Keywords child - maxillofacial development - orthodontics - snoring - tonsil
Introduction
Adenotonsillar hypertrophy (ATH) and altered maxillofacial morphology are strongly
associated with increased risk for developing sleep-disordered breathing (SDB) in
children,[1 ]
[2 ]
[3 ] with physiologic alterations, such as intermittent hypoxia and sleep fragmentation,
that may result in a wide array of morbid consequences, including neurocognitive and
behavioral deficits,[4 ] nocturnal enuresis, and cardiovascular and metabolic complications.[5 ]
The treatment of choice for SDB in children has traditionally consisted of surgical
removal of the tonsils and adenoids (T&A).[5 ] However, previous studies have shown that among children who underwent T&A, a substantial
proportion failed to display complete resolution of their respiratory disturbances
during sleep after surgery.[5 ] Maxillofacial disharmony can also be a significant predisposing factor in the development
and progression of pediatric SDB.[5 ] Similarly, measurements of the cross-sectional area of the oropharynx can be useful
in screening for SDB in both adult[6 ] and pediatric populations.[7 ]
[8 ] Cephalometric values commonly used in the evaluation of symptomatic patients include
maxillary–mandibular planes angle (MMPA), maxilla–mandibular relationship (ANB), and
hyoid bone position (H-ML).[9 ]
[10 ]
[11 ] Löfstrand-Tiderström and Hultcrantz[12 ] observed a reduction in the mandibular angle in 6-year-old children who underwent
T&A without dental arch narrowing correction. In another study, the same authors[13 ] suggested that orthodontic intervention was required because there were no changes
in maxillofacial development post-T&A.
Orthodontic and maxillofacial abnormalities related to pediatric obstructive sleep
apnea syndrome are commonly left unattended even though they have a potential harmful
impact on health.[14 ] Rapid maxillary expansion has been reported to achieve improvements in respiratory
function, even during sleep, and functional appliances have recently been applied
in children with SDB with favorable outcomes.[15 ]
[16 ]
[17 ]
[18 ] Myofunctional exercises are also recommended as complementary interventions.[19 ] However, the effect of an orthodontic and functional orthopedic oral appliance (OOA)
treatment in habitually snoring children with ATH on airway growth has not been systematically
examined.
The aim of this study was to evaluate the changes in pharyngeal dimensions and cephalometric
measurements related to SDB in snoring children with ATH, and narrow maxillary arch
before and 6 months after OOA treatment, and compare with those occurring in similar
children matched for ATH and maxillofacial morphology, who did not undergo OOA treatment.
Methods
The Ethics Committee approved the research protocol at the Hospital das Clinicas da
Faculdade de Medicina da University of São Paulo (HC-FMUSP), and all legal caretakers
provided signed informed consent. Forty children aged 6 to 9 years old who presented
with a history of chronic snoring and mouth breathing due to tonsil and adenoid hypertrophy,
and who were placed on the waiting list for T&A in the Department of Otolaryngology
of the USP Medical School from 2008 to 2011 were included. We should emphasize that
the mean waiting period for T&A at HC-FMUSP or anywhere else in the public health
service in São Paulo is approximately 12 months. The trial design was parallel paired
and randomized with an allocation ratio of 3:2. The sample size was determined according
to convenience due to the strict inclusion criteria and considering previous publications
with similar results.[16 ]
[20 ]
Eligibility criteria included: enlarged tonsil grades 3 or 4 according to the Brodsky
grading scale,[21 ] obstructive adenoids (> 50%) as per lateral radiographic film,[22 ] constricted maxilla, class II malocclusion, and sleep disturbances including habitual
snoring and witnessed apneas reported by parents and caregivers.[23 ] Exclusion criteria were previous orthodontic treatment, neurological diseases, or
genetic syndromes.
Patients were randomly allocated to one of the groups (OOA: n = 24 or Controls: n = 16). The number of patients included initially in the study group was higher than
the a priori cohort size estimates, and aimed to account for patients who may fail
to complete the study.
Otolaryngology evaluation : Otolaryngology evaluation included physical examination, pediatric sleep questionnaire
(PSQ), fiberoptic nasopharyngoscopy, and lateral head radiograph. All subjects included
in the study underwent a polysomnographic (PSG) diagnostic assessment that showed
the presence of an obstructive apnea index > 1/hour total sleep time (TST) or an obstructive
apnea–hypopnea index > 2/hour TST. These sleep disturbances are detrimental to children's
health and development as described in the introduction.
Acoustic pharyngometry : Subjects seated in an upright position on a straight-back chair breathed through
an acoustic pharyngometer (Sleep Group Solutions; Miami, Florida, United States).
Subjects were instructed to pause the breathing at end-exhalation for acoustic measurement
of upper airway minimal cross-sectional area (MCA). The MCA was measured between the
oropharyngeal junction (OPJ) up to but excluding the glottis (GL). The total volume
of the pharyngeal space (V) was also determined.[6 ]
[7 ]
[8 ] Parameters were calculated by the computer system that outputs the measurements
of the oropharynx in between OPJ and GL: volume, mean area, MCA, and distance of MCA
from incisor teeth contact. All patients from the treatment group had an extra register
with the OOA appliance installed in the mouth. [Fig. 1 ] shows a representative output of the acoustic pharyngogram of one child from the
treatment group overlapping the two pharyngograms and measurements registered at the
start: in red color without the OOA in the mouth and blue color with the OOA installed.
Fig. 1 Representative output of acoustic pharyngogram before and after placement of the
oral appliance.
Dental examination : Maxillary arch constriction was defined by the presence of two or more maxillary
posterior teeth in an edge-to-edge cuspal relationship with their antagonists or crossbite
and based on the Korkhaus index for maxillar arch constriction.[24 ] Class II malocclusion was present when the inferior molar was positioned posterior
to the upper molar cuspid reference.[25 ]
Cephalometric evaluation : All assessments were performed by the same operator who was blinded to the study
in the Department of Radiology of HC-FMUSP. Lateral head X-rays were taken on a cephalostat
in natural head position. A cephalometric evaluation was used to assess growth direction
on values related to sleep apnea[9 ]
[10 ]
[11 ] by comparing the measurements ([Fig. 2 ]).
Fig. 2 Schematic of cephalometric measurements performed in the participants. SNA, anteroposterior
position of the maxilla in relation to the anterior cranial base (the angle between
the lines S-N and N-A). SNB, anteroposterior position of the mandible in relation
to the anterior cranial base (the angle between the lines S-N and N-B). ANB, anteroposterior
position of the mandible in relation to the maxilla (the angle between the lines A-N
and N-B). MMPA, angle of the palatal line (anterior nasal spine [ANS] to posterior
nasal spine [PNS]) with the mandibular line (Me-Go). S-Go/N-Me, total facial index
(distance from S to Go divided by distance from N to Me). H-ML, hyoid bone position
related to the mandibular line (length in mm). S-Go, distance from S to gonion (in
mm).
Oral appliance : The appliance is designed to bring about orthopedic, functional, and orthodontic
changes. It consisted of an acrylic palatal body with a tongue-guide hole at the papilla,
a screw for active maxillary expansion, and a Hawley's vestibular arch with the possibility
of orthodontic activation at the canine region for reducing incisors inclination when
needed together with slowly removing the acrylic from behind the incisors at each
appliance expansion screw activation. Retention clasps with connection tubes were
attached to the upper molars. A removable lip bumper was connected to the molar clasps
and placed between the lower lip and the lower anterior teeth to promote proper lip
contact. On installation, a bite guide was molded with acrylic behind the upper incisors
to place the lower incisors in a more anterior contact with the upper incisors favoring
the advancement of the mandible to class I constructive bite. This bite guide was
opened in the middle with a fine cutting disc to not interfere on maxillary expansion.
Participants wore their appliances for a minimum of 4 hours during the day and approximately
8 to 12 hours at night. Patients were instructed to maintain contact between the tongue
and the hard palate inside the tongue-guide hole of the appliance always, even on
opening the mouth and during swallowing. The expansion screw was activated with three-fourths
turns (0.75 mm.) every 3 weeks. A total of 8 activations were completed during the
6-month study period, resulting in a total expansion between the upper first molars
of approximately 6 mm.
The main goals of the appliance were maxilla transverse expansion combined with upper
and anterior tongue repositioning and lip sealing. There was not one standard amount
of bite opening and advancement, and the constructive bite was built for each patient
bringing the lower incisors in close touch with the upper incisors. The hole at the
papilla acted as a reminder for tongue positioning training, and the lower vestibular
shield was used to help proper lip sealing supporting lower lip advancement. [Fig. 3 ] shows an example of the oral appliance Bioajusta X.
Fig. 3 Example of the BioAJustax oral appliance used in the orthodontic and orthopedic appliance
(OOA) treatment.
After 6 months, both groups underwent otorhinolaryngologic and dental exams, pharyngometry,
and cephalometric evaluation.
Data analysis : Using statistical software (SPSS 15.0; Chicago, Illinois, United States), normality
of data distribution was measured with the Kolmogorov–Smirnov test. Differences in
mean and standard deviation for pharyngometric measurements between groups were compared
using Student's unpaired t -tests. For the cephalometric values, analysis of variance (ANOVA) (repeated measures
ANOVA test) was used to verify differences between groups and time points. Statistical
significance was assumed at a two-tailed p -value of < 0.05.
Results
A total of 114 children were assessed for eligibility from 2008 to 2011, and 74 were
excluded for not meeting the inclusion criteria. All eligible candidates who consented
had normal body mass index (none were obese neither underweight), which remained stable
during the study period. The 40 participants were followed during the study period,
with no participants dropping out. The mean age was 7.6 ± 0.8 years old for the treated
group and 7.5 ± 0.9 years old in the controls (p -value > 0.05). The gender distribution between both groups was identical. Dental
occlusions were considered as being improved in all the children treated, and no complaints
of side effects were registered. The treated group achieved better improvements in
respiratory symptoms as corroborated by the PSQ ([Table 1 ]), while none of the participants or their caregivers from the control group reported
any improvements.
Table 1
Respiratory symptoms from PSQ at the treated group
Symptoms
T1
T2
p -Value
N
%
N
%
Snoring
< 0.001
Always
15
62.5
0
0.0
Frequent
8
33.3
0
0.0
Occasional
1
4.2
6
25.0
Rare
0
0.0
18
75.0
Mouth breathing
< 0.001
Always
9
37.5
0
0.0
Frequent
14
58.3
1
4.2
Occasional
1
4.2
4
16.7
Rare
0
0.0
19
79.2
Total
24
100
24
100
Abbreviation: PSQ, pediatric sleep questionnaire.
Note: Wilcoxon test.
Pharyngometry-related findings are shown in [Table 2 ]. Significant improvements in airway volume (V) and MCA in the treated group emerged,
while significant reductions in both MCA and V occurred in the controls (p < 0.001). Fiberoptic nasopharyngoscopy confirmed the results measured by pharyngometry.
Table 2
Acoustic pharyngometry measurements
Acoustic pharyngometry
T1
T2
Difference T2 − T1
p -Value
MCA (cm2 ) OOA
1.14 ± 0.2
1.29 ± 0.2
+0.15 ± 0.2
< 0.001
MCA (cm2 ) controls
1.46 ± 0.3
1.32 ± 0.3
–0.14 ± 0.2
< 0.001
Volume (cc) OOA
20.09 ± 2.8
23.24 ± 4.23
+3.15 ± 2.6
< 0.001
Volume (cc) controls
19.40 ± 2.5
18.02 ± 2.3
–1.25 ± 1.3
< 0.001
Abbreviations: MCA, minimum cross-section area; OOA, orthopedic oral appliance; SD,
standard deviation.
Note: Student's unpaired t -test (mean ± SD).
An illustrative example of lateral X-ray changes in airway caliber of a same child
treated in 6 months comparison is shown in [Fig. 4 ].
Fig. 4 Example of changes in airway caliber after 6 months of orthopedic oral appliance
(OOA) treatment in one child.
Cephalometric measurements related to sleep apnea on comparison between groups and
time points ([Table 3 ]), showed reductions in anteroposterior position of maxillla (SNA) and increases
in anteroposterior position of mandible (SNB) from T1 to T2 for the treatment group,
which resulted in a significant decrease in ANB (p < 0.001). The mean values for MMPA and H-ML increased from T1 to T2 in the control
group (p < 0.001), while the same measurements decreased in the treatment group (p < 0.001).
Table 3
Cephalometric assessments
Cephalometric measurements
Controls (N = 16)
OA treatment (N = 24)
T1
T2
T1
T2
p -Value
SNA
85.0 ± 3.2
85.5 ± 3.1
84.2 ± 3.1
83.1 ± 2.8
< 0.001
SNB
78.4 ± 2.7
78.3 ± 2.7
77.1 ± 2.9
78.3 ± 2.8
< 0.001
ANB
6.6 ± 1.6
7.1 ± 1.7
7.1 ± 1.8
4.9 ± 1.6
< 0.001
S-Go/N-Me
64.0 ± 3.1
63.9 ± 3.2
64.5 ± 3.1
66.2 ± 3.2
0.008
MMPA
28.3 ± 2.9
30.4 ± 2.8
31.3 ± 3.8
28.9 ± 3.8
< 0.001
H-ML
9.4 ± 4.1
10.7 ± 4.8
10.5 ± 3.0
6.5 ± 3.0
< 0.001
S-Go
69.1 ± 3.2
69.7 ± 3.2
69.8 ± 4.5
71.7 ± 4.5
< 0.001
ANOVA test (mean ± SD)
< 0.05
Abbreviations: ANB, maxilla–mandibular relationship; ANOVA, analysis of variance;
H-ML, hyoid bone position; MMPA, maxillary–mandibular planes angle; SD, standard deviation;
SNA, anteroposterior position of maxilla; SNB, anteroposterior position of mandible.
Most children underwent surgery after the study as severe tonsils hypertrophy may
interfere with orthodontic treatment stability. As mentioned earlier, public hospitals
in São Paulo such as HC-FMUSP had a waiting time of approximately 12 months for adenotonsillectomy
surgery at the time of the study. All children that performed the PSG after OOA treatment
and surgery showed marked improvement.
Discussion
In children as well as in adults, an elongated face and a steeper mandibular plane
are associated with smaller pharyngeal dimensions, which established early in life
may predispose to higher SDB risk in later years.[14 ] Maxillary constriction also plays a role in the development of obstructive sleep
apnea.[1 ]
[10 ]
[11 ] Remodeling of the maxillofacial structure can be achieved by the expansion of the
maxillary arch, associated with the functional training with the OOA treatment may
help to correct the tongue position, swallowing, and lip sealing, resulting in the
rehabilitation of normal nasal function.[20 ]
[26 ]
[27 ]
[28 ] The distance between gonion and point S, and the total facial index (S-Go/N-Me)
increased more in the treatment group. This outcome is possibly related to the normalization
of pharyngeal dynamics and the favorable breathing pattern achieved in the treatment
group with consequences for mandibular growth, probably by normalizing growth hormone
status, similar to the growth redirection observed after surgery.[2 ] This could be related to a more intense bone formation at the mandibular ramus,
reflecting an increase in the total facial index (S-Go/N-Me), thus helping normalize
the ANB as indicated by the current results.
Acoustic pharyngometry is a potentially useful tool which enables longitudinal assessments
of the changes in airway dimensions.[29 ] The MCA can be a valuable measurement for evaluating SDB risk factor in preadolescent
children.[7 ]
[8 ] Both the MCA and the volume of the airway improved in the treatment group and decreased
in the control group at the end of the study period. The pharyngograms shown in [Fig. 1 ], comparing the patient with and without the OOA in the mouth at the start, may help
to visualize the modification on pharyngeal dynamics with the tongue repositioning.
The modification obtained on oropharyngeal size and shape registered on the installation
of the OOA, possibly contributed against its collapsibility during the treatment time,
which may explain the improvements noted in the symptoms questionnaire of the treated
patients answered by the parents/caregivers.[30 ]
The current findings concur with a previous similar study by Jena et al.[31 ] The anterior displacement of the tongue that was made possible by the maxillary
expansion and the appliance tongue guide, influenced the position of the hyoid bone
and consequently improved the morphology of the upper airways.[6 ]
[20 ]
[31 ] An upper and anterior position of the tongue may favor an improved airway growth.[20 ] Adequate breathing requires proper tongue positioning and lip contact.[28 ]
The positive impact of the OOA therapy on airway dimension despite concurrent ATH
cannot be explained simply by skeletal changes, and we postulate that differences
in the posture of the tongue caused by increased genioglossus muscle tone or soft
tissue changes may have also contributed to forward positioning of the mandible during
treatment.[14 ]
[20 ]
[32 ]
We could objectively demonstrate the morphological changes, and the results achieved
can be related to the improvement of pharyngeal dynamics reflecting on a better breathing
and sleep pattern.
Some limitations should be mentioned in this study: First, the number of subjects
was relatively small (even though similar to previous similar publications),[16 ]
[20 ] and the follow-up period was relatively short, and dictated by the waiting times
for T&A. Second, we did not conduct any comparisons with other treatment modalities,
although previous publications show that at the 6 to 9 years old range surgery alone
does not correct the dentofacial alterations.[13 ]
[14 ]
[15 ]
[16 ]
[18 ]
[19 ]
[32 ]
[33 ] Third, and perhaps most importantly, we do not know whether OOA treatment followed
by T&A will result in better outcomes than T&A alone or T&A followed by OOA therapy.
Other limitations are some missed polysomnography and nasoendoscopy data, and no drug-induced
sleep endoscopy study to precisely detect the level of obstruction. These questions
will have to await future studies that are clearly beyond the scope of the present
trial. Since the control group presented worsening of the craniofacial characteristics
and pharyngeal measurements, the possibility of enlarging pharyngeal dimensions at
an early age together with normalized growth of the craniofacial skeleton should be
viewed as a favorable approach in preventing sleep apnea later in life, an issue that
will have to await longitudinal assessments.[34 ]
None of the children had temporomandibular joint or muscle pain that may happen in
adults with mandibular advancement, since on children under orthopedic treatment constructive
bite is common and well tolerated.
Conclusion
Six months of OOA treatment in snoring children with SDB promotes enlargement of the
pharyngeal dimensions and beneficial cephalometric changes.
