ABSTRACT

Objective

To compare the pharyngeal airway size and area between Class III patients exhibiting optimal vertical growth direction and Class I patients at the MP3cap stage, considering gender differences.

Methods

This retrospective study analyzed pre-treatment cephalograms of a total of 180 patients with Class I (45 girls, 45 boys) and Class III (maxilla or maxillo-mandibular origin) (45 girls, 45 boys) malocclusions. Linear and angular measurements were conducted on lateral cephalograms utilizing the GNU Image Manipulation Program (GIMP 2.10.18, NY, USA; https://www.gimp.org/). The pharyngeal airway areas were computed utilizing AUTOCAD (Autodesk 2018, San Rafael, CA, USA). The Independent Samples t-test and Mann-Whitney U test were employed for comparative analysis of variables across groups. The forward selection method was employed in conjunction with regression analysis.

Results

No significant differences were observed in the nasopharyngeal area (NA; mm2) across the malocclusion groups and genders. In Class III girls, the oropharyngeal area (OA; mm2), retroglossal (RG; mm2) area, and superior pharyngeal space (SPS; mm) were significantly larger than those of Class III boys, and Class I girls (p<0.05). The inferior pharyngeal space (IPS; mm) was significantly larger in Class III girls compared to Class III boys (p<0.05). Girls with Class I/III malocclusions demonstrated a more pronounced head posture than boys (p<0.05).

Conclusion

The findings indicate the necessity of accounting for gender-specific variations in Class I and III patients, as well as evaluating pharyngeal airway characteristics in orthodontic diagnosis and treatment planning. In Class III girls, the OA and RG areas, as well as the superior and inferior pharyngeal spaces, were larger compared to Class III boys.

Keywords:

Airway, Class I, Class III malocclusion, pharyngeal

Main Points

• The dimensions of the nasopharyngeal area were similar across different malocclusion groups and genders.

• The inferior pharyngeal space was larger in girls with Class III malocclusion compared to boys with the same condition.

• Girls displayed a more extensive head posture than boys in both Class I and Class III malocclusions.

• When planning orthodontic treatment during the growth and development period, it is important to consider the age, gender, and malocclusion characteristics in relation to the pharyngeal airway.

INTRODUCTION

The pharyngeal airway is a complex structure closely associated with the maxilla and mandible. The etiology of Class III malocclusion and the variability of the maxillomandibular sagittal relationship are associated with alterations in airway and breathing patterns.¹ In recent years, the number of studies evaluating the relationship between malocclusions and the pharyngeal airway has increased in the literature.^{2, 3} Although numerous studies have assessed the impact of various treatments for skeletal Class III malocclusion on the pharyngeal airway^4-7there is a paucity of research examining the pharyngeal airway in untreated Class III patients. Furthermore, disparate findings have emerged, attributed to variations in age, gender, and methodological approaches among the studies.^{2, 3, 8-11} Thus, it is essential to investigate the relationship between Class III malocclusion and the pharyngeal airway within homogeneous groups.

This study aimed to compare the pharyngeal airway size and area between Class III patients exhibiting optimal vertical growth and Class I patients during the MP3cap growth period, across both genders. The number of studies establishing pharyngeal airway normative values in Class I patients is limited, and current research frequently includes a small sample size and skeletal measurements.^12-14 Consequently, our secondary objective was to establish the normative values of airway dimensions in Class I subjects exhibiting optimal sagittal and vertical growth patterns, underscoring the necessity for additional research.

METHODS

This retrospective study examined the pre-treatment lateral cephalograms of 180 patients (90 boys and 90 girls) with Class I (45 girls, 45 boys) and Class III (45 girls, 45 boys) malocclusions, referred to the orthodontic clinic of the University. Parents of all participating children were informed, and the study protocol received approval from the Measurement and Evaluation Ethics Sub-Working Group of the Gazi University (approval no.: 2020-465, date: 08.09.2020). Informed consent forms were obtained from each patient.

Power analysis was performed utilizing G*Power 3.1.9.7 (University of Düsseldorf, Düsseldorf, Germany) to ascertain the necessary sample size for the skeletal Class I and III malocclusion groups. This study utilized data from analogous prior research as references for the ANB angle, nasopharyngeal airway area, and oropharyngeal airway area.¹⁶The sample size of 87 patients per group at α=0.05 provides a statistical power of 95% for this study; however, it was increased to 90 to achieve equal gender distribution. The inclusion criteria for the Class I group were established as follows: ANB angle ranging from 0 to 4°, SN/GoGn angle between 26 and 38°, MP3cap growth development period (the epiphysis of the middle phalanx of the third finger is equal to or wider than the metaphysis, with lateral sides exhibiting initial capping towards the metaphysis), and chronological age between 10 and 14 years. The inclusion criteria for the Class III group were: a negative ANB angle, a skeletal Class III anomaly originating from the maxilla or maxillo-mandibular region, Angle Class III malocclusion, an SN/GoGn angle ranging from 26° to 38°, anterior crossbite, MP3cap growth development period, and a chronological age between 10 and 14 years (Figure 1).

The study analyzed 11088 patients from the digital archive of the orthodontic department, excluding individuals with ANB angles exceeding 4°, SN/GoGn greater than 38°, SN/GoGN less than 26°, and those not in the MP3cap growth and development stage, as well as those exhibiting accelerated or retarded growth with a deviation of more than one year between chronological and skeletal ages. Furthermore, individuals with a prior history of orthodontic treatment, upper airway pathology, or oral respiration were excluded from the study. Patient selection for each malocclusion class and gender group was conducted using random number generation in Excel, yielding 45 randomly selected patients per group. Figure 1 illustrates the flow chart developed for patient selection criteria.

Lateral cephalograms were obtained under standardized conditions, with the head stabilized using a cephalostat, teeth in centric occlusion, and the Frankfort horizontal plane aligned parallel to the floor. Linear and angular measurements of lateral cephalograms were conducted by a single researcher utilizing the GNU Image Manipulation Program (GIMP 2.10.18, NY, USA; https://www.gimp.org/). Fifteen lateral cephalograms from each group were randomly selected, re-digitized, and recalculated by the same researcher two weeks later to assess the reliability of the method. The pharyngeal airway areas were calculated utilizing AUTOCAD (Autodesk 2018, San Rafael, CA, USA). Cephalometric radiographs were aligned based on a plane with a specified measurement in millimeters, after which the “Measure” command was utilized to select the corner points of the airway region for measurement purposes. Linear measurements and airway areas were ultimately compared across the groups (Figure 2, Table 1).

Statistical Analysis

Data analysis was conducted using IBM version 20.0 (IBM Corp., Armonk, NY, USA). The Shapiro-Wilk test was employed to assess normality. The statistical analysis utilized the Independent Samples t-test and the Mann-Whitney U test for comparing variables between groups. A significance level of p<0.05 was deemed statistically significant. A multiple linear regression analysis was conducted to identify cephalometric measurements that may influence pharyngeal airway measurements.

The multiple linear regression analysis utilized the “forward selection” method to select independent variables for inclusion in the model. Independent variables with a p-value less than 0.20 were deemed eligible for inclusion in the multiple linear regression model.

RESULTS

The measurements for each parameter were evaluated for reliability using the intra-class correlation coefficient, yielding statistically significant results (p<0.001), which indicates high reliability. The chronological ages of girls with skeletal Class I (137.2±9.1 months) and Class III (138.9±11.2 months) malocclusions were comparable. No significant differences were observed in the ages of boys with Class III (145.4±9.8 months) and Class I (143.8±9.4 months) malocclusions. The chronological and skeletal ages of boys with Class I malocclusions were significantly greater than those of girls with Class I malocclusions (p=0.001, p<0.001, respectively). The chronological and skeletal ages of the Class III boys were significantly higher than those of the Class III girls (p<0.01, p<0.001; respectively).

Comparisons Between Malocclusions

Boys with Class I malocclusion had higher Co-A and ANB values, and a smaller SNB angle than boys with Class III malocclusion (p<0.001). In Class I boys, AA’-Pm’ and AA-PNS dimensions were found to be significantly larger than those in Class III boys (p<0.05).

The Co-A length, SNA, and ANB angles were significantly higher in skeletal Class I girls compared to Class III girls (p<0.001, p<0.01, p<0.001; respectively). The SNB angle and Co-Gn distance were observed to be smaller in Class I girls compared to Class III girls (p<0.001, p<0.05, respectively). The oropharyngeal area (OA) and retroglossal (RG) area were significantly smaller in skeletal Class I girls compared to Class III girls (p<0.001, p=0.001; respectively). Class III girls exhibited greater nasopharyngeal height (S-PNS) and upper airway width (SPS), along with a more anterior and lower hyoid bone position compared to Class I girls (p<0.05) (Tables 2, 3).

Comparisons Between Gender

Mandibular effective length (Co-Gn) was found to be greater in Class I boys than Class I girls (p<0.01). N-Me, ANS-Me, and H-SN dimensions were found to be greater whereas SNB angle is smaller in Class I boys than in Class I girls (p<0.001). The S-PNS in Class I boys was found to be greater than in Class I girls (p<0.01). Girls with Class I malocclusion have a more extensive head position than boys due to SN/CVT angle (p<0.05).

The skeletal measurements of boys and girls exhibiting Class III malocclusion were comparable. In Class III girls, OA (p<0.05), RG (p<0.01), SPS (p<0.05), lower airway width (IPS) (p<0.05), and airway width at epiglottis level (eb-Peb) (p<0.05) were found to be greater than those in Class III boys. The hyoid position relative to the mandible (H-MP) was significantly lower in Class III girls compared to Class III boys (p<0.01). Class III girls exhibit a more pronounced head position compared to Class III boys (p<0.001) (Tables 2, 3).

Regression Analysis

The multiple linear regression analysis utilizing the “forward selection” method indicated that in Class III boys, cephalometric measurements and NA are significantly explained by SNA, while RP area is significantly explained by N-Me (p<0.05) (Tables 4, 5). The regression model indicates that the RP area is explained by the N-ANS and Co-A variables, while NA is explained by the Co-Gn length in Class III girls (p<0.05) (Tables 4, 5).

DISCUSSION

Orthodontic treatment may potentially affect the upper airway.¹⁵ Narrowing of the upper respiratory tract can lead to snoring and obstructive sleep apnea (OSA), adversely impacting sleep quality.¹⁵Recent investigations indicate that patients with OSA display dentofacial morphological characteristics linked to a constricted upper airway, including a retrusive mandible, a vertical mandibular plane, a dorsally positioned tongue, and an extended soft palate.¹⁷ The literature discusses the impacts of various orthodontic, orthopedic, functional, and orthognathic surgical interventions on the upper airway.^4-7 Additionally, several studies evaluated the upper airway according to various types of malocclusions.²^,³^,⁷^,¹¹^,¹⁸ However, these studies often had a wide distribution of ages among the malocclusion groups, based on chronological age, or evaluated both genders together. Buyukcavus et al.² did not consider the vertical dimension in their classification of Class III patients, grouping them solely based on the ANB, SNA, SNB values as maxillary retrognathism, mandibular prognathism, or a combination of them. In our study, we classified the patients based on the Co-A and Co-Gn values, the ideal SN/GoGn angle range was chosen considering the vertical dimension known to affect the airway. This study represents the first evaluation of airways in Class III patients during the MP3cap growth period. This study establishes the normative values of airway dimensions in patients with Class I dentofacial structure during the MP3cap growth period for both genders.

Bench et al.¹⁹reported that the level of the hyoid bone descends with chronological age. Developmental changes are observed in both pharyngeal airway depth and hyoid position with chronological age.¹⁹^,²⁰ The sagittal nasopharyngeal airway is narrowest at five years of age, increases until ten slightly decreases between 10-11 years of age, and increases again after 11 years of age.²⁰ However, there is no study in the literature that has considered skeletal ages during airway evaluation and several studies have reported a significant but low correlation between chronological ages and skeletal ages in girls.²¹^,²² Utilizing comparable skeletal ages and growth periods may reduce the influence of age, yielding more precise data in evaluating airway dimensions and facilitating a deeper comprehension of airway development and changes during growth. Boys in both malocclusion groups demonstrated greater skeletal and chronological ages compared to girls, with a statistically significant difference observed. This disparity is due to the earlier onset of the growth spurt (MP3cap) in girls compared to boys during the growth and development phase.

The gold standard method for diagnosing OSA is polysomnography (PSG).²³However, cone-beam computed tomography (CBCT) has gained popularity as a convenient and less time-consuming diagnostic tool, especially due to its relatively lower cost as compared to PSG.²⁴While lateral cephalograms created using CBCT images are considered a practical and convenient method to assess the airway, there may be differences observed on the right and left sides.²⁵ The lateral cephalogram is a simple, low-cost, and easily renewable 2-dimensional image that is more suitable for retrospective studies. Pracharktam et al.²⁶ evaluated the upper airway passage in two positions, sitting upright and lying down, and reported similar airway measurements between the two positions using 2D cephalograms. In our study, lateral cephalograms were taken while the patients were in their natural upright position.

Bozzini et al.²⁷ employed a 40-second protocol for CBCT scanning, sufficient for patients to hold their breath and stabilize their head position. Hong et al.²⁸ employed a 15-second time protocol for CBCT scanning. The duration required to obtain lateral cephalometric radiographs in our study was 14.9 seconds. The short duration facilitates breath-holding in patients, resulting in more dependable radiographs for airway evaluation.

Ucar et al.²⁹ observed that low-angle patients exhibited a greater nasopharyngeal airway area and upper airway dimensions than high-angle patients. Alhammadi et al.³⁰ reported that vertical positioning of the mandible enhances airway volume while accommodating collapse resulting from the posterior position of the mandible. Only patients exhibiting optimal vertical growth patterns were included in this study to minimize variation. Since the literature shows differing opinions on the relationship between gender and airway dimensions,¹⁰^,¹⁴^,³¹ the airway was evaluated separately for each gender in this study.

Jena et al.⁹ reported that skeletal parameters, particularly mandibular prognathism, influence airway dimensions. This study included only Class III patients from the maxilla or maxillomandibular regions, excluding those from the mandible. The present study indicates that Class III boys exhibited significantly lower measurements of pharyngeal width in the anteroposterior direction at the adenoid level (AA-PNS, AA’-Pm’) compared to Class I boys. Class III girls exhibited a significantly larger OA and RG area in comparison to Class I girls. Furthermore, SPS and IPS measurements exhibited greater values in Class III girls. The observed results may be attributed to the inferior and anterior positioning of the hyoid bone, along with an extended head posture in Class III girls. Consistent with our findings; Iwasaki et al.¹⁰ reported that Class III patients exhibited a wider oropharyngeal airway than Class I patients at 8 years of chronological age using CBCT images. Trenouth and Timms reported a positive correlation between oropharyngeal airway and mandibular length in children aged 10 to 13.³² However, Takemoto et al.¹³found that the lower pharyngeal airway size was larger in Class III girls originating from the mandible compared to those in Class I; however, no significant differences were noted in the sizes of the upper airway. The study found that an anterior mandibular position in girls aged 7-8 years correlates with an increased width of the lower pharyngeal airway.

Takemoto et al.¹³ observed no significant differences in upper airway dimensions between Class III and Class I girls at the age of 8. Zhong et al.³³ classified Class I and Class III Chinese children according to mandibular plane angle and ANB angle, revealing no significant differences in upper pharyngeal space measurements. Chan et al.³⁴ similarly found no significant differences in the nasopharyngeal region across various malocclusions. The authors found that NA was comparable in both Class III and Class I groups across genders. The patients in our study had an average age of approximately 12 years, and the growth and development of the airway were found to be more stable, as reported by Taylor et al.³⁵.

Ceylan and Oktay¹¹reported a negative impact of an elevated ANB angle on the dimensions of the NA in their study, which evaluated both genders collectively and compared Class I, II, and III malocclusions. All subjects in the study were aged between 13 and 15 years. No significant differences in NA were observed between Class I and Class III malocclusion groups across both genders. The regression analysis indicated that NA is explicable by SNA in Class III boys and Co-Gn in Class III girls. No significant difference was observed in the SNA angle between Class III and Class I boys. The anticipated increase in NA for Class III girls, linked to the rise in mandibular effective length, was not observed. This absence of difference may be explained by the malocclusion stemming from maxilla-mandibular discrepancy and a reduced SNA angle. The authors found that an increased ANB angle correlated with a decrease in OA and noted a higher positioning of the hyoid bone in Class III children compared to Class I children. In contrast to that study, our research indicates that the hyoid bone is positioned lower, and the OA was larger exclusively in Class III girls.

A significant regression model was identified in Class III girls, linking RP area, upper anterior facial height, and upper maxillary effective size. Bozzini et al.²⁷ reported a moderate positive correlation between nasal area and facial height, as well as between the RP area and upper anterior facial height in Class III girls approximately 26 years of age.

Gökçe et al.¹⁴ conducted a comparison of pharyngeal measurements between male and female adults with Class I malocclusion, revealing statistically significant greater sagittal pharyngeal dimensions in males, with the exception of craniocervical angles related to head posture. Our study revealed that only S-PNS was significantly greater in Class I boys, while other pharyngeal measurements were comparable between genders within the Class I malocclusion group. This discrepancy may be attributed to the age differences between our study and that of Gökçe et al.¹⁴.

Hellsing et al.³⁶ found correlation between head position and cervical lordosis, on lateral cephalograms; increase in the size of the pharyngeal airway. Huggare et al.³⁷found that head extension positively influenced nasorespiratory function. The present study noted an increase in airway dimensions in Class III females, characterized by an extended head (an increase of 200 in the SN/OPT angle) and a lowered hyoid bone position. In contrast to our study, Alves et al.²⁵ evaluated adult patients and found that RP and RG volumes were significantly larger in Class III males compared to Class III females.

The McNamara analysis¹² indicates that in the Ann Arbor adult samples, the average upper airway measurement is 17.4 mm, with a tendency for this measurement to increase with age. The mean lower airway measurements range from 10 to 12 mm, with no significant changes observed with age. In the present study, we found that the median [minimum, maximum (min., max.)] upper airway measurements (ad1-PNS) for Class I and Class III boys were 19 (11, 25) mm and 19 (7, 28) mm, respectively. The median lower airway measurements (IPS) were 9 (4, 14) mm and 9 (6, 18) mm, respectively. The median (min., max.) upper airway measurements (ad1-PNS) for Class I and Class III girls were 19.0 (7-28) mm and 19.0 (7-25) mm, respectively. The median lower airway measurements (IPS) were 9.7±3.2 mm and 10.7±2.9 mm, respectively. The findings underscore the importance of gender differences in airway measurements.

Our results indicate that the airway must be thoroughly assessed in orthodontic diagnosis and treatment planning, considering age-related factors for each gender. In particular, the application of treatments that narrow the airway and induce clockwise rotation of the mandible may be approached with reduced clinical concern in females, given that this area is wider compared to males of the same age. Furthermore, implementing multidisciplinary treatments in conjunction with ENT specialists would be advantageous.

Strengths and Limitations

All patients’ radiographs were obtained using the same cephalometric radiography device, in a consistent environment, and with subjects positioned in a natural head posture. Furthermore, patients were chosen within a defined age range (10-14 years) and at the same growth and development stage (MP3cap) to minimize age-related variations. Additionally, to control for gender effects, measurements were assessed independently for each gender and subsequently compared across genders.

Multiple measurements were conducted to characterize the airway, thus eliminating dependence on a singular parameter. The study participants demonstrated optimal vertical growth direction.

A limitation of this study may be the absence of assessment for body mass index or obesity scores, attributable to its retrospective design. Additional limitations include the absence of longitudinal follow-up and the reliance on two-dimensional evaluation for assessing the pharyngeal airway. Future research should employ longitudinal designs to monitor alterations in airway dimensions over time. Additionally, focusing on Class III patients with mandibular prognathism and integrating comprehensive clinical evaluations of breathing by ear, nose, and throat specialists would be advantageous.

CONCLUSION

There are no differences in the nasopharyngeal area dimensions when comparing different malocclusion groups or genders. In Class III girls, the oropharyngeal, RG, and superior pharyngeal space were larger than Class III boys, and larger than Class I girls. The inferior pharyngeal space was larger in Class III girls than Class III boys. Girls with both Class I and Class III malocclusions exhibited a more extensive head posture compared to boys.

Ethics

Ethics Committee Approval: The study protocol received approval from the Measurement and Evaluation Ethics Sub-Working Group of the Gazi University (approval no.: 2020-465, date: 08.09.2020).

Informed Consent: Informed consent forms were obtained from each patient.

Author Contributions: Surgical and Medical Practices - M.K., E.K.; Concept - M.K., E.K.; Design - E.K.; Data Collection and/or Processing - M.K.; Analysis and/or Interpretation - B.Ç.; Literature Search - M.K., B.Ç., E.K.; Writing - M.K., B.Ç., E.K.

Conflict of Interest: The authors have no conflicts of interest to declare.

Financial Disclosure: This study did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Gender-based Comparison of Pharyngeal Airway Between Class I and Class III Patients During MP3cap Growth Period