ORIGINAL ARTICLE
Effect of corticision and different force magnitudes on orthodontic tooth movement in a rat model Christopher A. Murphy,a Taranpreet Chandhoke,b Zana Kalajzic,c Rita Flynn,d Achint Utreja,e Sunil Wadhwa,f Ravindra Nanda,g and Flavio Uribeh Madison and Farmington, Conn, and New York, NY
Introduction: The aims of this study were to evaluate the effect of 2 distinct magnitudes of applied force with and without corticision (flapless corticotomy) on the rate of tooth movement and to examine the alveolar response in a rat model. Methods: A total of 44 male rats (6 weeks old) were equally divided into 4 experimental groups based on force level and surgical intervention: light force, light force with corticision, heavy force, and heavy force with corticision. The forces were delivered from the maxillary left first molar to the maxillary incisors using prefabricated 10-g (light force) or 100-g (heavy force) nickel-titanium springs. The corticision procedure was performed at appliance placement and repeated 1 week later on the mesiopalatal aspect of the maxillary left first molars, with the right sides serving as the untreated controls. Microcomputed tomography was used to evaluate tooth movement between the maxillary first and second molars, and the alveolar response in the region of the maxillary first molar on day 14. Osteoclasts and odontoclasts were quantified, and the expression of receptor activator of nuclear factor kappa ß ligand was examined. Results: Intragroup comparisons of bone volume fraction (BVF) and tissue density were found to be significantly less on the loaded sides, with the exception of BVF in the light force group. Intergroup comparisons evaluating magnitude of tooth movement, BVF, apparent density, and tissue density showed no significant differences. Histomorphometric analysis indicated that BVF was decreased in the light force group. No significant differences in the total numbers of osteoclasts and odontoclasts and the expression of receptor activator of nuclear factor kappa ß ligand were found between the groups. Conclusions: No differences in tooth movement or alveolar response were observed with microcomputed tomography based on force level or corticision procedure. A flapless surgical insult in the mesiopalatal aspect of the first molar with a single-site corticision was unable to induce clinical or histologic changes after 2 weeks of orthodontic tooth movement regardless of the force magnitude. Histologic analysis of the furcation area showed that light force significantly decreased BVF. (Am J Orthod Dentofacial Orthop 2014;146:55-66)
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lthough there are numerous benefits of orthodontic treatment, its prolonged duration is often seen as a drawback. The length of therapy is influenced by a number of factors, including the complexity of the malocclusion, the orthodontist's skill,
the patient's cooperation, and the rate of tooth movement. Extended treatment times have been associated with negative outcomes, such as increased risk for caries,1 periodontal disease,2,3 root resorption,4 and pulpal reactions.5 Reducing the duration of orthodontic
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h Associate professor and program director, Division of Orthodontics, Department of Craniofacial Sciences; Charles Burstone professor, School of Dental Medicine, University of Connecticut, Farmington, Conn. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Supported by a Biomedical Research Award 2012 from the American Association of Orthodontists Foundation. Address correspondence to: Flavio Uribe, University of Connecticut Health Center, 263 Farmington Ave, Farmington, CT 06030; e-mail, [email protected]. Submitted, October 2013; revised and accepted, March 2014. 0889-5406/$36.00 Copyright Ó 2014 by the American Association of Orthodontists. http://dx.doi.org/10.1016/j.ajodo.2014.03.024
Private practice, Madison, Conn. Assistant professor, Division of Orthodontics, Department of Craniofacial Sciences, School of Dental Medicine, University of Connecticut, Farmington, Conn. c Research associate, Division of Orthodontics, Department of Craniofacial Sciences, School of Dental Medicine, University of Connecticut, Farmington, Conn. d Undergraduate dental student, School of Dental Medicine, University of Connecticut, Farmington, Conn. e Resident, Division of Orthodontics, Department of Craniofacial Sciences, School of Dental Medicine, University of Connecticut, Farmington, Conn. f Assistant professor, Division of Orthodontics, College of Dental Medicine, Columbia University, New York, NY. g Professor and head, Division of Orthodontics, Department of Craniofacial Sciences; alumni endowed chair, School of Dental Medicine, University of Connecticut, Farmington, Conn. b
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treatment has the benefit of possibly minimizing these unwanted side effects and improving patient satisfaction and acceptance. Orthodontic tooth movement is a dynamic process of bone modeling involving anabolic and catabolic responses to mechanical loading.6 The strains generated by orthodontic forces are transmitted to the periodontal ligament (PDL) and supporting alveolar bone, producing areas of tension and pressure within the PDL, with bone resorption occurring at sites of compression, and bone formation occurring in regions of tension.7 The velocity of tooth movement is regulated by bone turnover, bone density, and the degree of hyalinization of the PDL in response to the forces being applied. Continuous light forces are widely believed to be the most effective means of producing efficient tooth movement.8,9 Ideally, a method to increase tooth movement should be directed by frontal resorption (tightly coupled osteoclast-driven resorption on the compression side) and also cause minimal patient discomfort.7,10 Efforts to enhance the rate of orthodontic tooth movement have targeted these factors and can be categorized as either pharmacological or physical. Pharmacologic agents have been shown to influence orthodontic tooth movement by altering bone metabolism. Despite augmenting tooth movement, these treatments have had limited clinical use because of many negative local and systemic side effects such as hyperalgesia,11 bone loss and osteoporosis, delayed wound healing, and root resorption.12,13 As a result, research has shifted toward physical methods aimed at enhancing tooth movement. A number of physical methods to increase tooth movement have been examined previously. These have included the use of pulsed and static magnetic fields,14,15 electrical currents,16,17 lasers,18 and surgical manipulation of the alveolar bone.19 Surgical methods to enhance the rate of tooth movement have garnered considerable attention in recent years and include alveolar surgery to undermine interseptal bone,19 corticotomies,20-26 dentoalveolar distraction,27-29 dental distraction,21,30 and corticision.31-33 By enhancing the local catabolic and anabolic processes of bone turnover, these surgical methods might have the potential to increase the rate of orthodontic tooth movement and reduce treatment times.34,35 The clinical applications of these surgical interventions have been hampered by a number of factors, including duration of the effect and poor patient acceptance because of the invasiveness of these procedures. Kim et al32,33 introduced the corticision procedure in an effort to develop a minimally invasive approach to induce a regional acceleratory phenomenon effect
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without flap reflection that could be repeated with less patient discomfort. Unlike corticotomies, in which the surgical insult is obtained by reflecting a full flap to gain access to the cortical bone, with corticision, a reinforced scalpel is used as a thin chisel to separate the interproximal cortices transmucosally without reflecting a flap. These authors demonstrated that even minimally invasive insults to the alveolus with corticision can invoke a regional acceleratory phenomenon effect and stimulate orthodontic tooth movement. More evidence is needed that examines the biologic process involved to fully understand the mechanism by which orthodontic tooth movement can be modulated by these procedures. In addition, determining the effects of light and heavy forces on the overall rate of tooth movement is needed to better understand the optimal range required. The ideal force level for efficient tooth movement also requires further study. This study was designed to assess the rate of tooth movement and the biologic effects of corticision with 2 distinct force magnitudes on the remodeling of alveolar bone 14 days after the initiation of orthodontic tooth movement in a rat model. MATERIAL AND METHODS
A total of 44 male Wistar rats (weight, 150-250 g; Charles River Laboratories, Wilmington, Mass) were used in this study after approval by the Animal Care Committee of the University of Connecticut (number 2010-668). The final sample size was determined by a power analysis performed with data from a pilot study. Based on the initial pilot data, it was determined that 11 rats would be required in each group to provide statistical power (1-ß) of 0.8 and type I error of 0.05.36 The rats were randomly allocated to 1 of the 4 groups (11 per group) based on the surgical procedure and the application of light (10 g) or heavy (100 g) force: (1) no corticision and 10 g of force (LF), (2) no corticision and 100 g of force (HF), (3) corticision at appliance insertion and 1 week later with 10 g of force (LF1C), and (4) corticision at appliance insertion and 1 week later with 100 g of force (HF1C). The contralateral (right) side was used as the unloaded control for each animal. The rats were subjected to orthodontic forces from the maxillary left first molar to the central incisors (Fig 1, A). Closed-coil nickel-titanium springs delivering 10 or 100 g of force were used for the application of the light and heavy orthodontic forces, respectively. The force/deflection rate for the spring was determined to calibrate the amount of force produced by activation of the spring. The animals were placed under general anesthesia with xylazine (13 mg/kg) and ketamine (87 mg/kg).
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Fig 1. A, Appliance design indicating placement of the nickel-titanium coil springs from the maxillary left first molar to the central incisors. The arrow indicates the location and extent of the corticision procedure. B, Rat maxilla after dissection of soft tissues. Arrow indicates the location and extent of the corticision procedure on the bone.
Only the left side of the maxilla was treated. The contralateral (untreated) side served as the unloaded control for histologic and microcomputed tomography purposes, and to evaluate the physiologic distal drift of the molars. All animals were bonded by 1 investigator (C.A.M.) to eliminate interinvestigator bias. A 0.008-in stainless steel ligature was threaded through the contact between the maxillary left first and second molars. A light or heavy spring was then attached to the 0.008in stainless steel ligature around the first molar and securely ligated at the mesial surface of the maxillary first molar. Self-etching primer (Transbond Plus; 3M Unitek, Monrovia, Calif) was applied to the mesiopalatal surface of the maxillary first molar, and the ligature was bonded with light-cured dental adhesive resin cement (Transbond; 3M Unitek) using a commercial unit (LEDemetron 1; Kerr, Orange, Calif). To prevent the ligatures from dislodging because of the lingual curvature and eruption pattern of the maxillary incisors, grooves were prepared 0.5 mm from the gingival margin on the distal surfaces of the maxillary central incisors. A second 0.008-in stainless steel ligature was then placed around both maxillary incisors, and the spring was activated and attached to this ligature. After the ligature had been tied and cut, composite resin (Transbond XT Light Cure Adhesive Paste; 3M Unitek) was placed over the wire to prevent slipping and gingival irritation, as well as pulpal irritation to the exposed dentin. Finally, the mandibular incisors were reduced to prevent appliance breakage as described previously.14 The appliance was checked twice weekly to evaluate its integrity. One week after the initial placement of the appliance, the animals were reanesthetized and the springs reactivated. Corticision was applied at the time of orthodontic appliance placement and 1 week later in the corticision groups while the animals were under anesthesia. This protocol was selected based on the results of a previous study in which an orthodontic force with 2 corticision
procedures resulted in significantly more tooth movement than with a single or no corticision procedure.36 Corticision was performed on the mesiopalatal aspect of the maxillary left first molar (Fig 1, A). This location was selected to ensure clear access to the bone adjacent to the first molar, with enough safety margin to prevent injury to the roots of the teeth. The tip of a reinforced surgical blade (number 11; Bard-Parker, Franklin Lakes, NJ) capable of making a surgical incision with a minimum thickness of 400 mm was used. The blade was positioned on the mesiopalatal gingiva, 0.5 mm from the corresponding tooth surface at an inclination of 45 to 60 to the long axis of the maxillary first molar. The blade was inserted gradually through the overlying gingiva into the cortical bone (Figs 1, B, and 2). The corticisions were performed by 1 investigator (C.A.M.) after being calibrated with deceased rats. This investigator used tactile sense to confirm penetration of the palatal gingiva and bone. Microcomputed tomography analysis was performed after the experimental period (day 14) for all animals. Each rat was killed, and the maxilla was excised, cleansed of soft tissue, and hemisected. Analysis was performed by the microcomputed tomography facility at the University of Connecticut. Scanning was done at 55 kV and 145 mA, collecting 1000 projections per rotation with a 300-ms integration time. Three-dimensional images were constructed using standard convolution and back projection algorithms with Shepp and Logan filtering and rendered in a 12.3-mm field of view at a discrete density of 578,704 voxels per cubic millimeter (isometric 12-mm voxels). Microcomputed tomography images were used for quantitative analysis of bone changes in the region of the maxillary first molar. Tooth movement and alveolar bone parameters were evaluated. The amount of tooth movement was assessed on 2-dimensional sagittal sections taken through the centers of the maxillary first
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Fig 2. High-resolution microcomputed tomography images of the right (control) and the left (experimental) hemimaxillae showing the location and depth (0.4 mm) of the corticision immediately after the surgical procedure (right panel). Note the location of the corticision adjacent to the mesiopalatal root of the first molar (1M). B, Buccal side; P, palatal side; 1M, first molar.
and second molars (the image plane that showed the most structure of the distobuccal and mesial root) and measured at the interproximal heights of contour between these teeth (the distance between the most mesial point of the second molar crown and the most distal point of the first molar crown, first and second molar distance) (Fig 3). The initial separation distance at day 1 was 0 mm in all groups (ie, convex crown surfaces were touching). Changes in the alveolar bone were studied by analyzing the furcation area of the maxillary first molar. The region of interest for the alveolar bone analysis was defined vertically as the most occlusal point of the furcation to the apex of the maxillary roots; transversely, it was defined as the space between the buccal and lingual cortical bone; sagittally, it included 40 sections (12 mm) beginning at the mesial root and continuing distally (Fig 4, A and B). Parameters studied included bone volume fraction (BVF),
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apparent density, and tissue density. BVF, which represents the amount of alveolar bone in the region of interest, was calculated as the percentage of bone volume (BV) to total volume (TV), denoted as BV/TV. Apparent density was a calibrated measure of hydroxyapatite equivalent to the total volumetric mineral density of the trabecular bone (including the bone marrow) normalized to the region of interest (TV). With tissue density, the hydroxyapatite was calibrated to only represent the volumetric mineral density of trabecular bone tissue (BV) and excluding marrow and porosities, thereby closely approximating the amount of mineralized bone. To quantify the osteoclast activity and relate it to the bone density changes, histomorphometric analysis was performed using 6 animals from each experimental group. Each hemisected maxilla was placed in 10% formalin for 5 days at 4 C with constant agitation. After fixation, the samples were decalcified in 14% EDTA for
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Fig 3. Representative microcomputed tomography image indicating the measurement of tooth movement between the first and second molars. A reference line was drawn between the points of greatest convexity between the 2 interproximal surfaces.
4 weeks and processed for standard paraffin embedding. Serial 5-mm sagittal sections of the hemimaxillae were obtained and stained with routine hematoxylin and eosin stains and tartrate-resistant acid phosphatase (TRAP) activity using an acid phosphatase leukocyte kit (Sigma Chemical, St Louis, Mo) according to the manufacturer's instructions. Three sections showing the most pulp structure of the distobuccal root (midroot sections) were used for the analysis (Fig 5, A). Active osteoclasts were identified as TRAP-positive, multinucleated cells (.2 nuclei) that were touching the bone surface. The exact area for osteoclast quantification included a rectangular box (450 3 450 mm) that was placed on compression side of the alveolar bone with the highest osteoclast activity (Fig 6, C). BVF was defined as the percentage of BV to TV. To quantify the level of osteoclastic activity, the osteoclast number was then standardized to the BVF. The osteoclast surface was defined as the total surface of active osteoclasts divided by total bone surface in a defined box and indicated as a percentage. Odontoclasts were identified as TRAP-positive multinucleated cells (.2 nuclei) on the dentin surface and were quantified on the mesial surface of the distobuccal root in the line starting from the bifurcation to the end of the apex of the distobuccal root (Fig 5, C). The odontoclast surface was calculated as the total surface of all odontoclasts divided by the total dentin surface in the defined area. Mean values for these parameters were calculated from 3 adjacent sections (midroot) for each experimental animal; these were then used for statistical tests.
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Histomorphometric analyses were carried out using Osteomeasure software (Osteometrics, Decatur, Ga). Immunohistologic analyses for receptor activator of nuclear factor kappa b ligand (RANKL) were performed on all experimental groups. RANKL is an osteoblast and osteocyte-derived factor that is essential for the differentiation, activation, and survival of osteoclasts and used as an indicator of osteoclastic activity. Tissue sections were deparaffinized with xylene and rehydrated with decreasing concentrations of ethanol. After rehydration in deionized water, the tissues were incubated in 1X citrate buffer (pH 6.0) at 60 C overnight to unmask the specific antigen. The next day, the tissues were washed in phosphate-buffered saline (PBS) and blocked with 10% normal goat serum in 1% bovine serum albumin for 2 hours. Incubation with the primary antibody was performed at 4 C overnight using rabbit polyclonal anti-RANKL antibody at a concentration of 1:200 in 1% bovine serum albumin (LS-B1425/46594; LifeSpan BioSciences, Seattle, Wash). The next day, the tissues were washed in PBS and incubated with Alexa Fluor 594 goat antirabbit secondary antibody (A11037; LifeTechnologies, Carlsbad, Calif) in 2% normal goat serum and 1% bovine serum albumin at a concentration of 1:200 for 60 minutes. The sections were counterstained with 40 ,6-diamidino-2-phenylindole (DAPI) to obtain a total cell number and mounted with 50% glycerol in PBS. The signal was visualized and photographed by fluorescence microscopy using fluorescein isothiocyanate (FITC) and DAPI filter cubes of the Axiovert 200 microscope (Carol Zeiss Microscopy, Jena, Germany). For quantification, 3 sagittal molar sections from 6 different experimental animals were analyzed. Ten-times magnified images of the compression area (mesial surface of distobuccal root) of alveolar bone were used to evaluate the area that included RANKL labeling. RANKL labeling (TRITC-red) was quantified using ImageJ software (National Institutes of Health, Bethesda, Md) and calculated as a percentage per total area in each magnified image. The values from 3 sections were then averaged for each rat, and the means from 6 animals in each experimental group were used to conduct statistical tests. Statistical analysis
Statistical analyses were performed using GraphPad Prism (GraphPad Software, La Jolla, Calif) with analysis of means and standard deviations for each study parameter. Intergroup comparisons for tooth movement, bone volume parameters by microcomputed tomography and histomorphometry, and RANKL expression were performed with 1-way analysis of variance (ANOVA). Considering multiple pairwise comparisons used across the 4 groups, Bonferroni post-hoc tests were performed to
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Fig 4. Region of interest for microcomputed tomography analysis of BVF, tissue density, and apparent density on day 14 from A, axial and B, coronal views. The region of interest highlighted in green. Measurements were made approximating the first molar region (molar roots denoted by: M, Mesial; MP, mesiopalatal; MB, mesiobuccal; DP, distopalatal; DB, distobuccal). Intragroup comparisons of C, BVF; D, tissue density; and E, apparent density on day 14 by microcomputed tomography between the loaded and unloaded sides. *P \0.05 denotes statistically significant differences by paired t test analysis of the loaded and treated sides vs the unloaded and untreated sides (n 5 11).
minimize the risk of type I errors. Intragroup comparisons of microcomputed tomography measures of bone density changes comparing the treated with the untreated control sides were performed by paired sample t tests. Significance was accorded at P \0.05. A total of 11 rats were used in each study group, and all were examined for tooth movement and bone volume assessments. RESULTS
The experimental phase for each study group was 14 days, and all data were reported as means and standard deviations for each parameter. To calculate the differences in the amount of tooth movement between the groups at the end of the experimental phase, maxillary molar mesialization was evaluated by measuring the distance between the distal height of contour of the maxillary first molar and the mesial height of contour of the maxillary second molar on microcomputed tomography images (Fig 3). Microcomputed tomography analysis
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performed on the hemimaxillae of the animals receiving a light force (10 g) without corticision for 14 days showed that the mean amounts of maxillary first molar mesialization were 0.627 6 0.271 mm on the loaded side and 0.150 6 0.224 mm on the unloaded side. The mean amounts of maxillary first molar mesialization in the animals receiving light force (10 g) plus corticision were 0.602 6 0.251 mm on the loaded side and 0.072 6 0.102 mm on the unloaded side. When the heavy force (100 g) group without corticision was studied using microcomputed tomography, the mean amounts of maxillary first molar mesialization were 0.673 6 0.334 mm on the loaded side and 0.060 6 0.173 mm on the unloaded side. In the heavy force (100 g) group plus corticision, the mean amounts of maxillary first molar mesialization were 0.6631 6 0.2553 mm on the loaded side and 0.029 6 0.054 mm on the unloaded side. There were no significant differences in the amounts of tooth
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Fig 5. A, Representative section indicating the field of view and the region of interest (black box) for the histomorphometric measurements (5-times magnification). B, Comparison of intergroup BVF on the compression side on day 14 by histomorphometry. ANOVA comparisons of the light (10 g) and heavy (100 g) force groups with and without corticision. Significant differences between groups are noted by *P \0.05 (n 5 6).
movement observed at day 14 between any groups (P 5 0.9354). To evaluate the effects of the differential forces with and without corticision on bone remodeling, microcomputed tomography images of the maxillary first molars were obtained for analysis (Fig 4, A and B). In each experimental group, side-by-side comparisons were performed to evaluate differences between the loaded and unloaded sides using paired t tests. The LF1C, HF, and HF1C groups each demonstrated a statistically significant reduction in BVF on the treated side when compared with the contralateral control side (P \0.05) (Fig 4, C). Side-by-side comparisons of apparent density and tissue density indicated a statistically significant
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decrease in both parameters for all 4 study groups on the treated side compared with the control side (P \0.05) (Fig 4, D and E). Intergroup comparisons of bone parameters from microcomputed tomography images on the treated sides indicated no statistically significant difference for BVF, apparent density, or tissue density. Histomorphometry was used to examine localized bone remodeling changes on the compression sides in all groups (Fig 5, A). Intergroup comparisons of BVF (%) indicated that the LF group (21.25 6 8.916) had significantly less BVF compared with the other groups (LF1C, 57.65 6 14.93; HF, 57.09 6 16.74; HF1C, 60.46 6 14.08) (P \0.001) (Fig 5, B). To investigate osteoclast activity, osteoclasts were counted, and the osteoclast surface area was measured histologically for each group (Fig 6). For osteoclast number normalized to BVF, intergroup comparisons indicated no statistically significant differences between the groups: LF, 0.3393 6 0.308; LF1C, 0.2238 6 0.1515; HF, 0.1671 6 0.1268; and HF1C, 0.1036 6 0.0716 (P 5 0.2437). Osteoclast surface measurements were not significantly different among the 4 groups: LF, 7.913 mm 6 5.267; LF1C, 7.787 mm 6 3.59; HF, 6.179 mm 6 4.663; and HF1C, 5.032 mm 6 3.899 (P 5 0.684). To evaluate odontoclastic activity, odontoclasts were counted along the entire mesial surface of the distal root of the maxillary left first molar. The odontoclast numbers were not significantly different by intergroup comparisons: LF, 5.044 6 3.376; LF1C, 2.267 6 3.443; HF, 3.472 6 3.116; and HF1C, 4.767 6 3.099 (P 5 0.4925). Odontoclast surface areas were also not significant between the groups: LF, 0.09691% 6 0.06517%; LF1C, 0.0414% 6 0.05317%; HF, 0.07205% 6 0.06672%; and HF1C, 0.1034% 6 0.06674% (P 5 0.3992). To study the effect of corticision and force magnitude on osteoclast and odontoclast differentiation, the activation of RANKL was evaluated (Fig 7). RANKL expression is seen in osteocytes, osteoblasts, some fibroblastic cells in the PDL, and many bone marrow cells. The quantification of RANKL-positive signal showed a trend of greatest expression in the LF group (11.08 6 10.75). In the LF1C group, the mean values were 4.65 6 10.09; in HF group, the values were 1.06 6 1.76; and in HF1C group, the values were 1.19 6 2.54. When the groups were compared using ANOVA, the differences among the groups were not significant (P 5 0.0875). Hematoxylin and eosin staining for architecture consistently indicated increased fibrous tissues and less alveolar bone in the region of interest of the LF group compared with the other 3 groups.
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Fig 6. TRAP-stained sections among the study groups. Arrows point to TRAP-positive cells lying on alveolar bone (osteoclasts) and dentin (odontoclasts) (10-times magnification). A.B., Alveolar bone; D, dentin. DISCUSSION
Multiple methods have been used to enhance orthodontic tooth movement. Physical efforts to enhance the rate of tooth movement have classically focused on titration of the optimal force magnitude and determining the ideal duration of force application to efficiently move teeth. To promote the maximum rate of physiologic
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tooth movement, the classically held theory for the optimal force level was for it to be as light as possible and distributed evenly along the root's surface to minimize hyalinization, undermining resorption, and irreversible root resorption.37-40 This brought forth work by Begg and Kesling39 and Begg41 and the differential force theory, in which light forces are used for effective tooth movement, and heavy forces are used to anchor
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Fig 7. RANKL expression on the compression side in each study group. Fluorescence imaging of the region of interest for RANKL. RANKL expression was detected by TRITC filter (first row). Total background cells detected by DAPI (second row). Merged TRITC and DAPI images (third row) with arrows indicating double-labeled, RANKL-positive cells. Note the high RANKL expression in the LF group. Negative control for RANKL (right-most column) indicated DAPI-positive staining in the absence of RANKL antibody. T, Tooth; D, dentin; A.B., alveolar bone; H&E, hematoxylin and eosin.
segments to prevent movement. Storey and Smith42 also reported a threshold for the optimal force levels, with forces higher than this threshold resulting in cessation of tooth movement. However, these findings were not reproduced, and the controversy as to the ideal force level continued.43-47 More recent studies have revisited these concepts in animal models. Van Leeuwen et al48 showed a dose-dependent increase in tooth movement in beagles when low forces were applied at early stages and then increased to heavier forces. In a study by Gonzales et al,49 lighter forces (10-50 g) resulted in more tooth movement in rats than did heavier forces (100 g), specifically at later time points (days 14 and 28). Individual variations and biologic responses can also contribute to differences in the rate of tooth movement. In a study of light force application (25 cN) in beagles over an 80-day period by von Bohl et al,50 there were variations in the rate of tooth movement among the animals observed despite use of a consistent, light, and constant force. The authors attributed this variability to a higher degree of hyalinization in animals with slower rates of tooth movement. Understanding
the biologic response to orthodontic forces as well as the range of optimal force values requires further study. From a biologic perspective, the rate of tooth movement might be ultimately dictated by the capacity of the alveolar bone to undergo remodeling. Based on these principles, more recently developed surgical techniques could accentuate this bone remodeling process, thereby resulting in accelerated tooth movement and reduced treatment times. In 2001, Wilcko et al26 suggested that the increased rate of orthodontic tooth movement observed after surgical manipulation of the alveolus was the result of a regional acceleratory phenomenon. Subsequent research has confirmed that the acceleration of tooth movement associated with surgical intervention is the result of increased localized bone turnover based on a regional acceleratory phenomenon20,34 and is in proportion to the severity of the insult.27 In an effort to develop a minimally invasive, repeatable method of inducing a regional acceleratory phenomenon effect with minimal patient discomfort, Kim et al33 introduced corticision and found it to be an efficient means of stimulating tooth movement by inducing a regional
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acceleratory phenomenon and accelerating bone remodeling. Thus, we surmised that the targeted application of corticision coupled with the use of sufficient forces could promote accelerated tooth movement. The purpose of this study was to assess the effect of corticision and 2 distinct force levels (10 and 100 g) on the amount of orthodontic tooth movement and changes in the alveolus in a rat model after 14 days. An outbred rat strain was used; this introduced a degree of genetic variability that mimics patient-to-patient variations. To evaluate the effect of heavy (100 g) and light (10 g) forces with or without corticision on orthodontic tooth movement, microcomputed tomography measurements were taken between the maxillary first and second molars of the rats in each group. The measurements made on day 14 at the end of the experimental period were not significantly different. Alveolar changes were studied using both microcomputed tomography analysis and histomorphometry. Microcomputed tomography analysis was used to study the effects of a high or a low force on the alveolus with or without corticision at the furcation of the maxillary first molars. Significant differences existed between the experimental and control sides for all groups with respect to apparent density and tissue density, with all experimental sides showing reductions in density overall. BVF also demonstrated a significant difference between the experimental and control sides for all groups, with the exception of the LF group (Fig 4, C). Again, the experimental sides had decreased values compared with their contralateral controls. These intragroup findings reflected the bony remodeling occurring at the alveolus during orthodontic tooth movement.7,51 When intergroup comparisons were made, no significant differences were found with respect to any of the parameters studied, indicating no differences in the amount of alveolar change at the furcation among the groups. This supports the lack of a significant difference in the amount of tooth movement observed among the groups. Histologic sections were also used to evaluate changes occurring at the furcation area of the maxillary left first molars. BVF was significantly less in the LF group compared with the other groups. Sections from the LF group showed more fibrous tissue, indicating possibly greater resorption of bone in this group on the compression side compared with the other groups. This finding was different from what was observed using microcomputed tomography, which did not indicate a significant difference in any alveolar bone parameter between the groups. This discrepancy might reflect that the region of interest evaluated by microcomputed tomography was larger and extended farther buccolingually, thereby making small changes less detectable and underestimating the changes observed histologically
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along the distobuccal root. In future studies, the region of interest will be modified to include a similar region as was analyzed by histomorphometry. To evaluate the osteoclast activity, the total number of osteoclasts was normalized to the amount of mineralized bone, and the number of active osteoclasts was divided by the BVF. The osteoclast numbers were slightly elevated in the LF group; this was consistent with the low bone density observed by histomorphometry in this group. However, statistical analysis showed no significant differences among the groups. A similar trend was observed with osteoclast surfaces in the LF group. Taken together, these data suggest that the low force could have caused greater osteoclast recruitment to the area of alveolar bone at an earlier time that resulted in greater bone resorption. Although not significant, immunohistochemistry data showed that higher proportions of cells were labeled with RANKL when a low force was applied. However, many fibroblastic cells express RANKL, and a large area of fibrous tissue was consistently present in the region of interest in the LF group. It is possible that higher RANKL labeling reflects fibrosis as a result of the overall lack of bone in the compression area. This reduction in bone density in the LF group did not translate to greater tooth movement, thereby suggesting that earlier time points should be evaluated to determine whether osteoclastic activity was elevated sooner in the experimental phase. Based on the results in this study, it is possible that changes in osteoclast and odontoclast numbers as well as the elevation in RANKL expression might have occurred earlier in the experimental period; this would be consistent with a short-lived regional acceleratory phenomenon reported by other investigators.20,21,33,34 Interestingly, despite reduced alveolar bone and a trend of increased osteoclastic activity and RANKL expression, the LF1C group did not show similar histologic findings. It is possible that corticision modulates the normal physiologic processes; therefore, examining earlier time points will provide additional information as to the acute effect of this procedure on the PDL, bone, and supportive cells. With no significant changes in most of the bone and cellular parameters as well as the amount of tooth movement at day 14, further studies are needed to examine earlier time points, soon after the corticision and the force application. Baloul et al20 demonstrated that over a 6-week time course after selective alveolar decortication in rats, tooth movement was significantly enhanced only during the first week when compared with a tooth movement only group. Furthermore, Kim et al32 observed that after application of corticision, most tooth movement occurs during the first 2 weeks.
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In our study, during the experimental phase (at days 4, 7, 11, and 14), tooth movement was measured in all groups using feeler gauges (data not shown). Significant differences were seen early on at day 4, with the HF and HF1C groups showing more tooth movement than the LF groups. In addition, at day 7, the HF1C group continued to show significantly greater tooth movement compared with the other groups. However, consistent with the microcomputed tomography measurements, no group had a difference in tooth movement by the feeler gauge measurements at day 14. Feeler gauge measurements were found to overestimate the amount of tooth movement when compared with the microcomputed tomography measurements at day 14 (data not shown), although they had a similar trend. Ongoing studies will examine bone volume changes, histomorphometry (including osteoclast activity), and expression of key factors including RANKL at these earlier stages in this experimental model. There are additional areas that could improve this study, including the application of the corticision procedure. In this study, corticision was applied with a reinforced scalpel blade on days 1 and 7 on the mesiopalatal aspect of the maxillary left first molar. Every effort to standardize the corticision procedure was used. Here, corticision was applied on the mesiopalatal gingiva, 0.5 mm from the corresponding tooth surface at an inclination of 45 to 60 to the long axis of the maxillary first molar, with the blade inserted gradually through the overlying gingiva, penetrating into the cortical bone. A further improvement on this method in the future would be to use a surgical guide to standardize the application and a blade that would limit or indicate the depth of the incision being made. In an effort to use a minimally invasive surgical procedure, the corticision performed in this study was highly localized and minor; this might have resulted in a lack of significance in many of the parameters observed. In contrast, Kim et al32,33 performed corticision on the mesiobuccal, distobuccal, and distopalatal aspects of feline maxillary canines and on the mesiobuccal, distobuccal, mesiopalatal, and distopalatal aspects of canine maxillary second premolars and found significant differences in both tooth movement and alveolar remodeling. Thus, increasing the number of sites where corticisions are performed might also result in an enhanced tissue response and possibly increase the magnitude of tooth movement. Finally, a combination of the parameters tested in this study might help to accelerate tooth movement. For example, an initial light force followed by a corticision plus a heavy force after 1 week could enhance the rate of tooth movement. Since the bone volume is reduced and more fibrous tissue is present in response
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to a light force, a heavy force and corticision after the initial remodeling process might be able to displace the tooth through a less resistant alveolar bone. Further studies are required to examine the changes in bone remodeling, osteoclast numbers, and the expression of osteoclastogenic factors at earlier times after force application and corticision. A more significant alveolar injury could be required to enhance the rate of tooth movement than a corticision at 1 location. CONCLUSIONS
At day 14, there were no significant differences in tooth movement, microcomputed tomography bone parameters, or numbers of osteoclasts or odontoclasts related to the magnitude of the force or the addition of corticision. Light force caused a significant decrease in bone volume in the compression side observed histologically. ACKNOWLEDGMENTS
We would like to thank Ms. Renata Rydzik for her analysis of the microcomputed tomography images and Mr. Mike Brault from Ultimate Wire Forms for providing the nickel-titanium coil springs. REFERENCES 1. Richter AE, Arruda AO, Peters MC, Sohn W. Incidence of caries lesions among patients treated with comprehensive orthodontics. Am J Orthod Dentofacial Orthop 2011;139:657-64. 2. Geiger AM. Mucogingival problems and the movement of mandibular incisors: a clinical review. Am J Orthod 1980;78:511-27. 3. Alexander SA. Effects of orthodontic attachments on the gingival health of permanent second molars. Am J Orthod Dentofacial Orthop 1991;100:337-40. 4. Weltman B, Vig KW, Fields HW, Shanker S, Kaizar EE. Root resorption associated with orthodontic tooth movement: a systematic review. Am J Orthod Dentofacial Orthop 2010;137:462-76. 5. Grunheid T, Morbach BA, Zentner A. Pulpal cellular reactions to experimental tooth movement in rats. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;104:434-41. 6. Roberts WE, Huja S, Roberts JA. Bone modeling: biomechanics, molecular mechanisms, and clinical perspectives. Semin Orthod 2004;10:123-61. 7. Krishnan V, Davidovitch Z. Cellular, molecular, and tissue-level reactions to orthodontic force. Am J Orthod Dentofacial Orthop 2006;129:469.e1-32. 8. Iwasaki LR, Haack JE, Nickel JC, Morton J. Human tooth movement in response to continuous stress of low magnitude. Am J Orthod Dentofacial Orthop 2000;117:175-83. 9. Daskalogiannakis J, McLachlan KR. Canine retraction with rare earth magnets: an investigation into the validity of the constant force hypothesis. Am J Orthod Dentofacial Orthop 1996;109:489-95. 10. Norton LA, Burstone C. The biology of tooth movement. Boca Raton, Fla: CRC Press; 1989. 11. Yamaguchi M, Kasai K. Inflammation in periodontal tissues in response to mechanical forces. Arch Immunol Ther Exp (Warsz) 2005;53:388-98.
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12. Sekhavat AR, Mousavizadeh K, Pakshir HR, Aslani FS. Effect of misoprostol, a prostaglandin E1 analog, on orthodontic tooth movement in rats. Am J Orthod Dentofacial Orthop 2002;122: 542-7. 13. Krishnan V. Critical issues concerning root resorption: a contemporary review. World J Orthod 2005;6:30-40. 14. Darendeliler MA, Sinclair PM, Kusy RP. The effects of samariumcobalt magnets and pulsed electromagnetic fields on tooth movement. Am J Orthod Dentofacial Orthop 1995;107:578-88. 15. Stark TM, Sinclair PM. Effect of pulsed electromagnetic fields on orthodontic tooth movement. Am J Orthod Dentofacial Orthop 1987;91:91-104. 16. Davidovitch Z, Finkelson MD, Steigman S, Shanfeld JL, Montgomery PC, Korostoff E. Electric currents, bone remodeling, and orthodontic tooth movement. II. Increase in rate of tooth movement and periodontal cyclic nucleotide levels by combined force and electric current. Am J Orthod 1980;77:33-47. 17. Davidovitch Z, Finkelson MD, Steigman S, Shanfeld JL, Montgomery PC, Korostoff E. Electric currents, bone remodeling, and orthodontic tooth movement. I. The effect of electric currents on periodontal cyclic nucleotides. Am J Orthod 1980;77:14-32. 18. Kawasaki K, Shimizu N. Effects of low-energy laser irradiation on bone remodeling during experimental tooth movement in rats. Lasers Surg Med 2000;26:282-91. 19. Ren A, Lv T, Kang N, Zhao B, Chen Y, Bai D. Rapid orthodontic tooth movement aided by alveolar surgery in beagles. Am J Orthod Dentofacial Orthop 2007;131:160.e1-10. 20. Baloul SS, Gerstenfeld LC, Morgan EF, Carvalho RS, Van Dyke TE, Kantarci A. Mechanism of action and morphologic changes in the alveolar bone in response to selective alveolar decorticationfacilitated tooth movement. Am J Orthod Dentofacial Orthop 2011;139(4 Suppl):S83-101. 21. Liou EJ, Huang CS. Rapid canine retraction through distraction of the periodontal ligament. Am J Orthod Dentofacial Orthop 1998; 114:372-82. 22. Mostafa YA, Fayed MM, Mehanni S, ElBokle NN, Heider AM. Comparison of corticotomy-facilitated vs standard tooth-movement techniques in dogs with miniscrews as anchor units. Am J Orthod Dentofacial Orthop 2009;136:570-7. 23. Murphy KG, Wilcko MT, Wilcko WM, Ferguson DJ. Periodontal accelerated osteogenic orthodontics: a description of the surgical technique. J Oral Maxillofac Surg 2009;67:2160-6. 24. Wang L, Lee W, Lei DL, Liu YP, Yamashita DD, Yen SL. Tissue responses in corticotomy- and osteotomy-assisted tooth movements in rats: histology and immunostaining. Am J Orthod Dentofacial Orthop 2009;136:770.e1-11; discussion, 770-1. 25. Wilcko MT, Wilcko WM, Pulver JJ, Bissada NF, Bouquot JE. Accelerated osteogenic orthodontics technique: a 1-stage surgically facilitated rapid orthodontic technique with alveolar augmentation. J Oral Maxillofac Surg 2009;67:2149-59. 26. Wilcko WM, Wilcko T, Bouquot JE, Ferguson DJ. Rapid orthodontics with alveolar reshaping: two case reports of decrowding. Int J Periodontics Restorative Dent 2001;21:9-19. 27. Cohen G, Campbell PM, Rossouw PE, Buschang PH. Effects of increased surgical trauma on rates of tooth movement and apical root resorption in foxhound dogs. Orthod Craniofac Res 2010;13: 179-90. 28. Iseri H, Kisnisci R, Bzizi N, Tuz H. Rapid canine retraction and orthodontic treatment with dentoalveolar distraction osteogenesis. Am J Orthod Dentofacial Orthop 2005;127:533-41. 29. Kisnisci RS, Iseri H, Tuz HH, Altug AT. Dentoalveolar distraction osteogenesis for rapid orthodontic canine retraction. J Oral Maxillofac Surg 2002;60:389-94.
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30. Ai H, Xu QF, Lu HF, Mai ZH, An AQ, Liu GP. Rapid tooth movement through distraction osteogenesis of the periodontal ligament in dogs. Chin Med J (Engl) 2008;121:455-62. 31. Dibart S, Sebaoun JD, Surmenian J. Piezocision: a minimally invasive, periodontally accelerated orthodontic tooth movement procedure. Compend Contin Educ Dent 2009;30:342-4, 346, 348-50. 32. Kim SJ, Moon SU, Kang SG, Park YG. Effects of low-level laser therapy after corticision on tooth movement and paradental remodeling. Lasers Surg Med 2009;41:524-33. 33. Kim SJ, Park YG, Kang SG. Effects of corticision on paradental remodeling in orthodontic tooth movement. Angle Orthod 2009; 79:284-91. 34. Sebaoun JD, Kantarci A, Turner JW, Carvalho RS, Van Dyke TE, Ferguson DJ. Modeling of trabecular bone and lamina dura following selective alveolar decortication in rats. J Periodontol 2008;79:1679-88. 35. Nimeri G, Kau CH, Abou-Kheir NS, Corona R. Acceleration of tooth movement during orthodontic treatment—a frontier in orthodontics. Prog Orthod 2013;14:42. 36. Vaziri H. Effect of corticision on the rate of orthodontic tooth movement in rats [thesis]. Farmington, Conn: University of Connecticut; 2012. 37. Begg PR, Kesling PC. The differential force method of orthodontic treatment. Am J Orthod 1977;71:1-39. 38. Oppenheim A. Human tissue response to orthodontic intervention of short and long duration. Am J Orthod Oral Surg 1942;28: 263-301. 39. Reitan K. Some factors determining the evaluation of forces in orthodontics. Am J Orthod 1957;43:32-45. 40. Weiland F. External root resorptions and orthodontic forces: correlations and clinical consequences. Prog Orthod 2006;7:156-63. 41. Begg PR. Differential force in orthodontic treatment. Am J Orthod 1956;42:481-510. 42. Storey E, Smith R. Force in orthodontics and its relation to tooth movement. Aust J Dent 1952;56:11-8. 43. Andreasen G, Johnson P. Experimental findings on tooth movements under two conditions of applied force. Angle Orthod 1967;37:9-12. 44. Andreasen GF, Zwanziger D. A clinical evaluation of the differential force concept as applied to the edgewise bracket. Am J Orthod 1980;78:25-40. 45. Boester CH, Johnston LE. A clinical investigation of the concepts of differential and optimal force in canine retraction. Angle Orthod 1974;44:113-9. 46. Hixon EH, Aasen TO, Clark RA, Klosterman R, Miller SS, Odom WM. On force and tooth movement. Am J Orthod 1970;57:476-8. 47. Hixon EH, Atikian H, Callow GE, McDonald HW, Tacy RJ. Optimal force, differential force, and anchorage. Am J Orthod 1969;55: 437-57. 48. Van Leeuwen EJ, Kuijpers-Jagtman AM, Von den Hoff JW, Wagener FA, Maltha JC. Rate of orthodontic tooth movement after changing the force magnitude: an experimental study in beagle dogs. Orthod Craniofac Res 2010;13:238-45. 49. Gonzales C, Hotokezaka H, Yoshimatsu M, Yozgatian JH, Darendeliler MA, Yoshida N. Force magnitude and duration effects on amount of tooth movement and root resorption in the rat molar. Angle Orthod 2008;78:502-9. 50. von Bohl M, Maltha JC, Von Den Hoff JW, Kuijpers-Jagtman AM. Focal hyalinization during experimental tooth movement in beagle dogs. Am J Orthod Dentofacial Orthop 2004;125:615-23. 51. Verna C, Dalstra M, Melsen B. The rate and the type of orthodontic tooth movement is influenced by bone turnover in a rat model. Eur J Orthod 2000;22:343-52.
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Effect of corticision and different force magnitudes on orthodontic tooth movement in a rat model Christopher A. Murphy,a Taranpreet Chandhoke,b Zana Kalajzic,c Rita Flynn,d Achint Utreja,e Sunil Wadhwa,f Ravindra Nanda,g and Flavio Uribeh Madison and Farmington, Conn, and New York, NY
Introduction: The aims of this study were to evaluate the effect of 2 distinct magnitudes of applied force with and without corticision (flapless corticotomy) on the rate of tooth movement and to examine the alveolar response in a rat model. Methods: A total of 44 male rats (6 weeks old) were equally divided into 4 experimental groups based on force level and surgical intervention: light force, light force with corticision, heavy force, and heavy force with corticision. The forces were delivered from the maxillary left first molar to the maxillary incisors using prefabricated 10-g (light force) or 100-g (heavy force) nickel-titanium springs. The corticision procedure was performed at appliance placement and repeated 1 week later on the mesiopalatal aspect of the maxillary left first molars, with the right sides serving as the untreated controls. Microcomputed tomography was used to evaluate tooth movement between the maxillary first and second molars, and the alveolar response in the region of the maxillary first molar on day 14. Osteoclasts and odontoclasts were quantified, and the expression of receptor activator of nuclear factor kappa ß ligand was examined. Results: Intragroup comparisons of bone volume fraction (BVF) and tissue density were found to be significantly less on the loaded sides, with the exception of BVF in the light force group. Intergroup comparisons evaluating magnitude of tooth movement, BVF, apparent density, and tissue density showed no significant differences. Histomorphometric analysis indicated that BVF was decreased in the light force group. No significant differences in the total numbers of osteoclasts and odontoclasts and the expression of receptor activator of nuclear factor kappa ß ligand were found between the groups. Conclusions: No differences in tooth movement or alveolar response were observed with microcomputed tomography based on force level or corticision procedure. A flapless surgical insult in the mesiopalatal aspect of the first molar with a single-site corticision was unable to induce clinical or histologic changes after 2 weeks of orthodontic tooth movement regardless of the force magnitude. Histologic analysis of the furcation area showed that light force significantly decreased BVF. (Am J Orthod Dentofacial Orthop 2014;146:55-66)
A
lthough there are numerous benefits of orthodontic treatment, its prolonged duration is often seen as a drawback. The length of therapy is influenced by a number of factors, including the complexity of the malocclusion, the orthodontist's skill,
the patient's cooperation, and the rate of tooth movement. Extended treatment times have been associated with negative outcomes, such as increased risk for caries,1 periodontal disease,2,3 root resorption,4 and pulpal reactions.5 Reducing the duration of orthodontic
a
h Associate professor and program director, Division of Orthodontics, Department of Craniofacial Sciences; Charles Burstone professor, School of Dental Medicine, University of Connecticut, Farmington, Conn. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Supported by a Biomedical Research Award 2012 from the American Association of Orthodontists Foundation. Address correspondence to: Flavio Uribe, University of Connecticut Health Center, 263 Farmington Ave, Farmington, CT 06030; e-mail, [email protected]. Submitted, October 2013; revised and accepted, March 2014. 0889-5406/$36.00 Copyright Ó 2014 by the American Association of Orthodontists. http://dx.doi.org/10.1016/j.ajodo.2014.03.024
Private practice, Madison, Conn. Assistant professor, Division of Orthodontics, Department of Craniofacial Sciences, School of Dental Medicine, University of Connecticut, Farmington, Conn. c Research associate, Division of Orthodontics, Department of Craniofacial Sciences, School of Dental Medicine, University of Connecticut, Farmington, Conn. d Undergraduate dental student, School of Dental Medicine, University of Connecticut, Farmington, Conn. e Resident, Division of Orthodontics, Department of Craniofacial Sciences, School of Dental Medicine, University of Connecticut, Farmington, Conn. f Assistant professor, Division of Orthodontics, College of Dental Medicine, Columbia University, New York, NY. g Professor and head, Division of Orthodontics, Department of Craniofacial Sciences; alumni endowed chair, School of Dental Medicine, University of Connecticut, Farmington, Conn. b
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treatment has the benefit of possibly minimizing these unwanted side effects and improving patient satisfaction and acceptance. Orthodontic tooth movement is a dynamic process of bone modeling involving anabolic and catabolic responses to mechanical loading.6 The strains generated by orthodontic forces are transmitted to the periodontal ligament (PDL) and supporting alveolar bone, producing areas of tension and pressure within the PDL, with bone resorption occurring at sites of compression, and bone formation occurring in regions of tension.7 The velocity of tooth movement is regulated by bone turnover, bone density, and the degree of hyalinization of the PDL in response to the forces being applied. Continuous light forces are widely believed to be the most effective means of producing efficient tooth movement.8,9 Ideally, a method to increase tooth movement should be directed by frontal resorption (tightly coupled osteoclast-driven resorption on the compression side) and also cause minimal patient discomfort.7,10 Efforts to enhance the rate of orthodontic tooth movement have targeted these factors and can be categorized as either pharmacological or physical. Pharmacologic agents have been shown to influence orthodontic tooth movement by altering bone metabolism. Despite augmenting tooth movement, these treatments have had limited clinical use because of many negative local and systemic side effects such as hyperalgesia,11 bone loss and osteoporosis, delayed wound healing, and root resorption.12,13 As a result, research has shifted toward physical methods aimed at enhancing tooth movement. A number of physical methods to increase tooth movement have been examined previously. These have included the use of pulsed and static magnetic fields,14,15 electrical currents,16,17 lasers,18 and surgical manipulation of the alveolar bone.19 Surgical methods to enhance the rate of tooth movement have garnered considerable attention in recent years and include alveolar surgery to undermine interseptal bone,19 corticotomies,20-26 dentoalveolar distraction,27-29 dental distraction,21,30 and corticision.31-33 By enhancing the local catabolic and anabolic processes of bone turnover, these surgical methods might have the potential to increase the rate of orthodontic tooth movement and reduce treatment times.34,35 The clinical applications of these surgical interventions have been hampered by a number of factors, including duration of the effect and poor patient acceptance because of the invasiveness of these procedures. Kim et al32,33 introduced the corticision procedure in an effort to develop a minimally invasive approach to induce a regional acceleratory phenomenon effect
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without flap reflection that could be repeated with less patient discomfort. Unlike corticotomies, in which the surgical insult is obtained by reflecting a full flap to gain access to the cortical bone, with corticision, a reinforced scalpel is used as a thin chisel to separate the interproximal cortices transmucosally without reflecting a flap. These authors demonstrated that even minimally invasive insults to the alveolus with corticision can invoke a regional acceleratory phenomenon effect and stimulate orthodontic tooth movement. More evidence is needed that examines the biologic process involved to fully understand the mechanism by which orthodontic tooth movement can be modulated by these procedures. In addition, determining the effects of light and heavy forces on the overall rate of tooth movement is needed to better understand the optimal range required. The ideal force level for efficient tooth movement also requires further study. This study was designed to assess the rate of tooth movement and the biologic effects of corticision with 2 distinct force magnitudes on the remodeling of alveolar bone 14 days after the initiation of orthodontic tooth movement in a rat model. MATERIAL AND METHODS
A total of 44 male Wistar rats (weight, 150-250 g; Charles River Laboratories, Wilmington, Mass) were used in this study after approval by the Animal Care Committee of the University of Connecticut (number 2010-668). The final sample size was determined by a power analysis performed with data from a pilot study. Based on the initial pilot data, it was determined that 11 rats would be required in each group to provide statistical power (1-ß) of 0.8 and type I error of 0.05.36 The rats were randomly allocated to 1 of the 4 groups (11 per group) based on the surgical procedure and the application of light (10 g) or heavy (100 g) force: (1) no corticision and 10 g of force (LF), (2) no corticision and 100 g of force (HF), (3) corticision at appliance insertion and 1 week later with 10 g of force (LF1C), and (4) corticision at appliance insertion and 1 week later with 100 g of force (HF1C). The contralateral (right) side was used as the unloaded control for each animal. The rats were subjected to orthodontic forces from the maxillary left first molar to the central incisors (Fig 1, A). Closed-coil nickel-titanium springs delivering 10 or 100 g of force were used for the application of the light and heavy orthodontic forces, respectively. The force/deflection rate for the spring was determined to calibrate the amount of force produced by activation of the spring. The animals were placed under general anesthesia with xylazine (13 mg/kg) and ketamine (87 mg/kg).
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Fig 1. A, Appliance design indicating placement of the nickel-titanium coil springs from the maxillary left first molar to the central incisors. The arrow indicates the location and extent of the corticision procedure. B, Rat maxilla after dissection of soft tissues. Arrow indicates the location and extent of the corticision procedure on the bone.
Only the left side of the maxilla was treated. The contralateral (untreated) side served as the unloaded control for histologic and microcomputed tomography purposes, and to evaluate the physiologic distal drift of the molars. All animals were bonded by 1 investigator (C.A.M.) to eliminate interinvestigator bias. A 0.008-in stainless steel ligature was threaded through the contact between the maxillary left first and second molars. A light or heavy spring was then attached to the 0.008in stainless steel ligature around the first molar and securely ligated at the mesial surface of the maxillary first molar. Self-etching primer (Transbond Plus; 3M Unitek, Monrovia, Calif) was applied to the mesiopalatal surface of the maxillary first molar, and the ligature was bonded with light-cured dental adhesive resin cement (Transbond; 3M Unitek) using a commercial unit (LEDemetron 1; Kerr, Orange, Calif). To prevent the ligatures from dislodging because of the lingual curvature and eruption pattern of the maxillary incisors, grooves were prepared 0.5 mm from the gingival margin on the distal surfaces of the maxillary central incisors. A second 0.008-in stainless steel ligature was then placed around both maxillary incisors, and the spring was activated and attached to this ligature. After the ligature had been tied and cut, composite resin (Transbond XT Light Cure Adhesive Paste; 3M Unitek) was placed over the wire to prevent slipping and gingival irritation, as well as pulpal irritation to the exposed dentin. Finally, the mandibular incisors were reduced to prevent appliance breakage as described previously.14 The appliance was checked twice weekly to evaluate its integrity. One week after the initial placement of the appliance, the animals were reanesthetized and the springs reactivated. Corticision was applied at the time of orthodontic appliance placement and 1 week later in the corticision groups while the animals were under anesthesia. This protocol was selected based on the results of a previous study in which an orthodontic force with 2 corticision
procedures resulted in significantly more tooth movement than with a single or no corticision procedure.36 Corticision was performed on the mesiopalatal aspect of the maxillary left first molar (Fig 1, A). This location was selected to ensure clear access to the bone adjacent to the first molar, with enough safety margin to prevent injury to the roots of the teeth. The tip of a reinforced surgical blade (number 11; Bard-Parker, Franklin Lakes, NJ) capable of making a surgical incision with a minimum thickness of 400 mm was used. The blade was positioned on the mesiopalatal gingiva, 0.5 mm from the corresponding tooth surface at an inclination of 45 to 60 to the long axis of the maxillary first molar. The blade was inserted gradually through the overlying gingiva into the cortical bone (Figs 1, B, and 2). The corticisions were performed by 1 investigator (C.A.M.) after being calibrated with deceased rats. This investigator used tactile sense to confirm penetration of the palatal gingiva and bone. Microcomputed tomography analysis was performed after the experimental period (day 14) for all animals. Each rat was killed, and the maxilla was excised, cleansed of soft tissue, and hemisected. Analysis was performed by the microcomputed tomography facility at the University of Connecticut. Scanning was done at 55 kV and 145 mA, collecting 1000 projections per rotation with a 300-ms integration time. Three-dimensional images were constructed using standard convolution and back projection algorithms with Shepp and Logan filtering and rendered in a 12.3-mm field of view at a discrete density of 578,704 voxels per cubic millimeter (isometric 12-mm voxels). Microcomputed tomography images were used for quantitative analysis of bone changes in the region of the maxillary first molar. Tooth movement and alveolar bone parameters were evaluated. The amount of tooth movement was assessed on 2-dimensional sagittal sections taken through the centers of the maxillary first
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Fig 2. High-resolution microcomputed tomography images of the right (control) and the left (experimental) hemimaxillae showing the location and depth (0.4 mm) of the corticision immediately after the surgical procedure (right panel). Note the location of the corticision adjacent to the mesiopalatal root of the first molar (1M). B, Buccal side; P, palatal side; 1M, first molar.
and second molars (the image plane that showed the most structure of the distobuccal and mesial root) and measured at the interproximal heights of contour between these teeth (the distance between the most mesial point of the second molar crown and the most distal point of the first molar crown, first and second molar distance) (Fig 3). The initial separation distance at day 1 was 0 mm in all groups (ie, convex crown surfaces were touching). Changes in the alveolar bone were studied by analyzing the furcation area of the maxillary first molar. The region of interest for the alveolar bone analysis was defined vertically as the most occlusal point of the furcation to the apex of the maxillary roots; transversely, it was defined as the space between the buccal and lingual cortical bone; sagittally, it included 40 sections (12 mm) beginning at the mesial root and continuing distally (Fig 4, A and B). Parameters studied included bone volume fraction (BVF),
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apparent density, and tissue density. BVF, which represents the amount of alveolar bone in the region of interest, was calculated as the percentage of bone volume (BV) to total volume (TV), denoted as BV/TV. Apparent density was a calibrated measure of hydroxyapatite equivalent to the total volumetric mineral density of the trabecular bone (including the bone marrow) normalized to the region of interest (TV). With tissue density, the hydroxyapatite was calibrated to only represent the volumetric mineral density of trabecular bone tissue (BV) and excluding marrow and porosities, thereby closely approximating the amount of mineralized bone. To quantify the osteoclast activity and relate it to the bone density changes, histomorphometric analysis was performed using 6 animals from each experimental group. Each hemisected maxilla was placed in 10% formalin for 5 days at 4 C with constant agitation. After fixation, the samples were decalcified in 14% EDTA for
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Fig 3. Representative microcomputed tomography image indicating the measurement of tooth movement between the first and second molars. A reference line was drawn between the points of greatest convexity between the 2 interproximal surfaces.
4 weeks and processed for standard paraffin embedding. Serial 5-mm sagittal sections of the hemimaxillae were obtained and stained with routine hematoxylin and eosin stains and tartrate-resistant acid phosphatase (TRAP) activity using an acid phosphatase leukocyte kit (Sigma Chemical, St Louis, Mo) according to the manufacturer's instructions. Three sections showing the most pulp structure of the distobuccal root (midroot sections) were used for the analysis (Fig 5, A). Active osteoclasts were identified as TRAP-positive, multinucleated cells (.2 nuclei) that were touching the bone surface. The exact area for osteoclast quantification included a rectangular box (450 3 450 mm) that was placed on compression side of the alveolar bone with the highest osteoclast activity (Fig 6, C). BVF was defined as the percentage of BV to TV. To quantify the level of osteoclastic activity, the osteoclast number was then standardized to the BVF. The osteoclast surface was defined as the total surface of active osteoclasts divided by total bone surface in a defined box and indicated as a percentage. Odontoclasts were identified as TRAP-positive multinucleated cells (.2 nuclei) on the dentin surface and were quantified on the mesial surface of the distobuccal root in the line starting from the bifurcation to the end of the apex of the distobuccal root (Fig 5, C). The odontoclast surface was calculated as the total surface of all odontoclasts divided by the total dentin surface in the defined area. Mean values for these parameters were calculated from 3 adjacent sections (midroot) for each experimental animal; these were then used for statistical tests.
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Histomorphometric analyses were carried out using Osteomeasure software (Osteometrics, Decatur, Ga). Immunohistologic analyses for receptor activator of nuclear factor kappa b ligand (RANKL) were performed on all experimental groups. RANKL is an osteoblast and osteocyte-derived factor that is essential for the differentiation, activation, and survival of osteoclasts and used as an indicator of osteoclastic activity. Tissue sections were deparaffinized with xylene and rehydrated with decreasing concentrations of ethanol. After rehydration in deionized water, the tissues were incubated in 1X citrate buffer (pH 6.0) at 60 C overnight to unmask the specific antigen. The next day, the tissues were washed in phosphate-buffered saline (PBS) and blocked with 10% normal goat serum in 1% bovine serum albumin for 2 hours. Incubation with the primary antibody was performed at 4 C overnight using rabbit polyclonal anti-RANKL antibody at a concentration of 1:200 in 1% bovine serum albumin (LS-B1425/46594; LifeSpan BioSciences, Seattle, Wash). The next day, the tissues were washed in PBS and incubated with Alexa Fluor 594 goat antirabbit secondary antibody (A11037; LifeTechnologies, Carlsbad, Calif) in 2% normal goat serum and 1% bovine serum albumin at a concentration of 1:200 for 60 minutes. The sections were counterstained with 40 ,6-diamidino-2-phenylindole (DAPI) to obtain a total cell number and mounted with 50% glycerol in PBS. The signal was visualized and photographed by fluorescence microscopy using fluorescein isothiocyanate (FITC) and DAPI filter cubes of the Axiovert 200 microscope (Carol Zeiss Microscopy, Jena, Germany). For quantification, 3 sagittal molar sections from 6 different experimental animals were analyzed. Ten-times magnified images of the compression area (mesial surface of distobuccal root) of alveolar bone were used to evaluate the area that included RANKL labeling. RANKL labeling (TRITC-red) was quantified using ImageJ software (National Institutes of Health, Bethesda, Md) and calculated as a percentage per total area in each magnified image. The values from 3 sections were then averaged for each rat, and the means from 6 animals in each experimental group were used to conduct statistical tests. Statistical analysis
Statistical analyses were performed using GraphPad Prism (GraphPad Software, La Jolla, Calif) with analysis of means and standard deviations for each study parameter. Intergroup comparisons for tooth movement, bone volume parameters by microcomputed tomography and histomorphometry, and RANKL expression were performed with 1-way analysis of variance (ANOVA). Considering multiple pairwise comparisons used across the 4 groups, Bonferroni post-hoc tests were performed to
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Fig 4. Region of interest for microcomputed tomography analysis of BVF, tissue density, and apparent density on day 14 from A, axial and B, coronal views. The region of interest highlighted in green. Measurements were made approximating the first molar region (molar roots denoted by: M, Mesial; MP, mesiopalatal; MB, mesiobuccal; DP, distopalatal; DB, distobuccal). Intragroup comparisons of C, BVF; D, tissue density; and E, apparent density on day 14 by microcomputed tomography between the loaded and unloaded sides. *P \0.05 denotes statistically significant differences by paired t test analysis of the loaded and treated sides vs the unloaded and untreated sides (n 5 11).
minimize the risk of type I errors. Intragroup comparisons of microcomputed tomography measures of bone density changes comparing the treated with the untreated control sides were performed by paired sample t tests. Significance was accorded at P \0.05. A total of 11 rats were used in each study group, and all were examined for tooth movement and bone volume assessments. RESULTS
The experimental phase for each study group was 14 days, and all data were reported as means and standard deviations for each parameter. To calculate the differences in the amount of tooth movement between the groups at the end of the experimental phase, maxillary molar mesialization was evaluated by measuring the distance between the distal height of contour of the maxillary first molar and the mesial height of contour of the maxillary second molar on microcomputed tomography images (Fig 3). Microcomputed tomography analysis
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performed on the hemimaxillae of the animals receiving a light force (10 g) without corticision for 14 days showed that the mean amounts of maxillary first molar mesialization were 0.627 6 0.271 mm on the loaded side and 0.150 6 0.224 mm on the unloaded side. The mean amounts of maxillary first molar mesialization in the animals receiving light force (10 g) plus corticision were 0.602 6 0.251 mm on the loaded side and 0.072 6 0.102 mm on the unloaded side. When the heavy force (100 g) group without corticision was studied using microcomputed tomography, the mean amounts of maxillary first molar mesialization were 0.673 6 0.334 mm on the loaded side and 0.060 6 0.173 mm on the unloaded side. In the heavy force (100 g) group plus corticision, the mean amounts of maxillary first molar mesialization were 0.6631 6 0.2553 mm on the loaded side and 0.029 6 0.054 mm on the unloaded side. There were no significant differences in the amounts of tooth
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Fig 5. A, Representative section indicating the field of view and the region of interest (black box) for the histomorphometric measurements (5-times magnification). B, Comparison of intergroup BVF on the compression side on day 14 by histomorphometry. ANOVA comparisons of the light (10 g) and heavy (100 g) force groups with and without corticision. Significant differences between groups are noted by *P \0.05 (n 5 6).
movement observed at day 14 between any groups (P 5 0.9354). To evaluate the effects of the differential forces with and without corticision on bone remodeling, microcomputed tomography images of the maxillary first molars were obtained for analysis (Fig 4, A and B). In each experimental group, side-by-side comparisons were performed to evaluate differences between the loaded and unloaded sides using paired t tests. The LF1C, HF, and HF1C groups each demonstrated a statistically significant reduction in BVF on the treated side when compared with the contralateral control side (P \0.05) (Fig 4, C). Side-by-side comparisons of apparent density and tissue density indicated a statistically significant
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decrease in both parameters for all 4 study groups on the treated side compared with the control side (P \0.05) (Fig 4, D and E). Intergroup comparisons of bone parameters from microcomputed tomography images on the treated sides indicated no statistically significant difference for BVF, apparent density, or tissue density. Histomorphometry was used to examine localized bone remodeling changes on the compression sides in all groups (Fig 5, A). Intergroup comparisons of BVF (%) indicated that the LF group (21.25 6 8.916) had significantly less BVF compared with the other groups (LF1C, 57.65 6 14.93; HF, 57.09 6 16.74; HF1C, 60.46 6 14.08) (P \0.001) (Fig 5, B). To investigate osteoclast activity, osteoclasts were counted, and the osteoclast surface area was measured histologically for each group (Fig 6). For osteoclast number normalized to BVF, intergroup comparisons indicated no statistically significant differences between the groups: LF, 0.3393 6 0.308; LF1C, 0.2238 6 0.1515; HF, 0.1671 6 0.1268; and HF1C, 0.1036 6 0.0716 (P 5 0.2437). Osteoclast surface measurements were not significantly different among the 4 groups: LF, 7.913 mm 6 5.267; LF1C, 7.787 mm 6 3.59; HF, 6.179 mm 6 4.663; and HF1C, 5.032 mm 6 3.899 (P 5 0.684). To evaluate odontoclastic activity, odontoclasts were counted along the entire mesial surface of the distal root of the maxillary left first molar. The odontoclast numbers were not significantly different by intergroup comparisons: LF, 5.044 6 3.376; LF1C, 2.267 6 3.443; HF, 3.472 6 3.116; and HF1C, 4.767 6 3.099 (P 5 0.4925). Odontoclast surface areas were also not significant between the groups: LF, 0.09691% 6 0.06517%; LF1C, 0.0414% 6 0.05317%; HF, 0.07205% 6 0.06672%; and HF1C, 0.1034% 6 0.06674% (P 5 0.3992). To study the effect of corticision and force magnitude on osteoclast and odontoclast differentiation, the activation of RANKL was evaluated (Fig 7). RANKL expression is seen in osteocytes, osteoblasts, some fibroblastic cells in the PDL, and many bone marrow cells. The quantification of RANKL-positive signal showed a trend of greatest expression in the LF group (11.08 6 10.75). In the LF1C group, the mean values were 4.65 6 10.09; in HF group, the values were 1.06 6 1.76; and in HF1C group, the values were 1.19 6 2.54. When the groups were compared using ANOVA, the differences among the groups were not significant (P 5 0.0875). Hematoxylin and eosin staining for architecture consistently indicated increased fibrous tissues and less alveolar bone in the region of interest of the LF group compared with the other 3 groups.
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Fig 6. TRAP-stained sections among the study groups. Arrows point to TRAP-positive cells lying on alveolar bone (osteoclasts) and dentin (odontoclasts) (10-times magnification). A.B., Alveolar bone; D, dentin. DISCUSSION
Multiple methods have been used to enhance orthodontic tooth movement. Physical efforts to enhance the rate of tooth movement have classically focused on titration of the optimal force magnitude and determining the ideal duration of force application to efficiently move teeth. To promote the maximum rate of physiologic
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tooth movement, the classically held theory for the optimal force level was for it to be as light as possible and distributed evenly along the root's surface to minimize hyalinization, undermining resorption, and irreversible root resorption.37-40 This brought forth work by Begg and Kesling39 and Begg41 and the differential force theory, in which light forces are used for effective tooth movement, and heavy forces are used to anchor
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Fig 7. RANKL expression on the compression side in each study group. Fluorescence imaging of the region of interest for RANKL. RANKL expression was detected by TRITC filter (first row). Total background cells detected by DAPI (second row). Merged TRITC and DAPI images (third row) with arrows indicating double-labeled, RANKL-positive cells. Note the high RANKL expression in the LF group. Negative control for RANKL (right-most column) indicated DAPI-positive staining in the absence of RANKL antibody. T, Tooth; D, dentin; A.B., alveolar bone; H&E, hematoxylin and eosin.
segments to prevent movement. Storey and Smith42 also reported a threshold for the optimal force levels, with forces higher than this threshold resulting in cessation of tooth movement. However, these findings were not reproduced, and the controversy as to the ideal force level continued.43-47 More recent studies have revisited these concepts in animal models. Van Leeuwen et al48 showed a dose-dependent increase in tooth movement in beagles when low forces were applied at early stages and then increased to heavier forces. In a study by Gonzales et al,49 lighter forces (10-50 g) resulted in more tooth movement in rats than did heavier forces (100 g), specifically at later time points (days 14 and 28). Individual variations and biologic responses can also contribute to differences in the rate of tooth movement. In a study of light force application (25 cN) in beagles over an 80-day period by von Bohl et al,50 there were variations in the rate of tooth movement among the animals observed despite use of a consistent, light, and constant force. The authors attributed this variability to a higher degree of hyalinization in animals with slower rates of tooth movement. Understanding
the biologic response to orthodontic forces as well as the range of optimal force values requires further study. From a biologic perspective, the rate of tooth movement might be ultimately dictated by the capacity of the alveolar bone to undergo remodeling. Based on these principles, more recently developed surgical techniques could accentuate this bone remodeling process, thereby resulting in accelerated tooth movement and reduced treatment times. In 2001, Wilcko et al26 suggested that the increased rate of orthodontic tooth movement observed after surgical manipulation of the alveolus was the result of a regional acceleratory phenomenon. Subsequent research has confirmed that the acceleration of tooth movement associated with surgical intervention is the result of increased localized bone turnover based on a regional acceleratory phenomenon20,34 and is in proportion to the severity of the insult.27 In an effort to develop a minimally invasive, repeatable method of inducing a regional acceleratory phenomenon effect with minimal patient discomfort, Kim et al33 introduced corticision and found it to be an efficient means of stimulating tooth movement by inducing a regional
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acceleratory phenomenon and accelerating bone remodeling. Thus, we surmised that the targeted application of corticision coupled with the use of sufficient forces could promote accelerated tooth movement. The purpose of this study was to assess the effect of corticision and 2 distinct force levels (10 and 100 g) on the amount of orthodontic tooth movement and changes in the alveolus in a rat model after 14 days. An outbred rat strain was used; this introduced a degree of genetic variability that mimics patient-to-patient variations. To evaluate the effect of heavy (100 g) and light (10 g) forces with or without corticision on orthodontic tooth movement, microcomputed tomography measurements were taken between the maxillary first and second molars of the rats in each group. The measurements made on day 14 at the end of the experimental period were not significantly different. Alveolar changes were studied using both microcomputed tomography analysis and histomorphometry. Microcomputed tomography analysis was used to study the effects of a high or a low force on the alveolus with or without corticision at the furcation of the maxillary first molars. Significant differences existed between the experimental and control sides for all groups with respect to apparent density and tissue density, with all experimental sides showing reductions in density overall. BVF also demonstrated a significant difference between the experimental and control sides for all groups, with the exception of the LF group (Fig 4, C). Again, the experimental sides had decreased values compared with their contralateral controls. These intragroup findings reflected the bony remodeling occurring at the alveolus during orthodontic tooth movement.7,51 When intergroup comparisons were made, no significant differences were found with respect to any of the parameters studied, indicating no differences in the amount of alveolar change at the furcation among the groups. This supports the lack of a significant difference in the amount of tooth movement observed among the groups. Histologic sections were also used to evaluate changes occurring at the furcation area of the maxillary left first molars. BVF was significantly less in the LF group compared with the other groups. Sections from the LF group showed more fibrous tissue, indicating possibly greater resorption of bone in this group on the compression side compared with the other groups. This finding was different from what was observed using microcomputed tomography, which did not indicate a significant difference in any alveolar bone parameter between the groups. This discrepancy might reflect that the region of interest evaluated by microcomputed tomography was larger and extended farther buccolingually, thereby making small changes less detectable and underestimating the changes observed histologically
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along the distobuccal root. In future studies, the region of interest will be modified to include a similar region as was analyzed by histomorphometry. To evaluate the osteoclast activity, the total number of osteoclasts was normalized to the amount of mineralized bone, and the number of active osteoclasts was divided by the BVF. The osteoclast numbers were slightly elevated in the LF group; this was consistent with the low bone density observed by histomorphometry in this group. However, statistical analysis showed no significant differences among the groups. A similar trend was observed with osteoclast surfaces in the LF group. Taken together, these data suggest that the low force could have caused greater osteoclast recruitment to the area of alveolar bone at an earlier time that resulted in greater bone resorption. Although not significant, immunohistochemistry data showed that higher proportions of cells were labeled with RANKL when a low force was applied. However, many fibroblastic cells express RANKL, and a large area of fibrous tissue was consistently present in the region of interest in the LF group. It is possible that higher RANKL labeling reflects fibrosis as a result of the overall lack of bone in the compression area. This reduction in bone density in the LF group did not translate to greater tooth movement, thereby suggesting that earlier time points should be evaluated to determine whether osteoclastic activity was elevated sooner in the experimental phase. Based on the results in this study, it is possible that changes in osteoclast and odontoclast numbers as well as the elevation in RANKL expression might have occurred earlier in the experimental period; this would be consistent with a short-lived regional acceleratory phenomenon reported by other investigators.20,21,33,34 Interestingly, despite reduced alveolar bone and a trend of increased osteoclastic activity and RANKL expression, the LF1C group did not show similar histologic findings. It is possible that corticision modulates the normal physiologic processes; therefore, examining earlier time points will provide additional information as to the acute effect of this procedure on the PDL, bone, and supportive cells. With no significant changes in most of the bone and cellular parameters as well as the amount of tooth movement at day 14, further studies are needed to examine earlier time points, soon after the corticision and the force application. Baloul et al20 demonstrated that over a 6-week time course after selective alveolar decortication in rats, tooth movement was significantly enhanced only during the first week when compared with a tooth movement only group. Furthermore, Kim et al32 observed that after application of corticision, most tooth movement occurs during the first 2 weeks.
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In our study, during the experimental phase (at days 4, 7, 11, and 14), tooth movement was measured in all groups using feeler gauges (data not shown). Significant differences were seen early on at day 4, with the HF and HF1C groups showing more tooth movement than the LF groups. In addition, at day 7, the HF1C group continued to show significantly greater tooth movement compared with the other groups. However, consistent with the microcomputed tomography measurements, no group had a difference in tooth movement by the feeler gauge measurements at day 14. Feeler gauge measurements were found to overestimate the amount of tooth movement when compared with the microcomputed tomography measurements at day 14 (data not shown), although they had a similar trend. Ongoing studies will examine bone volume changes, histomorphometry (including osteoclast activity), and expression of key factors including RANKL at these earlier stages in this experimental model. There are additional areas that could improve this study, including the application of the corticision procedure. In this study, corticision was applied with a reinforced scalpel blade on days 1 and 7 on the mesiopalatal aspect of the maxillary left first molar. Every effort to standardize the corticision procedure was used. Here, corticision was applied on the mesiopalatal gingiva, 0.5 mm from the corresponding tooth surface at an inclination of 45 to 60 to the long axis of the maxillary first molar, with the blade inserted gradually through the overlying gingiva, penetrating into the cortical bone. A further improvement on this method in the future would be to use a surgical guide to standardize the application and a blade that would limit or indicate the depth of the incision being made. In an effort to use a minimally invasive surgical procedure, the corticision performed in this study was highly localized and minor; this might have resulted in a lack of significance in many of the parameters observed. In contrast, Kim et al32,33 performed corticision on the mesiobuccal, distobuccal, and distopalatal aspects of feline maxillary canines and on the mesiobuccal, distobuccal, mesiopalatal, and distopalatal aspects of canine maxillary second premolars and found significant differences in both tooth movement and alveolar remodeling. Thus, increasing the number of sites where corticisions are performed might also result in an enhanced tissue response and possibly increase the magnitude of tooth movement. Finally, a combination of the parameters tested in this study might help to accelerate tooth movement. For example, an initial light force followed by a corticision plus a heavy force after 1 week could enhance the rate of tooth movement. Since the bone volume is reduced and more fibrous tissue is present in response
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to a light force, a heavy force and corticision after the initial remodeling process might be able to displace the tooth through a less resistant alveolar bone. Further studies are required to examine the changes in bone remodeling, osteoclast numbers, and the expression of osteoclastogenic factors at earlier times after force application and corticision. A more significant alveolar injury could be required to enhance the rate of tooth movement than a corticision at 1 location. CONCLUSIONS
At day 14, there were no significant differences in tooth movement, microcomputed tomography bone parameters, or numbers of osteoclasts or odontoclasts related to the magnitude of the force or the addition of corticision. Light force caused a significant decrease in bone volume in the compression side observed histologically. ACKNOWLEDGMENTS
We would like to thank Ms. Renata Rydzik for her analysis of the microcomputed tomography images and Mr. Mike Brault from Ultimate Wire Forms for providing the nickel-titanium coil springs. REFERENCES 1. Richter AE, Arruda AO, Peters MC, Sohn W. Incidence of caries lesions among patients treated with comprehensive orthodontics. Am J Orthod Dentofacial Orthop 2011;139:657-64. 2. Geiger AM. Mucogingival problems and the movement of mandibular incisors: a clinical review. Am J Orthod 1980;78:511-27. 3. Alexander SA. Effects of orthodontic attachments on the gingival health of permanent second molars. Am J Orthod Dentofacial Orthop 1991;100:337-40. 4. Weltman B, Vig KW, Fields HW, Shanker S, Kaizar EE. Root resorption associated with orthodontic tooth movement: a systematic review. Am J Orthod Dentofacial Orthop 2010;137:462-76. 5. Grunheid T, Morbach BA, Zentner A. Pulpal cellular reactions to experimental tooth movement in rats. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;104:434-41. 6. Roberts WE, Huja S, Roberts JA. Bone modeling: biomechanics, molecular mechanisms, and clinical perspectives. Semin Orthod 2004;10:123-61. 7. Krishnan V, Davidovitch Z. Cellular, molecular, and tissue-level reactions to orthodontic force. Am J Orthod Dentofacial Orthop 2006;129:469.e1-32. 8. Iwasaki LR, Haack JE, Nickel JC, Morton J. Human tooth movement in response to continuous stress of low magnitude. Am J Orthod Dentofacial Orthop 2000;117:175-83. 9. Daskalogiannakis J, McLachlan KR. Canine retraction with rare earth magnets: an investigation into the validity of the constant force hypothesis. Am J Orthod Dentofacial Orthop 1996;109:489-95. 10. Norton LA, Burstone C. The biology of tooth movement. Boca Raton, Fla: CRC Press; 1989. 11. Yamaguchi M, Kasai K. Inflammation in periodontal tissues in response to mechanical forces. Arch Immunol Ther Exp (Warsz) 2005;53:388-98.
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12. Sekhavat AR, Mousavizadeh K, Pakshir HR, Aslani FS. Effect of misoprostol, a prostaglandin E1 analog, on orthodontic tooth movement in rats. Am J Orthod Dentofacial Orthop 2002;122: 542-7. 13. Krishnan V. Critical issues concerning root resorption: a contemporary review. World J Orthod 2005;6:30-40. 14. Darendeliler MA, Sinclair PM, Kusy RP. The effects of samariumcobalt magnets and pulsed electromagnetic fields on tooth movement. Am J Orthod Dentofacial Orthop 1995;107:578-88. 15. Stark TM, Sinclair PM. Effect of pulsed electromagnetic fields on orthodontic tooth movement. Am J Orthod Dentofacial Orthop 1987;91:91-104. 16. Davidovitch Z, Finkelson MD, Steigman S, Shanfeld JL, Montgomery PC, Korostoff E. Electric currents, bone remodeling, and orthodontic tooth movement. II. Increase in rate of tooth movement and periodontal cyclic nucleotide levels by combined force and electric current. Am J Orthod 1980;77:33-47. 17. Davidovitch Z, Finkelson MD, Steigman S, Shanfeld JL, Montgomery PC, Korostoff E. Electric currents, bone remodeling, and orthodontic tooth movement. I. The effect of electric currents on periodontal cyclic nucleotides. Am J Orthod 1980;77:14-32. 18. Kawasaki K, Shimizu N. Effects of low-energy laser irradiation on bone remodeling during experimental tooth movement in rats. Lasers Surg Med 2000;26:282-91. 19. Ren A, Lv T, Kang N, Zhao B, Chen Y, Bai D. Rapid orthodontic tooth movement aided by alveolar surgery in beagles. Am J Orthod Dentofacial Orthop 2007;131:160.e1-10. 20. Baloul SS, Gerstenfeld LC, Morgan EF, Carvalho RS, Van Dyke TE, Kantarci A. Mechanism of action and morphologic changes in the alveolar bone in response to selective alveolar decorticationfacilitated tooth movement. Am J Orthod Dentofacial Orthop 2011;139(4 Suppl):S83-101. 21. Liou EJ, Huang CS. Rapid canine retraction through distraction of the periodontal ligament. Am J Orthod Dentofacial Orthop 1998; 114:372-82. 22. Mostafa YA, Fayed MM, Mehanni S, ElBokle NN, Heider AM. Comparison of corticotomy-facilitated vs standard tooth-movement techniques in dogs with miniscrews as anchor units. Am J Orthod Dentofacial Orthop 2009;136:570-7. 23. Murphy KG, Wilcko MT, Wilcko WM, Ferguson DJ. Periodontal accelerated osteogenic orthodontics: a description of the surgical technique. J Oral Maxillofac Surg 2009;67:2160-6. 24. Wang L, Lee W, Lei DL, Liu YP, Yamashita DD, Yen SL. Tissue responses in corticotomy- and osteotomy-assisted tooth movements in rats: histology and immunostaining. Am J Orthod Dentofacial Orthop 2009;136:770.e1-11; discussion, 770-1. 25. Wilcko MT, Wilcko WM, Pulver JJ, Bissada NF, Bouquot JE. Accelerated osteogenic orthodontics technique: a 1-stage surgically facilitated rapid orthodontic technique with alveolar augmentation. J Oral Maxillofac Surg 2009;67:2149-59. 26. Wilcko WM, Wilcko T, Bouquot JE, Ferguson DJ. Rapid orthodontics with alveolar reshaping: two case reports of decrowding. Int J Periodontics Restorative Dent 2001;21:9-19. 27. Cohen G, Campbell PM, Rossouw PE, Buschang PH. Effects of increased surgical trauma on rates of tooth movement and apical root resorption in foxhound dogs. Orthod Craniofac Res 2010;13: 179-90. 28. Iseri H, Kisnisci R, Bzizi N, Tuz H. Rapid canine retraction and orthodontic treatment with dentoalveolar distraction osteogenesis. Am J Orthod Dentofacial Orthop 2005;127:533-41. 29. Kisnisci RS, Iseri H, Tuz HH, Altug AT. Dentoalveolar distraction osteogenesis for rapid orthodontic canine retraction. J Oral Maxillofac Surg 2002;60:389-94.
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30. Ai H, Xu QF, Lu HF, Mai ZH, An AQ, Liu GP. Rapid tooth movement through distraction osteogenesis of the periodontal ligament in dogs. Chin Med J (Engl) 2008;121:455-62. 31. Dibart S, Sebaoun JD, Surmenian J. Piezocision: a minimally invasive, periodontally accelerated orthodontic tooth movement procedure. Compend Contin Educ Dent 2009;30:342-4, 346, 348-50. 32. Kim SJ, Moon SU, Kang SG, Park YG. Effects of low-level laser therapy after corticision on tooth movement and paradental remodeling. Lasers Surg Med 2009;41:524-33. 33. Kim SJ, Park YG, Kang SG. Effects of corticision on paradental remodeling in orthodontic tooth movement. Angle Orthod 2009; 79:284-91. 34. Sebaoun JD, Kantarci A, Turner JW, Carvalho RS, Van Dyke TE, Ferguson DJ. Modeling of trabecular bone and lamina dura following selective alveolar decortication in rats. J Periodontol 2008;79:1679-88. 35. Nimeri G, Kau CH, Abou-Kheir NS, Corona R. Acceleration of tooth movement during orthodontic treatment—a frontier in orthodontics. Prog Orthod 2013;14:42. 36. Vaziri H. Effect of corticision on the rate of orthodontic tooth movement in rats [thesis]. Farmington, Conn: University of Connecticut; 2012. 37. Begg PR, Kesling PC. The differential force method of orthodontic treatment. Am J Orthod 1977;71:1-39. 38. Oppenheim A. Human tissue response to orthodontic intervention of short and long duration. Am J Orthod Oral Surg 1942;28: 263-301. 39. Reitan K. Some factors determining the evaluation of forces in orthodontics. Am J Orthod 1957;43:32-45. 40. Weiland F. External root resorptions and orthodontic forces: correlations and clinical consequences. Prog Orthod 2006;7:156-63. 41. Begg PR. Differential force in orthodontic treatment. Am J Orthod 1956;42:481-510. 42. Storey E, Smith R. Force in orthodontics and its relation to tooth movement. Aust J Dent 1952;56:11-8. 43. Andreasen G, Johnson P. Experimental findings on tooth movements under two conditions of applied force. Angle Orthod 1967;37:9-12. 44. Andreasen GF, Zwanziger D. A clinical evaluation of the differential force concept as applied to the edgewise bracket. Am J Orthod 1980;78:25-40. 45. Boester CH, Johnston LE. A clinical investigation of the concepts of differential and optimal force in canine retraction. Angle Orthod 1974;44:113-9. 46. Hixon EH, Aasen TO, Clark RA, Klosterman R, Miller SS, Odom WM. On force and tooth movement. Am J Orthod 1970;57:476-8. 47. Hixon EH, Atikian H, Callow GE, McDonald HW, Tacy RJ. Optimal force, differential force, and anchorage. Am J Orthod 1969;55: 437-57. 48. Van Leeuwen EJ, Kuijpers-Jagtman AM, Von den Hoff JW, Wagener FA, Maltha JC. Rate of orthodontic tooth movement after changing the force magnitude: an experimental study in beagle dogs. Orthod Craniofac Res 2010;13:238-45. 49. Gonzales C, Hotokezaka H, Yoshimatsu M, Yozgatian JH, Darendeliler MA, Yoshida N. Force magnitude and duration effects on amount of tooth movement and root resorption in the rat molar. Angle Orthod 2008;78:502-9. 50. von Bohl M, Maltha JC, Von Den Hoff JW, Kuijpers-Jagtman AM. Focal hyalinization during experimental tooth movement in beagle dogs. Am J Orthod Dentofacial Orthop 2004;125:615-23. 51. Verna C, Dalstra M, Melsen B. The rate and the type of orthodontic tooth movement is influenced by bone turnover in a rat model. Eur J Orthod 2000;22:343-52.
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