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Evaluation of architectural changes in mandibular trabecular and cortical bone pattern after functional treatment

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Introduction

Using the principle of directing growth, functional appliance therapy is performed during a patient’s accelerated growth and development period. During function, muscle contraction creates pressure vibrations which may cause alterations in trabecular form. According to Wolff’s Law, these stimuli cause changes in the internal and external structural architecture of bone. No significant change occurs in bone experiencing a normal functional stimulus but when the intensity and direction of the stimuli are changed, the shape and architectural structure of the bone are also changed.1 The alteration in bone architecture as a result of functional appliance therapy has been a matter of intrigue for researchers.

There is sufficient support for the view that the effect of functional appliance therapy is to inhibit maxillary growth.26 However, it has been further suggested that treatment outcome is mainly due to mandibular growth activation711 or a combination of maxillary growth inhibition and mandibular growth.12 Some who support the concept of growth activation believed that a mandibular deficiency is mainly treated by dentoalveolar compensation,4 while others consider that the problem is managed by both dentoalveolar and skeletal effects.811,13 Using cephalometry, only anteroposterior and vertical, angular and linear differences can be appreciated, and the detection of condylar apposition and cortical bone increase is difficult. A non-invasive method termed fractal dimension (FD) analysis has been introduced to evaluate the microstructure of bone.14 The technique describes a statistical ratio of complexity and was initially used to define intricate structures in nature such as coastlines. A feature of fractal analysis is self-similarity, meaning that magnified portions of a surface look similar to some extent. The relationship between FD on 2D projection and 3D bone structure has been investigated whereupon it has been claimed that trabecular microarchitecture could be adequately assessed on 2D radiographs.15 Furthermore, FD has been reported to describe complex bone structure and help identify bony changes associated with osteoporosis16 and that fractal dimension analysis can be used as a supplementary method for bone regeneration measurements.17 Mandibular bone structural changes18 and periodontitis-induced trabecular changes19 have also been investigated using fractal dimension analysis and the measurement of cortical bone thickness (CorT) is a technique whereby mandibular bone status is assessed.20 Panoramic radiographs are cost-effective and are routinely-used imaging methods which show trabecular structural changes and therefore may be utilised for FD analysis and CorT.20 To date, there are only two studies that have evaluated functional appliance-induced changes using the fractal method and no study has investigated changes in CorT resulting from functional appliance treatment. Therefore, the current study aimed to investigate and assess, using FD and CorT analyses, whether functional appliance treatment alters the microarchitecture of the mandible.

Material and methods

The present retrospective study was conducted using the archive files of the Orthodontic Department at Recep Tayyip Erdoğan University. The study protocol was approved by the local Ethics Committee (2020/199) and was conducted according to the principles described in the Declaration of Helsinki, including all amendments and revisions.

The database was obtained from archival files between 2017 and 2019. The study consisted of 30 cases treated using functional appliances and 15 control patients who had poor oral hygiene and who were not treated for a period of one year. After providing oral care, the control cases were later orthodontically treated by conventional means. The inclusion criteria identified: 1. Males and females who were pooled; 2. a treatment period of one year; 3. an observation period of the control group also of one year; 4. all groups had a Class II malocclusion (ANB≥5, 30≤SN-GoGn≤35) as a result of a retrognathic mandible; 5. participants were in their pubertal growth phase and had no systemic diseases nor impacted teeth; 6. monoblock or twin-block appliances were applied to the treatment group; 7. patients in the control group had inadequate oral hygiene but after oral-care was provided and deemed satisfactory, they were later orthodontically treated. Radiographic images without sufficient diagnostic quality were excluded.

G* Power 3.1.9.4 software package (Heinrich Heine University, Dusseldorf, Germany) was used in the sample size calculation due to its ability to detect significant differences at α=0.05 error probability (critical t: 1.68107, non-centrally parameters: 2.90929). An effect size was detected to be 0.925, with a power of 0.888. Cesur et al.21 also found an effect size to be 0.8074 in a similar study.

Two two-dimensional panoramic radiographs were obtained for the treatment (T) and control (C) groups with a one-year interval (T1, T2) (C1, C2). The panoramic radiographs were taken using a Planmeca Promax 2D S2 device (Planmeca, Helsinki, Finland) at 66 kVp, 8 Ma and an exposure time of 16.6 sec. Patients were positioned such that the Frankfurt horizontal plane was parallel to the floor.

The FD analysis involved the following steps: the panoramic radiographs were converted to tagged image file formats (TIFF) because of their high resolution. Each ROI (standardised square region of interest) was selected at a 20×20 pixel size, cropped, and subsequently duplicated (Fig. 1A). A Gaussian filter (sigma 35 pixels) was used to remove the large-scale variations in brightness of the image (Fig. 1B). The resulting heavily blurred image was then subtracted from the original image (Fig. 1C). Bone marrow cavities and trabeculae were distinguished by adding 128 gray values to each pixel location (Fig. 1D). The image was then made binary and thus was segmented into components representing trabeculae and marrow. The resultant image was eroded (Fig. 1E) and dilated (Fig. 1F) to reduce noise. The image was subsequently inverted to highlight the trabeculae (Fig. 1G) and eroded until only the central line of pixels remained (skeletonisation) (Fig. 1H). Three different areas of each mandible were chosen (both right and left sides) for analysis and identified as the condylar process, the antegonial notch and the ramus (Fig. 2). FD measurements were determined with the help of ImageJ version 1.3 software (National Institutes of Health, Bethesda, Md, USA), a Java-based image-processing program. The measurements were conducted using customised software designed by White and Rudolph22 and by applying a box-counting method. Image dimensions on the skeletonised image were divided into squares of 2, 3, 4, 6, 8, 12, 16, 32, 64 pixels. The frames with trabeculae and the total number of frames in the image were calculated for each pixel size. These values were plotted on a logarithmic scale and the line that best fitted the points was drawn. The slope of the line produced the fractal dimension value that showed the complexity of the structure. To measure CorT on panoramic radiographs, the inferior edge of the mental foramen was identified and a line parallel to the body of the mandible and tangential to the inferior border was constructed. A line perpendicular to this tangent intersecting the inferior border of the mental foramen was derived (Fig. 2). Using digital callipers, the thickness of the mandibular cortex was bilaterally measured along this line and the mean CorT was calculated using Planmeca Romexis 4.6.2.R software (Planmeca Romexis, Helsinki, Finland).

Figure 1.

Steps of fractal dimension analysis. A. Cropped and duplicated region of interest. B. Gaussian blur. C. Subtracted blurred image from the original image. D. Addition of a gray value of 128 to each pixel location. E. Erosion. F. Dilatation. G. Inversion. H. Skeletonization.

Figure 2.

Right side; selected ROI areas for fractal dimension analysis selection, Left side; presentation of cortical thickness measurement.

The generated data were statistically analysed using the SPSS 21 package software (SPSS Inc., Chicago, IL, USA) with a level of significance set at 5% (p < 0.05) to provide descriptive analysis. A paired t-test was performed to analyse FD and CorT in dependent groups (in the treatment group (T1, T2) and control group (C1, C2)). To evaluate the efficiency of the treatment method, ΔT (∆T = T2−T1) and ΔC (∆C = C2−C1) were compared using an independent t-test. The images were analysed by an oral and maxillofacial radiologist (D.N.G) who had 6-years’ experience. For an intra-observer evaluation, 10 randomly selected patients were re-evaluated two weeks later. For the evaluation of intra-observer agreement, Cohen’s kappa was applied.

Results

A total of 45 cases were included in the study, of whom the treatment group consisted of 30 patients (8 males and 22 females) and the control group was comprised of 15 patients (6 males and 9 females). The mean age of the treatment and control groups was 12.4 and 11.5 years, respectively. The weighted Kappa coefficient for the re-evaluation of panoramic radiography images was found to be 0.869 revealing good intra-observer reliability.21

The descriptive analysis of FD and CorT values in the treatment and control groups are shown in Table I.

Fractal dimension analysis and cortical thickness measurement descriptive analysis in treatment and control groups.

Treatment Control
Pre treatment (T1) Post treatment (T2) Pre control (C1) Post control (C2)
Mean SD Min Max Mean SD Min Max Mean SD Min Max Mean SD Min Max
FD
 Processus condylaris 1.4013 0.09661 1.14 1.54 1.4551 0.08854 1.17 1.56 1.4205 0.11219 1.21 1.65 1.4493 0.13707 1.18 1.66
 Antegonial notch 1.3601 0.09513 1.08 1.50 1.3914 0.09535 1.21 1.53 1.4055 0.06633 1.30 1.50 1.4254 0.06592 1.29 1.52
 Ramus mandible 1.3537 0.08615 1.11 1.48 1.3744 0.10603 1.14 1.53 1.3939 0.07847 1.26 1.49 1.3955 0.14297 1.17 1.67
Cortical thickness 3.6000 0.56125 2.55 4.50 3.7750 0.47810 3.05 4.55 3.1417 0.38602 2.30 3.65 3.3042 0.43509 2.30 3.90

SD: indicates standard deviation; FD: Fractal dimension analysis.

When the before and after treatment values in the study groups were compared, statistically significant differences were found in the FD analysis of the right (p < 0.05) and left condyles (p < 0.05) and in the CorT measurements of the right (p < 0.01) and the left side (p < 0.05) (Table II).

Comparisons of T1–T2 (Pretreatment – Posttreatment) and C1–C2 (Precontrol-Postcontrol) with paired t-test.

T (n=30) C (n=12)
T1 (Mean±SD) T2 (Mean±SD) p value C1 (Mean±SD) C2 (Mean±SD) p value
Processus condylaris (R) 1.402 ± 0.121 1.450 ± 0.098 0.033* 1.420 ± 0.118 1.450 ± 0.117 0.519
Antegonial notch (R) 1.361 ± 0.126 1.406 ± 0.138 0.228 1.409 ± 0.098 1.421 ± 0.083 0.762
Ramus mandible (R) 1.364 ± 0.098 1.370 ± 0.141 0.822 1.394 ± 0.109 1.390 ± 0.173 0.949
Cortical thickness of the mandible (R) 3.620 ± 0.589 3.807 ± 0.491 0.006** 3.167 ± 0.405 3.292 ± 0.434 0.063
Processus condylaris (L) 1.400 ± 0.105 1.460 ± 0.101 0.037* 1.421 ± 0.130 1.448 ± 0.165 0.601
Antegonial notch (L) 1.359 ± 0.113 1.377 ± 0.115 0.509 1.402 ± 0.056 1.430 ± 0.120 0.501
Ramus mandible (L) 1.343 ± 0.124 1.378 ± 0.119 0.273 1.394 ± 0.091 1.401 ± 0.160 0.877
Cortical thickness of the mandible (L) 3.580 ± 0.599 3.743 ± 0.517 0.021* 3.117 ± 0.504 3.317 ± 0.488 0.046*

R: right, L: left. SD: indicates standard deviation. *p<0.05; **p<0.01.

When comparing control groups, at the beginning of the observation period and after one year (C1, C2), a significant difference was found only in the left CorT measurement (p < 0.05).

To evaluate the efficiency of the treatment, ΔT (∆T = T2−T1) and ΔC (∆C = C2−C1) were compared using the independent t-test. It was noted that there was no significant difference between the groups in relation to the changes in FD and CorT values (Table III).

Comparisons of T1–T2 (Pretreatment – Posttreatment) and C1–C2 (Precontrol – Postcontrol) with independent t-test.

ΔT (Mean±SD) ΔC (Mean±SD) p value
Processus condylaris (R) 0.048 ± 0.118 0.030 ± 0.155 0.677
Antegonial notch (R) 0.045 ± 0.198 0.012 ± 0.135 0.606
Ramus mandible (R) 0.006 ± 0.151 −0.004 ± 0.195 0.861
Cortical thickness of the mandible (R) 0.187 ± 0.343 0.125 ± 0.209 0.566
Processus condylaris (L) 0.059 ± 0.149 0.028 ± 0.179 0.56
Antegonial notch (L) 0.018 ± 0.148 0.028 ± 0.139 0.845
Ramus mandible (L) 0.035 ± 0.172 0.007 ± 0.149 0.621
Cortical thickness of the mandible (L) 0.163 ± 0.365 0.200 ± 0.307 0.761

R: right, L: left, SD: indicates standard deviation, ΔT: T2−T1, ΔC: C2−C1.

Discussion

A functional orthopaedic approach is a common treatment option to manage a skeletal dysplasia. Treatment using a functional appliance primarily aims to enhance mandibular growth. However, there have been contradictory opinions regarding the treatment effects. While some believe that skeletal mandibular changes occur as a result of functional treatment811,13, others are of the opinion that the effect is substantially dentoalveolar.2,4

The present study aimed to investigate the effects of mandibular protraction appliances (monoblock and twin-block) on mandibular bony structure using FD analysis and CorT measurements. As it has been shown that the monoblock and twin-block appliances have identical effects on mandibular growth,23 the treatment group included patients managed with either appliance.

In the present study, even if some favourable effects might have been earlier observed, the patients wore the monoblock or twin-block appliances for at least 16 hr per day for a standard period of one year as documented in the patient charts. A corrective effect was evident and all patients were eligible for subsequent fixed appliance therapy. Pre- and post-treatment panoramic films were evaluated in order to track the likely effects of functional appliance treatment on the structure of the mandibular bone.

It has been stated that trabecular bone has higher metabolic activity than cortical bone, and is therefore more suitable for evaluating bony changes.24 Fractal Dimension analysis, as a mathematical concept, proved to be an efficient and exacting way of evaluating trabecular bone changes on radiographs.16,22,24,25 It has been shown that FD provides a better assessment and outcome in the determination of bone mineral density (BMD) and the prediction of fracture risk in osteoporotic patients.26

A limited number of studies using FD analysis have been published in the orthodontic literature. Arsan et al. evaluated FD analysis in an examination of osteoarthritic changes in patients with temporomandibular joint disorders.27 Rothe et al. used CorT and FD measurements in relapse assessment after orthodontic treatment,28 while Heo et al. examined bone healing after orthognathic surgery using FD analysis. Increased bony activity was detected along with changes in bone architecture in the surgical areas.29 It has been suggested that, rapid palatal expansion success might be predicted via fractal analysis, which can quantitively and objectively be used to evaluate mid-palatal suture maturation.30 In a recent study, Ok and Kaya31 used fractal analysis to assess the skeletal and dental effects of rapid maxillary expansion. Amuk et al.,32 in an investigation of the effects of the Herbst appliance on mandibular trabecular structure by fractal analysis, found that the supero-anterior and central parts of the condyles were affected differently but the structural complexity of the mandibular angle did not change. Recently, Cesur et al. conducted a similar study to test the effectiveness of functional treatment using FD measurement of the condyle, mandibular angle and mandibular corpus to compare with a Class I control group. Significant changes were found in the trabeculation of the mandibular condyle after functional orthopaedic treatment.21 However, in the present study, although FD measurement of both condylar processes increased significantly after functional treatment, no statistically significant differences were found in comparison with the control group. Unlike Cesur et al., a Class II control group was used which may be responsible for this inconsistency. Moreover, the current control group was almost one year younger than the treatment group, and therefore a possible therapeutic effect in the treatment group may have been counterbalanced by rapid growth in the control group.

CorT measurement, which is claimed to reflect overall bone mass and density20,28 was also found to be very similar between functional treatment and the control group in the present study. Therefore, the results imply that mandibular protraction appliances (monoblock and twin-block) do not significantly affect mandibular trabecular nor cortical structure when compared to a Class II control group. Within the limitations of the present investigation, it may be inferred that, functional appliance therapy does not produce skeletal changes and the effect of these appliances may substantially be confined to the dentoalveolar level.

Conclusions

Although FD of both condylar processes and bilateral CorT values increased significantly in the study group after functional appliance therapy, no significant differences were found when treatment and control groups were compared. Monoblock and Twin block appliances did not alter the bony structure of the mandibular condyles, the antegonial notch and ramus regions as determined by fractal dimension analysis.

Author contributionsBarcın Eroz Dilaver conceived the ideas; Barcın Eroz Dilaver collected the datas; Dilara Nil Gunacar assessed and analysed the data, Barcın Eroz Dilaver led the writing. Ali Kiki edited the article. All authors approved the final form of the manuscript.

Availability of data and material: all data can be made available if required.

Conflicts of interestThe authors declare no conflicts of interest.

Ethics approvalThe study design was approved by the Ethics Committee of the X University Faculty of Medicine.

Consent for publicationAll authors consent for publication.

eISSN:
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Medicine, Basic Medical Science, other