Vibration paradox in orthodontics: Anabolic and catabolic effects

Abstract

Vibration in the form of High Frequency Acceleration (HFA) is anabolic on the craniofacial skeleton in the absence of inflammation. Orthodontic forces trigger an inflammation-dependent catabolic cascade that is crucial for tooth movement. It is unknown what effect HFA has on alveolar bone if applied during orthodontic treatment. The objectives of this study are to examine the effect of HFA on the rate of tooth movement and alveolar bone, and determine the mechanism by which HFA affects tooth movement. Adult Sprague Dawley rats were divided to control, orthodontic force alone (OTM), and different experimental groups that received the same orthodontic forces and different HFA regimens. Orthodontic tooth movement was assessed when HFA parameters, frequency, acceleration, duration of exposure, and direct or indirect application were varied. We found that HFA treatment significantly enhanced the inflammation-dependent catabolic cascade during orthodontic tooth movement. HFA treatment increased inflammatory mediators and osteoclastogenesis, and decreased alveolar bone density during orthodontic tooth movement. Each of the HFA variables produced significant changes in the rate of tooth movement and the effect was PDL-dependent. This is the first report that HFA enhances inflammation-dependent catabolic cascades in bone. The clinical implications of our study are highly significant, as HFA can be utilized to enhance the rate of orthodontic tooth movement during the catabolic phase of treatment and subsequently be utilized to enhance retention during the anabolic remodeling phase after orthodontic forces are removed.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. HFA effect on the rate of tooth movement depends on acceleration and the dynamic nature of the load.

(A) Animals were exposed to orthodontic force alone or in combination with direct application of different HFA on the occlusal surface of maxillary right first molar using a device depicted in this schematic. Strain gauge and accelerometer are shown placed in the maxillary alveolar bone in the proximity of the first molar. (B) Tooth movement was measured in the axial slice from the microCT scan of maxillary right molars at the level maximum convexity (height of contour) for Control (no movement), OTM and OTM + HFA shown here for 14 days treatment with 10 cN force and 120Hz, 0.05g for 5 min a day. (C) Rate of tooth movement on day 7, 14 and 28 after application of 10cN or 25cN orthodontic forces in absence or presence of HFA for 5 min a day. Each value represents the mean ± SEM of 4 samples. (* Significantly different from day 0, for both 10 and 25 cN, # significantly different from all previous time points, for both for both 10 and 25 cN, ## significantly different from corresponding force group in the absence of HFA, for both 10 and 25 cN) (D) Effect of different accelerations on the rate of tooth movement at 120 Hz, in animals that received 10 cN or 25 cN orthodontic forces (* Significantly different from OTM group; # significantly different from 0.01g acceleration) (E) Average peak strain (mean ± SEM) in the alveolar bone surrounding the maxillary first molar in response to different accelerations with a set frequency of 120 Hz under 10 με load. HFA was directly applied to the occlusal surface of fresh rat skulls (n = 4) and average peak strain was registered using a strain gauge attached to the buccal and palatal surface of the alveolar bone close to upper right first molar (* Significantly different from OTM; # significantly different from 0.01g acceleration) (F) Effect of static or dynamic (120 Hz for 5 minutes per day for 14 days) load application to the first molar at a peak strain of 30 με (registered at the level of alveolar bone) on the rate of tooth movement, in the presence of 10cN orthodontic force (* Significantly different from OTM group; # significantly different from Static load group).

Fig 2. Effect of frequency and duration of HFA on the rate of tooth movement is not linear.

(A) Effect of different frequencies on the rate of tooth movement under 0.05 g acceleration, 5 minutes per day for 14 days, in the presence of 10 cN orthodontic force (* Significantly different from OTM; # significantly different from 30Hz). (B) Effect of duration of HFA application on the rate of tooth movement under 120 Hz, 0.05g acceleration for 14 days in the presence of 10cN orthodontic force. Each value represents the mean ± SEM of 4 samples (* Significantly different from OTM).

Fig 3. HFA effect on orthodontic tooth movement is PDL-dependent and through enhancement of cytokine release.

(A) Animals were exposed to orthodontic force (OTM) alone or in combination with direct application of HFA for 5 minutes per day on the occlusal surface of the maxillary right first molar or indirect application of HFA on the adjacent tooth. HFA was calibrated so that the accelerometer measured the same acceleration and frequency on the buccal cortical plate of the maxillary first molar (120 Hz, 0.05g) in response to both direct or indirect loading. Tooth movement was measured in occlusal μCT images as the distance between the maxillary right first and second molars after 14 days. Each value represents the mean ± SEM of 4 samples. (* Significantly different from OTM group; # significantly different from Indirect load group). Mean “fold” increase in mRNA levels of different chemokines (B), cytokines (C), and their receptors (D) in maxillary right alveolar bone 24 hours after application of orthodontic force in the presence or absence of HFA (120 Hz, 0.05g) mechanical stimulation. Data expressed as the mean ± SEM of 5 samples (* Significantly different from control; ** significantly different from OTM). Mean protein concentration of CCL2 (E), IL-1ß (F), and TNF-α(G) in the maxillary right alveolar bone after 1, 3, 7 and 14 days of OTM or OTM + HFA. Data expressed as the mean ± SEM of concentration in picograms per 100 mg of tissue of 5 samples (* Significantly different from control; ** significantly different from OTM group). (H) Representative occlusal view of microCT images of right maxillary molars 14 days after application of orthodontic forces in OTM and OTM+HFA groups in absence or presence daily anti-inflammatory medication (OTM+HFA+AI). These images demonstrate blockage of stimulatory effect of HFA on rate of orthodontic tooth movement by anti-inflammatory medication. Arrow demonstrate the direction of the force application.

Fig 4. Osteoclast markers and number of osteoclasts increase in response to HFA mechanical stimulation.

(A) Mean concentration of RANKL protein in the maxillary right alveolar bone after 1, 3, 7 and 14 days as measured by ELISA. Data expressed as the mean ± SEM of RANKL concentration in picograms per 100 mg tissue of 5 samples. (* Significantly different from control; **significantly different from OTM group). (B) Light microphotographs of Cathepsin K–positive osteoclasts in immunohistochemically stained sections of mesiopalatal root of the maxillary first molar. Images were collected close to the alveolar crest 28 days after application of force. Osteoclasts are stained as brown multinucleated cells (arrow heads) in sections from different groups and in the detail higher magnification. (C) Mean number of osteoclasts at different time points, in PDL and adjacent alveolar bone of mesiopalatal root of maxillary first molar. Each value represents the mean ± SEM of four animals (*Significantly different from control; **significantly different from OTM group). (D) Representative axial μCT sections showing decrease in bone density in OTM+ HFA at 14 days. Arrow demonstrates the direction of force application. (E) Average bone volume fraction (bone volume/total volume [BV/TV]) was calculated for Control, OTM and OTM+HFA group for the alveolar bone in the area of the maxillary first molar. Each value represents the mean ± SEM of four animals. (* Significantly different from control; ** significantly different from OTM group).