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The Effect of The Extent of Surgical Insult On Orthodontic Tooth Movement
The Effect of The Extent of Surgical Insult On Orthodontic Tooth Movement
doi:10.1093/ejo/cjz006
Original article
Correspondence to: Sumit Yadav, Division of Orthodontics, 263 Farmington Avenue, University of Connecticut Health Center,
Farmington, CT 06030, USA. E-mail: Yadav_sumit17@yahoo.com
Summary
Objective: The primary objective of this study was to investigate how the extent of surgical insult
affects the orthodontic tooth movement (OTM) and the alveolar bone modelling and remodelling
in a rodent model.
Material and methods: 15-week-old male Wistar rats were used in the research and they were
randomly divided into three treatment groups: (1) OTM only (N = 8); (2) OTM + 2 alveolar
decortication (AD) (less surgical insult) (N = 8); and (3) OTM + 4 AD (more surgical insult) (N = 8).
A nickel-titanium spring delivering 5–8 g of force was used to protract the molar mesially using
maxillary incisors as an anchorage. AD was done using a hand piece and a round bur, adjacent to
the left first maxillary molar on the palatal alveolar bone. After 14 days of OTM Wistar rats were
killed and microfocus computed tomography and histological analysis were performed.
Results: The OTM + 4AD group presented with a significant increase (P < 0.05) in the rate of tooth
movement when compared to OTM + 2AD group and OTM only group. In addition, the OTM + 4AD
group had a significant decrease in bone volume and tissue density (P < 0.05) and a significant
increase (P < 0.05) in the trabecular spacing and trabecular thickness when compared to OTM only.
Histological quantification of tartrate-resistant acid phosphatase indicated a significant percent
increase (P < 0.05) in OTM + 4AD group, when compared to OTM + 2AD and OTM only group.
Results: Increased surgical insult increases the rate of OTM. Additionally, increased surgical insult
decreases the bone volume and the tissue density.
Introduction White spot lesions are found in 96% and caries in 2.3% of ortho-
dontic patients, with prolonged treatment time as a risk factor for
Orthodontic treatment ranges from 18 to 36 months, averaging
their development (5,8). External apical root resorption is highly
around 20 months to complete (1). The duration of treatment can be
correlated to the duration of orthodontic treatment, as longer period
influenced by factors such as the severity of malocclusion, incidence
of hyalinization precedes external apical root resorption (9). Poor
of impacted teeth, treatment mechanics, and patient compliance (2).
gingival health is also significantly influenced by the duration of
Perhaps the most important determinant of the duration of treatment
orthodontic treatment (7).
are the biological principles underpinning orthodontic tooth move-
With the myriad of complications associated with orthodontic
ment (OTM), an inflammatory process resulting in bone modelling
treatment duration, the advent of interventions to accelerate OTM
and remodelling (3,4).
has gained momentum in the last decade. Adjunctive modalities to
Long treatment duration is not only associated with an increased
accelerate OTM could be divided into non-invasive and invasive
financial burden to the clinician, but also detrimental to the patient’s oral
interventions (10,11). Non-invasive interventions include mechani-
health. Adverse consequences from long treatment time include white
cal vibration, low-level light energy, and low-intensity pulsed
spot lesions, caries, root resorption, and poor gingival health (5–7).
© The Author(s) 2019. Published by Oxford University Press on behalf of the European Orthodontic Society.
1
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2 European Journal of Orthodontics, 2019
extending to the points of the most distal parts of the mesiobuccal roots. The positive pixels for TRAP (yellow fluorescent pixels gener-
and mesiopalatal roots. The parameters evaluated were bone vol- ated by ELF97) were counted by selecting each pixel colour. The
ume fraction (BVF), tissue density, trabecular spacing, and trabecular number of positive fluorescent pixels were divided by the total num-
thickness. ber of pixels in the region of interest and multiplied by 100, obtain-
After imaging, the maxilla from each rat was rehydrated and ing the percentage of positive pixels. The osteoclast numbers were
decalcified using 14% ethylenediaminetetraacetic acid for 2 weeks counted in three sections from four rats in each group, and the values
at 4°C. Subsequently samples were processed for standard paraf- were then averaged for each animal to run a statistical test.
fin embedding and serial sagittal sections 5–7 µm in thickness were
obtained. Tartrate-resistant acid phosphatase (TRAP) staining Statistical analysis
was performed using the yellow fluorescent substrate ELF97 (Life Statistical analysis was done using the GraphPad prism software (La
Technologies, Grand Island, New York, USA) according to the manu- Jolla, California, USA). The power analysis was based on a previ-
facturer’s instructions. Quantification of fluorescent staining (TRAP) ously published study. The number of animals was calculated by the
was performed by Adobe Photoshop (Adobe Systems Incorporated) G power software and was determined to be six in each group. For
on the alveolar bone surfaces on the mesial sides of the distobuccal this calculation, an alpha level of 0.05 and beta level of 0.8 were
4 European Journal of Orthodontics, 2019
Figure 2. Micro-CT data showing BVF, tissue density, trabecular thickness, and trabecular spacing in the OTM only, OTM + 2AD, and OTM + 4AD. (a) Coronally
reconstructed micro-CT image of OTM group; (b) coronal reconstructed micro-CT image of OTM + 2AD group; (c) coronal reconstructed micro-CT image of OTM
group + 4AD; (d) histogram showing significant decrease (P < 0.05) in the BVF in OTM + 4AD group; (e) histogram showing significant decrease (P < 0.05) in the
tissue density in OTM + 4AD group when compared to OTM only; (f) histogram showing significant decrease (P < 0.05) in the trabecular thickness in OTM + 4AD
group; and (g) histogram showing significant increase (P < 0.05) in the trabecular spacing in OTM + 4AD group. # P < 0.05, *P < 0.05. AD, alveolar decortication;
BVF, bone volume fraction; micro-CT, microfocus computed tomography; OTM, orthodontic tooth movement.
selected. The outcome variables examined were intermolar distance D’Agostino and Pearson omnibus normality test. The osteoclast
(IMD), BVF, tissue density, trabecular number, trabecular spaces, and percentage (TRAP positive pixels) was not normally distributed and
osteoclast percentage. Mean, standard deviation, percentile distribu- Wilcoxon signed rank test was used to compare osteoclast percent-
tion, and confidence interval were computed for all the outcome age (TRAP positive pixels) between the control and experimental
variables. Normality of the data distribution was examined using groups. Nonparametric tests were used to examine the outcome
J. Chang et al. 5
variables between the control and the experimental groups. Kruskal– (P = 0.0004). OTM + 4AD group had 60.71% more tooth movement
Wallis test was used to compare the intermolar distance (IMD), BVF than OTM + 2AD group and 119.51% more than OTM only group.
tissue density, trabecular number, and trabecular spaces. All statisti- However, there was no significant distance in the IMD between OTM
cal tests were two-sided and a P value of <0.05 was deemed to be + 2AD and OTM group (P = 0.3214) (IMD: OTM = 0.418 ± 0.199;
statistically significant. 95% confidence interval [CI] = 0.208 to 0.627; OTM + 2AD = 0.568 ±
0.195; 95% CI = 0.363 to 0.774; OTM + 4AD = 0.904 ± 0.127; 95%
CI = 0.786 to 1.023) (Figure 1g, Table 1).
Results
Overall weight and health of the rats Bone parameters in the region of interest
All rats used in the study were 15 weeks old at the start of the experi- Our micro-CT analysis showed a significant decrease in BVF in the
ments and 17 weeks old when they were killed. None of the rats lost OTM + 4AD group when compared to OTM + 2AD (P = 0.0004) and
the spring during the entire duration of the study in all the three OTM group only (P = 0.0004). In addition, there was also a signifi-
experimental groups. The rats in all the groups for the entire dura- cant difference in the BVF between OTM + 2AD and OTM group
tion remained healthy and had a slight increase in the body weight. (P = 0.0004). OTM + 4AD group had a 37.47% decrease in BVF when
compared to OTM + 2AD group and 57.7% decrease when com-
Intermolar distance (OTM) pared to OTM only group (BVF%: OTM only = 62.52 ± 11.68; 95%
The IMD was significantly higher in the OTM + 4AD group, when CI = 50.26 to 74.77; OTM + 2AD = 42.46 ± 7.61; 95% CI = 33.01
compared to OTM + 2AD (P = 0.0088) and OTM only group to 51.91; OTM + 4AD = 26.55 ± 7.35; 95% CI = 18.83 to 34.27)
6 European Journal of Orthodontics, 2019
Table 1. Distribution of data (orthodontic tooth movement). AD, alveolar decortication; CI, confidence interval; OTM, orthodontic tooth
movement; SD, standard deviation.
Table 2. Distribution of data (bone parameters). AD, alveolar decortication; BVF, bone volume fraction; CI, confidence interval; OTM, ortho-
dontic tooth movement; SD, standard deviation.
Mean 62.52 42.46 26.55 1146 1034 941.5 97.8 77.83 64.67 73.4 94.33 111.5
SD 11.68 7.611 7.358 88.01 65.1 97.76 7.014 13.27 9.136 5.32 9.771 8.432
Minimum 46.6 32.1 17.1 1036 935 814 89 56 53 66 79 101
Maximum 77.4 51.3 37.2 1270 1110 1110 107 93 76 79 107 121
Percentiles
25 50.13 34.95 20.18 1071 980.5 882.3 91 67.25 54.5 68.5 86.5 102.5
50 64.9 43.9 25.85 1134 1030 925 99 79 66 73 95 112.5
75 71.85 49.25 33.38 1229 1090 1005 104 90 73 78.5 102.5 119.5
Lower 95% CI 50.26 33.01 18.83 1037 953.4 838.9 89.09 63.9 55.08 66.79 84.08 102.7
Upper 95% CI 74.77 51.91 34.27 1256 1115 1044 106.5 91.76 74.25 80.01 104.6 120.3
Table 3. Distribution of data (histological evaluations) AD, alveolar compared to OTM + 2AD group and 17.84% decrease when com-
decortication; BVF, bone volume fraction; CI, confidence interval; pared to OTM only group (tissue density: OTM only = 1146 ±
OTM, orthodontic tooth movement; SD, standard deviation; TRAP, 88.01; 95% CI = 1037 to 1256; OTM + 2AD = 1034 ± 65.1; 95%
tartrate resistant acid phosphatase. CI = 953.4 to 1115; OTM + 4AD = 941.5 ± 97.76; 95% CI = 838.9
to 1044) (Figure 2a–2c and 2e, Table 2).
Distribution of data (histological evaluation)
There was a significant decrease in the trabecular thickness in
TRAP (%) OTM + 4AD group when compared to OTM only group. Similarly,
we observed a significant decrease in the trabecular thickness in
OTM OTM + 2AD OTM + 4AD OTM + 2AD group when compared to OTM only group. However,
there was no difference significant between OTM + 4AD and OTM
Mean 0.4183 0.5688 0.9043
+ 2AD groups (trabecular thickness: OTM only = 97.8 ± 7.01; 95%
SD 0.1997 0.1958 0.1278
Minimum 0.203 0.324 0.712
CI = 89.09 to 106.5; OTM + 2AD = 77.83 ± 13.27; 95% CI = 63.9
Maximum 0.713 0.896 1.053 to 91.76; OTM + 4AD = 64.67 ± 9.13; 95% CI = 55.08 to 74.25)
Percentiles (Figure 2a–2c and 2f, Table 2). There was a significant increase in
25 0.2728 0.4178 0.796 the trabecular spacing in the OTM + 4AD group when compared
50 0.343 0.5455 0.924 to OTM + 2AD and OTM only group. Similarly, significant increase
75 0.6373 0.7138 1.032 was observed in OTM + 2D group when compared with OTM
Lower 95% CI 0.2087 0.3633 0.7861 only group (trabecular spacing: OTM only = 73.4 ± 5.32; 95%
Upper 95% CI 0.6279 0.7744 1.023 CI = 66.79 to 80.016; OTM + 2AD = 94.33 ± 9.77; 95% CI = 84.08
to 104.6; OTM + 4AD = 111.5 ± 8.43; 95% CI = 102.7 to 120.3)
(Figure 2a–2c and 2g, Table 2).
(Figure 2a–2d). However, tissue density was significantly lower
in the OTM + 4AD group when compared to OTM only group
(P = 0.006). There was no significant difference between OTM + TRAP staining for osteoclast
4AD group when compared to OTM + 2AD group and no signifi- Our histological analysis revealed significant increase in the TRAP
cant difference between OTM + 2AD group and OTM only group. positive pixels (TRAP staining for osteoclast) OTM + 4D when com-
OTM + 4AD group had a 8.95% decrease in tissue density when pared to OTM + 2D (P = 0.002) and OTM only group (P = 0.002)
J. Chang et al. 7
(TRAP (%): OTM = 2.41 ± 1.20; 95% CI = 1.65 to 3.18; OTM + rats, unlike humans, do not have osteonal remodelling (secondary
2AD = 11.28 ± 6.58; 95% CI = 6.56 to 16.00; OTM + 4AD = 24.57 ± remodelling). Nonetheless, our in vivo study has provided insight on
5.78; 95% CI = 19.73 to 29.41) (Figure 3, Table 3). titration of the amount of AD on the rate of tooth movement, and its
corresponding change in osteoclast number and bone turnover. Our
future goals involve studying the long-term effects of differing amounts
Discussion of ADs on the alveolar bone modelling and remodelling. Our future
goals involve studying, the adverse effects, especially root resorption,
acceleration of tooth movement: a systematic review and meta-analysis. 22. Tsai, C.Y., Yang, T.K., Hsieh, H.Y. and Yang, L.Y. (2016) Comparison of
Progress in Orthodontics, 17, 33. the effects of micro-osteoperforation and corticision on the rate of ortho-
12. El-Angbawi, A., McIntyre, GT., Fleming, P.S., and Bearn, D.R. (2015) dontic tooth movement in rats. Angle Orthodontist, 86, 558–564.
Non-surgical adjunctive interventions for accelerating tooth movement in 23. Alikhani, M., et al.et al. (2013) Effect of micro-osteoperforations on the
patients undergoing fixed orthodontic treatment. Cochrane Database of rate of tooth movement. American Journal of Orthodontics and Dentofa-
Systematic Reviews, 18, CD010887. cial Orthopedics, 144, 639–648.
13. Fleming, P.S., Fedorowicsz, Z., Johal, A., El-Angbawi, A., and Pandis, N. 24. Dutra, E.H., Ahmida, A., Lima, A., Schneider, S., Nanda, R. and Yadav, S.