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. 2021 Jun 19;239(4):788–800. doi: 10.1111/joa.13479

Effect of septal deviation on nasomaxillary shape: A geometric morphometric study

Roni Abou Sleiman 1,✉, Antoine Saadé 1
PMCID: PMC8450481  PMID: 34148243

Abstract

Nasal cavities in their primitive stage communicate with the oral cavity until the 8th week of intrauterine life where the posterior palate initiates its development. Hence, starting from the initial growth phases, a significant connection lays between the nasal structures and the maxillary bone and witnessing key functional roles, among which the respiration. Proper nasal breathing has been proven to be a crucial factor for the maturity of the craniofacial complex, and obstruction of the respiratory airway due to nasal septum deviation can generate clinically significant reduction of the nasal airflow. This situation will imply irreversible repercussions that hinders the harmonious development of the craniofacial complex. In order to understand such potential impacts of septal deviation, our first objective was to materialize the relation between septum deviation, and both nasal cavity and maxillary structures. For the second objective, we used Procrustes analysis to assess the shape variation of these two anatomical regions, the bivariate plots of Principal Components to evaluate their shape space, and a two‐block Partial Least Square (PLS) to explore their covariation. We analysed, in this cross‐sectional study, 62 posteroanterior cephalometric radiographs of adult subjects from both sexes (23 males, 39 females; mean age 25.3 years) collected from the database of the Department of Orthodontics at Lebanese University. Landmarks were plotted and variables were calculated and divided into nasal septum, nasal cavity and maxillary ones. The sample was further divided into two groups based on septal deviation severity (a septal deviation is considered minor if <6). The results suggested that nasal septum deviation was correlated to reduced nasal cavity area and a reduced maxillary area. Moreover, the comparison of the two groups concluded that the difference between all variables was statistically significant with higher scores in the minor septal deviation group. These findings were corroborated with the shape analysis where the mean centroid size of nasal cavity and that of the maxilla in the group of reduced septal deviation were significantly greater than those of the group with increased angle of deviation. Results of PLS analysis concluded to a strong covariation between nasal septum and nasomaxillary complex. These conclusions support the early septoplasty in growing patients as a solution to redirect the normal course of growth and re‐establish a good function of the nasomaxillary complex.

Keywords: cephalometry, geometric morphometrics, maxilla, nasal cavity, septal deviation

Proper nasal breathing has been proven to be a crucial factor for the maturity of the craniofacial complex, and obstruction of the respiratory airway due to nasal septum deviation can generate clinically significant reduction of the nasal airflow. This situation will imply irreversible repercussions that hinders the harmonious development of the craniofacial complex. The results suggested that nasal septum deviation was correlated to reduced nasal cavity area and a reduced maxillary area. Moreover, the comparison of the two groups concluded that difference between all variables were statistically significant with higher scores in the minor septal deviation group. These findings were corroborated with the shape analysis where the mean centroid size of nasal cavity and that of the maxilla in the group of reduced septal deviation, were significantly greater than those of the group with increased angle of deviation. Results of PLS analysis concluded to a strong covariation between nasal septum and nasomaxillary complex. These conclusions support the early septoplasty in growing patients as a solution to redirect the normal course of growth and reestablish a good function of the nasomaxillary complex.

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1. INTRODUCTION

The skeleton of the face and the upper jaw is mainly formed by the maxillary bone which is a paired bone consisting of four processes (zygomatic, alveolar, frontal and palatine) and a body (Sobiesk & Munakomi, 2019). The nasal cavity is the highest part of the respiratory tract that forms the internal part of the nose and is delimited by six walls (Sobiesk & Munakomi, 2019). Nasal cavities and nasal septum in their primitive stage communicate with the oral cavity until the 8th week of intrauterine life where the posterior palate begins its formation (Ballanti et al., 2016; Farronato et al., 2012). For this reason, an important anatomical connection exists between the nasal structures and the maxillary bone starting from their initial growth phases (Ballanti et al., 2016).

A deviation of either the cartilaginous or the bony part of the septum from the midline is defined as Nasal Septum Deviation (NSD) (Aziz et al., 2015). A straight septum would allow for optimized gas exchange because it gives the opportunity to the inhaled air to be cleaned, humidified and warmed (Aziz et al., 2014; Filho et al., 2001). When nasal respiration is not possible due to obstructions, such as NSD, the alternative pathway for air inhalation remains the mouth (Aziz et al., 2014; Kim et al., 2014; Wang et al., 2016), wherein this case the habit of mouth breathing could lead to various complications in growing patients (D’Ascanio et al., 2010). In adults, according to the severity of septal deviation, the resulting nasal obstruction and altered breathing vary in degrees (Aziz et al., ,2014, 2015).

The relationship between the development of craniofacial structures and nasal respiratory function has been a subject of interest and controversy in the last decades (D’Ascanio et al., 2010). Moss states in his functional matrix theory that lowering of the palate and lateral growth of the maxilla are stimulated by an uninterrupted flow of air inside the nasal cavities thus strongly relating nasal breathing to dentofacial morphology (Moss, 1997). Several articles discussed malocclusion due to oral breathing (Bakor et al., 2011; Gungor & Turkkahraman, 2009; Harvold et al., 1981; Indiarti et al., 2017; Yamada et al., 1997), and one stated that nasal respiration is of utmost importance when it comes to the development of the facial morphology (Linder‐Aronson, 1979). Delaire was among the first authors to mention the effects of nasal septum on growth highlighting the direct role of the nasal septum in the growth of the premaxilla, and demonstrating its indirect role in the growth of the maxilla (Delaire & Precious, 1986). Poublon, in his study on the effect of the septolateral cartilage in midfacial growth, conducted resection experiments on growing rabbits to deduce that the triangular cartilages are of major importance for the normal development of the nasal bones, the transverse expansion of the dorsal nasal meatus and the normal development of the nasal conchae (Poublon, 1987). Other studies also found an association between NSD and its neighbouring structures (Elahi et al., 1997; Freng et al., 1988; Saylisoy et al., 2014; Serifoglu et al., 2017), or with the development of facial growth asymmetries (Hartman et al., 2016; Kim et al., 2011). Proper nasal breathing has been proven to be an indispensable factor for the maturity of the craniofacial complex, and obstruction of the respiratory airway resulting from NSD could compromise the growth of the nasomaxillary complex (Cingi et al., 2016; D’Ascanio et al., 2010; Hartman et al., 2016; Lawrence, 2012).

Geometric morphometrics (GM) is a method that studies shape (2D or 3D) relying on Cartesian landmark and semi‐landmark coordinates used to capture the morphological shape of complex objects, and to statistically analyse their shape variations (Bookstein, 1982). Using GM tools will enable the study of objects following their shape depiction, the comparison of their anatomical structures and the selection of individuals according to their shape (Radulesco et al., 2019). Visualizing changes of shape remains a major tool for comprehending morphological variation (Klingenberg, 2010). These differences may indicate dissimilar functional roles played by the same parts, as well as differences in procedures of growth and morphogenesis (Zelditch et al., 2004). After extracting information from the geometry of biologic shape, practitioners of morphometrics will use this information for particular comparative purposes such as abnormality, the study of growth or taxonomic differences (Bookstein, 1982, 1993). Scientific literature is profuse with numerous publications analysing shape variation of the skull (Bastir & Rosas, 2013; Ferros et al., 2015; Halazonetis, 2004; Manyama et al., 2014), or addressed explicitly the nasal cavity (Fukase et al., 2016; Keustermans et al., 2018; McDowell et al., 2012; Noback et al., 2011), and the nasal septum (Buyukertan et al., 2003; Goergen et al., 2017; Holton et al., 2012; Radulesco et al., 2019).

This study aims to find, using geometric morphometric tools, if any relationship exists between nasal septum deviation, nasal cavity and maxillary bone in a sample of adult patients using posteroanterior cephalometric radiographs. Another aim will be to assess the severity of septal deviation and its correlation with nasal cavity and maxillary variables. Therefore, early septoplasty in growing patients could be a solution to redirect the normal course of growth and re‐establish a good function of the nasomaxillary complex. From this perspective, we hypothesize that NSD is not correlated with the nasal cavity and the maxillary bone, and that severity of septal deviation does not affect the maxillary and nasal cavity variables.

2. MATERIALS AND METHODS

2.1. Sample

This study was performed on posteroanterior cephalometric radiographs (PA ceph) selected from the database of the Department of Orthodontics and Dentofacial Orthopedics at Lebanese University, Faculty of Dental Medicine. Written consent was previously obtained from patients during the initial consultation, allowing the use of records for educational and scientific purposes.

The sample included 62 subjects (23 males, 39 females; mean age 25.3 years). Inclusion criteria were as follows: patients aged more than 18 years having in their orthodontic file a high‐quality PA ceph presenting a ruler to measure linear variables and showing clearly all the anatomical structures required for the study.

Patients with craniofacial syndromes, facial trauma previous septal surgery or rhinoplasty and history of orthodontic treatment were excluded from the study. In addition, radiographs of patients that reported in their medical history a rhinitis allergy, rhinosinusitis or obstructive sleep apnoea were not incorporated in the sample. This retrospective cross‐sectional study was approved by the scientific committee of the Faculty of Dental Medicine at Lebanese University.

2.2. Landmark selection

Due to the superimposition of numerous anatomical structures on the PA cephs and the difficult identification of reliable and reproducible points, strict criteria were used to locate specific landmarks. Three unilateral landmarks, four bilateral ones and 25 semi‐landmarks (Table 1, Figure 1) were selected and digitized using Viewbox cephalometric tracing software (Viewbox, version 4.0.I.6—dHAL software, Kifissia, Greece).

TABLE 1.

Landmarks and cephalometric points used in the study

Landmark Definition
1 Crista Galli Geometric centre of crista galli (Ulkur et al., 2016)
2 Anterior Nasal Spine Centre of the intersection of the nasal septum and the palate (Ulkur et al., 2016)
3 Point of Septal Deviation Most lateral point of deviation of the nasal septum (Kim et al., 2011)
4 Nasal Cavity Right Most lateral aspect of the right piriform aperture (Ricketts et al., 1972)
5 Nasal Cavity Left Most lateral aspect of the left piriform aperture (Ricketts et al., 1972)
6 Jugale Right Intersection of the outline of the tuberosity of the maxilla and the zygomatic buttress on the right side (Ricketts et al., 1972) which is a landmark commonly used in conventional transverse analysis
7 Jugale Left Intersection of the outline of the tuberosity of the maxilla and the zygomatic buttress on the left side (Ricketts et al., 1972) which is a landmark commonly used in conventional transverse analysis
8 Maxillary Middle Point Right A constructed radiological point between the intersection of the temporal surface of the greater wing of the sphenoid (STENVERS Line) (Vion, 1984) and the lower border of the orbit on the right side
9 Maxillary Middle Point Left A constructed radiological point between the intersection of the temporal surface of the greater wing of the sphenoid (STENVERS Line) (Vion, 1984) and the lower border of the orbit on the left side
10 Maxillary Upper Point Right A constructed radiological point between the intersection of the superior border of the lesser wing of the sphenoid bone and the medial orbital margin on the right side
11 Maxillary Upper Point Left A constructed radiological point between the intersection of the superior border of the lesser wing of the sphenoid bone and the medial orbital margin on the left side
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25 Semi‐landmarks delimiting the nasal cavity and reaching crista galli superiorly. As the upper part of the nasal cavity is not visible on the PA ceph, crista galli was selected as a reference (reproducible landmark) to complete the shape of this region.

FIGURE 1.

FIGURE 1

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Cephalometric landmarks and analysis used to capture nasal and maxillary morphologies in the study: 1, crista galli; 2, anterior nasal spine; 3, point of septal deviation; 4, nasal cavity right; 5, nasal cavity left; 6, jugale right; 7, jugale left; 8, maxillary middle point right; 9, maxillary middle point left; 10, maxillary upper point right; 11, maxillary upper point left; VRL, vertical reference line; DSA, deviated septal angle; DSL, deviated septal length; NCW, nasal cavity width; NCA, nasal cavity area; J‐J, maxillary width; MA, maxillary area

2.3. Cephalometric and shape analysis

After landmarks selection on the PA ceph, a vertical reference line was constructed from crista galli to anterior nasal spine in order to measure the deviation of the nasal septum (Figure 1). In the next step, linear, angular and shapes were constructed and measurements were calculated for each subject. These measurements are divided into nasal septum variables, nasal cavity variables and maxillary variables (Table 2) aiming to assess the nasal septum deviation, the width and area of the nasal cavity and the width and area of the maxilla. Deviated Septal Angle (DSA) and Deviated Septal Length (DSL) are the two variables used to measure the nasal septum deviation. DSA is the angle formed between the vertical reference line and a line drawn from crista galli to point of septal deviation, whereas DSL is the length of the horizontal line from point of septal deviation to the vertical reference line. The nasal cavity area is delimited by 25 semi‐landmarks. As for the maxillary area, the maxillary middle and upper points were specifically chosen because they delimit the maxillary bone in its upper and middle parts. Regarding the lower part of the maxilla, the jugale points were selected. These three bilateral points once joined form the maxillary shape from which the maxillary area is measured.

TABLE 2.

Variables and definitions used in the study

Variable Definition
Nasal septum variables Deviated Septal Angle (DSA) (°) Angle formed between the vertical reference line and a line drawn from crista galli to point of septal deviation. This angle represents the degree of deviation of the septum relative to a vertical reference line
Deviated Septal Length (DSL) (mm) Length of the horizontal line from point of septal deviation to the vertical reference line. This line represents the length of deviation of the septum relative to a vertical reference line
Nasal cavity variables Nasal Cavity Width (mm) Distance from nasal cavity right to nasal cavity left. This distance represents the transverse dimension of the nasal cavity
Nasal Cavity Area (mm2) Area of the polygon formed by the 25 semi‐landmarks delimiting the nasal cavity
Maxillary variables Maxillary Width (mm) Distance from jugale right to jugale left. This distance represents the transverse dimension of the maxilla
Maxillary Area (mm2) Area of the polygon formed by jugale right, maxillary middle point right, maxillary upper point right, maxillary upper point left, maxillary middle point left, jugale left
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Following the acquisition of the maxillary shape and nasal cavity shape, the centroid of each configuration was produced, then Maxillary Centroid Size and Nasal Cavity Centroid Size were calculated for each configuration. The centroid of a figure, a common tool used in GM, is the arithmetic mean position of all the landmarks of the figure (Bookstein, 1993), and the centroid size of a landmark configuration is the square root of the sum of squared distances of a set of landmarks from their centroid (Bookstein, 1993). As centroid size is a measure of size which is mathematically independent of shape (Zelditch et al., 2004), it is the reason behind its use as a size variable when geometric morphometrics is applied.

At the next step, one common Generalized Procrustes Analysis was carried out for the whole sample. Subsequently, a Principal Component Analysis (PCA) was done to obtain principal components (PCs) of shape variation for a more detailed examination of landmarks displacements patterns in the sample (Halazonetis, 2004). Bivariate plots were also conducted to display the shape space and differences among groups and sex along principal component axes.

A two‐block partial least squares (PLS) analysis (Rohlf & Corti, 2000) was performed to explore the patterns of covariation between the following two sets of variables:

  • Block 1: nasal septum landmarks (1–3).

  • Block 2: nasomaxillary complex landmarks (all landmarks except 1–3).

These two blocks were also pooled by sex to assess if any sexual dimorphism is present. This analysis was performed using MorphoJ software (Klingenberg, 2011) (MorphoJ, version 1.07a).

It is admitted that nasal breathing is affected by severity of septal deviation (Aziz et al., ,2014, 2015). In order to explore the effect of DSA variation on the nasal cavity and the maxilla, the sample was further divided into two groups according to the DSA value, using a common Generalized Procrustes Analysis (the DSA values were imported as classifier variables):

  • Group 1 comprising 29 subjects (8 males, 21 females; mean age 25.7 years) presenting minor septal deviation (DSA < 6°).

  • Group 2 comprising 33 subjects (15 males, 18 females; mean age 25 years) presenting a more important septal deviation (DSA > 6°).

2.4. Error analysis

In order to observe possible errors in landmark identification and measurement 10 PA cephs were randomly selected and re‐digitized by the same examiner (RA) 1 month following the initial measurement to determine intraobserver agreement and Pearson correlation coefficient r between the first and second measurements was calculated for each variable.

2.5. Statistical analysis and assessment of shape variation

Normality was assessed for the variables in the whole sample using Shapiro–Wilk and Kolmogorov–Smirnov tests and Pearson coefficient was calculated for a further understanding of the correlation among variables of nasal septum, nasal cavity and maxilla. Independent sample t‐test was used for comparison of parametric continuous data between the DSA groups. p‐values of less than 0.05 were considered statistically significant. PCA was performed for both shapes recovered to assess total shape variability. The data were analysed using the Statistical Package Software system (SPSS, version 18, Chicago, Illinois, USA). The Viewbox software, version 4.0.I.6 was used for shape superimposition, identification of principal components and analysing the shape space of the maxilla and the nasal cavity.

3. RESULTS

A high degree of reliability (r values between 0.81 and 0.99) was noticed for all variables.

3.1. Association between nasal septum, nasal cavity and maxilla

Descriptive statistics of all the radiographs included in the sample are summarized in Table 3. Patient's age ranged from 18 to 53.7 years (mean age 25.3 ± 7.7 years). The mean DSA was 6.85 ± 2.79°, and that of DSL was 3.79 ± 1.34mm. As for the width of the maxilla and the nasal cavity, the mean was 63.05 ± 4.47 mm and 33.59 ± 2.49 mm respectively. Nasal cavity area was 1157.75 ± 141.03 mm2, whereas maxillary area was 2820.95 ± 377.13 mm2. In addition, centroid size calculation of the maxilla and the nasal cavity showed means of 34.54 ± 2.13 mm and 21.76 ± 1.3 mm respectively.

TABLE 3.

Descriptive statistics of the variables in the whole sample

Variables N Range Minimum Maximum Mean SD
Age 62 35.7 18 53.7 25.3 7.7
Deviated septal angle (°) 62 12.2 1.2 13.4 6.85 2.79
Deviated septal length (mm) 62 6.4 0.9 7.3 3.79 1.34
Maxillary width (mm) 62 17.8 55.4 73.2 63.05 4.47
Nasal cavity width (mm) 62 9.8 28.8 38.6 33.59 2.49
Nasal cavity area (mm2) 62 588.3 917.2 1505.5 1157.75 141.03
Maxillary area (mm2) 62 1652.8 2120.1 3772.9 2820.95 377.13
Maxillary centroid size (mm) 62 9.55 30.18 39.73 34.54 2.13
Nasal cavity centroid size (mm) 62 6.65 18.54 25.19 21.76 1.30
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Table 4 displays the correlations between variables of the nasal septum, nasal cavity and maxilla. The strong correlation between DSA and nasal cavity area was inversely associated (−0.669); hence, whenever the angle of nasal septum deviation increases, the nasal cavity area decreases. The moderate negative correlation (−0.559) between DSL and nasal cavity area suggests that whenever the length of nasal septum deviation increases, this area decreases. Although both DSL and DSA represent variables of nasal septum deviation, the latter showed higher correlations with nasal cavity area. As for nasal cavity width, it is less affected than nasal cavity area by the deviation of the nasal septum (correlations of −0.429 and −0.357 respectively with DSA and DSL). The septum angle deviation and both maxillary area and width are moderately correlated (−0.535 and −0.573 respectively) and inversely proportional. As for the septal length, a weak negative correlation is shown with the maxillary variables (−0.47 and −0.483). Pearson correlation between nasal cavity area and maxillary area was 0.605 and a close result (0.581) was noted between nasal cavity centroid size and maxillary centroid size. These two outcomes imply the direct relationship between the nasal cavity and the maxilla. Also, correlation coefficients between nasal cavity width and area with maxillary width were equal to 0.442 and 0.564, respectively, indicating a relative proportional increase in width and area of the nasal cavity in relation with the maxillary width.

TABLE 4.

Correlations between variables of the nasal septum, nasal cavity and maxilla

Variables Correlations Correlation coefficient (r) p‐value
Nasal septum vs. Nasal cavity Deviated Septal Angle with Nasal Cavity Area −0.669 0.00*
Deviated Septal Length with Nasal Cavity Area −0.559 0.00*
Deviated Septal Angle with Nasal Cavity Width −0.429 0.001*
Deviated Septal Length with Nasal Cavity Width −0.357 0.004*
Nasal septum vs. Maxilla Deviated Septal Angle with Maxillary Area −0.535 0.00*
Deviated Septal Length with Maxillary Area −0.47 0.00*
Deviated Septal Angle with Maxillary Width −0.573 0.00*
Deviated Septal Length with Maxillary Width −0.483 0.00*
Nasal cavity vs. Maxilla Nasal Cavity Area with Maxillary Area 0.605 0.00*
Nasal Cavity Centroid Size with Maxillary Centroid Size 0.581 0.00*
Nasal Cavity Width with Maxillary Width 0.442 0.00*
Nasal Cavity Area with Maxillary Width 0.564 0.00*
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∗

Statistically significant at p < 0.05.

3.2. Shape analysis

3.2.1. Maxilla

A total of eight PCs was necessary to describe the shape variability of the maxilla. PC1, PC2 and PC3 embodied more than 85% of total shape variability (Table 5). PC1 summarized 48.5% of the modification and described a combination of transversal–vertical disparity of the maxilla (Figure 2). When compared to the mean shape, positive PC1 values relate to a relatively larger and stretched maxilla (more of transverse growth) on middle and lower regions (maxillary middle points and jugale points) and shorter on the upper one (maxillary upper points). Negative PC1 values are associated with a quite elongated maxilla (more of vertical growth on maxillary upper points and jugale points), which turns narrower on middle and lower areas (maxillary middle points and jugale points) while not much vertical translation is seen on maxillary middle points. PC2 accounts 24.2% of the shape variation and translates the vertical modifications. Positive PC2 values are related to the vertical development on upper and middle maxillary regions (maxillary upper points and maxillary middle points), while jugale points are repositioned upper relative to the mean shape. As a result, the whole maxilla is displaced to the upper. Negative PC2 values reflect the downward movement of the maxilla on maxillary upper points and jugale points; however, maxillary middle points are repositioned upward. PC3 totalize 12.5% of the variations and display transverse modifications mainly on middle and lower portions while little change is seen on maxillary upper points. Positive PC3 shows larger maxillary upper points and narrower jugale points, whereas the opposite is seen with negative PC3 (Supplementary Figure S1). Bivariate plots of the first three PCs of the maxilla for both sexes in the two groups are also observed in Figure 2. Females in both groups had larger PC1 values than males with bigger values for Group 2. The greater PC2 values are shown for males with DSA <6˚. As for PC3, both sexes included in Group 2 revealed greater values than Group 1. Shape space of the maxilla for the whole sample depicting extreme subjects from both groups is shown in supplementary Figure S2.

TABLE 5.

Principal component analysis of the maxillary and nasal cavity shapes with the percentage of variance and cumulative variance for the first five principal components (PC)

PC Variance (%) Cumulative variance (%)
Maxilla PC 1 48.5 48.5
PC 2 24.2 72.7
PC 3 12.5 85.2
PC 4 6.8 91.9
PC 5 3.9 95.9
Nasal cavity PC 1 64.3 64.3
PC 2 11.9 76.2
PC 3 7.6 83.8
PC 4 4.8 88.6
PC 5 2.6 91.1
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FIGURE 2.

FIGURE 2

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Bivariate plots of the first three PCs of the maxilla. The middle and right sides represent the subjects plotted in the 3D shape space of PC2 versus PC1, and PC2 versus PC3 respectively. Black: group 1 subjects; Orange: group 2 subjects. Circle: females; Square: males. Large markers show group means with standard deviation lines. Left and bottom sides represent the shape variation along the PC1, PC2, and PC3 axes with ±1 SD, and the arrows reflect the changes within each PC

3.2.2. Nasal cavity

The PCA of Procrustes analysis for the nasal cavity landmarks yielded 38 PCs in order to describe 100% of shape variability of the nasal cavity; however, the first three PCs embodied approximately 84% of total shape variability (Table 5). PC1 accounted 64.3% of the shape and describe orientation of the nasal cavity, PC2 11.9% and PC3 7.6%. Figure 3 shows the first three PCs of the nasal cavity shape with ±1 SD of variability per PC. PC1 positive values display a comparable shape in regard to the mean, but more elongated, rotated and deviated at landmark Crista Galli. A relatively narrower upper nasal cavity medio‐lateral diameter is shown for the negative values, and the top of the pyramid is also deviated but oppositely oriented to PC1+. PC2 totalized 11.9% of the shape and defined the vertical–transverse modifications of the cavity. Shape for the positive values is seen thinner and longer than the mean, whereas the negative values displayed a squat‐shaped, shorter and larger. As for PC3, it amounted 7.6% of the variations and depicts the vertical translation of the nasal cavity, upward for positive values and downward for negative results (Supplementary Figure S3). Bivariate plots of the first three PCs of the nasal cavity for both sexes in the two groups are also shown in Figure 3. Similar to the maxillary shape, females in both groups had greater PC1 values than males. Females included in Group 2 have the larger PC1 in opposition to the males who showed comparatively larger values in Group 1. No significant differences are shown in PC2 results, while for PC3, males have larger values than females (slightly larger in Group 2). Shape space of the nasal cavity for the whole sample depicting extreme subjects from both groups is shown in supplementary Figure S4.

FIGURE 3.

FIGURE 3

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Bivariate plots of the first three PCs of the nasal cavity. The middle and right sides represent the subjects plotted in the 3D shape space of PC2 versus PC1, and PC2 versus PC3 respectively. Black: group 1 subjects; Orange: group 2 subjects. Circle: females; Square: males. Large markers show group means with standard deviation lines. Left and bottom sides represent the shape variation along the PC1, PC2 and PC3 axes with ±1 SD, and the arrows reflect the changes within each PC

3.2.3. Two‐block partial least squares analysis

Two‐block PLS analysis was used to detect patterns of covariation between the nasal septum and the nasomaxillary complex. We found that the shapes of these two structures do not vary independently of each other, instead, one seems to be changing with the other. In addition, one structure appears to have an effect on the other one in a linear manner (Figure 4). The covariation detected in the PLS1 shows that the modification on the nasal septum occurs the most on the Crista Galli point (landmark 1). Moreover, a rotation is occurring on both structures of nasomaxillary complex. The magnitude of rotation is less important on the maxilla which seems also undergoing a rotation that occurs in the same direction as the septum deviation. Also, same amount of modification appears on Jugale right and Jugale left. As for the nasal cavity, the modification is shown the most on its lateral walls while a little is observed on the nasal cavity floor. Also, the data points distribution of the two sexes shows that no sexual dimorphism is present between the NSD and the nasomaxillary complex as the two components are overlapping. The PLS analysis revealed one statistically significant singular value and two statistically significant correlations of PLS scores, with RV coefficient of 0.4. The first three PLS amounted almost 99% of covariation (Table 6). The contribution of PLS1 (Figure 5) to the total covariation was 95% (p < 0.001) and the correlation was 0.93. As for PLS2 and PLS3, they described, respectively, 2.248% and 1.599% of the covariance and 0.47 and 0.43 of the correlation.

FIGURE 4.

FIGURE 4

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Two‐block Partial Least Square analyses (PLS1) pooled by sex: Blue data points represent the males; red data points represent the females

TABLE 6.

Two‐block partial least squares (PLS) analyses showing the covariation and the correlation between the nasal septum (block 1) and the nasomaxillary complex (block 2)

RV coefficient = 0.404331
p‐value < 0.001
Singular value p‐value % total covariance Correlation p‐value
PLS1 0.00233795 <0.001 95.094 0.92829 <0.001
PLS2 0.00035948 0.252 2.248 0.47654 0.156
PLS3 0.00030315 0.016 1.599 0.43489 0.22
PLS4 0.0001848 0.144 0.594 0.61049 <0.001
PLS5 0.00015414 0.004 0.413 0.50629 0.008
PLS6 0.00005426 0.08 0.051 0.46514 0.04
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FIGURE 5.

FIGURE 5

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Transformation grids of Partial Least Square analysis (PLS1) showing the covariation between the nasal septum in red (block 1) and the nasomaxillary complex in light blue (block 2)

3.3. Comparison between DSA groups

The whole sample was divided into two groups (group 1 with a DSA< 6°; group 2 with a DSA > 6°). Descriptive statistics (Table 7) show that all variable means were greater in group 1 compared to group 2. This conclusion is true for linear measurements, as well as for surface measurements, or for centroid size of the maxilla and the nasal cavity.

TABLE 7.

Descriptive statistics of the variables in the two groups

Variables Range Minimum Maximum Mean SD
Group 1 (N = 29) Age 35.7 18 53.7 25.7 8.1
Maxillary width (mm) 16.3 56.9 73.2 65.6 4.32
Nasal cavity width (mm) 7.3 31.3 38.6 35.03 2.13
Maxillary area (mm2) 1378.3 2394.6 3772.9 3006.94 407.53
Nasal cavity area (mm2) 456.5 1049 1505.5 1267.47 116.64
Maxillary centroid size (mm) 7.8 31.97 39.73 35.68 2.2
Nasal cavity centroid size (mm) 4.2 20.96 25.19 22.72 1.07
Group 2 (N = 33) Age 24.8 18.1 42.9 25 7.3
Maxillary width (mm) 13.8 55.4 69.2 60.82 3.27
Nasal cavity width (mm) 8.5 28.8 37.3 32.33 2.08
Maxillary area (mm2) 1271.7 2120.1 3391.8 2657.49 258.64
Nasal cavity area (mm2) 361.2 917.2 1278.4 1061.32 74.24
Maxillary centroid size (mm) 6.8 30.18 36.99 33.53 1.47
Nasal cavity centroid size (mm) 4.3 18.54 22.85 20.92 0.8
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A t‐test was used for comparison between the two groups after testing for normality of their variables through Shapiro–Wilk analysis. All variables were statistically significant maxillary width (p = 0.00), nasal cavity width (p = 0.00), maxillary area (p = 0.00), nasal cavity area (p = 0.00), maxillary centroid size (p = 0.00) and nasal cavity centroid size (p = 0.00) when the two groups were compared together (Table 8) denoting that the evidence obtained in the descriptive analysis was confirmed by the inferential statistical results. These results highlight the contribution of the septal deviation on nasal cavity and maxilla sizes implying that a small nasal septum deviation is yielding a statistically significant bigger nasal cavity width, maxillary width, maxillary area, nasal cavity area, nasal cavity centroid size and maxillary centroid size.

TABLE 8.

Student's t‐test for comparison of the variables between the two groups

Variables Group 1 Group 2 Mean difference p‐value
Maxillary width (mm) 65.6 (±4.31) 60.82 (±3.27) 4.78 0.00*
Nasal cavity width (mm) 35.03 (±2.12) 32.33 (±2.08) 2.71 0.00*
Maxillary area (mm2) 3006.94 (±407.53) 2657.49 (±258.64) 349.45 0.00*
Nasal cavity area (mm2) 1267.47 (±116.64) 1061.32 (±74.24) 206.15 0.00*
Maxillary centroid size (mm) 35.68 (±2.2) 33.53 (±1.47) 2.15 0.00*
Nasal cavity centroid size (mm) 22.72 (±1.07) 20.92 (±0.8) 1.80 0.00*
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∗

Statistically significant at p < 0.05.

4. DISCUSSION

Based on statistical analyses, both hypotheses stated at departure regarding absence of correlation between NSD and nasomaxillary complex were rejected.

Several studies use the DSA to measure the deviation of the nasal septum. Elahi classified groups having DSA < 9° as mild, 9°<DSA < 15°as moderate and DSA > 15° as severe (Elahi et al., 1997). This classification was based on a sample of patients only presenting nasal septum deviation as a criteria. Other studies included patients having or not NSD in their sample with different DSA values varying from 6.27° to 7.11° (Nomura et al., 2015; Saylisoy et al., 2014). The present study included a sample of adult patients presenting or not a nasal septal deviation. The DSA mean value was 6.85 ± 2.79°. As these values were similar to the ones found in the literature; therefore, it was decided here to adopt the DSA of 6° as a threshold value.

Although both DSA and DSL represent variables of the NSD, the present results suggested higher correlations coefficients in all DSA values when compared to those of the DSL. Consequently, for the same DSA, different DSL values might be obtained depending on the vertical position of septum's deviation; for a higher position of point of septal deviation, the length of its projection to the vertical reference line will be shorter when compared to a lower position of this point. Thus, for a severe DSA, a DSL value less representative of the NSD could be reached if point of septal deviation is highly positioned. For this reason, DSA could be more reliable when assessing NSD, and this is clearly explained by higher correlations coefficients when DSA was compared to the other variables.

4.1. NSD and nasal cavity

A weak negative correlation was found between DSA and nasal cavity width (−0.429) and a strong negative correlation exists between the DSA and nasal cavity area (−0.669). Hence, a deviation of the nasal septum would affect the overall surface of the nasal cavity more than its width, and the bigger the septal deviation, the smaller the nasal cavity is. Research conclusions on animals also clearly stated that cartilage of the nasal framework affects significantly the bony nasal skeleton development (Poublon, 1987). Moreover, NSD was correlated with asymmetries all over the nasal cavity (anterior nasal aperture, posterior nasal aperture, posterior nasal floor, plane of the internal nasal cavity, lateral walls of the external and internal aspects of the nasal region…) (Hartman et al., 2016). Previous study performed on lateral cephalograms observed smaller nasal cavity in a group of patients with airway problems referred for septoplasty (Freng et al., 1988). Similarly, the present results on PA ceph support the findings that the effect of the NSD is on the overall nasal cavity and not only its width.

4.2. NSD and maxilla

A deviation of the nasal septum would have an impact on the physiology of the nose and will alter proper nasal function leading to possible mouth breathing (Aziz et al., 2014; Kim et al., 2014; Wang et al., 2016). Conversely, a NSD could be the result of abnormal development of adjacent bones such as the maxilla and the nasal bone (Gray, 1978). In this study, a relationship between NSD and the maxilla was observed (−0.573). Moreover, an increase in nasal septum deviation led to a decrease in the overall area size and shape of the maxilla (Table 4). These findings are in agreement with previous results which established that mouth breather patients had various morphological alterations in addition to facial and dental anomalies (D’Ascanio et al., 2010; Gungor & Turkkahraman, 2009; Indiarti et al., 2017; Linder‐Aronson, 1979). These growth disturbances were earlier displayed on animals, and concluded that induced mouth breathing produced a downward displacement of the maxilla (Harvold et al., 1981) or permanent craniofacial deformities (Yamada et al., 1997).

4.3. Nasal cavity and maxilla

An important anatomical connection exists between the nasal structures and the maxillary bone starting from their initial intrauterine growth phases (Ballanti et al., 2016). Moreover, a relationship exists between the morphology of the overall face and the shape and size of the nasal cavity. More precisely, larger faces house larger nasal cavities (Bastir & Rosas, 2013). The present study showed similar results between nasal cavity area and maxillary area, and nasal cavity centroid size and maxillary centroid size (r = 0.605 and r = 0.581 respectively), highlighting the association between the nasal cavity and the maxilla, implying a homothetic increase in size between these two structures. Measurement of nasal cross‐sectional areas with acoustic rhinometry revealed also that patients with maxillary transverse deficiency have in the posterior region small nasal cross‐sectional areas (Baraldi et al., 2007). In the current results, a moderate correlation (r = 0.564) was found between nasal cavity area and maxillary width, while the correlation dropped to 0.442 when both nasal cavity and maxillary widths were compared. Interestingly, this value is lower than previous results of longitudinal cephalometric study (0.56 in males and 0.54 in females) (Snodell et al., 1993). The difference could be due to the small sample size of growing patients for each sex, whereas only adult patients were included in the current sample.

4.4. DSA groups

In adults, according to the severity of septal deviation, the resulting nasal obstruction and altered breathing vary in degrees (Aziz et al., 2014, 2015). Accordingly, the comparison between the two groups of DSA in this sample led to statistically significant smaller nasal cavity width, maxillary width, maxillary area, nasal cavity area, maxillary centroid size and nasal cavity centroid size in the group with the more severe DSA; patients having a bigger nasal septum deviation display smaller maxilla and nasal cavity. Some controversies are exposed in the literature where heavy nasal obstruction in monkeys was found associated with some type of malocclusion (Yamada et al., 1997), in opposition to the conclusions who showed no significant differences between mild and severe septal deviation on the adjacent structures such as nasal bone morphology (Serifoglu et al., 2017).

As for the maxillary width, a larger mean value was displayed in the mild DSA group in comparison with the more severe DSA group (respectively 65.6mm and 60.82mm) in line with the results found in the literature (Bakor et al., 2011). However, Ballanti did not find any association between NSD and maxillary transverse deficiency (Ballanti et al., 2016). Moreover, his conclusions failed to demonstrate differences in nasal cavity dimensions between groups. However, these disagreements are explained by the methodology used where the angles of the nasal cavity are measured and compared, instead of area and width like in this study.

4.5. Shape analysis

As Geometric Morphometrics aims to analyse and compare the shape of objects in two or three dimensions and provides an objective investigation (Radulesco et al., 2019), hence, some studies used GM to analyse features of the skull, among which the correlation between the cranial base and the nasomaxillary complex in artificially deformed skulls, where the nasomaxillary complex was affected—among other anatomical structures—by a modification of the shape of the cranial vault (Ferros et al., 2015). Also, facial morphometrics of cleft lip and palate patients displayed that the mean facial shape differed significantly between children having or not orofacial clefts (Manyama et al., 2014).

Furthermore, the observation of the nasal cavity shape variations concluded that nasal cavity morphology is significantly correlated with temperature, and vapour pressure variables and a variation of climatic contexts in different geographic places would functionally affect the nasal cavity, thus creating different nasal cavity morphologies (Fukase et al., 2016; Noback et al., 2011). Maddux also found that the internal nasal fossa is associated with climate changes and regional variations (Maddux et al., 2017). These conclusions and the results of this study highlight the adaptive process of the nasal cavity towards environmental and functional variations. Nasal cavity dimensions seem also to be affected by sex. Studies suggest that males tend to have larger nasal cavities due to oxygen demand particularly when looking at nasal height and choanae size (Bastir et al., 2011; Holton et al., 2016; Rosas & Bastir, 2002). However, the results of this study indicate that NSD does not present a sexually dimorphic pattern as observed in the PLS analysis. These results could be explained by the unequal distribution of patients between both sexes.

GM was also used to study the interactions between parts of the skeleton and the nasal septum (Buyukertan et al., 2003; Goergen et al., 2017; Holton et al., 2012; Radulesco et al., 2019) however, to the best of our knowledge, none of them studied the relationship between NSD, maxilla and nasal cavity. Goergen found a statistically significant association between the nasofacial region and the magnitude of NSD on CBCT and demonstrated that variation in the magnitude of this deviation was established at younger age group and maintained during ontogeny (Goergen et al., 2017). Also, Holton found a significant association between the craniofacial shape and the size of the nasal septum, which appears mainly to be a reaction to the requirement to accommodate variation in nasal septal size (Holton et al., 2012). These outcomes are similar to the ones found in this study since a variation of the deviation of the nasal septum resulted in a change of the shape of the nasal cavity and the maxilla. Besides, it is highlighted in the PLS analysis that the shapes of the DSA and the nasomaxillary complex do not change independently of each other, but one appears to be changing with the other. However, it seems that maxillary upper points right and left follow more closely the septal displacement than other nasofacial landmarks. This could be explained by the difference between growth maturation gradients from the cranial base towards the periphery. Adult morphology is established in the facial periphery later than facial attachments close to the cranial base (Bastir et al., 2006; Enlow & Hans, 1996). This spatiotemporal craniofacial growth gradients could explain why the more superiorly located nasofacial landmarks follow more strictly the septal deviation than the inferior ones. In addition, inferior structures are closer and more tightly involved functionally in mastication that could also influence the results obtained. In many use of PCA, the first few PCs represents most of the total anatomical variation included in a dataset (Halazonetis, 2004; Klingenberg & McIntyre, 1998). This study showed that more than 80% of the total shapes variability were observed in the first three PCs of both analysed structures.

The statistically significant differences between all variables in these two groups highlight the importance of diagnosing a severe NSD since it had a negative impact on the overall size and shape of the maxilla and the nasal cavity when compared with a mild NSD group. Hence, early septoplasty in growing patients could be a solution in order to redirect the normal course of growth and re‐establish a good function of the nasomaxillary complex (Cingi et al., 2016; D’Ascanio et al., 2010). The finding of a mouth breathing pattern associated with an underdeveloped maxilla and a posterior rotation of the mandible could benefit from an early intervention on the nasal septum to re‐establish appropriate function and growth patterns (Freng et al., 1988). Moreover, a correction of the NSD in growing patients would induce favourable effects on the growth pattern of the maxilla (Farronato et al., 2012). Long‐term follow‐up studies found that early septoplasty will not produce negative repercussions on nasal and facial growth (Lawrence, 2012). Thus, conservative management and avoidance of septoplasty when needed in growing patient may cause greater damage, worsen the facial growth and lead to facial asymmetries (Cingi et al., 2016; Lawrence, 2012).

5. CONCLUSION

This study showed an association between breathing abnormalities (NSD) and abnormal growth of the nasomaxillary complex. A negative correlation was found between NSD variables with the nasal cavity and the maxillary variables while a positive correlation was found between the nasal cavity variables and the maxillary variables. A smaller nasal cavity width, maxillary width, maxillary area and nasal cavity area were found in a group of more severe septal deviation when compared with a mild group. These results were confirmed by Procrustes analysis of both anatomical regions. Since mouth breathing habits could harm the craniofacial development, a recognition and correction of this breathing abnormality may support a physiological and harmonious growth of the nasomaxillary complex. Thus, early septoplasty in growing patients could be a solution to redirect the normal course of growth and re‐establish a good function of this complex. Future studies are needed to assess the cephalometric changes after restoration of nasal breathing following septoplasty in children.

AUTHOR CONTRIBUTIONS

Roni Abou Sleiman: Data collection, data analysis and interpretation, manuscript preparation. Antoine Saadé: Data analysis and interpretation, manuscript preparation. All authors gave final approval, drafted and critically revised the manuscript.

Supporting information

Fig S1

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Fig S2

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Fig S3

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Fig S4

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ACKNOWLEDGEMENTS

We would like to acknowledge Dr. Jad Azar, who assisted with the statistical analysis. We also thank Dr D. Halazonetis for his valuable contribution on Geometric Morphometric methods, and two anonymous reviewers for their precious suggestions and comments on the manuscript.

Abou Sleiman, R.&Saadé, A. (2021) Effect of septal deviation on nasomaxillary shape: A geometric morphometric study. Journal of Anatomy, 239, 788–800. 10.1111/joa.13479

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Associated Data

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Supplementary Materials

Fig S1

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Fig S2

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Fig S3

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Fig S4

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