computed for all variables. D’Agostino and Pearson omnibus normality test was used to examine the normality of the data distribution. Since osteoclast numbers were not normally distributed, Wilcoxon Signed Rank test was used to compare osteoclast numbers between groups. Because of the sample size, nonparametric tests were used to examine the outcome variables between the treatment groups. Kruskal–Wallis test was used to compare the IMD, BVF, tissue density, trabecular number, and trabecular spaces. All statistical tests were two sided and a P-value of less than 0.05 was deemed to be statistically significant. Statistical analyses were computed using Graph Pad software (La Jolla, CA, USA). Results Alveolar decortication increases the rate of orthodontic tooth movement All rats used in the study remained healthy and had a slight increase in the body weight. We observed a significant increase in the rate of tooth movement for the group of rats that received ADs in addition to orthodontic spring. This was represented by a significant higher IMD in the spring + AD group when compared with spring only group at day 7 (Table 1 and Figure 2B) and day 14 (Table 2 and Figure 2C). Table 1. Distribution of data at 7 days. IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.1635 0.3575 61.45 22.3 1121 997.8 113 84.2 85.2 102.6 1.233 8.826 SD 0.06999 0.08692 11.01 7.931 29.73 24.78 6.083 5.63 9.859 5.595 1.168 2.957 Minimum 0.08 0.269 47.4 10.8 1087 970 108 77 72 96 0.2 5.142 Maximum 0.287 0.491 82.3 33.3 1164 1034 121 91 98 109 2.5 12.33 Percentiles  25 0.106 0.2893 53.3 15.3 1096 977.5 108 78.5 76 97 0.2 5.982  50 0.152 0.3325 59.4 22.55 1114 990 110 86 86 103 1 8.915  75 0.2128 0.4408 68.78 29.18 1150 1022 119.5 89 94 108 2.5 11.58 Lower 95% CI 0.105 0.2663 52.24 13.98 1084 967 105.4 77.21 72.96 95.65 1.66 4.121 Upper 95% CI 0.222 0.4487 70.66 30.62 1158 1029 120.6 91.19 97.44 109.5 4.134 13.53 Spring only versus Spring + AD P < 0.003 P < 0.0007 P < 0.0001 P < 0.0089 P < 0.0079 P < 0.05 IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.1635 0.3575 61.45 22.3 1121 997.8 113 84.2 85.2 102.6 1.233 8.826 SD 0.06999 0.08692 11.01 7.931 29.73 24.78 6.083 5.63 9.859 5.595 1.168 2.957 Minimum 0.08 0.269 47.4 10.8 1087 970 108 77 72 96 0.2 5.142 Maximum 0.287 0.491 82.3 33.3 1164 1034 121 91 98 109 2.5 12.33 Percentiles  25 0.106 0.2893 53.3 15.3 1096 977.5 108 78.5 76 97 0.2 5.982  50 0.152 0.3325 59.4 22.55 1114 990 110 86 86 103 1 8.915  75 0.2128 0.4408 68.78 29.18 1150 1022 119.5 89 94 108 2.5 11.58 Lower 95% CI 0.105 0.2663 52.24 13.98 1084 967 105.4 77.21 72.96 95.65 1.66 4.121 Upper 95% CI 0.222 0.4487 70.66 30.62 1158 1029 120.6 91.19 97.44 109.5 4.134 13.53 Spring only versus Spring + AD P < 0.003 P < 0.0007 P < 0.0001 P < 0.0089 P < 0.0079 P < 0.05 IMD, intermolar distance; BVF, bone volume fraction; TD, tissue density; Tb.Th, trabecular thickness; Tb. Sp, trabecular spacing; OcN: osteoclast number. View Large Table 1. Distribution of data at 7 days. IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.1635 0.3575 61.45 22.3 1121 997.8 113 84.2 85.2 102.6 1.233 8.826 SD 0.06999 0.08692 11.01 7.931 29.73 24.78 6.083 5.63 9.859 5.595 1.168 2.957 Minimum 0.08 0.269 47.4 10.8 1087 970 108 77 72 96 0.2 5.142 Maximum 0.287 0.491 82.3 33.3 1164 1034 121 91 98 109 2.5 12.33 Percentiles  25 0.106 0.2893 53.3 15.3 1096 977.5 108 78.5 76 97 0.2 5.982  50 0.152 0.3325 59.4 22.55 1114 990 110 86 86 103 1 8.915  75 0.2128 0.4408 68.78 29.18 1150 1022 119.5 89 94 108 2.5 11.58 Lower 95% CI 0.105 0.2663 52.24 13.98 1084 967 105.4 77.21 72.96 95.65 1.66 4.121 Upper 95% CI 0.222 0.4487 70.66 30.62 1158 1029 120.6 91.19 97.44 109.5 4.134 13.53 Spring only versus Spring + AD P < 0.003 P < 0.0007 P < 0.0001 P < 0.0089 P < 0.0079 P < 0.05 IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.1635 0.3575 61.45 22.3 1121 997.8 113 84.2 85.2 102.6 1.233 8.826 SD 0.06999 0.08692 11.01 7.931 29.73 24.78 6.083 5.63 9.859 5.595 1.168 2.957 Minimum 0.08 0.269 47.4 10.8 1087 970 108 77 72 96 0.2 5.142 Maximum 0.287 0.491 82.3 33.3 1164 1034 121 91 98 109 2.5 12.33 Percentiles  25 0.106 0.2893 53.3 15.3 1096 977.5 108 78.5 76 97 0.2 5.982  50 0.152 0.3325 59.4 22.55 1114 990 110 86 86 103 1 8.915  75 0.2128 0.4408 68.78 29.18 1150 1022 119.5 89 94 108 2.5 11.58 Lower 95% CI 0.105 0.2663 52.24 13.98 1084 967 105.4 77.21 72.96 95.65 1.66 4.121 Upper 95% CI 0.222 0.4487 70.66 30.62 1158 1029 120.6 91.19 97.44 109.5 4.134 13.53 Spring only versus Spring + AD P < 0.003 P < 0.0007 P < 0.0001 P < 0.0089 P < 0.0079 P < 0.05 IMD, intermolar distance; BVF, bone volume fraction; TD, tissue density; Tb.Th, trabecular thickness; Tb. Sp, trabecular spacing; OcN: osteoclast number. View Large Figure 2. View largeDownload slide (A) Intermolar distance (M1–M2) in the orthodontic spring only and the orthodontic spring + AD groups; (B) histogram showing the significant increase (P < 0.05) in the orthodontic tooth movement with AD at day 7; (C) histogram showing the significant increase (P < 0.05) in the orthodontic tooth movement with AD at day 14. Figure 2. View largeDownload slide (A) Intermolar distance (M1–M2) in the orthodontic spring only and the orthodontic spring + AD groups; (B) histogram showing the significant increase (P < 0.05) in the orthodontic tooth movement with AD at day 7; (C) histogram showing the significant increase (P < 0.05) in the orthodontic tooth movement with AD at day 14. Table 2. Distribution of data at 14 days. IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.4998 0.8827 60.85 30.25 1152 997.8 96.6 64.2 78.8 112 0.3 3.875 SD 0.1953 0.1463 8.333 5.717 32.24 71.06 5.505 9.834 4.658 9.327 0.2646 2.987 Minimum 0.296 0.679 51.3 23.9 1105 935 89 52 73 101 0 0.625 Maximum 0.713 1.053 72.3 37.2 1187 1110 102 76 86 121 0.5 6.5 Percentiles  25 0.3165 0.7668 55.28 24.88 1121 937.5 91 54.5 75.5 102 0 0.625  50 0.495 0.868 57.45 29.95 1164 990 98 65 78 116 0.4 4.5  75 0.6878 1.037 70.58 35.93 1179 1062 101.5 73.5 82.5 120 0.5 6.5 Lower 95% CI 0.189 0.7291 52.1 21.15 1112 909.6 89.77 51.99 73.02 100.4 0.16 2.87 Upper 95% CI 0.8105 1.036 69.6 39.35 1192 1086 103.4 76.41 84.58 123.6 1.43 9.29 Spring only versus spring + AD P < 0.014 P < 0.0095 P < 0.0159 P < 0.0079 P < 0.0079 P < 0.05 IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.4998 0.8827 60.85 30.25 1152 997.8 96.6 64.2 78.8 112 0.3 3.875 SD 0.1953 0.1463 8.333 5.717 32.24 71.06 5.505 9.834 4.658 9.327 0.2646 2.987 Minimum 0.296 0.679 51.3 23.9 1105 935 89 52 73 101 0 0.625 Maximum 0.713 1.053 72.3 37.2 1187 1110 102 76 86 121 0.5 6.5 Percentiles  25 0.3165 0.7668 55.28 24.88 1121 937.5 91 54.5 75.5 102 0 0.625  50 0.495 0.868 57.45 29.95 1164 990 98 65 78 116 0.4 4.5  75 0.6878 1.037 70.58 35.93 1179 1062 101.5 73.5 82.5 120 0.5 6.5 Lower 95% CI 0.189 0.7291 52.1 21.15 1112 909.6 89.77 51.99 73.02 100.4 0.16 2.87 Upper 95% CI 0.8105 1.036 69.6 39.35 1192 1086 103.4 76.41 84.58 123.6 1.43 9.29 Spring only versus spring + AD P < 0.014 P < 0.0095 P < 0.0159 P < 0.0079 P < 0.0079 P < 0.05 IMD, intermolar distance; BVF, bone volume fraction; TD, tissue density; Tb.Th, trabecular thickness; Tb. Sp, trabecular spacing; OcN, osteoclast number. View Large Table 2. Distribution of data at 14 days. IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.4998 0.8827 60.85 30.25 1152 997.8 96.6 64.2 78.8 112 0.3 3.875 SD 0.1953 0.1463 8.333 5.717 32.24 71.06 5.505 9.834 4.658 9.327 0.2646 2.987 Minimum 0.296 0.679 51.3 23.9 1105 935 89 52 73 101 0 0.625 Maximum 0.713 1.053 72.3 37.2 1187 1110 102 76 86 121 0.5 6.5 Percentiles  25 0.3165 0.7668 55.28 24.88 1121 937.5 91 54.5 75.5 102 0 0.625  50 0.495 0.868 57.45 29.95 1164 990 98 65 78 116 0.4 4.5  75 0.6878 1.037 70.58 35.93 1179 1062 101.5 73.5 82.5 120 0.5 6.5 Lower 95% CI 0.189 0.7291 52.1 21.15 1112 909.6 89.77 51.99 73.02 100.4 0.16 2.87 Upper 95% CI 0.8105 1.036 69.6 39.35 1192 1086 103.4 76.41 84.58 123.6 1.43 9.29 Spring only versus spring + AD P < 0.014 P < 0.0095 P < 0.0159 P < 0.0079 P < 0.0079 P < 0.05 IMD Spring only IMD Spring + AD BVF Spring only BVF Spring + AD TD Spring only TD Spring + AD Tb Th. Spring only Tb Th. Spring + AD Tb.Sp Spring only Tb.Sp Spring + AD OcN Spring only OcN Spring + AD Mean 0.4998 0.8827 60.85 30.25 1152 997.8 96.6 64.2 78.8 112 0.3 3.875 SD 0.1953 0.1463 8.333 5.717 32.24 71.06 5.505 9.834 4.658 9.327 0.2646 2.987 Minimum 0.296 0.679 51.3 23.9 1105 935 89 52 73 101 0 0.625 Maximum 0.713 1.053 72.3 37.2 1187 1110 102 76 86 121 0.5 6.5 Percentiles  25 0.3165 0.7668 55.28 24.88 1121 937.5 91 54.5 75.5 102 0 0.625  50 0.495 0.868 57.45 29.95 1164 990 98 65 78 116 0.4 4.5  75 0.6878 1.037 70.58 35.93 1179 1062 101.5 73.5 82.5 120 0.5 6.5 Lower 95% CI 0.189 0.7291 52.1 21.15 1112 909.6 89.77 51.99 73.02 100.4 0.16 2.87 Upper 95% CI 0.8105 1.036 69.6 39.35 1192 1086 103.4 76.41 84.58 123.6 1.43 9.29 Spring only versus spring + AD P < 0.014 P < 0.0095 P < 0.0159 P < 0.0079 P < 0.0079 P < 0.05 IMD, intermolar distance; BVF, bone volume fraction; TD, tissue density; Tb.Th, trabecular thickness; Tb. Sp, trabecular spacing; OcN, osteoclast number. View Large Alveolar decortication decreases alveolar bone volume and density We next evaluated if ADs in combination to orthodontic force would have an effect in bone volume and quality. Our micro-CT analysis showed a significant decrease in BVF in the spring + AD group when compared with spring only at day 7 (Table 1 and Figure 3A, 3B, and 3E) and at day 14 (Table 2 and Figure 3C, 3D, and 3F). Similarly, tissue density was significantly lower in the spring + AD at day 7 (Table 1 and Figure 3A, 3B, and 3G) and at day 14 (Table 2 and Figure 3C, 3D, and 3H). Figure 3. View largeDownload slide Micro-CT data showing BVF, tissue density, and trabecular thickness at day 7 and day 14 in the orthodontic spring only and orthodontic spring + AD group A, coronally reconstructed micro-CT image of orthodontic spring only group at day 7; (B) coronally reconstructed micro-CT image of orthodontic spring + AD group at day 7; (C) coronally reconstructed micro-CT image of orthodontic spring only group at day 14; (D) coronally reconstructed micro-CT image of orthodontic spring + AD group at day 14; (E and F) histogram showing the significant decrease (P < 0.05) in the BVF with alveolar decortication at day 7 and day 14, respectively; (G and H) histogram showing the significant decrease (P < 0.05) in the tissue density with alveolar decortication at day 7 and day 14, respectively; (I and J) histogram showing the significant increase (P < 0.05) in the trabecular spacing with AD at day 7 and day 14, respectively; (K and L) histogram showing the significant decrease (P < 0.05) in the trabecular thickness with AD at day 7 and day 14, respectively. The white shaded rectangle in Figure 4C is the region of interest where the bone parameters (BVF, tissue density, and trabecular thickness were measured). Figure 3. View largeDownload slide Micro-CT data showing BVF, tissue density, and trabecular thickness at day 7 and day 14 in the orthodontic spring only and orthodontic spring + AD group A, coronally reconstructed micro-CT image of orthodontic spring only group at day 7; (B) coronally reconstructed micro-CT image of orthodontic spring + AD group at day 7; (C) coronally reconstructed micro-CT image of orthodontic spring only group at day 14; (D) coronally reconstructed micro-CT image of orthodontic spring + AD group at day 14; (E and F) histogram showing the significant decrease (P < 0.05) in the BVF with alveolar decortication at day 7 and day 14, respectively; (G and H) histogram showing the significant decrease (P < 0.05) in the tissue density with alveolar decortication at day 7 and day 14, respectively; (I and J) histogram showing the significant increase (P < 0.05) in the trabecular spacing with AD at day 7 and day 14, respectively; (K and L) histogram showing the significant decrease (P < 0.05) in the trabecular thickness with AD at day 7 and day 14, respectively. The white shaded rectangle in Figure 4C is the region of interest where the bone parameters (BVF, tissue density, and trabecular thickness were measured). Additionally, there was a significant increase in the trabecular spacing in the spring + AD group at day 7 (Table 1 and Figure 3A, 3B, and 3I) and at day 14 (Table 2 and Figure 3C, 3D, and 3J). However, there was a significant decrease in the trabecular thickness in spring + AD group at day 7 (Table 1 and Figure 3A, 3B, and 3K) and at day 14 (Table 2 and Figure 3C, 3D, and 3L). Alveolar decortication increases the number of osteoclasts at the pressure site Next, we evaluated whether the increased tooth movement rate and decreased bone volume and density associated with ADs were correlated with changes in osteoclast numbers. Our histological analysis revealed a significant increase in the osteoclast numbers at day 7 (Table 1 and Figure 4A–C and I) and at day 14 (Table 2 and Figure 4E–H and J). Furthermore, at day 14, we observed fibrous tissue replacing the alveolar bone in the spring + AD group when compared with the spring only group (Figure 4G–H). Figure 4. View largeDownload slide Histologic examination and quantification of osteoclast number day 7 and day 14 in the orthodontic spring only and orthodontic spring + AD groups. (A and B) TRAP positive cells in orthodontic spring only group at day 7; (C and D) TRAP positive cells in orthodontic spring + AD group at day 7; (E and F) TRAP positive cells in orthodontic spring only group at day 14; (G and H) TRAP positive cells in orthodontic spring + AD group at day 14; (I) histogram showing the significant increase (P < 0.05) in the osteoclast number with alveolar decortication at day 7; (J) histogram showing the significant increase (P < 0.05) in the osteoclast number with alveolar decortication at day 14. Black arrows depict the number of TRAP positive cells. Figure 4. View largeDownload slide Histologic examination and quantification of osteoclast number day 7 and day 14 in the orthodontic spring only and orthodontic spring + AD groups. (A and B) TRAP positive cells in orthodontic spring only group at day 7; (C and D) TRAP positive cells in orthodontic spring + AD group at day 7; (E and F) TRAP positive cells in orthodontic spring only group at day 14; (G and H) TRAP positive cells in orthodontic spring + AD group at day 14; (I) histogram showing the significant increase (P < 0.05) in the osteoclast number with alveolar decortication at day 7; (J) histogram showing the significant increase (P < 0.05) in the osteoclast number with alveolar decortication at day 14. Black arrows depict the number of TRAP positive cells. Discussion Our null hypothesis that there will be no difference in the amount of tooth movement between the control (spring only) and experimental (spring + AD) groups was rejected. With AD, there was a significant increase in the rate of tooth movement at 7 and 14 days after the application of orthodontic force. We selected them to study the effects of ADs on the rate of tooth movement, since this mildly invasive procedure is feasible to be performed by orthodontists in day-to-day clinical practice. It has been shown that alveolar perforations performed after raising a full-thickness flap induced a RAP in the experimental tooth movement region in animal studies (29–31). Likewise, we found increased osteoclastogenesis (by an increased number of TRAP positive cells) and decreased BVF and tissue density when AD was associated with orthodontic tooth movement, 7 and 14 days after the placement of orthodontic springs, in comparison to spring only group (no alveolar decortications). These observations suggest that alveolar decortications with no surgical incision or flap could induce similar acceleratory remodelling effects to the more invasive procedures. In addition, the RAP induced by ADs seemed to persist for at least 2 weeks after the procedure. Similarly to our study, Cheung et al. studied the effects of placing five osteoperforations around the maxillary first molars of rats during experimental tooth movement. The authors found a 1.86-fold increase in the rate of tooth movement in relation to the opposite side (orthodontic spring only) 3 weeks after the placement of springs. In addition, the alveolar bone at the side that received osteoperforations presented with a significant decrease in bone density (26). Although the split mouth study design would avoid interanimal variation, the degree of tooth movement acceleration could not be fully determined because the induction of the RAP does not seem to be restricted locally (18), suggesting that the control side could also be under the effects of RAP. Tsai et al. also found an increased rate of tooth movement when osteoperforations were performed in the adjacent region of tooth movement in rats (25). In this study, three flapless osteoperforations in the palatal region of the first molar of rats were compared with the effects of alveolar corticision in the same region in the tooth movement rate and tissue reaction. An orthodontic force of 50 g was used in the surgical and control groups, and the rate of tooth movement was assessed weekly, whereas the tissue reaction was evaluated after 3 and 6 weeks. However, a force of 50 g in a rodent model could be too high when comparing with ideal clinical forces (27). In our study, an orthodontic force of 8–10 g was used, and the rate of tooth movement and tissue changes were evaluated after 1 and 2 weeks so that the early responses could also be understood. Furthermore, in our study, we made four holes adjacent to the maxillary first molar on the palatal alveolar bone using a high-speed quarter round bur. A decrease in the number of osteoclasts was observed from day 7 to 14 after the application of orthodontic force. Maximum osteoclast recruitment in experimental tooth movement in rodents has been suggested to occur between days 3 and 5, with the number of osteoclast drastically decreasing at day 7 (25). In addition, 14 days is the duration of a remodelling cycle (activation–resorption–formation) in rodents; that is the reason we have examined the orthodontic tooth movement and bone parameters after alveolar decortication at an earlier time point (7 days) and at a later time point (14 days). We observed fibrous tissue replacing the alveolar bone in the spring + AD group at day 14. This finding was also reported by Wang et al., and the authors found fibrous tissue around the dental roots at the tension side 21 days after experimental corticotomy-assisted tooth movement in rats, which was then replaced by bone at day 60 (32). We plan to investigate the effect of AD associated with tooth movement in later time points to further study the temporal changes in bone quality and osteoclast recruitment in response to this small surgical procedure. The only clinical trial studying the effects of osteoperforations in the alveolar bone in orthodontic patients evaluated the rate of canine retraction with or without osteoperforations (split mouth study design). In addition, the effect of osteoperforations in the stimulation of inflammatory markers in the gingival crevicular fluid (GCF) was studied at different time points. Finally, the pain and discomfort reported by patients during the treatment were also evaluated (23). The authors have shown a 2.3-fold increased rate of canine retraction and a significant increase in the expression of inflammatory markers. In addition, patients reported minimal discomfort at the location of the alveolar perforations, suggesting that osteoperforation is an effective and likely acceptable clinical procedure to decrease orthodontic treatment duration. Although our study showed significant increase in the rate of the orthodontic tooth movement, extrapolation of our findings to the clinical situation must be done with caution as there is no osteonal remodelling (secondary remodelling) in rats, unlike in humans. Moreover, a frictionless space closure mechanism was used in this study. Nevertheless, this in vivo study helped us to understand the effect of alveolar decortication on the orthodontic tooth movement and bone modelling and remodelling. Our future research study will focus on the extent and area of the surgical insult (through alveolar decortications) and its effect on the orthodontic tooth movement and bone modelling and remodelling. Our future study will also focus on the long-term effects of alveolar decortication on the rate of the orthodontic tooth movement and alveolar bone remodelling. Moreover, we will also study the correlation, if any, between increase in osteoclast number and root resorption. Conclusions 1. There was a significant increase in the rate of the tooth movement at day 7 and day 14 with alveolar decortication. 2. There was a decrease in BVF and tissue density and increase in trabecular spacing with alveolar decortications. 3. There was an increase in the osteoclast number with alveolar decortications. Conflict of interest None to declare. References 1. Krishnan , V. and Davidovitch , Z . ( 2009 ) On a path to unfolding the biological mechanisms of orthodontic tooth movement . 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For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)

Journal

The European Journal of OrthodonticsOxford University Press

Published: Aug 1, 2018

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