Influences of Airway Obstruction Caused by Adenoid Hypertrophy on Growth and Development of Craniomaxillofacial Structure and Respiratory Function in Children.

Adenoid hypertrophy (AH) is a common disease in otorhinolaryngology. Children with chronic snoring and hypoxia are susceptible to long-term nasal obstruction, while long-term open-mouth breathing may cause craniofacial bone development disorders and dull facial expressions, the so-called adenoid face. The purpose of this work is to analyze the influence of AH-induced airway obstruction (AO) on the growth and development of craniomaxillofacial structure and respiratory function (RF) in children. The clinical data of 56 AH children (observation group) and 42 healthy children with physical examination (control group) who visited the Hebei Eye Hospital during the same period were retrospectively analyzed. All children received acoustic rhinometry and X-ray cephalometric measurements. The upper airway structure, sleep disorder score, and A/N value of nasopharyngeal lateral X-ray images were compared between cases and controls. For AH children, sleep tests were also performed to assess their RF. X-ray cephalometric measurements of facial morphology showed obvious vertical growth, mandibular retrognathia, and enlarged mandibular angle in AH children. AH mainly affects the size of the nasopharyngeal and oropharyngeal airway. AH children presented with higher nasal airway resistance (5.11 ± 1.95 cmH2O/L min) and lower nasopharyngeal volume (NPV) (16.86 ± 3.93 cm3) than controls. Of the AH children, 45 had abnormal RF, including 4 with obstructive sleep apnea syndrome. The A/N value of nasopharyngeal lateral X-ray images was significantly higher in AH children than in controls. Besides, worse sleep quality was found in AH children. The above differences were all of statistical significance. The above indicates that AH can affect the size of the nasopharyngeal and oropharyngeal airway, change children's respiratory mode and RF, increase nasal resistance, and decrease NPV, resulting in upper respiratory tract stenosis, as well as craniomaxillofacial and oral malformations, which affects children's normal growth and development.

1. Introduction

Adenoid hypertrophy (AH), the most common cause of upper airway obstruction (AO) in children and adolescents, is a natural response to the increase of immune activity in childhood [1, 2]. The normal breathing pattern of human beings is nasal respiration, which means that air travels through the nasal, nasopharyngeal, oropharyngeal, and laryngopharyngeal cavity into the lower airway [3]. If the airflow is obstructed through the respiratory tract, that is, the passage is partially or completely blocked, the human body will adaptively change the nasal breathing mode into the oral breathing mode, so as to obtain sufficient ventilation to maintain normal physiological functions [4]. Open-mouth breathing (OMB), nasal diseases, asthma, speech disorders, and obstructive sleep apnea syndrome (OSAS) are common health issues that can be induced to some extent by inflammation and/or obstruction of the upper respiratory tract [5, 6]. The adenoid is a local immune organ [7] and an important part of the pharyngeal lymphatic ring, which, together with the palatine tonsil, lingual tonsil, eustachian tube tonsil, lateral pharyngeal bands, and posterior pharyngeal lymphoid follicles, forms an endolymphatic ring, surrounding the airway and esophageal entrance [8, 9]. It is the site of the earliest exposure to inhaled and ingested antigens. When the adenoids or the peripheral lymphoid tissues are exposed to antigen stimulation and immune response occurs, adenoid tissue proliferates and increases in volume, resulting in AH [10].

AH can cause a wide spectrum of diseases, including secretory otitis media [11], sinusitis [12], obstructive sleep apnea-hypopnea syndrome (OSAHS) [13], lower respiratory tract inflammation [14], long-term hypoxia-induced abnormal growth and development, and mental and psychological disorders. AH is an important factor for children to breathe with their mouths open. Long-term OMB in childhood will inevitably lead to abnormal development of maxillofacial bone structure. For example, narrow dental arch, high-arched palate, anterior protrusion of upper incisors, crowded and uneven dentition leading to malocclusion, and uneven development of facial bones can cause abnormal development of nasal septum, resulting in deviation of nasal septum and turbinate hypertrophy [15, 16]. Children with OMB can suffer from sleep deprivation at night, long-term lack of oxygen, lethargy, and dull facial expression, resulting in the classic adenoid face [17]. As for the time of craniofacial development, the increase of upper airway resistance in any period may change the normal breathing mode and thus affect craniofacial development, while the age group with high incidence of AH is in the critical period of craniofacial development. At this stage, the detection and diagnosis of AH are still relatively complex, requiring nasal endoscopy, nasopharyngeal palpation, and X-ray examinations to make a definite diagnosis [18]. So far, the research on AH mainly focuses on its resultant nasal obstruction, while its effect on upper airway bone structure is rarely reported [19, 20].

Consequently, it is crucial to master diagnostic methods and timely judge the degree of illness. The novelty and motivation of the presented study is to use X-ray cephalometry as the breakthrough point to measure the maxillofacial structure of AH children in lateral cephalometric radiographs, so as to study the changes of facial morphology in AH children, and to analyze the impact of AH on children's respiratory function (RF).

2. Data and Methods

2.1. General Data

This research retrospectively analyzed the clinical data of 56 AH children (observation group) and 42 healthy children (control group) who visited the Hebei Eye Hospital between May 2020 and June 2021. Inclusion criteria for AH children are as follows: (1) age: 4-12 with a medical history ≥ 2 years; (2) presence of typical clinical symptoms such as nasal obstruction, sleep snoring, and OMB; and b(3) diagnosis of AH, with the A/Nratio of X − ray lateral cephalogram ≥ 0.71, and adenoid blockage of posterior nostril > 51% by nasopharyngeal-fiberoscope. Exclusion criteria are as follows: (1) history of chronic rhinitis, turbinate hypertrophy, temporomandibular joint, or craniofacial trauma; (2) history of otolaryngology surgery or previous cranial-maxillofacial orthodontic treatment; and (3) congenital developmental disorders. The two cohorts of children were not statistically different in terms of gender, age, and other general data, indicating comparability (Table 1). This study was approved by the Ethics Committee of Xingtai People's Hospital, and the subjects' guardians all signed the informed consent.

Table 1

General data.

	Gender (male/female)	Age	Delivery mode		Symptom			Type of hypertrophy
			Natural childbirth	Cesarean delivery	Snoring	Mouth breathing	Both	Simple adenoid hypertrophy	Combined with tonsil hypertrophy
Observation group (n = 56)	34/22	6.36 ± 1.41	32 (57.1)	24 (42.9)	21 (37.5)	24 (42.9)	11 (19.6)	41 (73.2)	15 (26.8)
Control group (n = 42)	23/19	6.76 ± 1.54	25 (59.5)	17 (40.5)	—	—	—	—	—
χ 2/t	0.3495	1.3358	0.0559
P	0.5544	0.1848	0.8131

2.2. Research Methods and Outcome Measures

X-ray examination: all children underwent an X-ray skull examination. The lateral radiographs were fixed and measured when the child was in the standing position, with the midline of the skull vertical to the ground, the plane of the eyes and ears parallel to the ground, the mouth naturally closed, the facial muscles relaxed, and even breathing maintained. The outcome measures included the following: ANS-Me (distance from the anterior nasal spine to the submental point), N-ANS (distance from the nasion to the anterior nasal spine), FH ratio (ratio of anterior superior height to anterior inferior height), Ar-ANS (maxillary length: distance from the articulare to the anterior nasal spine), Go-Gn (mandibular body length: distance from the mandibular angle to the submental apex), Go-Ar (mandibular ramus height), SNA (anteroposterior position of maxillary basal bone and anterior skull base plane), SNB (anteroposterior position of mandibular basal bone and anterior skull base plane), ANB (anteroposterior position of upper and lower jaws), Go angel (vertical relationship of mandibular body relative to mandibular ramus), and MP-SN (angle between mandibular plane and anterior skull base plane)

Upper airway measurement analysis by X-ray: A (the most protruding point across the lower margin of the adenoid is the vertical line of the external cranial tangent of the occipital slope. The distance between the most protruding point and the vertical foot is the thickness of the adenoid); N (the root of the pterygium meets the cranial surface of the ramp, and the length between the junction point and the point of the posterior nasal spine is the width of the bony nasopharyngeal cavity); PNS-R (the distance between the posterior nasal spinous point and the pharyngeal apex); PNS-UPW (the distance from the posterior nasal spinous point to the superior pharyngeal wall); SPP-SPPW (the distance from the back of the soft palate to the wall of the pharynx); U-MPW (the distance between the apical uvula and the middle pharyngeal wall); TB-TPPW (Pharyngeal airway space); and V-LPW (the distance between epiglottis valley and hypopharyngeal wall)

Nasal airway volumetric measurement using acoustic rhinometry (AR): half an hour before the examination, the investigator entered the air-conditioned examination room that was maintained at 21°C with a humidity of 50%-60%. Nasopharyngeal volume (NPV) and nasal airway resistance (NAR) were measured by the acoustic reflection nasal measurement system (ECCOVISION, USA). Children were asked to sit quietly for a moment to prepare for examination, and the influences of temperature, humidity, movement, and noise on nasal mucosa were eliminated. When measuring, an appropriate nasal probe was used to prevent the nasal cavity from being deformed by extrusion. Breathing and swallowing were stopped during the test, and the left and right nasal cavities were tested separately

RF determination: AH children were monitored for sleeping with a portable PSG device, with the detection time not less than 7 hours per night. Polysomnography was interpreted by two technicians and a pediatrician trained in sleep medicine, all blinded to clinical outcomes. Sleep stages were classified based on the American Academy of Sleep Medicine guidelines [21], and subjects with an obstructive apnea-hypopnea index (OAHI) score ≥ 1 were defined as OSAS [22]

The sleep quality, efficiency, and time of both cohorts of children were assessed using the Pittsburgh Sleep Quality Index (PSQI) [23]. The scale consists of self-assessment items and other items, including seven modules: sleep quality, sleep latency, sleep duration, sleep efficiency, sleep disturbance, sleep medication, and daytime sleep dysfunction. On a scale of 0-21, higher scores are associated with more severe sleep disorders

2.3. Statistical Processing

Data analysis was performed by SPSS 22.0 (IBM SPSS 22.0, Chicago, IL), and statistical significance was considered when P < 0.05. A Chi-square test was used for counting data described in the form of n (%). The measurement data of normal distribution were represented by mean ± SD, and the difference was determined by an independent sample t-test.

3. Results

3.1. Sagittal Diameter of Upper Airway in Children

As shown in Table 2, the A value, PNS-R value, and PNS-UPW value showed statistically differences between the control group and the observation group, indicating that AH mainly affected the size of nasopharyngeal and oropharyngeal airway. While no significant difference was observed in the N value, indicating no difference in bony structure of nasopharyngeal cavity between the two groups, nor was there any statistical difference in other indicators, suggesting no difference in the middle and lower segments of the upper airway.

Table 2

Sagittal diameter of upper airway on cephalic radiographs.

Parameters	Observation group (n = 56)	Control group (n = 42)	t	P
A (mm)	16.13 ± 1.40	8.61 ± 1.88	22.7064	<0.0001
N (mm)	20.34 ± 1.55	19.85 ± 1.69	1.4898	0.1396
PNS-R (mm)	18.21 ± 1.41	19.80 ± 1.83	4.8596	<0.0001
PNS-UPW (mm)	9.16 ± 1.81	15.35 ± 1.97	16.1302	<0.0001
SPP-SPPW (mm)	10.83 ± 2.07	11.25 ± 1.84	1.0418	0.3001
U-MPW (mm)	9.70 ± 2.02	9.87 ± 1.49	0.4594	0.6469
TB-TPPW (mm)	8.93 ± 2.49	9.31 ± 2.33	0.7683	0.4442
V-LPW (mm)	18.87 ± 1.37	19.20 ± 1.82	1.0245	0.3082

Notes: Bold text means statistical significance.

3.2. Cephalometric Parameters of Children

Among the craniofacial measurement parameters, SNB angle, MP-SN angle, and FH ratio showed statistical significance between groups. Meanwhile, a significant difference was observed in ANS-Me (P < 0.05). The other indexes were not statistically significant (P > 0.05) Table 3.

Table 3

Comparison of craniofacial morphological parameters between the two groups of children.

Parameters	Observation group (n = 56)	Control group (n = 42)	t	P
ANS-Me (mm)	67.14 ± 5.73	63.40 ± 5.41	3.2744	0.0015
N-ANS (mm)	46.30 ± 3.72	49.53 ± 5.22	1.8453	0.0681
FH ratio	0.71 ± 0.10	0.79 ± 0.09	4.0886	<0.0001
Ar-ANS (mm)	78.89 ± 7.06	80.13 ± 7.49	0.8383	0.4040
Go-Gn (mm)	60.74 ± 5.48	61.95 ± 7.84	0.8992	0.3708
Ar-Gn (mm)	94.71 ± 7.08	94.29 ± 9.75	0.2471	0.8053
Go-Ar (mm)	45.82 ± 6.88	45.15 ± 8.07	0.4428	0.6589
SNA (°)	88.93 ± 4.53	89.26 ± 5.25	0.3333	0.7396
SNB (°)	76.69 ± 4.60	80.93 ± 5.22	4.2613	<0.0001
ANB (°)	8.61 ± 2.05	8.59 ± 2.03	0.0480	0.9618
MP-SN (°)	40.05 ± 5.76	34.32 ± 5.03	5.1411	<0.0001
Go angle (°)	134.23 ± 5.25	132.38 ± 5.33	1.7151	0.0896

3.3. Nasal Airway Resistance Results in Two Groups

The results identified a lower total NAR (2.35 ± 0.83 cmH2O/L min) in controls than in AH children (5.11 ± 1.95 cmH2O/L·min) and a higher NPV in controls compared with cases (20.78 ± 4.44 cm3 vs. 16.86 ± 3.93 cm3), with statistical significance (P < 0.05) Figure 1.

Figure 1

Comparison of acoustic rhinometry measurement parameters between two groups of children. (a) Comparison of total nasal airway resistance (TNAR). (b) Comparison of nasopharyngeal volume (NPV). ∗∗∗P < 0.001.

3.4. Respiratory Function of Adenoidal Hypertrophy Children

The RF test results (Table 4) identified 11 children with an OAHI score of 0, 41 children with 0 < OAHI score < 1, and 4 with an OAHI score ≥ 1. The results indicate that 45 children developed respiratory dysfunction, including 4 with OASA.

Table 4

Results of respiratory function indexes in children with adenoid hypertrophy.

Measured value	Number	Percentage
OAHI = 0	11	19.6
0 < OAHI < 1	41	73.2
OAHI ≥ 1	4	7.2

3.5. Children's Sleep Quality and A/N Value of Nasopharyngeal X-Ray Lateral Films in Two Groups

After evaluating the sleep quality, we found that compared with controls, the sleep latency (23.09 ± 3.93 min) and PSQI score (14.46 ± 3.43 points) were significantly higher in AH children. A higher A/N value (0.89 ± 0.09) of nasopharyngeal X-ray lateral films was also determined in AH children (Figure 2).

Figure 2

Comparison of sleep quality and A/N value of nasopharyngeal X-ray lateral films between the two groups. (a) Comparison of average sleep latency. (b) Comparison of PSQI score. (c) Comparison of A/N. ∗∗∗P < 0.05.

4. Discussion

Adenoids are lymphatic organs located in the nasopharynx and the top of the posterior pharyngeal wall [8]. According to previous views, adenoids existed at birth, increased with age under physiological conditions, and reached their maximum size at the age of 6-7. They began to atrophy after the age of 10 and completely shrank by puberty, merging with the mucous membrane of the nasopharyngeal wall. AH is rare in adulthood [24, 25]. However, some other studies have shown that among adults with pharyngeal diseases, the proportion of adenoids remains high and hypertrophy is common [26]. The location and function determine that adenoids, once stimulated, will evoke immune responses, increase in volume, and occupy the space of the nasopharyngeal cavity, which may block the ventilation and drainage of posterior nostril and nasopharynx, resulting in pathological AH [10]. OMB is a reflex activity of the body to enlarge the upper airway. If the upper airway is blocked for a long time, children will still keep OMB even when the obstruction is removed, as the bad habit has already been developed. Craniofacial growth and development are influenced by both genetic factors and functional stimuli. According to Moss's functional matrix theory, the change of breathing pattern is bound to break the original balance of teeth, jaw, tongue, and muscles around the face, resulting in the growth and reconstruction of teeth and jaw to a new equilibrium, which will ultimately affect the position of teeth and the shape of jaw and give rise to craniomaxillofacial deformities [27].

In this study, the nasal RF and craniofacial morphology of AH children were objectively evaluated by AR and X-ray cephalometry. The results showed higher NAR and statistically lower NPV in AH children compared with controls. It shows that the nasal cavity and nasopharyngeal cavity became smaller after mechanical obstruction of adenoid tissue in children, resulting in nasal obstruction and nasal blood circulation disorders. Most of the previous studies on pediatric AH and craniofacial dysplasia did not objectively measure children's nasal RF but confirmed nasal AO only by OMB. Although some studies have also used the combination of signs and symptom scores to subjectively quantify the nasal opening degree, the reliability of subjective sensation of nasal obstruction is not high, because some children with AH are too young to accurately describe and express their feelings. The AR used in this study has obvious advantages because it does not rely on airflow in the nasal cavity, which is suitable for patients with complete nasal obstruction and kids aged under 3. The basic principle of AR is to describe the two-dimensional information of the cavity to be measured by using the acoustic reflection signals and to sketch the cross-sectional shape of nasal airway by measuring the amplitude of the reflected wave and the reflected time, which directly reflects the patency of the airway [28, 29]. Then, we observed the craniofacial morphology of two groups of children and found statistical differences in SNB angle, MP-SN angle, FH ratio, and ANS-Me. Nasal obstruction caused by AH will affect children's craniofacial development. First, it has a great impact on the position and morphology of mandible. The narrowing of the upper respiratory tract changes children's RF and breathing pattern, which triggers a certain degree of changes in oral muscles, as well as damage to the balance between oral muscles and the jaw, eventually leading to abnormal growth of the jaw and teeth, which is mainly manifested as mandibular retraction and smaller SNB angle on the sagittal plane, similar to previous studies [30, 31]. In addition, long-term OMB promoted the progressive extension of the head and neck, leading to an increase in craniocervical angle anteversion [32]. Wang et al. explored the influence of AH on both the morphological development characteristics of the upper airway and the craniofacial features in children. The results showed that AH altered a child's breathing mode and function by inducing upper airway stenosis, as well as craniomaxillofacial and oral deformities [16].

Finally, we observed the sleep quality and RF of children. Significantly worse sleep quality was observed in AH cases compared with healthy children; in addition, 45 AH children developed respiratory dysfunction, including 4 with OSAS. AH is considered the most important risk factor for the development of OSAS in children [33, 34]. Sleep monitoring is an important means to identify sleep-related respiratory disorders in children. The clinical manifestations of sleep-disordered breathing in children are different from those in adults, mainly characterized by obstructive hypopnea accompanied by varying number of apnea episodes and periodic hypoxemia. There is no obvious sleep structure disorder, and respiratory disorder is generally not accompanied by microawakening. In addition, children with similar severity of OSAS and similar adenoid or tonsil sizes have different clinical presentations [35]. All these suggest that the OSAS phenotype is highly variable. Hence, we should pay attention not only to apnea-hypopnea index but also to clinical manifestations, sleep structure characteristics, and respiratory regulation. It is important to note that if left untreated, OSAS can lead to neurobehavioral and cardiovascular complications and growth disorders [36]. Therefore, close attention should be paid to the sleep status of children with AH. However, this research still shows some limitations. As only 56 AH children were included in this study, the results may not be representative. Besides, people in plateau areas have respiratory compensation due to different growing environments, so differences in different growing environments need to be further analyzed.

5. Conclusion

To sum up, AH will significantly affect the growth of craniomaxillofacial structure of children and their RF, resulting in reduced sleep quality of such children. Oral respiration mainly affects mandibular development, which can cause back rotation or extension of mandible, decrease of mandibular body length, and lip tilt of upper and lower front teeth. However, it has little influence on maxillary development.