INTRODUCTION

Application of a mechanical force causes tooth movement because of remodeling changes in the paradental tissues. Recent cellular, molecular, and tissue-level studies1 on the biologic mechanism of tooth movement suggest that a mechanical force is not the only stimulus for inducing tooth movement. Although clinical orthodontic systems generally use mechanical forces to induce bone remodeling, the use of pharmaceutical,2–3 electromagnetic,4–5 laser,6 and surgical stimuli in combination with the mechanical force for accelerating orthodontic tooth movement has attracted considerable scientific interest.

A common feature of these various stimuli is that their biologic mechanism is based on the regional acceleratory phenomenon (RAP). In 1983, Frost7 demonstrated that regional noxious stimuli of sufficient magnitude can result in markedly accelerated reorganizing activity in the osseous and soft tissues; he termed this cascade of physiologic healing processes as the RAP. This phenomenon is characterized by a burst of the localized remodeling process, which accelerates healing, particularly following the surgical wounding of cortical bone.

Surgical injury is a potentiating factor for the induction of RAP. The use of supplemental dentoalveolar surgeries to accelerate tooth movement has been recommended. For rapid canine retraction, Liou and Huang8 proposed periodontal ligament distraction, and Iseri et al9 reported dentoalveolar distraction in accordance with the principles of distraction osteogenesis. Selective alveolar decortication by Wilcko et al.10 invoked a RAP, leading to a transient osteoporotic condition. These modified surgical techniques were reported to be effective in reducing clinical orthodontic treatment time. However, the actual drawback was little acceptance by patients due to the aggressive nature of these procedures, increasing postoperative discomfort, and the risk of complications.

“Corticision” was introduced as a supplemental dentoalveolar surgery in orthodontic therapy to achieve accelerated tooth movement with minimal surgical intervention. In this technique, a reinforced scalpel is used as a thin chisel to separate the interproximal cortices transmucosally without reflecting a flap. Because Corticision has the clinical value of accelerating tooth movement, it is regarded as a convenient procedure for both patients and orthodontists. The purpose of this study was to elucidate the biologic effects of Corticision on alveolar remodeling in orthodontic tooth movement in cats.

MATERIALS AND METHODS

In this study, 16 domestic male cats weighing 2.8– 3.5 kg were used. The cats were divided into three groups, designated as groups A, B, and C. Thirty-two canine teeth were included in the experiments. The treatment protocol for each group was as follows:

1. Group A: Only orthodontic force (control)

2. Group B: Orthodontic force plus Corticision

3. Group C: Orthodontic force plus Corticision and periodic mobilization

In all experimental animals, the group B and C treatment protocols were applied to the left and right maxillary canines, respectively. The control animals were individually separated from the experimental ones to rule out the possibility of systemic acceleratory phenomenon (SAP) following surgical injury. These three groups were further divided into four subgroups according to the duration of force application: group I, 7 days; group II, 14 days; group III, 21 days; and group IV, 28 days. The cats in group IV were intramuscularly injected with oxytetracycline hydrochloride (Fluka, China; yellow orange; 30 mg/kg), calcein (Fluka, Switzerland; green; 10 mg/kg), and alizarin red (Fluka, UK; red; 30 mg/kg) to label the newly formed mineralized bone for quantitative analysis. The injection schedule is summarized in Table 1.

Table 1.  Administration Schedule of Fluoresceins in Group IV

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The maxillary second and third premolars on both sides of all animals were connected with flowable composite resin (3M Unitek, Monrovia, Calif) that was extended onto the buccal surfaces to reinforce anchorage. Single buccal tubes (MBT, 3M Unitek) were bonded to the buccal surface of third premolars with Transbond (3M Unitek). Canine brackets (MBT, 3M Unitek) were bonded to the maxillary canines, and a 0.016 × 0.022-inch stainless steel sectional wire (RMO, Denver, Colo) was passively inserted from the canine brackets to the buccal tubes. The canines were retracted using 0.010 × 0.030-inch precalibrated closed Sentalloy coil springs (Ormco Co, Orange, Calif) (Figure 1B). The orthodontic force exerted by the appliance was 100 g at the beginning of the experiment. The magnitude of force was checked every week and was reactivated if required.

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After local anesthesia, Corticision was performed on the mesiobuccal, distobuccal, and distopalatal aspects of both maxillary canines in the experimental groups (Figure 1A). The mesiopalatal aspect was excluded due to the extremely thin palatal bone with a suture line, which had been confirmed in the cat skull. A reinforced surgical blade (No. 15T, Paragon, Sheffield, UK) capable of making a surgical incision with a minimum thickness of 400 μm was employed. The blade was positioned on the interradicular attached gingiva at an inclination of 45°–60° to the long axis of the canine and was inserted gradually into the bone marrow by malleting the blade holder penetrating the overlying gingiva, cortical bone, and cancellous bone. The surgical injury was left 2 mm from the papillary gingival margin in order to preserve the alveolar crest and was extended 1 mm beyond the mucogingival junction because of the presence of a narrow attached gingiva in cats. The blade was pulled out by a swing motion.

Mobilization was performed only on the right maxillary canines (group C) using a pincet immediately following Corticision and was repeated every 3 days throughout the experimental period. Postoperative care included gentamicin (DaeSung Co, Seoul, Korea; 0.1 mL/kg) injections for 3 days, tooth brushing, and daily hexamedine (Bukwang Co, Seoul, Korea) irrigation.

Tissue blocks were resected from the separated maxillae, including the canines, the surrounding paradental tissues, and Corticision site. They were fixed in 10% neutral buffered formalin, decalcified in 10% ethylene diamine tetraacetic acid (EDTA) solution, dehydrated in a series of ethyl alcohol concentrations, embedded in paraffin, and longitudinally sectioned in the mesiodistal direction parallel to the direction of orthodontic force application. The 4-μm sectioned slices were examined under a light microscope with hematoxylin and eosin stain and Masson's trichrome stain.

For the histomorphometric analysis, nondecalcified specimens were prepared from the group IV cats. These were examined under an ultraviolet (UV) fluorescent microscope (Olympus BH-2, Olympus Co, Tokyo, Japan) with a UV filter (λ = 515 nm). Microphotographs of all specimens were obtained using a digital charge-coupled-device (CCD) camera (KAPPA PS30C) and were processed by a computer (Intel Pentium, 4.2 GHz). An outline of the labeled bone was traced from the microphotographs, and the areas of newly formed mineralized bone were measured using an image analysis software (Metreo version 2.5, KAPPA Image Base, KAPPA Optoelectronics, Accusoft Co, Gleichen, Germany). A subsequent examination of the slides by an oral pathologist confirmed these evaluations.

RESULTS

Light microscopic findings of the compression side are shown in Figure 2. In the control group, extensive hyalinization of the periodontal ligament (PDL) and indirect resorption of the bundle bone adjacent to the compressed PDL was observed from the marrow spaces on day 7. On day 14, indirect resorption was widespread, and areas of local unresorbed bundle bone were observed with the remaining hyalinized PDL. These findings corresponded to the lag phase of tooth movement. On day 21, resorption activity in the existing bundle bone ceased temporarily, causing markedly wide and traumatic PDL. In the Corticision group, the compressed PDL on day 7 contained less hyalinized tissue and more viable PDL cells than in the control group. Multinucleated osteoclast-like cells appeared on the margin of the bundle bone adjacent to the compressed PDL, thereby resulting in direct bone resorption subjacent to these cells. On day 14, the wide area of old bundle bone was resorbed leading to the development of large resorption cavities with increased recruitment of osteoclast-like cells. This facilitated the resumption of tooth movement followed by tissue remodeling as well as osteoid formation on the tension side.

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The microscopic findings of the tension side are shown in Figure 3. In the control group, band-like osteoid formation was observed on day 7, which is associated with slow tooth movement including the movement within the PDL. New bone formation associated with stretched Sharpey's fibers and proliferative PDL cells was observed on day 14. The osteoblasts gradually flattened and developed into quiescent lining cells, and a few of them became embedded in the newly formed bone matrix on day 21. In the Corticision group, spike-like osteoid formation associated with rapid tooth movement was observed along with proliferative PDL cells and active osteoblasts on day 7. The osteoblasts were plump and vigorous and produced a thick layer of osteoid. On day 14, the number of osteoblasts and new osteocytes increased in the actively forming bone matrix. This newly formed bone containing multiple newly developed marrow spaces was easily distinguishable from the old lamellar bone. The process of lamellation by the remodeling of the new bone had progressed on day 21.

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The microscopic appearance of the healing processes at the Corticision site is shown in Figure 4. After 21 days, healing progressed in group B at the mesiobuccal aspect of the injury site. New bone developed at the site of the bone defect, and lamellation of the new bone was almost complete at this stage. On the contrary, the surgical gap was still wide, and both the resorption and the apposition of bone continued in group C.

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Fluorescent microscopic findings are shown in Figure 5. Triple-fluorochrome labeled surfaces are an index of new mineralized bone formation. The lines demarcated the amount of new bone formed 7, 14, 21, and 28 days after treatment. While sharp and thin labeling lines were evident on the alveolar wall ahead of the direction of tooth movement in the control group, diffuse and thick lines were observed in groups B and C. These thick bands implied that the formation rate of new bone was accelerated at the time of fluorochrome injection. The amount and the rate of bone formation were similar in groups B and C, except for the remodeling pattern. In group B, active remodeling of the lamellar bone was observed to occur around the new Haversian systems at days 14–21; this was indicated by multiple concentric circles labeled in red (stained by first alizarin red) and yellow (subsequently stained by second oxytetracycline).

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The histomorphometric analysis indicated that the mean apposition length (mm) and accumulated mean apposition area (mm²/mm) were higher in the experimental groups than in the control group during all experimental periods (Figure 6). The mean apposition rate of the control group peaked on day 21 after demonstrating low values for the first 14 days, while it peaked earlier, ie, on day 14 in the experimental groups (Figure 7). There was no remarkable difference in the accumulated apposition area between groups B and C; however, it was 3.5-fold higher in group B (0.2771 mm²/mm) than in the control group (0.0798 mm²/mm; Table 2).

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Table 2.  Measurements for Histomorphometric Analysis

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DISCUSSION

Corticision could activate catabolic remodeling in the direction of tooth movement. This was represented by extensive direct resorption of bundle bone with less hyalinization and more rapid removal of hyalinized tissue in group B than in the control group. Corticision accelerated the anabolic remodeling activity as well. On day 28, mean apposition area of the mineralized bone was observed to be 3.5-fold higher in group B than in the control group. Histologic findings revealed neither pathologic changes in the paradental tissues nor root resorption following “Corticision.”

For accelerating orthodontic tooth movement, it is essential to minimize hyalinization of the PDL tissue or to stimulate the removal process of the hyalinized tissue. Considering that it is impossible to control the force magnitude clinically not to produce hyalinization, in the view of a biologic approach rather than a mechanical control, the lag phase of tooth movement can be shortened by stimulating the removal of hyalinized tissue. This can be attributed to the RAP because it stimulates cell-mediated responses around the tooth, thereby providing a favorable microenvironment for tissue remodeling. Various researchers have focused on controlling the microenvironment of the alveolar bone by using the RAP in an attempt to reduce tissue resistance.10 The transient osteoporotic condition involved increased release of calcium, decreased bone density, and increased bone turnover, all of which would facilitate tooth movement.11 This mechanism based on the RAP differed from the classical concepts of tooth movement such as the pressure-tension theory,12 bone-bending theory,13 mechanostat theory,14 and bony block movement in corticotomy.15

It is important that the cortical bone itself is not a barrier or resistance to orthodontic tooth movement. Garg16 emphasized that the RAP is primarily a phenomenon observed in the cortical bone. This new concept of cortical remodeling enabled the continuous advancement of supplemental surgical procedures involving minimal and conservative interventions. Germec et al17 revealed that single-sided partial corticotomy in the mandible appeared to be sufficient to stimulate rapid tooth movement.

Corticision minimized the degree of the surgical injury by excluding flap reflection. Only mucoperiosteal flap reflection without any decortication, as studied by Yaffe et al,18 could serve the RAP, resulting in widening of the periodontal ligament space and tooth mobility without any force application. However, the possible complications after flap surgery, such as crestal bone resorption and bone dehiscence were troublesome.18 Frost7 stated that the duration and intensity of the RAP are proportional to the extent of injury and soft tissue involvement in the injury. Hence, it was necessary to investigate whether Corticision was a logical modification to sufficiently elicit the RAP for accelerating tooth movement.

Clinically, additional manipulation intended to lengthen the duration of the RAP is initiated immediately after Corticision and repeated every 2 weeks thereafter. In this experiment, it was performed every 3 days considering the difference in the time cycle between humans and cats. This manipulation would involve the interception of the lamellation process of woven bone at the injury site and provide repeated microdamage. However, the effect of periodic manipulation on the remodeling of alveolar bone proper and on the rate of tooth movement could not be elucidated. Although additional manipulation would delay the healing process at the injury site, this was insufficient to last the duration of the RAP and the SAP.

CONCLUSIONS

• Corticision stimulated orthodontic tooth movement in 28 days by accelerating the rate of alveolar bone remodeling.

• The biologic exploration of Corticision is crucial for broadening the scope of orthodontics by reducing the treatment duration.