INTRODUCTION

Alternative methods have been tested to increase the rate, magnitude, and stability of tooth movement. The historical background of intentional injury dates to the late 1990s, when Kole¹ introduced a surgical procedure to accelerate tooth movement.

In 1981, Frost² found a direct link between the severity of bone injury and intensity of the healing response. High bone turnover was triggered at the surgical site. Consequently, corticotomy was used as a surgical procedure to accelerate tooth movement. These events constitute a temporary stage of bone remodeling that results in the reconstruction of injured sites to their normal state, known as the “regional acceleratory phenomenon” (RAP).^3,4

This phenomenon occurs through osteoclast and osteoblast recruitment via regional intercellular mediators. A cascade of physiologic events occurs in corticotomized sites.⁵ The rate of tooth movement is influenced by bone remodeling, bone density, and the hyalinized periodontal ligament.^6–8

The purpose of performing corticotomy to accelerate tooth movement is to maximize injury to the alveolus to promote abundant bleeding. It is suggested that alveolar perforation triggers mild RAP activity and, consequently, accelerates the rate of tooth movement. The surgical procedure involves round bur perforations that barely reach medullary bone adjacent to the dental roots and poses no significant risk to tooth vitality.^4,9,10

Based on previous findings, it can be hypothesized that shallow perforations on the buccal cortical plate of the mandible result in temporary bone injury and do not cause permanent harm to patients. Thus, the aims of this study were to (1) analyze histologic findings of bone remodeling at baseline and 90 days after corticotomy in corticotomized and noncorticotomized sites and (2) provide scientific data to determine whether bone conditions in corticotomized subjects are unaltered 3 months after surgery.

MATERIALS AND METHODS

For this preliminary study, a sample of eight adult patients (three men, five women; mean age = 40.2 years) with bilaterally tipped mandibular second molars were identified from the orthodontic clinic at Rio de Janeiro State University. Ethical approval was obtained from the Brazilian Research Ethics Committee, and informed consent was acquired from patients who decided to participate in the study. The study was designed to use each patient as his or her own control in order to increase the power with a small sample. To be included in the study it was mandatory that mandibular molars would be uprighted bilaterally, regardless of the malocclusion type. Patients were excluded if any of the following conditions were present: autoimmune disease, long-term use of medication 3 months before the beginning of the study (nonsteroidal anti-inflammatory, cortisone, immune suppressive, and, bisphosphonate drugs), or probing depth values exceeding 4 mm; women who were pregnant or lactating were also excluded.

The trial was initiated with 17 patients, though six were excluded at an early stage (four patients considered the treatment invasive and decided not to participate; two presented with autoimmune disease). Of the 11 remaining patients, three did not return for follow-up. At the end of the study, eight patients were evaluated. A great amount of cooperation was necessary; although the biopsies were minimally invasive, the patients were expected to undergo a second surgery to harvest bone. The research team followed a transparent conduct that did not allow any financial compensation for the patients.

Clinical Procedures

All eight patients presented with bilaterally inclined mandibular second molars and, for some, the third molars were present (Figure 1A). In this split-mouth study, corticotomy was randomly assigned to either the left or right quadrant using open access software (randomization.com, August 3, 2007). Goals of the treatment were to upright teeth and prepare the open space generated by the missing molars for future implant insertion. Orthodontic biomechanics consisted of a cantilever inserted into the inclined mandibular molars and ligated mesially to anchor teeth.

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A week before the corticotomy, 0.017 × 0.025 inch beta-titanium (titanium-molybdenum alloy, American Orthodontics, Sheboygan, Wis) cantilevers with an L loop incorporated were fabricated at chairside and stored for the next appointment. At this stage, a full fixed appliance was in place, and a 0.019 × 0.025 inch stainless steel archwire was used to provide anchorage in the lower arch.

Patients returned the next week for corticotomy, bone harvest, and cantilever activation on both lower quadrants. Full-thickness flaps were elevated from the edentulous space to the distal aspect of the second molars. Approximately 10 to 12 perforations were made in the cortical plate using a round bur (1012 bur, KG Sorensen, Cotia, Sao Paulo, Brazil) with a high-speed handpiece under abundant irrigation (Figure 1B, C). The depth of the perforations approximated the width of the buccal cortical plate. Mandibular bone blocks were harvested using a trephine bur (total length 53 mm, internal diameter 4.25 mm, Titanium, Ace Surgical Supply, Brockton, MA, USA) in a location mesial to the mandibular second molars (Figure 1D). Thereafter, the flap was repositioned and sutured (4-0 nonresorbable silk, 1.7 cm needle, Ethicon, Sao Paulo, SP, Brazil). Immediately after surgery, cantilevers were bilaterally inserted into each second molar tube and hooked between the canine and the premolars (Figure 2).

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Osteoblastic Activity in Alveolar Bone

Images were captured at 20× magnification in an optic microscope (Axio Observer A1; Carl Zeiss, LLC, Pleasanton, CA, USA) attached to a digital camera (AxioCam HRcl; Carl Zeiss, LLC) and connected to a computer. Images were assessed by two blinded evaluators (F.R., R.B.) who were previously calibrated. The regions of interest were those with the highest bone and tissue volume.

The following parameters were collected: (1) ratio between secondary and primary bone, (2) ratio between inorganic and organic bone, (3) quantity of osteocytes, and (4) reversal lines of bone remodeling:

1. The ratio between secondary and primary bone was assessed using a grid that divided each image into 48 units. For bone formation, evaluators indicated the predominant color (red or blue) for every unit. Secondary bone had histologic features compatible with red tissue and primary bone had blue color (Figure 3).

2. The ratio between inorganic and organic bone was measured with the same grid described previously. Bone matrix is mostly made of a composite material incorporating the inorganic mineral calcium phosphate in the chemical arrangement and termed calcium hydroxyapatite and organic collagen. The score result reflected the overall mineralized portion of bone (Figure 4).

3. The quantity of osteocytes was assessed in H&E images, and all lacunae occupied by osteocytes within bone matrix were counted regardless of whether their nuclei were absent (Figure 5A) or present (Figure 5B). Organic portions were not considered in the osteocyte count (Figure 5C). Horizontal lines were placed over the images to guide the evaluators and avoid double counts (Figure 5D).

4. The quantity of reversal lines was assessed through direct visual analysis to identify the most distinct reversal lines. According to the framing needed, 24 units of the grid were positioned either horizontally or vertically to include the complete extent of the reversal line (Figure 6A). The grid's inner section was erased to facilitate a clear view (Figure 6B), and green arrows were positioned over the identified reversal lines for subsequent counting (Figure 6C).

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RESULTS

Descriptive analyses of baseline characteristics are presented in Table 1. Levels obtained from corticotomy stimulation after a period of 90 days are presented in Table 2.

Table 1. Baseline Characteristics

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Table 2. Estimated Marginal Means Obtained in Generalized Estimating Equation Model 90 Days After Surgery

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DISCUSSION

In this study, it was hypothesized that shallow and limited perforations on the buccal cortical plate of the mandible would not provoke permanent damage in corticotomized patients. The surgical approach included cortical perforations in the buccal plate without reflection of a lingual flap and vertical cuts. A more invasive approach does not necessarily mean more tooth movement,¹¹ and the thought was that a localized intervention would trigger the desired events.

There is scarce evidence to indicate that bone homeostasis is restored after corticotomy. Only 3 studies^12–14 reported histologic follow-up, one at 7 weeks and the other two at 2 months after surgery, and all of them reported that baseline characteristics (osteoblast and osteoclast levels) were restored. The current study showed that levels of primary bone and osteocytes increased significantly in corticotomized patients at the 90-day follow-up. Alterations in the inorganic portion and reversal lines were mild and insignificant in both groups, suggesting that the baseline characteristics of these two features were preserved.

Due to ethical reasons, it was not possible to harvest additional bone between the two time points evaluated in this study. Therefore, we can only speculate as to which alterations took place between the surgical intervention and 90-day follow-up time points. Most likely, bone characteristics were changed in corticotomized patients as a response to the intentional injury. Based on scientific evidence from this study, there was no significant damage in either group, and there were indications of new bone formation in the test group at the 90-day follow-up.

The main problem with small clinical trials is in interpreting the results. It is important not to make strong conclusions about a trial intervention and to avoid extrapolating or generalizing the results. Even though only a small group was evaluated in this clinical study (n = 8), no other clinical study has assessed histologic data from patients with a 3-month follow-up.

Animal studies have confirmed the underlying mechanism of corticotomy as a coupled interaction of bone resorption and bone formation during initial tooth displacement.^4,11–13 Ninety days after corticotomy new bone formation was detected in the current study as an increased level of primary bone and osteocytes. These findings are in agreement with the results from animal research conducted by Baloul et al.¹² and Teng and Liou,¹³ suggesting that an accelerated bone turnover is still active 3 months after surgery.

Regarding the study design, it may be questioned whether trephined bone extraction may cause an injury capable of triggering RAP. However, there is no scientific evidence to correlate the extent of bone injury necessary to induce accelerated bone turnover.

Patterns in the mandibular trabecular bone can be influenced by many factors, such as genetics, dissipation of masticatory load, and soft diet, thus resulting in great morphologic diversity. In this study, there was a noticeable difference between the quantity and quality of bone biopsies despite the standardized harvesting protocol. This research was designed to extract 6mm bone blocks containing cortical and trabecular bone, but unfortunately, these expectations were not met in 3 patients.

The bone harvest results were influenced by great morphologic diversity among patients and were accompanied by abundant transoperatory bleeding. In patients with dense and compact bone, it was difficult to disrupt the cortical barrier, and, once the trephine perforation reached its working length, the bone block would still be attached to its base. In such cases where the bone biopsies were not captured by the trephine, there was a high risk of fracturing the specimen into multiple small pieces during extraction.

During bone harvest, the suction should be conducted from a safe distance of 2 cm from the extraction sites to avoid accidental aspiration. However, in cases of abundant bleeding, a greater proximity to the extraction site was inevitable. In this study, 3 of 32 biopsies were accidentally aspirated, and it was possible to perform a second extraction in only one of those cases.

In the past decade, considerable progress has been made in understanding RAP and the implications on corticotomy-facilitated orthodontics.^4,12,15–21 A clinical split-mouth study reported that tooth movement was significantly higher on the corticotomy side than on the control side during the first 4 months.¹⁹ During the first 2 months after surgery, the corticotomized teeth exhibited an average monthly rate approximately two times faster than the control side. During the third and fourth months, the mean monthly rate declined but it was still higher on the corticotomy than on the control side. This information is consistent with the transient nature of RAP. Animal studies were able to identify RAP peak days, observed at 7, 14, and 22 days after corticotomy.^4,12,20 Scientific evidence seems to agree that high bone turnover rate lasts approximately 90 days after corticotomy.^4,17,20

The RAP peak and its duration. as determined by previous studies,^4,12,17,20 were extremely relevant for planning the treatment protocol used in the current study. The importance of orthodontic activation immediately after surgery was emphasized as a means to extract the most out of the tooth movement rates during RAP peak days. The second bone biopsy was planned according to evidence suggesting that RAP effects subside 3 months after surgery. Therefore it was safe to evaluate tissue repair in specimens harvested in that period.

CONCLUSIONS

• Based on the findings of this study, it is possible to conclude that corticotomy surgeries performed in adult patients promote a reversible and transient bone injury.