Efficiency evaluation of rapid maxillary expansion treatment on nasal septal deviation using tortuosity ratio from cone-beam computer tomography images

Efficiency evaluation of rapid maxillary expansion treatment on nasal septal deviation using tortuosity ratio from cone-beam computer tomography images

Efficiency Evaluation of Rapid Maxillary Expansion Treatment on Nasal Septal Deviation using Tortuosity Ratio from Cone-Beam Computer Tomography Image...

3MB Sizes 0 Downloads 182 Views

Efficiency Evaluation of Rapid Maxillary Expansion Treatment on Nasal Septal Deviation using Tortuosity Ratio from Cone-Beam Computer Tomography Images

Journal Pre-proof

Efficiency Evaluation of Rapid Maxillary Expansion Treatment on Nasal Septal Deviation using Tortuosity Ratio from Cone-Beam Computer Tomography Images Gokcenur Gokce, Ilknur Veli, Yilmaz Kemal Yuce, Yalcin Isler PII: DOI: Reference:

S0169-2607(19)31434-8 https://doi.org/10.1016/j.cmpb.2019.105260 COMM 105260

To appear in:

Computer Methods and Programs in Biomedicine

Received date: Revised date: Accepted date:

26 August 2019 12 November 2019 2 December 2019

Please cite this article as: Gokcenur Gokce, Ilknur Veli, Yilmaz Kemal Yuce, Yalcin Isler, Efficiency Evaluation of Rapid Maxillary Expansion Treatment on Nasal Septal Deviation using Tortuosity Ratio from Cone-Beam Computer Tomography Images, Computer Methods and Programs in Biomedicine (2019), doi: https://doi.org/10.1016/j.cmpb.2019.105260

This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier B.V.

HIGHLIGHTS • The measure of tortuosity ratio is used to evaluate the efficiency of rapid maxillary expansion on improving the nasal septal deviation. • A new Matlab application was developed to measure nasal septal deviations from Cone-beam computer tomography images. • Changes in nasal septal deviation were measured before the rapid maxillary expansion treatment (T0), just after the treatment (T1), and 3 months after the treatment (T2). • Statistically significant differences were observed between T0-T1 and between T0-T2 using the ANOVA test. • There is no statistically significant difference obtained between T1-T2 times.

1

Efficiency Evaluation of Rapid Maxillary Expansion Treatment on Nasal Septal Deviation using Tortuosity Ratio from Cone-Beam Computer Tomography Images

Gokcenur Gokce a Ilknur Veli a Yilmaz Kemal Yuce b Yalcin Isler c,∗ a Izmir

Katip Celebi University, Faculty of Dentistry, Department of Orthodontics, Cigli, Izmir, Turkey

b Alanya

Alaaddin Keykubat University, Rafet Kayis Faculty of Engineering,

Department of Computer Engineering, Alanya, Antalya, Turkey c Izmir

Katip Celebi University, Faculty of Engineering and Architecture,

Department of Biomedical Engineering, Cigli, Izmir, Turkey

Abstract Background and Objective: This study aims to assess the effect of Rapid Maxillary Expansion (RME) on Nasal Septal Deviation (NSD) changes from three-dimensional (3D) images. Methods: In this study, cone-beam computed tomography (CBCT) images from 15 patients with maxillary constriction (mean age 12 ± 1.6 years) were included. RME treatment with Hyrax appliance was performed in all patients. CBCT scans were taken at three different times; before appliance insertion (T0), after active expansion (T1) and 3 months after appliance insertion (T2). We developed a novel Matlab-based application to quantify NSD based on the tortuosity ratio by

Preprint submitted to Computer Methods and Programs in Biomedicine3 December 2019

dividing the actual length of the septum by the ideal length in the mid-sagittal plane by using this application. Results: Tortuosity ratio (TR) values were found as 1.03 ± 0.03 (T0), 1.02 ± 0.02 (T1), and 1.02 ± 0.02 (T2). Differences of TR values among these groups were evaluated using the statistical method of ANOVA (ANalysis Of VAriance) for repeated measures with the significance level of p < 0.05. Results showed significant reductions in TR values between T0-T1 (p < 0.05) and between T0-T2 (p < 0.05). Nonetheless, a significant difference between T1-T2 was not determined (p > 0.05). Conclusions: As a result, we can conclude that the NSD degree is affected by the RME treatment. The developed application can be used for both educational and research purposes. Key words: Nasal septal deviation, Rapid maxillary expansion, Cone-beam computed tomography, Tortuosity ratio, Matlab application.

1

1.1

INTRODUCTION

Nasal Septal Deviation

The nasal septum is a separating wall that divides the nasal cavity into two halves [1]. The nasal septum, which is composed of cartilage and bone tissues, provides the underlying structure of the nose and gives its shape [2]. It also plays a significant role in the downward and forward displacement of the maxilla [3,4]. Enlow [5] stated that the nasal septum is still considered as the ∗ Corresponding author. Email addresses: [email protected] (Gokcenur Gokce), [email protected] (Ilknur Veli), [email protected] (Yilmaz Kemal Yuce), [email protected] (Yalcin Isler).

3

symbol for the force that causes displacement of the nasomaxillary complex even if the growth process is multifactorial. On the other hand, Moss et al. [6,7] advocated that the nasal septum had an only passive role in the displacement of the maxilla and functional matrix mechanism in relation with expanding nasal septum is just responsible for the forward and downward displacement of the maxilla. Therefore, the role of the nasal septum on craniofacial growth is controversial. Nasal septal deviation (NSD), is one of the most common nasal diseases, is defined as the deflection to one or both sides of the bone or septum cartilage at varying degrees [8]. The incidence of NSD has been reported about 19.4%-65% [9,10] and intrauterine pressures and trauma from birth are regarded as one of the leading reasons for NSD [11]. Even about 80% rate at some degree of deviation has been encountered when adult skulls of more than one ethnicity were evaluated [11]. Analysis of ethnic backgrounds has revealed an increased prevalence of septal deviation in Caucasian children compared to African children [12]. Some researchers have reported that the variation in the incidence is caused by the difference in the definition of the deviations [13]. Stallman et al. [10] classified deviations as mild, moderate, or severe. However, Smith et al. [9] described it as a deflection of more than 4 mm from the midline. From a rhinological aspect, the NSD raises the nasal airway resistance on the affected side and poses a crucial problem that leads to asymmetric airflow in the nasal cavity [14,15]. Some common dental problems like narrow maxilla and posterior crossbite associated with mouth breathing [16] lead to an increase in rhinological diseases such as upper airway infections, sinusitis, and obstructive sleep apnea syndrome [17,18]. On the other hand, some controversial studies found no statistically significant relationships between the dimension and the 4

morphology of upper airways and skeletal malocclusion [19]. The potential effect of NSD on craniofacial growth in childhood is still a challenging issue. D’Ascanio et al. [20] compared skeletal and dental features in children with chronic nasal-breathing obstruction secondary to NSD and nose-breathing controls in their multicenter cephalometric study. They reported that mouth-breathing children show both skeletal and dental anomalies in comparison to the nose-breathing control group.

1.2

Nasal Septal Deviation and Rapid Maxillary Expansion Treatment

Angell [21] described the mechanical principals of widening the arch using rapid maxillary expansion (RME). Widening the arch is a standard technique to correct the transverse maxillary deficiency of children and adolescents in orthodontic treatment. During the expansion, lateral forces from the RME appliance separate mid-palatal suture [22], affect lateral nasal walls and increase of nasal cavity dimensions [23]. The positive effect of RME treatment on NSD was firstly reported in 1975 by Gray [24]. More recently, Farronato et al. [25] and Maspero et al. [26] treated children with a transverse maxillary deficiency with RME and reported a 94% reduction in NSD. Although there are many studies about the effect of RME on the dimensions of the nasal cavity and airway [27,28,29,30,31], only a few authors evaluated the changes in the nasal septum following to the RME.Furthermore, most studies used two-dimensional (2D) images only, instead of three-dimensional (3D) images, in cephalometric analysis to assess the NSD changes produced by RME in the literature. 5

1.3

Use of Cone-Bean Computed Tomography

Cone-beam computed tomography (CBCT) is one of the medical imaging techniques based on X-rays. In this technique, the X-rays are applied in different ways to form a conic shape [33]. CBCT has been a very common imaging technique due to its advantageous including reasonably high-quality, relatively lower exposing radiation, low-cost, appreciable easy-to-access among other 3D imaging techniques [35]. From its invention, it takes a substantial role in different applications in the field of implant dentistry [35], endodontics [34], ear-nose-throat [25,26,32,42,40], orthopedics [36], and interventional radiology (IR) [37], image-guided radiation therapy (IGRT) [38], and many other medical applications. Besides, the CBCT has become the gold standard in dentistry. It is very useful in imaging the oral and maxillofacial area [39].

Professional dentists can notice maxillary sinuses even in 2D images easily. On the other hand, they are able to capture all sinuses and nasal cavity by using high-quality CBCT scans [41]. Also, they can diagnose anatomic variants of the deviated nasal septum, concha bullosa, and paradoxical turbinate.

In a recent review article, the authors investigated the quality of CBCT studies for evaluating the effects of RME treatment on upper airway morphology. They scanned 1088 articles from the literature that are published before the end of 2016. They focused only on CBCT studies based on visualizing the upper airway before and after an RME treatment. The mean quality score of these studies is 50% (ranged from 36% to 68%). They emphasized the inconsistency in CBCT protocols including the head posture, the tongue position, and segmentations. They concluded a requirement of a validated and consistent 6

protocol [32].

Shokri et al studied CBCT scans to explain anatomical variations of the nasal cavity and ethmoidal sinuses. They evaluated 250 CBCT scans in their study. They concluded that operating surgeons and radiologists must be careful about the nasal region before the operation to avoid complications after the operation [42]. In another study, Mudgade et al. [40] investigated the existence of anatomic variations in maxillary sinuses. They evaluated CBCT images acquired from 150 subjects. They reported that the precise assessment of maxillary sinuses is very important to prevent non-essential surgical operations [40].

1.4

Aim of the Study

This study aimed to evaluate the changes of NSD following RME, using tortuosity ratio measured from three-dimensional (3D) images that are acquired by a cone-beam computed tomography (CBCT). For this purpose, we developed a novel Matlab application to analyze 3D images and constituted the null hypothesis as there was no significant effect (or difference) of RME treatment on the degree of NSD. 7

2

2.1

MATERIALS AND METHODS

Data

This retrospective study satisfied all ethical obligations. Ethical permission was confirmed by the Health Research Ethics Board at Izmir Katip Celebi University (IKCU). A total of 15 patients whose ages ranged from 11 to 14 years (six male and nine female) were selected from the archive of Department of Orthodontics in the Faculty of Dentistry at IKCU. All patients had a bilateral posterior crossbite and their septal deviations were detected with a medical history, endoscopic nasal examination by the same otolaryngologist. The exclusion criteria were previous nasal surgery, history of rhinitis, any disease in the nose, use of topical steroids, presentation of nasal polyps, any pathology in the nose, or having severe skeletal asymmetry [44,45].

All patients had undergone RME treatment with a Hyrax appliance. Treatments were continued up to achieving posterior dental crossbite overcorrection by 20% (maxillary lingual cusps overlapping with lingual inclines of mandibular buccal cusps). The appliance consisted of a mid-palatal jackscrew assemblage with four rigid steel wires. These wires were soldered to the bands of the first premolars and the first molars. The jackscrew was screwed one quarter-turn twice a day. After an average of 2 weeks of expansion, the screw was fixated with a composite resin placed into the turn-key mechanism of the appliance. This had been retained for three months since the fixation time.

CBCT scans were taken at IKCU, Department of Maxillofacial Radiology at three different times: T0 (at baseline, before expansion) and T1 (after 8

active expansion, i.e. the fixation time of the screw), and T2 (after appliance removal). All images were acquired by Newtom 5G (QR, Verona, Italy) scanner yielding high-resolution reconstructions of the examined anatomical structure. All patients were located in a horizontal position. The Frankfort horizontal plane was set perpendicular to the table and patients’ head was placed into the circular gantry housing the X-ray tube. The X-ray tube detector system performed a 360◦ rotation around the head. In addition, the following parameters were chosen for exposure: the maximum output of 110 kV, 1-20 mAs with 18x16 field of view (FOV), standard resolution mode (0.25 mm voxel size) and a typical exposure time of 3.6 seconds. Also, we adjusted the contrast and brightness of images using the image-processing tool provided in the standard software of the equipment to ensure an optimal visualization. The coronal views in CBCT sections were formed in the sensitivity of 0.15 mm. The coronal images were investigated to determine the slices in which the septal body was typically seen bilaterally and the most prominent [46].

2.2 The Metric: Tortuosity Ratio

Tortuosity ratio (TR), or Tortuosity factor, is defined as the ratio of the actual distance traveled between two points (Lactual ), including any curves encountered, divided by the straight line distance (Lideal ) (Fig. 1) [49]. TR can be calculated by using TR =

Lactual Lideal

(1)

TR is used to define the degree of NSD [48], to evaluate flow and diffusion properties in chemical mediums [49], to find ethnical factors on the intracranial 9

Fig. 1. Tortuosity ratio is the ratio of the actual length (Lactual ) to the ideal length (Lideal ).

artery in stroke [50], to quantify optic nerve in thyroid eye disease [51], etc. For this study, NSD was evaluated by calculating the tortuosity ratio. TR values were calculated from both the actual length and the ideal length of the septum [47]. The ratio gives a quantitative measurement of NSD from the midline at each identified landmark in coronal images [48]. Septal deviation (i.e. actual length which was the length of the superior aspect to the inferior aspect of the septum) was assessed at two different levels in coronal view: (1) At Crista Galli, and (2) at Anterior Nasal Spine, and traced in entirety from superior to inferior direction by placing points 1-2 mm apart [48].

2.3

Matlab Application for Computing Tortuosity Ratio

MATLAB, which is the abbreviation of Matrix Laboratory, is a programming environment for especially engineering studies. MATLAB applications are written to perform some technical computations. These applications are incorporated into many MATLAB products. They consist of a graphical user interface (GUI), code that performs the underlying actions, associated data, and any other supporting files. MATLAB App Builder tool [66] helps to package the developed application into a single file so that the developer can share with other users. Besides, developers can share their applications with the community 10

by uploading them to the official website of Mathworks File Exchange [67]. When other users install the application, they do not need to concern with the MATLAB path or other installation details [68]. In this study, an application was developed in MATLAB (Matrix Laboratory) to trace the distance and to calculate the NSD. The program is a script file so that it requires MATLAB installed on the user’s computer (Fig. 2). The source code of the program consists of 521 lines. When it runs, an empty main page is screened. The main page consists of Find Directory, Zoom, Measure, Maximize, and Export commands (Fig. 3).

Fig. 2. The Matlab interface.

By using the button of Find Directory, the user chooses the folder that contains 3D CBCT images (Fig. 4). These images will be shown on the screen (Fig. 5). The selected folder is shown at the bottom edge of the user interface aligned to the middle. The slice numbers of the active view from axial, sagittal, and coronal axes are shown at the bottom right of the main screen. User can change the active slice by keys of Page Up and Page Down. The Page Up key decreases the active slice number and the Page Down key increases it. 11

Fig. 3. The main page with no loaded image.

Fig. 4. The window to select a folder that contains the DICOM images.

The Maximize command enlarges the active view while other views remain in default size (Fig. 6). The Zoom command zooms in the selected view or zooms out default size (Fig. 7). After zooming the selected view (Fig. 8), the user can zoom out to the default size by right-clicking on the image. After clicking the Measure command, it calculates the distance between each click on the left button of the mouse (Fig. 9). When the user clicks the right 12

Fig. 5. The main page with a loaded image.

Fig. 6. The main page with the maximized view of the image.

button of the mouse on the view, it reports the total distance on the screen. The Export command exports the measurements to a Microsoft Excel file. 13

Fig. 7. The zoom-in option.

Fig. 8. The zoomed image.

2.4

Statistical Analysis

In an attempt to test the magnitude of the measurement error in this study, all of the CBCT scans were randomly selected and were re-evaluated by the same operator (IKCU) four weeks after the first measurements, which were so-called the first measure and the second measure throughout the paper. 14

Fig. 9. The NSD calculation.

The normality of the data should exist to apply many statistical tests. The normality test of Shapiro-Wilk can be applied for this purpose. When the p-value is higher than 0.05, the distribution of the data is assumed as normal. After the normality is guaranteed, the other tests can be used [69]. Then, the reliability of the data should be tested using the Intra-Class Correlation (ICC) test. Similarly, if the p-value of this test is less than 0.05, this test is determined as significant. If the test result (p) of a group is less than 0.05, this group can be assumed as unreliable. In such a case, the study should be repeated and a new data should be collected again. Also, the paired t-test is used to determine whether a statistically significant difference between the first measure and the second one. If the test value (p) of a pair of measures is less than 0.05, this measure can be assumed as unreliable too, which means the similar TR values cannot be obtained from the same figures. After the normality and the reliability are guaranteed, we can use the Analysis of variance (ANOVA) for repeated measures test to compare the differences 15

of TR values among the time intervals (T0, T1, and T2). If the p-value of the ANOVA test is less than 0.05, there is a statistically significant difference among periods. While applying the ANOVA tests, the homogeneity of each group should also be tested. If the p-value of the homogeneity test is greater than 0.05, then the homogeneity of groups is accepted and the test result of ANOVA is meaningful. But ANOVA test cannot indicate which period(s) differ(s) from others. In this case, a post-hoc test should be used to determine differences among periods. To determine the statistical differences of TR among groups, multiple comparisons using the Bonferroni test are conducted. If a p-value of any two groups is less than 0.05, there is a statistical difference between these two groups. Otherwise, there is no significant difference between these groups if the p-value is higher than 0.05. To determine the reliability of the data and statistically significant differences of the changes in TR among the periods (T0, T1, and T2), the Statistical Package for Social Sciences software package (SPSS for Windows, version 25.0, SPSS Inc, Chicago, USA) is used to apply all these statistical tests in this study.

3

3.1

RESULTS

Experimental Results

All NSD measurements were performed on an aforementioned computer program. It can compute TR and enables its user to methodically trace and analyze 16

measurements. In this study, all TR measurements were carried out by two operators from IKCU. The NSD measurements (Fig. 10) from MATLAB application were transferred to an Excel spreadsheet to simplify statistical analysis (Table 1).

Fig. 10. The ratio is a definite measurement of the degree of septal deviation where the ratio is calculated using the actual and the ideal lengths.

3.2

Results of Statistical Analysis

The normality test of Shapiro-Wilk was applied to the data. Since the calculated p-value was 0.074 ¿ 0.05, the data has the normal distribution. Therefore, we can use statistical tests of ICC, paired t-test, and ANOVA. 17

Table 1 Tortuosity ratios at T0, T1, and T2 for each subject. Each value shows the mean of obtained values by two expert orthodontists. Subject

Gender

T0

T1

T2

1

M

1.0655

1.0240

1.0490

2

M

1.0210

1.0150

1.0160

3

M

1.0170

1.0175

1.0135

4

M

1.0065

1.0040

1.0045

5

F

1.0040

1.0040

1.0055

6

F

1.0300

1.0250

1.0225

7

M

1.0055

1.0030

1.0020

8

M

1.0170

1.0080

1.0045

9

F

1.0075

1.0080

1.0085

10

F

1.0280

1.0205

1.0160

11

M

1.0265

1.0280

1.2005

12

F

1.0035

1.0035

1.0020

13

M

1.1065

1.0720

1.0825

14

M

1.0055

1.0020

1.0045

15

F

1.0055

1.0065

1.0050

ICC tests were conducted, all ICCs were found high for all measurements (Table 2). Since p values of these ICC measures are less than 0.05, there is a consistency in measurements of all patients for each period (T0, T1, and T2). Besides, since p values (the last column of the table) from paired t-test are not less than 0.05, there are no significant differences between the repeated two measures. Consequently, good reliability of the data was confirmed, which means we can use ANOVA test and multiple comparisons to determine statistical significant differences among periods. 18

Table 2 Intra-class correlation (ICC) measures of tortuosity ratio (TR) values and paired t-test results of two measures at different times. T0, T1, and T2 values are given as the mean value ± standard deviation. Measure

ICC

p

The first measure

The second measure

p

T0

0.992

<0.001

1.0244±0.0289

1.0222±0.0276

0.095

T1

0.949

<0.001

1.0154±0.0192

1.0167±0.0174

0.542

T2

0.944

<0.001

1.0167±0.0174

1.0193±0.0235

0.321

Descriptive statistics, including mean and standard deviation, of TR values and ANOVA comparisons were shown in Table 3. TR values were found as 1.03 ± 0.03 (T0), 1.02 ± 0.02 (T1), and 1.02 ± 0.02 (T2), respectively at three different times. ANOVA comparisons revealed that there was a statistically significant difference in NSD according to T0-T1 (p=0.03) and T0-T2 (p=0.01). Also, there was no statistically significant difference between T1-T2 (p=1.00) (Table 3). Thanks to these results, the null hypothesis was rejected since the differences in the degree of septal deviation were proved among periods after the RME treatment. Table 3 Statistical comparison of tortuosity ratio using repeated-measures ANOVA. T0, T1, and T2 values are given as the mean value ± standard deviation. † p < 0.05 shows that there exists a statistically significant difference among groups. ‡ p < 0.05 shows that these groups are statistically different.

Tortuosity ratios

T0

T1

T2

p

1.03±0.03

1.02±0.02

1.02±0.02

0.00†

post-hoc test of the T0–T1

0.03‡

post-hoc test of the T0–T2

0.01‡

post-hoc test of the T1–T2

1.00

19

3.3

Matlab Application

Two experts used the aforementioned application. They reported that the developed application can be used for both educational and research purposes. Our research group aimed to develop computer programs to analyze neuronal behaviors [70,71] previously. This application will be sent via email upon any request from readers.

4

DISCUSSION

The potential role of nasal respiration is important in the development of the craniofacial complex [52]. Moderate to severe NSD is one of the significant reasons for nasal obstruction which can cause an unfavorable response to the growth of craniofacial structures [52]. Moss et al. [6,7] noted that the functional matrix mechanism by expanding nasal septal structures had an active role in the forward and downward displacement of the maxilla. Thus, this retrospective study aimed to evaluate the effect of RME treatment on NSD in 3D. Due to the complexity and a large number of anatomical structures in the nasal region, 2D techniques suffer from the superimposition of all structures that lie in the path between the X-ray source and the film or detector [53]. With the recent widespread introduction of CBCT, dentists and otolaryngologists are better able to identify anatomical abnormalities and pathological conditions within the structures of the nasal cavity and the surrounding paranasal sinuses [54]. In the current study, the degree of the septal deviation was analyzed based on 3D measurements on CBCT. 20

Reitzen et al. [47] concluded that NSD occurs at a higher frequency in older children and adults when calculations of tortuosity are used as a measure. According to the literature, after the age of 20, the prevalence of nasal septum deformities does not change [55]. It is connected with the end of the development of the nasomaxillary complex and a lower number of nasal injury after this age. To eliminate the growth of the nasomaxillary complex, non-growing patients were included in the current study. Furthermore, patients with craniofacial syndromes or history of orthodontic treatment and/or facial trauma and/or were excluded from the study, since these factors directly influence the pattern of facial development [56,57]. For the evaluation of the degree of septal deviation, different protocols have been introduced in the literature [58]. When the literature is reviewed, a single test is not defined as the gold standard in the diagnosis of septal deviation. The diagnosis of NSD is usually determined after assimilating the patient’s history, physical examination of the nose, and information collected from a variety of sources, including anterior rhinoscopy, nasal endoscopy, and imaging [59]. Surgery should be supported by a diagnosis based on objective tests and criteria. Anterior rhinoscopy and nasal endoscopy can detect the location and severity of NSD, but it is an uncomfortable test for patients [59,60]. Imaging studies such as CBCT scans and MRIs may provide an accurate three-dimensional diagnosis of NSD [59,60]. In the present study, the degree of tortuosity measurement was used to compare the deviated septum’s length to the optimum straight septum’s length on CBCT images. This measurement method was proper to the aim of our study because it did not include nasal pathology such as turbinate hypertrophy. Aziz et al. [48] also developed a Matlab program to calculate reliable TR 21

measurements of NSD. They evaluated CBCT scans to measure changes in NSD with MATLAB after RME treatment in adolescent patients. Researchers concluded that there were no significant changes in NSD after RME treatment. However; in the present study, the degree of NSD was reduced after RME. The reasons for the differences in the findings of both studies are thought to be caused by differences in the measured CBCT sections and RME treatment protocol. Numerous studies have focused on the effect of RME on the nasal structures [52]. Some of such studies are computational fluid dynamic studies by Liu et al. [13] and Garcia et al. [61]. Researchers investigated the relationship between septal deviation and air resistance after RME treatment. They reported that septal deviations which occur in the anterior and inferior part of the septum increase nasal resistance more than posterior and superior septal deviations. As a result, significant septal deviations may occur in the posterior nasal cavity without a significant increase in nasal airway resistance [61]. Rapid maxillary expansion affects the nasal airway because it is thought to modify the nasal valve region representing the narrowest nasal sectional area [62]. While there are many studies about the effects of RME on the nasal airway, only a few of those have reported that RME reduces the degree of the septal deviation [24,25,26,30,63]. Gray [24] analyzed posteroanterior (PA) radiographs to identify the changes in the curve of NSD. They reported correction of the deviation visually instead of a percentage. In another study, the researcher found similar results and reported corrected septal deviation after RME [64]. As opposed to our study, Schwarz et al. [64] examined nine adult patients with transverse maxillary deficiency to evaluate the incidence of NSD after surgically assisted rapid maxillary expansion (SARME) with 3D images. Coronal 22

scans were taken before and 4 months after the surgical procedure. Researchers concluded that there was no significant change in the nasal septal position from before to after SARME. This is parallel to the conclusions of Aziz et al. [48] who used CBCT scans to analyze changes in NSD after RME treatment with bone-anchored maxillary expansion apparatus. They calculated tortuosity and didn’t identify significant changes in NSD following RME. In our study, unlike Aziz et al. [48], tooth-borne Hyrax appliance was used during RME treatment. NSD degrees of patients before treatment were also different. So, we believe that these may lead to differences in the results obtained. Due to the lack of similar studies that associate the changes in the NSD after RME with 3D images, we couldn’t compare our findings directly with the earlier publications. It would be beneficial to plan further studies with the elimination of some other factors such as nasal pathology and growth as much as possible for the evaluation without any contributing factors. Since septal deformities can affect the growth and development of the maxilla, Subaric and Mladina [65] recommended the examination of the nasal septum by a rhinologist who will be a part of a team performing the regular systematic health examination of children.

5

CONCLUSION

In conclusion, this study considers a pre-selection of subjects with maxillary deficiency and investigates a possible relationship between the degree of deviation (tortuosity ratio) and RME. Furthermore, there was a positive relationship between RME and NSD and this relationship seems stable after 3 months. However, the results should be interpreted carefully due to the small sample 23

size and large variation amongst individual patient characteristics.

Acknowledgment

This retrospective study satisfied all ethical obligations. Ethical permission was confirmed by the Health Research Ethics Board at Izmir Katip Celebi University (IKCU) with the additional confirmation of the Ministry of Health by August 08, 2016.

Conflict of Interest Statement

None declared.

References

[1] Sandham A, Murray JA. Nasal septal deformity in unilateral cleft lip and palate. Cleft Palate Craniofac J 1993; 30: 222-226. [2] Swenson KE. Nasal septal deviation in a longitudinal growth sample. Thesis. University of Iowa, 2012. [3] Babula Jr WJ, Smiley GR, Dixon AD. The role of the cartilaginous nasal septum in midfacial growth. Am J Orthod 1970; 58: 250-263. [4] Scott JH. The analysis of facial growth from fetal life to adulthood. Angle Orthod 1963; 33: 110-113. [5] Enlow DH. Facial Growth. 3rd ed, Philadelphia: WB Saunders Company, 1990.

24

[6] Moss ML, Bromberg BE, Song IC, Eisenman G. The passive role of nasal septal cartilage in mid-facial growth. Plast Reconstr Surg 1968; 41: 536-542. [7] Moss ML, Salentijn L. The primary role of functional matrices in facial growth. Am J Orthod Dentofacial Orthop 1969; 55: 566-577. [8] Orlandi RR. A systematic analysis of septal deviation associated with rhinosinusitis. Laryngoscope 2010; 120: 1687-1695. [9] Smith KD, Edwards PC, Saini TS, Norton NS. The prevalence of concha bullosa and nasal septal deviation and their relationship to maxillary sinusitis by volumetric tomography. Int J Dent 2010; pii: 404982. [10] Stallman JS, Lobo JN, Som PM. The incidence of concha bullosa and its relationship to nasal septal deviation and paranasal sinus disease. Am J Neuroradiol 2004; 25: 1613-1618. [11] Gray LP. Deviated nasal septum, incidence and etiology. Ann Otol Rhinol Laryngol Suppl 1978; 87: 3-20. [12] Mooney

MP,

Siegel

MI.

Developmental

relationship

between

premaxillary-maxillary suture patency and anterior nasal spine morphology. Cleft Palate J 1986; 23: 101-107. [13] Liu T, Han D, Wang J, Tan J, Zang H et al. Effects of septal deviation on the airflow characteristics using computational fluid dynamics models. Acta otolaryngologica 2012; 132: 290-298. [14] Bayerlein T, Proff P, Koppe T, Fanghaenel J, Hosten N. Cartilaginous septum deviation in children with cleft lip, alveolus and palate-an MRI analysis. J Craniomaxillofac Surg 2006; 34: 49-51. [15] Chen XB, Lee HP, Chong VF, Wang Y. Assessment of septal deviation effects on nasal air flow: a computational fluid dynamics model. Laryngoscope 2009; 119: 1730-1736.

25

[16] Vig KW. Nasal obstruction and facial growth: the strength of evidence for clinical assumptions. Am J Orthod Dentofacial Orthop 1998; 113: 603-611. [17] Ishikawa Y, Kawano M, Honjo I, Amitani R. The cause of nasal sinusitis in patients with cleft palate. Arch Otolaryngol Head Neck Surg 1989; 115: 442-446. [18] Josephson GD, Levine J, Cutting CB. Septoplasty for obstructive sleep apnea in infants after cleft lip repair. Cleft Palate Craniofac J 1996; 33: 473-476. [19] Di Carlo G, Polimeni A, Melsen B, Cattaneo PM. The relationship between upper airways and craniofacial morphology studied in 3D: A CBCT study. Orthod Craniofac Res 2015; 18: 1-11. [20] D’Ascanio L, Lancione C, Pompa G, Rebuffini E, Mansi N et al. Craniofacial growth in children with nasal septum deviation: a cephalometric comparative study. Int J Pediatr Otorhinolaryngol 2010; 74: 1180-1183. [21] Angell EH. Treatment of irregularity of permanent adult teeth. Dent Cosm 1860; 1: 540-554. [22] Haas AJ. The treatment of maxillary deficiency by opening of the midpalatal suture. Angle Orthod 1965; 35: 200-217. [23] Warren DW, Hershey HG, Turvey TA, Hinton VA, Hairfield WM. The nasal airway following maxillary expansion. Am J Orthod Dentofacial Orthop 1987; 91: 111-116. [24] Gray LP. Results of 310 cases of rapid maxillary expansion selected for medical reasons. J Laryngol Otol 1975; 89: 601-614. [25] Farronato G, Giannini L, Galbiati G, Maspero C. RME: influences on the nasal septum. Minerva Stomatol 2012; 61: 125-134. [26] Maspero C, Galbiati G, Del Rosso E, Farronato M, and Giannini L. RME: effects on the nasal septum. A CBCT evaluation. Eur J Paediatr Dent 2019;

26

20(2): 123-126. [27] Enoki C, Valera FC, Lessa FC, Elias AM, Matsumoto MA et al. Effect of rapid maxillary expansion on the dimension of the nasal cavity and on nasal air resistance. Int J Pediatr Otorhinolaryngol 2006; 70: 1225-1230. [28] Kilic N, Oktay H. Effects of rapid maxillary expansion on nasal breathing and some naso-respiratory and breathing problems in growing children: a literature review. Int J Pediatr Otorhinolaryngol 2008; 72: 1595-1601. [29] Baratieri C, Alves M Jr, Souza MM, Araujo MTS, Maia LC. Does rapid maxillary expansion have long-term effects on airway dimensions and breathing? Am J Orthod Dentofacial Orthop 2011; 140: 146-156. [30] Bicakci AA, Agar U, Sokucu O, Babacan H, Doruk C. Nasal airway changes due to rapid maxillary expansion timing. Angle Orthod 2005; 75: 1-6. [31] Baccetti T, Franchi L, Cameron CG, McNamara JA. Treatment timing for rapid maxillary expansion. Angle Orthod 2001; 71: 343-350. [32] Di Carlo G, Saccucci M, Ierardo G, Luzzi V, Occasi F et al. Rapid maxillary expansion and upper airway morphology: a systematic review on the role of cone beam computed tomography. BioMed Research International 2017; 2017: 1-10. [33] Scarfe WC, Farman AG, Sukovic P (February 2006). ”Clinical applications of cone-beam computed tomography in dental practice”. Journal of the Canadian Dental Association. 72 (1): 7580. [34] American Association of Endodontists. Cone Beam-Computed Tomography in Endodontics. 2011. Retrieved October 21, 2019 from www.aae.orgcolleagues [35] Palomo JM, El H, Stefanovic N, Bous R, Elshebiny T. Treatment Planning, Outcome Assessment, and Upper Airway Imaging Using CBCT in Clinical

27

Orthodontics. In: Kadioglu O., Currier G. (eds) Craniofacial 3D Imaging. Springer, Cham, 2019. [36] Barg A, Bailey T, Richter M, de Cesar Netto C, Lintz F, Burssens A, Phisitkul P, Hanrahan CJ, and Saltzman CL. Weightbearing Computed Tomography of the Foot and Ankle: Emerging Technology Topical Review. Foot Ankle Int 2018; 39(3): 376386. [37] Orth RC, Wallace MJ, Kuo MD. C-arm cone-beam CT: general principles and technical considerations for use in interventional radiology. J Vasc Interv Radio 2008; 19(6): 814820. [38] Srinivasan K, Mohammadi M, and Shepherd J. Applications of linac-mounted kilovoltage Cone-beam Computed Tomography in modern radiation therapy: A review. Pol J Radiol. 2014; 79: 181193. [39] Hatcher DC. Operational principles for cone-beam computed tomography. J Am Dent Assoc 2010; 141(Suppl 3): 3S6S. [40] Mudgade DK, Motghare PC, Kunjir GU, Darwade AD, Raut AS. Prevalence of anatomical variations in maxillary sinus using cone beam computed tomography. J Indian Acad Oral Med Radiol 2018; 30: 18-23. [41] Parks ET. Cone Beam Computed Tomography for the Nasal Cavity and Paranasal Sinuses. Dent Clin N Am 2014; 58: 627651. [42] Shokri A, Faradma MJ, Hekmat B. Correlations between anatomical variations of the nasal cavity and ethmoidal sinuses on cone-beam computed tomography scans. Imaging Sci Dent 2019; 49(2): 103113. [43] Altug-Atac AT, Atac MS, Kurt G, Karasud HA. Changes in nasal structures following orthopaedic and surgically assisted rapid maxillary expansion. Int J Oral Maxillofac Surg 2010; 39: 129-135.

28

[44] Xiong GX, Zhan JM, Jiang HY, Li JF, Rong LW et al. Computational fluid dynamics simulation of airflow in the normal nasal cavity and paranasal sinuses. Am J Rhinol 2008; 22: 477-482. [45] Dowley AC, Homer JJ. The effect of inferior turbinate hypertrophy on nasal spray distribution to the middle meatus. Clin Otolaryngol Allied Sci 2001; 26: 488-490. [46] Setlur J, Goyal P. Relationship between septal body size and septal deviation. Am J Rhinol Allergy 2011; 25: 397-400. [47] Reitzen SD, Chung W, Shah AR. Nasal septal deviation in the pediatric and adult populations. Ear Nose Throat J 2011; 90: 112-115. [48] Aziz T, Wheatley FC, Ansari K, Lagravere M, Major M et al. Nasal septum changes in adolescent patients treated with rapid maxillary expansion. Dental Press J Orthod 2016; 21: 47-53. [49] Epstein N. On tortuosity and the tortuosity factor in flow and diffusion through porous media. Chem Eng Sci 1989; 44(3): 777-779. [50] Kim BJ, Lee KM, Lee S-H, Kim H-G, Kim EJ, Heo SH, Chang D, Kim JS. Ethnic differences in intracranial artery tortuosity: a possible reason for different locations of cerebral atherosclerosis. J Stroke 2018; 20(1): 140-141. [51] Ugradar S, Rootman DB. Quantification of optic nerve length and tortuosity in thyroid eye disease. Can J Opthhalmol 2019; 54(5): 611614. [52] Aziz T, Ansari K, Lagravere MO, Major MP, Flores-Mir C. Effect of non-surgical maxillary expansion on the nasal septum deviation: a systematic review. Prog Orthod 2015; 16: 15. [53] Caglayan F, Tozoglu U. Incidental findings in the maxillofacial region detected by cone beam CT. Diagn Interv Radiol 2012; 18: 159-163.

29

[54] Smith KD, Edwards PC, Saini TS, Norton NS. The prevalence of concha bullosa and nasal septal deviation and their relationship to maxillary sinusitis by volumetric tomography. Int J Dent 2010; Article ID 404982. [55] Takahashi R. Malformations of the nasal septum. In: A collection of ear, nose and throat studies, editor Takahashi R, Tokyo: Kyoya Co. Ltd, 1971. [56] Arun T, Isik F, Sayinsu K. Vertical growth changes after adenoidectomy. Angle Orthod 2003; 73: 146-150. [57] Sousa JB, Anselmo-Lima WT, Valera FC, Gallego AJ, Matsumoto MA. Cephalometric assessment of the mandibular growth pattern in mouth-breathing children. Int J Pediatr Otorhinolaryngol 2005; 69: 311-317. [58] Aziz T, Biron VL, Ansari K, Flores-Mir C. Measurement tools for the diagnosis of nasal septal deviation: a systematic review. J Otolaryngol Head Neck Surg 2014; 43(1): 11. [59] Mamikoglu B, Houser S, Akbar I, Ng B, Corey JP. Acoustic rhinometry and computed tomography scans for the diagnosis of nasal septal deviation, with clinical correlation. Otolaryngol Head Neck Surg 2000; 123: 61-68. [60] Cummings CW, Fredrickson JM, Harker LA, Krause CJ, Richardson MA et al. Otolaryngology, Head & Neck Surgery. St Louis, Missouri: Mosby-Yearbook, 1998. [61] Garcia GJ, Rhee JS, Senior BA, Kimbell JS. Septal deviation and nasal resistance: an investigation using virtual surgery and computational fluid dynamics. Am J Rhinol Allergy 2010; 24: 46-53. [62] MacGinnis M, Chu H, Youssef G, Wu KW, Machado AW et al. The effects of micro-implant assisted rapid palatal expansion (MARPE) on the nasomaxillary complexa finite element method (FEM) analysis. Prog Otrhod 2014; 15: 52.

30

[63] Schwarz GM, Thrash J, Byrd DL, Jacobs JD. Tomographic assessment of nasal septal changes following surgical-orthodontic rapid maxillary expansion. Am J Orthod 1985; 87: 39-45. [64] Gray LP, Brogan WF. Septal deformity malocclusion and rapid maxillary expansion. Orthodontist 1972; 4: 2-14. [65] Subaric M, Mladina R. Nasal septum deformities in children and adolescents: a cross sectional study of children from Zagreb, Croatia. Int J Pediatr Otorhinolaryngol 2002; 63: 41-48. [66] Create

and

run

a

simple

app

using

App Designer. Mathworks 2019; https://www.mathworks.com/help/matlab/ creating_guis/create-a-simple-app-or-gui-using-app-designer.html. [67] Mathworks

File

Exchange

website.

https://www.mathworks.com/matlabcentral/fileexchange/. [68] Garrison

D.

Writing apps in MATLAB. Mathworks 2012; https://www.mathworks.com/ company/newsletters/articles/writing-apps-in-matlab.html. [69] Akgul A. Tibbi Arastirmalarda Istatistiksel Analiz Teknikleri: SPSS Uygulamalari. Seckin Yayincilik, Ankara, Turkey, 2003, in Turkish. [70] Ozer

M,

Isler

Y,

Ozer

H.

A computer software for simulating single-compartmental model of neurons. Computer Methods and Programs in Biomedicine 2004; 75(1): 51-57. [71] Isler Y. A software for simulating passive dendrite properties based on the cable theory. Computer Methods and Programs in Biomedicine 2007; 88(3): 264-272.

31