Introduction
Structural or anatomic differences may arise during the development of the maxillary sinus and the process of fusion of the palate in the presence of cleft lip and palate. The present study aimed to compare the maxillary sinus volume of patients with unilateral cleft lip and palate and a control group (noncleft patients).
Methods
In this retrospective case-control study, 160 cone-beam computed tomography images of 80 unilateral cleft lip and palate patients (41 males and 39 females; mean age, 12.7 ± 6.03 years) and 80 control patients (43 males and 37 females; mean age, 13.1 ± 6.27 years) were evaluated through the ITK-SNAP software (Cognitica, Philadelphia, Pa) to access the maxillary sinus volume. Analysis of covariance and regression analysis were used to assess the differences between the groups while considering the relationship between maxillary sinus volume, age, and sex.
Results
No statistically significant differences were found in the maxillary sinus volume analyzing a unilateral cleft lip and palate and a control group ( P = 0.677). Considering the cleft group, there is a tendency for the maxillary sinus volume of the cleft side to be smaller than its contralateral ( P < 0.001). Statistically significant differences were found in the maxillary sinus volume, regarding the age and sex of cleft and noncleft patients ( P < 0.001 for age; P = 0.001 for sex).
Conclusions
According to these results, the presence of unilateral cleft lip and palate did not affect the maxillary sinus volume, comparing cleft and noncleft patients. A biphasic growth pattern of the maxillary sinus and a presence of sexual dimorphism were found.
Highlights
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The maxillary sinus volume in patients with cleft and noncleft palate were compared.
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Patients with cleft and noncleft palate present similar maxillary sinus volumes.
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The cleft side maxillary sinus volume tends to be smaller than its contralateral.
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The maxillary sinus volume was larger in males older than 6.70 years.
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A biphasic growth pattern of the maxillary sinus was observed on both samples.
The maxillary sinus is a part of the maxillary bone and is considered the largest of the paranasal sinuses and a major component of the midface. It is generally described as having a pyramidal shape in a 3-dimensional (3D) view bounded medially by the lateral process of the maxilla, superiorly by the floor of the orbit, inferiorly by the palate, and with its vertex formed by the zygomatic process of the maxillary bone.
It is widely accepted that the beginning of its development is around the 10th week of intrauterine life, from the mucosa of the primitive ethmoidal infundibulum. , After birth, growth of the maxillary sinus is considered biphasic: it grows rapidly during the first 3 years of life followed by another growth phase from the age of 7 to 12 years. Pneumatization continues until adulthood, with a close relation to the eruption of the maxillary permanent molars. ,
The theoretical functions of these paired air-filled cavities are related to an increase in voice resonance, a decrease in the skull weight, insulation of the tooth roots against temperature fluctuations, humidification of inhaled air, and a contribution to the growth of the maxillary bone. , For these reasons, it is important for clinicians to understand the anatomy and dimensions of the maxillary sinuses, especially in patients with cleft lip and palate (CLP) who may present various odontological, otological, and rhinological disorders.
Previous studies were performed to clarify whether the presence of CLP affects the size and development of the maxillary sinus based on the following assumptions. First, in these patients, an absence of adhesion between the medial nasal process and the maxillary process is at the origin of the defect. The medial nasal process is responsible not only for the development of the primary palate, comprising premaxilla and its alveolus, but also for other midface structures, such as the medial portion of the maxilla, lip, and nose. This relation suggests an anatomic or structural difference in maxillary sinus development between cleft and noncleft patients. Second, patients affected by CLP are most susceptible to developing midfacial hypoplasia associated with a dental and skeletal Class III malocclusion and there is evidence that maxillary hypoplasia is a cause of the hypoplastic maxillary sinus. , , , However, this remains under debate as there are conflicting results in the literature.
In addition, other previous studies performed a 2-dimensional evaluation of a 3D structure, focusing on the size and area of the maxillary sinus. This approach not only introduced biases but also did not accurately describe the total dimension of the maxillary sinus. , , ,
Cone-beam computed tomography (CBCT) has been recently used in maxillary sinus volumetric evaluation, but there is a limited number of studies based on a 3D evaluation of maxillary sinus volume that includes patients with unilateral cleft lip and palate (UCLP). , , The advent of high-resolution images can help to explain some of the variability in the volume of the maxillary sinus between different populational groups, allowing a better knowledge of the development of the maxillary sinus and the impact of age and sex on its dimensions.
This study intended to evaluate the effect of possible influencing factors on the volume of the maxillary sinus, including side, age, sex, and the presence of congenital anomalies such as CLP. Therefore, the authors hypothesized that (1) there are differences in the maxillary sinus volume between patients with UCLP and healthy controls (noncleft group), (2) maxillary sinus volume of the cleft side is smaller than the noncleft side in the UCLP group, (3) there are no differences in the maxillary sinus volume on the left and right sides in the control group, and (4) age and sex influence the maxillary sinus volume in both groups.
Material and methods
In this retrospective case-control study, the tomographic images of all participants were collected from the database of the patients who underwent CBCT scans of the skull at the Medical Imaging Department of the Coimbra Hospital and University Centre between January 2016 and April 2019.
Initially, 924 patients were included in the study after applying the following inclusion criteria: white patients of both sexes aged between 4 and 25 years, with at least 1 CBCT image acquired before the beginning of orthodontic treatment. In the remaining patients, the exclusion criteria were then applied, with 502 patients being excluded because of the presence of pathologic processes, radiopacifications or image artifacts on the maxillary sinus, CBCT images with a small field of view, craniofacial syndromes, patients with cleft lip or cleft palate only, and bilateral CLP.
Among the remaining 422 patients, 93 were allocated to the UCLP group (n = 40 right UCLP; n = 53 left UCLP) and 329 to the control group.
To ensure a reliable and unbiased comparison between the UCLP groups, the left UCLP patients were matched with the right ones, regarding age and sex.
The control group was also matched to the UCLP group, reducing patients from 329 to 80. Thus, the final sample consisted of 160 patients ( Fig 1 ): (1) 80 UCLP patients (41 males and 39 females; mean age, 12.70 ± 6.03 years), and (2) 80 control patients (43 males and 37 females; mean age, 13.10 ± 6.27 years).
All participants, or parents when applicable, signed written informed consent for their participation. The protocol was approved by the ethics committee of the institution mentioned above (Reference no. 060-CE-2019) in accordance with the Declaration of Helsinki.
The imaging data were obtained using an i-CAT Vision scanner (Imaging Sciences International, Hatfield, Pa) with the following imaging parameters: 120 kVp, 5 mA, 4 seconds scanning time with an axial layer thickness of 1 mm, 16 × 10 cm field of view, and 0.30 mm 3 voxel size.
The data were saved and stored in Digital Imaging and Communications in Medicine files, and the volumes of the maxillary right and left sinuses, 320 in total, were subsequently measured and analyzed using a 3D-imaging software package, ITK-SNAP (version 3.8.0; Cognitica, Philadelphia, Pa), according to a semiautomatic segmentation method ( Fig 2 ). This software was validated as a segmentation tool used in neuroimaging and biomedical imaging research with the advantage of being free to access (available at www.itksnap.org ), and is therefore widely used by medical professionals. Furthermore, previous studies confirm its reproducibility and reliability in the segmentation of distinct anatomic structures, demonstrating its ease of use for different observers.
Statistical analysis
The statistical analysis was performed using SPSS (version 24.0; SPSS Inc, Chicago, Ill). A statistical significance level of 0.05 was adopted.
The sample size was obtained by using G-Power (version 3.1.9.2; Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany). A minimum of 44 patients was required in each group, assuming a bilateral Student t test for independent samples, an allocation rate of 1:1, a significance level of 0.05, and a power of 80% to display an effect size of 0.61 for the maxillary sinus volume in a UCLP and control groups.
Descriptive statistics for the current data were obtained using mean and standard deviation values.
Considering that both right and maxillary left sinus volumes were measured, either one could be used in the analyses. Thus, to determine which one would be better, the volumes of both sides in each group were compared using an agreement test and a linear regression equation. The results obtained suggest that the volume is independent of the side; hence, the average volume of both sides was used in the remaining analyses.
To assess the differences regarding age and sex frequencies between groups, we used the Mann-Whitney U test and Fisher exact test, respectively.
The difference between the average volumes of the maxillary sinuses on both groups was tested with an analysis of covariance (ANCOVA) test using age as a covariate. To determine the error of the performed analysis, we randomly selected and measured 50 CBCT images twice by the same investigator (M.R.) 1 month after the first examination. The agreement level between observations was assessed by intraclass correlation coefficient (ICC) and Bland-Altman analysis.
Results
The results for intrarater reliability have shown a very strong agreement (ICC = 0.997; P < 0.001) on the maxillary sinus volume measurements.
Table I presents descriptive statistics concerning age and sex distribution of the subjects studied. A homogenous distribution, with no statistically significant differences between both groups (control vs UCLP) was observed.
| Variables | Control group (n = 80) | UCLP group (n = 80) | P value |
|---|---|---|---|
| Age, y | 13.10 ± 6.27 | 12.70 ± 6.03 | 0.723 ∗ |
| Sex | |||
| Male | 43 (53.80) | 41 (51.30) | 0.874 † |
| Female | 37 (56.30) | 39 (48.80) |
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