INTRODUCTION

Bronchial asthma is characterized as a chronic inflammation of the lower airways, leading to episodes of partial obstruction of the airflow, which are reversible spontaneously or with drug therapy.1,2 Such episodes usually occur when a patient inhales an antigen to which he or she is allergic or shows irritation.3,4

Although the prevalence of asthma in the adolescent population is nearly 6.9%, the disease has shown a significant increase in incidence in the past few years. Thus, it has become an ever-growing problem in public health, with more than 300 million patients throughout the world.5

Even if asthma is described as a pathology of the lower airways, a number of studies have shown that an impairment of the upper airways (UAWs) is often also observed, thereby affecting the normal conditions of craniofacial development.6–8 Patients with asthma may have a greater prevalence of malocclusions, especially presence of an overbite, an overjet, a maxillary growth deficiency, and a smaller intercanine and intermolar distance, all of which increase the chance of overcrowding, particularly when the disease is established prematurely or before the age of 14.6,9 Thus, it is important that, when evaluating a child, an adolescent, or an adult, the orthodontist observe these signals and symptoms in order to propose a correct treatment for the patient, together with the medical treatment.6

Regarding image diagnosis, a lateral cephalogram is part of early orthodontic documentation, and its assessment has allowed orthodontists to observe possible UAW obstructions. Measurements in the sagittal plane, however, are not accurate as this methodology has important limitations, with errors that are inherent to a two-dimensional representation of complex three-dimensional structures.9–11 Hence, cone-beam computed tomography (CBCT) has been introduced as a new and effective diagnosis method to evaluate UAWs, because images are obtained in three dimensions.10–14

Taking into account the lack of studies involving three-dimensional assessment of the UAWs in patients with asthma, this study aimed to test the following null hypothesis: no difference exists between the total volume (TV) of the UAWs, the nasopharyngeal narrowest area (NNA), and the oropharyngeal narrowest area (ONA) in patients with or without bronchial asthma.

MATERIALS AND METHODS

UAW TV Assessment

To delimit UAW TV (nasopharynx and oropharynx), the analysis was started by an image sagittal plane reconstruction. Hence, the following anatomic limits were determined sequentially:

1. Lower limit: the caudal medial point of the third cervical vertebra was located and, in a straight line, continued toward the front limit, so that the projection of the posterior nasal spine (PNS) could be seen;14

2. Anterior limit: a straight vertical line passing through the PNS point;

3. Upper limit: a horizontal line passing through the lower point in the border of the sphenoidal sinus;

4. Posterior limit: a vertical plane was determined from the upper limit up to the caudal medial point of the third cervical vertebra, so that the anatomic delimitation was completed in the sagittal plane (Figure 1).

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In addition, the limits were checked in the coronal and axial planes to certify that the lateral wall of the pharynx included all lateral projections. After the anatomic delimitation, the entire aerial space was lined out and filled in with seed points. Another check had to be made in all planes of visualization to make sure that the area lined out with seed points had been totally filled (Figure 2).

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RESULTS

The asthmatic and control groups were paired regarding age (P  =  .28), gender (P  =  .57), type of malocclusion (P  =  08), and cephalometric characteristics (SNA, P  =  .10; SNB, P  =  .28; ANB, P  =  .25; FMA, P  =  .19). Excellent reliability was observed in the methods to evaluate UAWs and cephalometric variables18 (Table 1).

Table 1. Reliability of the Method for Assessing UAW and Cephalometric Variables According to Mean, Standard Deviation (SD), Intraclass Correlation Coefficient (ICC), and Bland-Altman Agreement

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The asthmatic group had a significantly lower TV (16.76%; P  =  .01) and a lower ONA (25.78%; P  =  .007) than the control group. However, no statistical difference was observed in NNA between the groups (P  =  .54) (Table 2).

Table 2. TV, NNA, and ONA in Control and Asthmatic Groups According to Mean, Standard Deviation (SD), and Independent t-Test (P)

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No statistical differences were found between TV (P  =  .91), NNA (P  =  .31), and ONA (P  =  .07) between the groups of patients with intermittent/mild or moderate/severe asthma (Table 3).

Table 3. TV, NNA, and ONA in the Asthmatic Group by Severity of Asthma According to Mean, Standard Deviation (SD), and Independent t-Test (P)

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DISCUSSION

This study compared the dimensions of the UAWs in youths with and without asthma. The TV and the ONA had significantly smaller dimensions for the asthmatic group compared with the control group (Table 2). These results can be explained by the strong relationship of asthma with alterations in the UAW,3,4,6,19–21 especially chronic allergic rhinitis.6–8

Several studies4,21–24 have shown that asthma and allergic rhinitis are clinical manifestations of the same disease. In fact, rhinitis is a risk factor for the development and aggravation of asthma. Kim and Rubin22 also suggested a neural interaction between upper and lower airways as the inflammation of the nasal mucosa and the nasal aspiration of secretions in patients with rhinitis induce inflammation of the bronchial mucosa. Moreover, the airway walls were thicker in patients with asthma than in healthy persons, which could indicate a greater narrowing of this region.6–8

Gupta et al.25 evaluated 185 computed tomography scans of patients with severe asthma, and found anatomic abnormalities of the airways in 80% of them. Of these, 62% had greater thickness of the airway walls. In addition, also using quantitative techniques, Aysola et al.23 and Niimi et al.24 found the same indexes of thickening of airway walls. These authors found a strong relationship between the thickness of airway walls and the severity and time of occurrence of the asthma as well as an inverse correlation between the thickness of the wall and the airway area.

However, no significant difference was observed for the NNA between the groups in our study (Table 2). These results are probably due to the great topographic variability of the nasopharyngeal region, observed patients with and without asthma. This characteristic of the nasopharynx has been previously described.4,12–14,26,27

Asthma has different degrees of severity, which may influence patients' different responses to several conditions.4,6,21,28 For this sample, however, no statistical difference was found between the groups with intermittent/mild and moderate/severe asthma (Table 3). It may be that when the asthmatic group was stratified for asthma severity, each subgroup had 13 persons, which probably limited the evaluation of this variable. Therefore, studies with a greater number of patients with moderate/severe degrees of severity are suggested to better understand the role of this variable in UAW alterations. In the present study, the asthmatic and control groups were similar in terms of age, gender, type of malocclusion, and cephalometric characteristics.

Taking age into account, the airways show rapid development in childhood; after this period, these structures seem to show little alteration, which only occurs again after adulthood.26 Regarding gender, Grauer et al.14 suggested that males have significantly greater volumetric measurements than females, and they emphasized the importance of controlling this parameter when dimensions of the UAWs are assessed. Considering the type of malocclusion (Class I and Class II) when assessing the UAW, Freitas et al.29 showed that persons with Class II malocclusion with a pattern of vertical development had a narrower pharnyx. Grauer et al.14 showed that persons with different patterns of maxillomandibular development in the anteroposterior and vertical directions could have differences in the shape of the UAW. Kim et al.13 showed that the total airway volume in patients with a retrognathic profile was significantly lower than that found for patients with clinically normal growth. In this study, care was taken to match the groups regarding the characteristics described previously, so it was possible to eliminate the interference of these variables in comparisons between the groups.

The sample analysis showed that 52 CBCT scans are sufficient to detect differences between groups, with an 80% testing power. Other studies have evaluated airways with a similar number of patients.11–14,26,27

Another relevant aspect was the concern for the standardization of the patients' position and the breathing/swallowing relationship while the CBCT scan was taken. Exams carried out with the patient in a supine position may reflect a mandibular position that is different from that which is habitual.30 For this study, patients remained seated while the CBCT scans were taken, as this position better reproduces the daily state of the UAWs.14

Regarding the results obtained, special attention should be given to patients with bronchial asthma, because the reduction in the dimensions of the airways may reflect the mandibular posture and lip closure, leading to functional and esthetic alterations and malocclusion. Therefore, a multidisciplinary treatment should be proposed in order to reach clinical success and long-term stability.

CONCLUSIONS

• The proposed null hypothesis was rejected because the patients with asthma showed significant reductions in the dimensions of the UAWs.