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ORIGINAL ARTICLE
New insights on age-related
association between nasopharyngeal
airway clearance and facial
morphology
A. T. Macari
M. A. Bitar
J. G. Ghafari
Authors' affiliations:
A. T. Macari, J. G. Ghafari, Division of
Orthodontics and Dentofacial Orthopedics,
Department of Otolaryngology-Head and
Neck Surgery, American University of Beirut
Faculty of Medicine and Medical Center,
Beirut, Lebanon
M. A. Bitar, Section of Pediatric
Otolaryngology, Department of
Otolaryngology-Head and Neck Surgery,
American University of Beirut Faculty of
Medicine and Medical Center, Beirut,
Lebanon
Correspondence to:
Joseph G. Ghafari
Division of Orthodontics and
Dentofacial Orthopedics American
University of Beirut Medical Center
6th Floor
PO Box 11-0236
Riad El-Solh, Beirut 1107 2020, Lebanon
E-mail: jg03@aub.edu.lb
Macari A. T., Bitar M.A., Ghafari J.G. New insights on age-related associ-
ation between nasopharyngeal airway clearance and facial morphology
Orthod Craniofac Res 2012. Ó 2012 John Wiley & Sons A ⁄ S
Structured Abstract
Objectives – To evaluate the relation between adenoid hypertrophy and
facial morphology across age in a pediatric population.
Setting and Sample Population – The American University of Beirut
Department of Otolaryngology. Two-hundred consecutive children (age
6.00 ± 2.62 years) referred from the Pediatric Otolaryngology unit to the
Orthodontic division and requiring a lateral cephalogram for adenoid
hypertrophy assessment.
Methods – Cephalometric measurements included relations among
cranial base, maxilla and mandible, and airway clearance measured from
adenoid to soft palate (AD). The children were classified into two age groups,
Group 1: £ 6 years (n = 124) and Group 2: ‡ 6.01 years (n = 76), and also
stratified in four subgroups (A, B, C, D) based on maxillo-mandibular
divergence (palatal to mandibular plane angle, PP-MP): A- PP-MP £ 27.5°,
n = 34; B- 27.5° < PP-MP £ 32°, n = 68; C- 32°<PP ⁄ MP<36.5°, n = 67;
D- PP-MP ‡ 36.5°, n = 31. Statistics included t-tests and ANOVA for group
differences.
Results – Differences between groups 1 and 2 were statistically significant
(p < 0.05) for AD (Group 1: 3.19 ± 2.32 mm, Group 2: 4.78 ± 2.80 mm),
ANB (5.38 ± 2.24°, 4.38 ± 2.54°), LFH (56.61 ± 1.95%, 55.38 ± 1.84%),
PP-H ()8.41 ± 3.28°, )6.49 ± 3.46°), and overbite (0.55 ± 2.00 mm,
1.16 ± 2.36 mm). Among subgroups, statistically significant differences
(p < 0.05) occurred mainly between the most hyperdivergent group (D)
and the hypodivergent (A) and normodivergent (B) groups.
Conclusions – Airway measurements were smallest in children £ 6 years
and those presenting severe hyperdivergent pattern, which denoted the
most severe airway obstruction. The findings suggest airway clearance before
age 6 in the most severely affected children, but follow-up research on
actualadenoidectomiesinyoungerchildrenisneededtodetermineguidelines.
Key words: adenoid; facies; jaw relation; malocclusion; nasal obstruction
Dates:
Accepted 4 February 2012
DOI: 10.1111/j.1601-6343.2012.01540.x
Ó 2012 John Wiley & Sons A ⁄ S
Introduction
Adenoid hypertrophy is the source of various
diseases because of consequent nasal obstruction
and oral respiration. The medical symptoms
(snoring, otitis media, sinusitis, sleep apnea)
affect the well-being of the patient but also of the
family, often placing in second order the long-
term effects on facial morphology, such as aber-
rant development of maxillary and mandibular
structures. Yet, such alterations can lead to per-
manent dysmorphology that might require
orthognathic surgery in adulthood, when it may
have been partially or totally avoided in child-
hood. A revealing reference to the long-standing
association between airway clearance and facial
morphology is the description of Ôadenoid faciesÕ
or long-face syndrome (1). This ÔhyperdivergentÕ
skeletal pattern characteristically includes in-
creased lower face height, constriction of the
maxillary arch, open bite between the anterior
teeth, increased gingival display above the max-
illary anterior teeth, and retrognathic mandible.
Hence, the fully developed long-face syndrome
includes both functional and esthetic impairment.
Orthodontic results do not achieve optimal
esthetic outcome because facial elongation,
particularly subnasal, gingival smile, and chin
retrusion may not be adequately corrected.
Orthognathic surgery better addresses the skeletal
deviations.
The relationship between mouth breathing and
malocclusion is not clear-cut (1–3), probably
because the extent and severity of morphologic
alterations depend on timing, duration, and rate
of oral respiration. The issue is further con-
founded by the diagnostic accuracy of mouth
breathing (4). Quantitative definitions of this
condition have been advocated but have yet to be
proven effective or practical (rhinometry, nasal
flow, nasal resistance), especially in children.
Newer devices that are easier to use discern dif-
ferences between nasal and oral breathing during
clinical examination (5–7) but apparently need
additional validation for universal application.
Otolaryngologists and orthodontists regularly
use lateral cephalometric imaging to evaluate
adenoid contribution in blocking normal respi-
ration (8). Correspondence of cephalometric
measurement and subjective rating of airway
clearance indicates the practicality of cephalo-
metric imaging as a guide to diagnosis and
decision making (8). This finding is supported by
systematic review of the literature regarding the
validity of lateral cephalograms in diagnosing
enlarged adenoids and obstructed posterior
nasopharyngeal airways in children and adoles-
cents (9). Moderate to strong correlations were
noted between actual adenoid size (determined
post-adenoidectomy) and both quantitative
measures of adenoid area and subjective grading
of adenoid size on lateral cephalographs. The
shortest distance between adenoid and soft pal-
ate (termed in our study AD) was the princi-
pal measurement validated from various studies
(9).
The evidence from post-surgical studies in
children (10, 11) revealed a more anterior sym-
physeal growth, reversal of the tendency to pos-
terior mandibular rotation, increased mandibular
growth, and unchanged direction of maxillary
growth. In addition, our clinical observations,
indirectly supported by research (12, 13), indi-
cated that late removal of the adenoids does not
improve the set orofacial dysmorphology. Despite
such findings, timing the adenoidectomy on
individual basis has yet to be achieved. While a
significant amount of evidence is available on the
relation between mode of breathing and orofacial
morphology, a number of research limitations are
difficult to overcome. The collection of cephalo-
graphs in younger children who normally breath
through their nose is understandably restrained
by the reluctance of Internal Review Boards and
parents to accept the procedure. Available inves-
tigations in early childhood relied on pre-existing
cephalometric or other imaging (MRI) records
(14, 15). Small samples or inconclusive results
point to the need for more generalizable research
findings. Finally, there is a need to determine
earlier morphological effects of altered respira-
tion than available in the literature. Extensively
quoted in the orthodontic and otolaryngology
literature, the key studies by Linder-Aronson and
co-workers do not include children younger than
age 6 years (16).
2 Orthod Craniofac Res 2012
Macari et al. Airway clearance and long-face characteristics
In this context, we hypothesized that the rec-
ognition of severe morphological deviations in
children younger than age 6 should lay the ground
for future investigation of the optimal timing of
adenoidectomy that would prevent the attain-
ment of irreversible or non-improvable orofacial
alterations. Also, regardless of the existence of
clinically diagnosed mouth breathing, we sought
to evaluate the association between the cephalo-
metric measurement of airway patency and oro-
facial deviations from normal relation, particu-
larly in children below age 6.
Therefore, our specific aims were to 1-evaluate,
in a prepubertal population diagnosed with
chronic mouth breathing, the association
between facial morphology and airway obstruc-
tion by the adenoid across age, including ages
younger (< 6 years) than available in the literature
and 2-compare dysmorphologic features accord-
ing to severity of facial morphological pattern.
Patients and methods
Patients
The study population consisted of 200 consecu-
tive children (127 boys, 73 girls) referred by
the pediatric otolaryngologist to the Division of
Orthodontics and Dentofacial Orthopedics,
American University of Beirut Medical Center, for
cephalometric imaging of pharyngeal airway
impingement by the adenoid. The otolaryngolo-
gist (MAB) had diagnosed these children as having
chronic mouth breathing (> 3 months duration)
based on the history taken. On physical exami-
nation, the adenoid was suspected as the only
contributor to the airway obstruction, after ruling
out the presence of other causes (as detailed in
the exclusion criteria). No reference was made to
lip posture as not all children with open lip are
mouth breathers. Adenoid hypertrophy is com-
monly evaluated by soft tissue nasopharyngeal
radiographs (10), but the lateral cephalogram
used by orthodontists is more dependable be-
cause of controlled head position in the cepha-
lostat. Although regularly requested and taken,
and not an addition for research purposes, insti-
tutional approval of the radiograph is required for
any research usage of the data; thus, the Institu-
tional Review Board clearance was obtained and
required standards followed.
Exclusion criteria were as follows: septal devi-
ation, bilateral inferior turbinate hypertrophy,
kissing tonsils, previous surgery related to nasal
obstruction (including adenoidectomy and ton-
sillectomy), recent medical treatment of nasal
airway impairment, systemic disease, congenital
malformations.
The mean age of the children was 6.0 years
(range: 1.71–12.61; Fig. 1). Most patients (62%,
n = 124) were below age 6. Nearly half (46%;
n = 93) were < 5 years and the greatest percent-
age (24.5%, n = 49) ranged between 4 and 4.9
years.
Fig. 1. Age distribution intervals
by increment of 6 months.
Orthod Craniofac Res 2012 3
Macari et al. Airway clearance and long-face characteristics
Lateral cephalometry
The cephalographs were taken in the same digital
cephalostat (GE, Instrumentarium, Tuusula,
Finland) following a uniform procedure. With the
body covered by a lead apron, the head of the
child was placed in natural head position, which
is a standardized orientation when one focuses on
a distant reference at eye level (17). This posi-
tioning helps determine the horizontal reference
(H) as defined by Moorrees et al. (17). This ÔtrueÕ
or ÔcorrectedÕ plane is prone to less error than the
Frankfort horizontal defined by two variable
landmarks, nasion and porion (18).
The children were guided to occlude their teeth
in the retruded contact position and keep the lips
in gentle touch. As the distance between the facial
midsagittal plane and the film is set by the man-
ufacturer, the corresponding radiographic mag-
nification is adjusted for automatically. Images
were saved and stored directly in a dedicated
computer.
To avoid inter-examiner variation, a single
investigator (ATM) imported and digitized the
radiographs into the imaging program (Dolphin
Imaging and Management Solutions, La Jolla,
California). Angular and linear measurements
were computed to evaluate the sagittal and verti-
cal positions of the maxilla, the mandible, and
their dental components, relative to the cranial
base and to each other (Fig. 2A). Selected mea-
surements included in this article are SNA, SNB,
ANB, palatal plane (ANS-PNS) to horizontal
(PP-H); mandibular plane (menton-gonion:
Me-Go) to SN (MP-SN), to horizontal (MP-H), and
to palatal plane (PP-MP); ratio between lower and
total facial heights (LFH).
The shortest distance between adenoid and soft
palate (AD) and the distance between the most
convex adenoid point and soft palate (CD) were
used to quantify airway clearance (Fig. 2). The
occlusion of the children was examined and noted.
Taking cephalograms on children who must
keep the teeth in contact and be still during
exposure was difficult in several patients below
age 5. When the teeth were apart more than
2 mm, the radiographs were discarded, reducing
the total number to the reported 200. In a small
number (17 of 200), the imaging program allowed
ÔautorotationÕ of the parted mandible for mea-
surement of parameters related to the mandible.
In 14 children, all below 5 years, who would not
be alone when taking the radiograph, a parent
volunteered to hold the child; both were covered
with lead aprons. Many children who could not
remain still for taking the cephalograph were not
A B C
Fig. 2. (A) Cephalogram of 4.39-year-old boy. Landmarks: N (nasion), S (sella), ANS (anterior nasal spine), PNS (posterior nasal
spine), A (deepest point on the premaxilla between anterior nasal spine and dental alveolus), B (deepest midline point on the
mandible between infradentale and pogonion), Me (menton- most inferior point on mandibular symphysis), Go (gonion- external
angle of the mandible, bisecting the angle formed by tangents to the posterior border of the ramus and the inferior border of the
mandible), H (horizontal corresponding to natural head position), PP (palatal plane through ANS and PNS), MP (mandibular plane
through Me and Go), selected measurements: SNA; SNB; ANB; PP-H; MP-SN; MP-H; PP-MP; AD- shortest distance between adenoid
and soft palate. CD- distance between most convex adenoid point and soft palate. Various airway clearances are shown in B and C.
The latter is most severe, nearly total as indicated by arrow.
4 Orthod Craniofac Res 2012
Macari et al. Airway clearance and long-face characteristics
recruited for the study. To determine intra-ob-
server reliability, the same investigator repeated
the entire cephalometric procedure and measures
on 20 randomly selected cephalographs (10% of
sample).
Study groups
The children were classified into two age groups:
Group 1: £ 6 years (n = 124; 75 boys, 49 girls) and
Group 2: > 6 years (n = 76; 52 boys, 24 girls).
They were also categorized into four subgroups: A
(n = 34), B (n = 68), C (n = 67), and D (n = 31),
based on cephalometric vertical divergence
derived from the angle between mandibular (MP)
and palatal (PP) planes. Though the normative
angulation could have been used (Bjo¨rk:
29°± 5.4°), we stratified the subgroups on the
average angulation within our population:
32° ± 4.5°. This mean was higher than the norm,
favoring an error toward increased hyperdiver-
gence commensurate with the long-face syn-
drome.
The angle PP-MP sums up various characteris-
tics of this syndrome: it is related to the lower face
height, and maxillary inclination is factored in,
avoiding the classification on mandibular angle
only. Furthermore, the dentition is contained be-
tween the jaws, affecting and affected by their
positions. The categorization yielded two groups
(A, B) at one and two standard deviations lower
than the mean, and two groups (C, D) at one and
two standard deviations higher than the mean.
The extreme groups represented severe hypodi-
vergent (A) and hyperdivergent (D) patterns.
Statistical methods
To assess examiner variability of repeated mea-
surements, the intraclass correlation coefficients
were calculated for each of the parameters stud-
ied. Differences between age groups for different
measurements were evaluated by t-tests. Where
applicable, the analysis of variance (ANOVA) gauged
differences for all measurements between various
age and vertical pattern groups, as well as gender
differences within age and vertical pattern groups.
Statistical significance was set at p £ 0.05.
Results
The intraclass correlation coefficients for the
intra-examiner repeated measurements were
high, with 0.91 < r < 0.99 for the reported mea-
surements, except for PP-H (r = 0.88), which
included the horizontal H and thus was more
closely related to reproducing the orientation on
natural head position in the imaging program.
Differences between groups 1 and 2 were
statistically significant for AD and CD, ANB, LFH,
PP-H, and overbite (p = 0.05–0.000; Table 1). Both
groups had measurements of mandibular plane
that were on average compatible with hyperdi-
vergence. Accordingly, the corresponding values
(MP-SN, PP-MP) were not statistically signifi-
cantly different. Posteroinferior tip of the palatal
plane (PP-H) was observed in both groups, but
was less severe in the older group (p = 0.000). The
tilt was highest ()8.9°) between 4 and 4.9 years.
The groups stratified on mandibular divergence
showed age similarities and statistically significant
differences between younger and older groups in
each subgroup (A-D; Table 2). The ANOVA revealed
statistically significant differences among these
groups for all measurements except for age, AD,
Table 1. Means of age and selected cephalometric mea-
surements in age groups
Group 1
N = 124
Group 2
N = 76
pMean SD Mean SD
Age (years) 4.30 0.99 8.79 1.00 0.000
AD (mm) 3.19 2.32 4.78 2.80 0.000
CD (mm) 3.83 2.74 5.54 3.21 0.000
Sagittal measurements
SNA (°) 81.04 3.69 80.73 4.01 0.58
SNB (°) 75.68 3.56 76.35 3.38 0.21
ANB (°) 5.38 2.24 4.38 2.54 0.004
Overjet (mm) 2.7 1.82 2.78 2.31 0.78
Vertical measurements
LFH (%) 56.61 1.95 55.38 1.84 0.000
PP-H (°) )8.41 3.28 )6.49 3.46 0.000
MP-SN (°) 39.64 4.85 39.56 5.63 0.91
PP-MP (°) 32.25 4.35 31.48 4.82 0.25
Overbite (mm) 0.55 2.00 1.16 2.36 0.05
Orthod Craniofac Res 2012 5
Macari et al. Airway clearance and long-face characteristics
CD, and overjet (Table 3). Differences were statis-
tically significant (p = 0.02–0.000) for all vertical
measurements (LFH, PP-H, MP-SN, PP-MP, and
overbite) among all group comparisons (except
overbite between groups A,B and B,C, and PP-H
between A and B); for AD and CD only between the
most severe group (D) and the hypodivergent and
normodivergent groups (A and B, respectively);
and for sagittal measurements mainly between
groups D and A, and D and B.
As might be expected, gender differences
(p < 0.05) within age groups were limited to linear
measurements such as SN, ANS-PNS, NGn and
were found for all measurements between age
groups. In the divergence-stratified groups, gen-
der differences occurred only in the B group (44
boys, 24 girls) for the distances AD (male: 4.59 ±
2.57 mm; female: 3.01 ± 2.25 mm; p = 0.02) and
CD (male: 5.50 ± 3.18 mm; female: 3.63 ± 3.23
mm; p = 0.03).
Table 2. Descriptive statistics of groups stratified on PP ⁄ MP
Groups
A
PP ⁄ MP £ 27.5°
B
27.5° < PP ⁄ MP £ 32°
C
32° < PP ⁄ MP < 36.5°
D
PP ⁄ MP ‡ 36.5°
p  
N 34 (17%) 68(34%) 67 (33.5%) 31 (15.5%)
Group 1 (< 6 years)
n = 124 n = 20 [16.12%] n = 38 [30.64%] n = 47 [37.90%] n = 19 [15.32%]
Age (years)
[range]
4.46 ± 0.74
[2.89–5.94]
4.27 ± 1.05
[1.94–5.85]
4.26 ± 1.12
[1.71–5.98]
4.28 ± 0.77
[3.17–5.87]
NS
Group 2 (> 6 years)
n = 76 n = 14 [18.42%] n = 30 [39.47%] n = 20 [26.31%] n = 12 [15.78%]
Age (years)
[range]
9.91 ± 1.73
[7.06–12.01]
8.61 ± 2.06
[6.09–12.62]
8.39 ± 1.75 [6.02–12.52] 8.58 ± 2.19
[6.15–12.59]
NS
p 
0.000 0.000 0.000 0.000
 
Statistically significant differences for age between age groups 1 (age < 6 years) and 2 (age > 6 years)
  
Statistically significant differences for age among subgroups (A–D).
Table 3. Means of age and selected cephalometric measurements in groups stratified on PP ⁄ MP
Groups
A
PP ⁄ MP
£ 27.5°
B
27.5° <
PP ⁄ MP £ 32°
C
32° <
PP ⁄ MP < 36.5°
D
PP ⁄ MP
‡ 36.5°
p
ANOVA
p
Comparisons among groups A, B, C, D
Mean SD Mean SD Mean SD Mean SD AB AC AD BC BD CD
Age (years) 6.70 2.99 6.19 2.67 5.49 2.31 5.94 2.58 NS NS 0.03 NS NS NS NS
AD (mm) 4.30 2.83 4.03 2.55 3.81 2.67 3.11 2.38 NS NS NS 0.01 NS 0.03 NS
CD (mm) 4.94 3.039 4.84 3.3 4.22 2.92 3.76 2.74 NS NS NS 0.03 NS 0.04 NS
Sagittal measurements
SNA (°) 81.49 4.32 81.72 3.78 80.61 3.39 79.25 3.98 0.02 NS NS 0.03 0.074 0.004 NS
SNB (°) 77.05 4.31 77.06 3.45 75.46 2.84 73.26 3.88 0.000 NS NS 0.000 0.004 0.000 0.002
ANB (°) 4.45 2.19 4.68 2.16 5.14 2.68 5.98 2.38 0.03 NS NS 0.009 NS 0.008 NS
Overjet (mm) 3.18 2.186 2.65 2.01 2.55 1.99 2.81 1.89 NS NS NS NS NS NS NS
Vertical measurements
LFH (%) 55.85 1.76 56.83 1.76 58.02 2.12 59.18 1.65 0.000 0.009 0.000 0.000 0.000 0.000 0.02
PP-H (°) )6.24 3.03 )6.19 3.19 )8.46 3.16 )10.94 2.38 0.000 NS 0.001 0.000 0.000 0.003 0.000
MP-SN (°) 33.68 3.35 37.72 3.37 41.30 2.93 46.62 3.73 0.000 0.000 0.000 0.000 0.000 0.000 0.000
PP-MP (°) 25.72 1.82 29.79 1.23 33.91 1.25 39.31 2.66 0.000 0.000 0.000 0.000 0.000 0.000 0.000
Overbite (mm) 1.87 1.88 1.09 2.44 0.58 1.75 )0.67 1.74 0.000 NS 0.000 0.000 NS 0.000 0.001
6 Orthod Craniofac Res 2012
Macari et al. Airway clearance and long-face characteristics
Dental relations ranged from normal occlusion
with adequate overjet ⁄ overbite to malocclusions
with one or more of the following characteristics:
posterior crossbite, overjet, distoclusion, open
bite, anterior crossbite.
Discussion
This study yielded important contributions re-
ported for the first time because the significant
number of children < age 6 years (most of whom
are below 5 years – Fig. 1) allowed the description
of very early stages of morphologic alteration.
Association between nasal obstruction and facial
dysmorphology
Many differences between younger and older age
groups could be related to the effect of normal
growth of the nasopharynx leading to increase in
airway clearance (11). Other ameliorations with
age include decreases in the lower face height and
in the postero-inferior tilt of the palatal plane
(Table 1). However, both age groups include
important characteristics ascribed to hyperdiver-
gence (MP-SN, PP-MP), suggesting that this pat-
tern on average would persist. Chosen at more
than one SD of the total sample average and
exceeding the one SD of normative data, Group D
possessed, at statistically significant levels, the
most severe airway obstruction (AD and CD), and
the most severely associated characteristics of the
long-face syndrome, both skeletal (LFH, PP-H,
MP-SN) and dental (overbite), as well as man-
dibular retrognathism (SNB) (Table 3). While hy-
perdivergence occurred less in group 2 (n = 12)
than in group 1 (n = 19), percentages were simi-
lar: 15.78 and 15.32%, respectively (Table 2).
The findings suggest that facial dysmorphology
develops in a sequential process, apparently
starting in structures closest to the obstruction
namely the maxilla, which tilted postero-inferi-
orly as gauged by the inclination of the palatal
plane, with a maximal tilt ()8.41°) in the younger
group, mostly between 4 and 4.9 years ()8.9°),
compared to the Caucasian norm [PP-H = 0° ±
2.5° (19)].
The oropharyngeal space is a primary entity
that influences the position and behavior of the
surrounding soft tissues, which in turn shape the
associated skeletal units (20). Impingement on the
oropharyngeal space leads to adaptive reorgani-
zation of adjacent structures, the long-face syn-
drome representing the extreme expression of
prolonged functional disturbance. Conversely,
any degree of adaptive morphologic change may
result in a level of restoration of nasal breathing.
As adaptation to either total or partial airway
obstruction is an individual response to preserve
the oropharyngeal matrix, the occlusal variation
from normal relation to different malocclusions is
not surprising. Similar variations were found in
experimental animal studies whereby the nostrils
of monkeys were obstructed to induce oral res-
piration (21).
Longitudinal data are not available on normal
growth of the distances AD and CD, which in-
creased between ages 4.3 years (Group 1 average)
and 8.79 years (Group 2 average) by 50% (4.78–
3.19 = 1.59 mm) and 45% (5.54–3.83 = 1.71 mm),
respectively (Table 1). In contrast, longitudinal
data on a corresponding hard tissue measure-
ment, such as the distance between PNS and
hormion (at the bottom of the spheno-occipital
synchondrosis), indicate an increase of nearly 13%
(14% in males, 12% in females) between ages 4
and 9 years (22). The seemingly smaller percent-
age increase in the hard tissue parallel to AD and
CD would suggest that the soft tissue airway
clearance improved at a proportion greater than
the underlying skeletal structures. Given that the
skeletal distance is nearly 24 mm at younger ages
(range: 23–26 mm) (22, 23), 13% would corre-
spond to approximately 3 mm. The 1.6–1.7 mm
(45–50%) improvement in AD or CD is less than
the skeletal change, notwithstanding the fact that
the skeletal data were derived from individuals
who did not necessarily have mouth breathing, the
prevailing condition of the children in this study.
Clinical implications
Primary care physicians often delay or oppose
removal of the adenoids because these tissues
contribute to immunological defenses and are
Orthod Craniofac Res 2012 7
Macari et al. Airway clearance and long-face characteristics
expected to decrease in size around adolescence
(15). Medical and craniofacial characteristics are
not competitive reasons for adenoidectomy.
Medical reasons may dictate the surgery without
craniofacial alterations having risen to the pri-
mary cause of the surgery. Yet, nasal airway
obstruction, of any etiology, has the potential to
severely affect only craniofacial morphology, jus-
tifying intervention.
Stating that adenoids lead to mouth breathing
primarily in children with a small nasopharynx,
Linder-Aronson advocates adenoidectomy in
these children (15, 16), but this recommendation
is not tested in clinical trials. Our research indi-
cates that the children in group D, who combined
both the severe vertical pattern (beyond 1 SD) and
the smallest distances between the adenoid and
soft palate (AD and CD), are probably the likeliest
candidates for adenoidectomy for reasons that
include facial dysmorphology. The deviant fea-
tures were present below and above age 6 years.
These data would suggest that: 1 – decreased
airway clearance in the presence of dysmorphol-
ogy would warrant adenoidectomy, at least for the
cohort already exhibiting severe characteristics of
long-face syndrome least affected by orthodontic
treatment (e.g. gummy smile in conjunction with
anterior open bite and overerupted posterior
teeth); 2 – the optimal timing of the surgery
should be before age 6 years. The average age of
the children in group D below age 6 years was
4.37 years, ranging from 3 to 6 years (Table 2).
Perhaps this age bracket should be considered for
future research on optimal timing of early ade-
noidectomy.
A later surgery, such at the average age of group
2 (8.79 years), would not lead to reversal of the
dysmorphology. In a 6-year longitudinal study
(12) in which adenoidectomy was recommended
for 26 children with nasal obstruction, half had
surgery within the first year of diagnosis (age
9.1 ± 2 years), and the other half served as con-
trols (9.4 ± 1.5 years). The results indicated that
adenoidectomy may change the breathing pattern
without a significant effect on malocclusion and
facial type.
The suspicion of enlarged adenoids as the pre-
dominant reason for the diagnosed mouth
breathing may be questioned in at least the chil-
dren with wider airway clearance (groups A, B, C)
unless other obstructions justify intervention.
Upon evaluation of the x-rays of these children,
tonsillar and ⁄ or inferior turbinate hypertrophy
was documented when present. The former is
readily diagnosed clinically, and the latter is best
confirmed with endoscopy. The referring pediat-
ric otolaryngologist followed up on these findings,
having requested the cephalograph to image the
adenoid as the only or combined cause of mouth
breathing for a complete diagnosis and a com-
prehensive treatment plan.
A clear differentiation between the effects of
enlarged tonsils and hypertrophied adenoids is not
available in the literature. When either enlarged
adenoids, tonsils, or both block nasal breathing,
the effect on facial morphology is commonly
thought to include characteristics toward the long-
face syndrome. However, in his pioneering
description of the Class III malocclusion, Angle
relates its early origin, at or before the age of
emergence of the permanent first molars, solely to
enlarged tonsils Ôand the habit of protruding the
mandibleÕ to afford Ôrelief in breathing.Õ (24)
Research is needed to discern these possibilities.
Research considerations
The study supports findings from systematic re-
views that AD best reflects the status of airway
clearance in a two-dimensional record (9). Three-
dimensional imaging of nasopharyngeal space
and structures may yield more accurate informa-
tion (25), but their potential association with
mouth breathing still requires quantitative
assessments of respiration.
A cause-and-effect relationship between nasal
airway obstruction and dysmorphology is both
difficult and unethical to investigate with longi-
tudinal radiation in children with untreated
obstruction (26). The difficulty in recruiting nor-
mally breathing children with normal occlusion,
particularly between the ages of 2 and 5 years, who
would be subjected to cephalometric radiation,
precluded the inclusion of a control group. Also,
defining normal ÔnasalÕ respiration is questionable
in the absence of objective assessment, which
8 Orthod Craniofac Res 2012
Macari et al. Airway clearance and long-face characteristics
remains difficult to obtain in younger children.
Although no matched controls were available, the
stratification on vertical pattern discriminated
between the children with long-face syndrome
characteristics and those with less severe or no
dysmorphology.
Research, particularly longitudinal, is needed to
formulate definitive projections of irreversible
changes that would warrant the timely early
adenoidectomy.
Conclusions
In a study that included for the first time a sig-
nificant number of children early in childhood
(ages 2–6 years), initial stages of morphologic
alteration from nasal obstruction were described.
Narrowing of the posterior pharyngeal airway by
enlarged adenoids apparently leads to a sequen-
tial process of morphologic alteration, starting
with the closest structure (maxilla), and encom-
passing variable occlusal changes. Facial adjust-
ments were more severe with greater airway
obstruction (group D). These findings suggest
early clearance of the nasal passageway to avert,
arrest, or reverse facial alterations in the most
severely affected children.
Guidelines must be defined for early adenoid-
ectomy in relation to facial morphology, not-
withstanding the medical imperatives for the
surgery. Research to determine such guidelines
should be based on the premise that optimal
conditions may include severe airway obstruction
at age < 6 years in individuals on track to develop
irreversible characteristics of the long-face
syndrome.
A set dysmorphology is difficult to resolve with
increasing age. While primary care physicians do
not readily accept the tenet that prevention of
craniofacial dysmorphology represents an indi-
cation for adenoidectomy (and ⁄ or tonsillectomy),
the potential craniofacial problems and associ-
ated difficulty in treatment (including eventual
orthognathic surgery) cannot be dismissed and
require due attention.
Clinical relevance
We evaluated the cephalometric relationship be-
tween nasopharyngeal obstruction by adenoid
hypertrophy and facial morphology in children
referred by the otolaryngologist. Long-face syn-
drome characteristics are difficult to treat back to
normal in late childhood. Decreased airway
clearance in children with most severe hyperdi-
vergent features suggests removing obstacles to
nasal respiration early (age < 6 years), laying the
ground for more longitudinal research.
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Macari et al. Airway clearance and long-face characteristics

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New insights on age related association between nasopharyngeal airway clearance and facial morphology

  • 1. ORIGINAL ARTICLE New insights on age-related association between nasopharyngeal airway clearance and facial morphology A. T. Macari M. A. Bitar J. G. Ghafari Authors' affiliations: A. T. Macari, J. G. Ghafari, Division of Orthodontics and Dentofacial Orthopedics, Department of Otolaryngology-Head and Neck Surgery, American University of Beirut Faculty of Medicine and Medical Center, Beirut, Lebanon M. A. Bitar, Section of Pediatric Otolaryngology, Department of Otolaryngology-Head and Neck Surgery, American University of Beirut Faculty of Medicine and Medical Center, Beirut, Lebanon Correspondence to: Joseph G. Ghafari Division of Orthodontics and Dentofacial Orthopedics American University of Beirut Medical Center 6th Floor PO Box 11-0236 Riad El-Solh, Beirut 1107 2020, Lebanon E-mail: jg03@aub.edu.lb Macari A. T., Bitar M.A., Ghafari J.G. New insights on age-related associ- ation between nasopharyngeal airway clearance and facial morphology Orthod Craniofac Res 2012. Ó 2012 John Wiley & Sons A ⁄ S Structured Abstract Objectives – To evaluate the relation between adenoid hypertrophy and facial morphology across age in a pediatric population. Setting and Sample Population – The American University of Beirut Department of Otolaryngology. Two-hundred consecutive children (age 6.00 ± 2.62 years) referred from the Pediatric Otolaryngology unit to the Orthodontic division and requiring a lateral cephalogram for adenoid hypertrophy assessment. Methods – Cephalometric measurements included relations among cranial base, maxilla and mandible, and airway clearance measured from adenoid to soft palate (AD). The children were classified into two age groups, Group 1: £ 6 years (n = 124) and Group 2: ‡ 6.01 years (n = 76), and also stratified in four subgroups (A, B, C, D) based on maxillo-mandibular divergence (palatal to mandibular plane angle, PP-MP): A- PP-MP £ 27.5°, n = 34; B- 27.5° < PP-MP £ 32°, n = 68; C- 32°<PP ⁄ MP<36.5°, n = 67; D- PP-MP ‡ 36.5°, n = 31. Statistics included t-tests and ANOVA for group differences. Results – Differences between groups 1 and 2 were statistically significant (p < 0.05) for AD (Group 1: 3.19 ± 2.32 mm, Group 2: 4.78 ± 2.80 mm), ANB (5.38 ± 2.24°, 4.38 ± 2.54°), LFH (56.61 ± 1.95%, 55.38 ± 1.84%), PP-H ()8.41 ± 3.28°, )6.49 ± 3.46°), and overbite (0.55 ± 2.00 mm, 1.16 ± 2.36 mm). Among subgroups, statistically significant differences (p < 0.05) occurred mainly between the most hyperdivergent group (D) and the hypodivergent (A) and normodivergent (B) groups. Conclusions – Airway measurements were smallest in children £ 6 years and those presenting severe hyperdivergent pattern, which denoted the most severe airway obstruction. The findings suggest airway clearance before age 6 in the most severely affected children, but follow-up research on actualadenoidectomiesinyoungerchildrenisneededtodetermineguidelines. Key words: adenoid; facies; jaw relation; malocclusion; nasal obstruction Dates: Accepted 4 February 2012 DOI: 10.1111/j.1601-6343.2012.01540.x Ó 2012 John Wiley & Sons A ⁄ S
  • 2. Introduction Adenoid hypertrophy is the source of various diseases because of consequent nasal obstruction and oral respiration. The medical symptoms (snoring, otitis media, sinusitis, sleep apnea) affect the well-being of the patient but also of the family, often placing in second order the long- term effects on facial morphology, such as aber- rant development of maxillary and mandibular structures. Yet, such alterations can lead to per- manent dysmorphology that might require orthognathic surgery in adulthood, when it may have been partially or totally avoided in child- hood. A revealing reference to the long-standing association between airway clearance and facial morphology is the description of Ôadenoid faciesÕ or long-face syndrome (1). This ÔhyperdivergentÕ skeletal pattern characteristically includes in- creased lower face height, constriction of the maxillary arch, open bite between the anterior teeth, increased gingival display above the max- illary anterior teeth, and retrognathic mandible. Hence, the fully developed long-face syndrome includes both functional and esthetic impairment. Orthodontic results do not achieve optimal esthetic outcome because facial elongation, particularly subnasal, gingival smile, and chin retrusion may not be adequately corrected. Orthognathic surgery better addresses the skeletal deviations. The relationship between mouth breathing and malocclusion is not clear-cut (1–3), probably because the extent and severity of morphologic alterations depend on timing, duration, and rate of oral respiration. The issue is further con- founded by the diagnostic accuracy of mouth breathing (4). Quantitative definitions of this condition have been advocated but have yet to be proven effective or practical (rhinometry, nasal flow, nasal resistance), especially in children. Newer devices that are easier to use discern dif- ferences between nasal and oral breathing during clinical examination (5–7) but apparently need additional validation for universal application. Otolaryngologists and orthodontists regularly use lateral cephalometric imaging to evaluate adenoid contribution in blocking normal respi- ration (8). Correspondence of cephalometric measurement and subjective rating of airway clearance indicates the practicality of cephalo- metric imaging as a guide to diagnosis and decision making (8). This finding is supported by systematic review of the literature regarding the validity of lateral cephalograms in diagnosing enlarged adenoids and obstructed posterior nasopharyngeal airways in children and adoles- cents (9). Moderate to strong correlations were noted between actual adenoid size (determined post-adenoidectomy) and both quantitative measures of adenoid area and subjective grading of adenoid size on lateral cephalographs. The shortest distance between adenoid and soft pal- ate (termed in our study AD) was the princi- pal measurement validated from various studies (9). The evidence from post-surgical studies in children (10, 11) revealed a more anterior sym- physeal growth, reversal of the tendency to pos- terior mandibular rotation, increased mandibular growth, and unchanged direction of maxillary growth. In addition, our clinical observations, indirectly supported by research (12, 13), indi- cated that late removal of the adenoids does not improve the set orofacial dysmorphology. Despite such findings, timing the adenoidectomy on individual basis has yet to be achieved. While a significant amount of evidence is available on the relation between mode of breathing and orofacial morphology, a number of research limitations are difficult to overcome. The collection of cephalo- graphs in younger children who normally breath through their nose is understandably restrained by the reluctance of Internal Review Boards and parents to accept the procedure. Available inves- tigations in early childhood relied on pre-existing cephalometric or other imaging (MRI) records (14, 15). Small samples or inconclusive results point to the need for more generalizable research findings. Finally, there is a need to determine earlier morphological effects of altered respira- tion than available in the literature. Extensively quoted in the orthodontic and otolaryngology literature, the key studies by Linder-Aronson and co-workers do not include children younger than age 6 years (16). 2 Orthod Craniofac Res 2012 Macari et al. Airway clearance and long-face characteristics
  • 3. In this context, we hypothesized that the rec- ognition of severe morphological deviations in children younger than age 6 should lay the ground for future investigation of the optimal timing of adenoidectomy that would prevent the attain- ment of irreversible or non-improvable orofacial alterations. Also, regardless of the existence of clinically diagnosed mouth breathing, we sought to evaluate the association between the cephalo- metric measurement of airway patency and oro- facial deviations from normal relation, particu- larly in children below age 6. Therefore, our specific aims were to 1-evaluate, in a prepubertal population diagnosed with chronic mouth breathing, the association between facial morphology and airway obstruc- tion by the adenoid across age, including ages younger (< 6 years) than available in the literature and 2-compare dysmorphologic features accord- ing to severity of facial morphological pattern. Patients and methods Patients The study population consisted of 200 consecu- tive children (127 boys, 73 girls) referred by the pediatric otolaryngologist to the Division of Orthodontics and Dentofacial Orthopedics, American University of Beirut Medical Center, for cephalometric imaging of pharyngeal airway impingement by the adenoid. The otolaryngolo- gist (MAB) had diagnosed these children as having chronic mouth breathing (> 3 months duration) based on the history taken. On physical exami- nation, the adenoid was suspected as the only contributor to the airway obstruction, after ruling out the presence of other causes (as detailed in the exclusion criteria). No reference was made to lip posture as not all children with open lip are mouth breathers. Adenoid hypertrophy is com- monly evaluated by soft tissue nasopharyngeal radiographs (10), but the lateral cephalogram used by orthodontists is more dependable be- cause of controlled head position in the cepha- lostat. Although regularly requested and taken, and not an addition for research purposes, insti- tutional approval of the radiograph is required for any research usage of the data; thus, the Institu- tional Review Board clearance was obtained and required standards followed. Exclusion criteria were as follows: septal devi- ation, bilateral inferior turbinate hypertrophy, kissing tonsils, previous surgery related to nasal obstruction (including adenoidectomy and ton- sillectomy), recent medical treatment of nasal airway impairment, systemic disease, congenital malformations. The mean age of the children was 6.0 years (range: 1.71–12.61; Fig. 1). Most patients (62%, n = 124) were below age 6. Nearly half (46%; n = 93) were < 5 years and the greatest percent- age (24.5%, n = 49) ranged between 4 and 4.9 years. Fig. 1. Age distribution intervals by increment of 6 months. Orthod Craniofac Res 2012 3 Macari et al. Airway clearance and long-face characteristics
  • 4. Lateral cephalometry The cephalographs were taken in the same digital cephalostat (GE, Instrumentarium, Tuusula, Finland) following a uniform procedure. With the body covered by a lead apron, the head of the child was placed in natural head position, which is a standardized orientation when one focuses on a distant reference at eye level (17). This posi- tioning helps determine the horizontal reference (H) as defined by Moorrees et al. (17). This ÔtrueÕ or ÔcorrectedÕ plane is prone to less error than the Frankfort horizontal defined by two variable landmarks, nasion and porion (18). The children were guided to occlude their teeth in the retruded contact position and keep the lips in gentle touch. As the distance between the facial midsagittal plane and the film is set by the man- ufacturer, the corresponding radiographic mag- nification is adjusted for automatically. Images were saved and stored directly in a dedicated computer. To avoid inter-examiner variation, a single investigator (ATM) imported and digitized the radiographs into the imaging program (Dolphin Imaging and Management Solutions, La Jolla, California). Angular and linear measurements were computed to evaluate the sagittal and verti- cal positions of the maxilla, the mandible, and their dental components, relative to the cranial base and to each other (Fig. 2A). Selected mea- surements included in this article are SNA, SNB, ANB, palatal plane (ANS-PNS) to horizontal (PP-H); mandibular plane (menton-gonion: Me-Go) to SN (MP-SN), to horizontal (MP-H), and to palatal plane (PP-MP); ratio between lower and total facial heights (LFH). The shortest distance between adenoid and soft palate (AD) and the distance between the most convex adenoid point and soft palate (CD) were used to quantify airway clearance (Fig. 2). The occlusion of the children was examined and noted. Taking cephalograms on children who must keep the teeth in contact and be still during exposure was difficult in several patients below age 5. When the teeth were apart more than 2 mm, the radiographs were discarded, reducing the total number to the reported 200. In a small number (17 of 200), the imaging program allowed ÔautorotationÕ of the parted mandible for mea- surement of parameters related to the mandible. In 14 children, all below 5 years, who would not be alone when taking the radiograph, a parent volunteered to hold the child; both were covered with lead aprons. Many children who could not remain still for taking the cephalograph were not A B C Fig. 2. (A) Cephalogram of 4.39-year-old boy. Landmarks: N (nasion), S (sella), ANS (anterior nasal spine), PNS (posterior nasal spine), A (deepest point on the premaxilla between anterior nasal spine and dental alveolus), B (deepest midline point on the mandible between infradentale and pogonion), Me (menton- most inferior point on mandibular symphysis), Go (gonion- external angle of the mandible, bisecting the angle formed by tangents to the posterior border of the ramus and the inferior border of the mandible), H (horizontal corresponding to natural head position), PP (palatal plane through ANS and PNS), MP (mandibular plane through Me and Go), selected measurements: SNA; SNB; ANB; PP-H; MP-SN; MP-H; PP-MP; AD- shortest distance between adenoid and soft palate. CD- distance between most convex adenoid point and soft palate. Various airway clearances are shown in B and C. The latter is most severe, nearly total as indicated by arrow. 4 Orthod Craniofac Res 2012 Macari et al. Airway clearance and long-face characteristics
  • 5. recruited for the study. To determine intra-ob- server reliability, the same investigator repeated the entire cephalometric procedure and measures on 20 randomly selected cephalographs (10% of sample). Study groups The children were classified into two age groups: Group 1: £ 6 years (n = 124; 75 boys, 49 girls) and Group 2: > 6 years (n = 76; 52 boys, 24 girls). They were also categorized into four subgroups: A (n = 34), B (n = 68), C (n = 67), and D (n = 31), based on cephalometric vertical divergence derived from the angle between mandibular (MP) and palatal (PP) planes. Though the normative angulation could have been used (Bjo¨rk: 29°± 5.4°), we stratified the subgroups on the average angulation within our population: 32° ± 4.5°. This mean was higher than the norm, favoring an error toward increased hyperdiver- gence commensurate with the long-face syn- drome. The angle PP-MP sums up various characteris- tics of this syndrome: it is related to the lower face height, and maxillary inclination is factored in, avoiding the classification on mandibular angle only. Furthermore, the dentition is contained be- tween the jaws, affecting and affected by their positions. The categorization yielded two groups (A, B) at one and two standard deviations lower than the mean, and two groups (C, D) at one and two standard deviations higher than the mean. The extreme groups represented severe hypodi- vergent (A) and hyperdivergent (D) patterns. Statistical methods To assess examiner variability of repeated mea- surements, the intraclass correlation coefficients were calculated for each of the parameters stud- ied. Differences between age groups for different measurements were evaluated by t-tests. Where applicable, the analysis of variance (ANOVA) gauged differences for all measurements between various age and vertical pattern groups, as well as gender differences within age and vertical pattern groups. Statistical significance was set at p £ 0.05. Results The intraclass correlation coefficients for the intra-examiner repeated measurements were high, with 0.91 < r < 0.99 for the reported mea- surements, except for PP-H (r = 0.88), which included the horizontal H and thus was more closely related to reproducing the orientation on natural head position in the imaging program. Differences between groups 1 and 2 were statistically significant for AD and CD, ANB, LFH, PP-H, and overbite (p = 0.05–0.000; Table 1). Both groups had measurements of mandibular plane that were on average compatible with hyperdi- vergence. Accordingly, the corresponding values (MP-SN, PP-MP) were not statistically signifi- cantly different. Posteroinferior tip of the palatal plane (PP-H) was observed in both groups, but was less severe in the older group (p = 0.000). The tilt was highest ()8.9°) between 4 and 4.9 years. The groups stratified on mandibular divergence showed age similarities and statistically significant differences between younger and older groups in each subgroup (A-D; Table 2). The ANOVA revealed statistically significant differences among these groups for all measurements except for age, AD, Table 1. Means of age and selected cephalometric mea- surements in age groups Group 1 N = 124 Group 2 N = 76 pMean SD Mean SD Age (years) 4.30 0.99 8.79 1.00 0.000 AD (mm) 3.19 2.32 4.78 2.80 0.000 CD (mm) 3.83 2.74 5.54 3.21 0.000 Sagittal measurements SNA (°) 81.04 3.69 80.73 4.01 0.58 SNB (°) 75.68 3.56 76.35 3.38 0.21 ANB (°) 5.38 2.24 4.38 2.54 0.004 Overjet (mm) 2.7 1.82 2.78 2.31 0.78 Vertical measurements LFH (%) 56.61 1.95 55.38 1.84 0.000 PP-H (°) )8.41 3.28 )6.49 3.46 0.000 MP-SN (°) 39.64 4.85 39.56 5.63 0.91 PP-MP (°) 32.25 4.35 31.48 4.82 0.25 Overbite (mm) 0.55 2.00 1.16 2.36 0.05 Orthod Craniofac Res 2012 5 Macari et al. Airway clearance and long-face characteristics
  • 6. CD, and overjet (Table 3). Differences were statis- tically significant (p = 0.02–0.000) for all vertical measurements (LFH, PP-H, MP-SN, PP-MP, and overbite) among all group comparisons (except overbite between groups A,B and B,C, and PP-H between A and B); for AD and CD only between the most severe group (D) and the hypodivergent and normodivergent groups (A and B, respectively); and for sagittal measurements mainly between groups D and A, and D and B. As might be expected, gender differences (p < 0.05) within age groups were limited to linear measurements such as SN, ANS-PNS, NGn and were found for all measurements between age groups. In the divergence-stratified groups, gen- der differences occurred only in the B group (44 boys, 24 girls) for the distances AD (male: 4.59 ± 2.57 mm; female: 3.01 ± 2.25 mm; p = 0.02) and CD (male: 5.50 ± 3.18 mm; female: 3.63 ± 3.23 mm; p = 0.03). Table 2. Descriptive statistics of groups stratified on PP ⁄ MP Groups A PP ⁄ MP £ 27.5° B 27.5° < PP ⁄ MP £ 32° C 32° < PP ⁄ MP < 36.5° D PP ⁄ MP ‡ 36.5° p   N 34 (17%) 68(34%) 67 (33.5%) 31 (15.5%) Group 1 (< 6 years) n = 124 n = 20 [16.12%] n = 38 [30.64%] n = 47 [37.90%] n = 19 [15.32%] Age (years) [range] 4.46 ± 0.74 [2.89–5.94] 4.27 ± 1.05 [1.94–5.85] 4.26 ± 1.12 [1.71–5.98] 4.28 ± 0.77 [3.17–5.87] NS Group 2 (> 6 years) n = 76 n = 14 [18.42%] n = 30 [39.47%] n = 20 [26.31%] n = 12 [15.78%] Age (years) [range] 9.91 ± 1.73 [7.06–12.01] 8.61 ± 2.06 [6.09–12.62] 8.39 ± 1.75 [6.02–12.52] 8.58 ± 2.19 [6.15–12.59] NS p  0.000 0.000 0.000 0.000   Statistically significant differences for age between age groups 1 (age < 6 years) and 2 (age > 6 years)    Statistically significant differences for age among subgroups (A–D). Table 3. Means of age and selected cephalometric measurements in groups stratified on PP ⁄ MP Groups A PP ⁄ MP £ 27.5° B 27.5° < PP ⁄ MP £ 32° C 32° < PP ⁄ MP < 36.5° D PP ⁄ MP ‡ 36.5° p ANOVA p Comparisons among groups A, B, C, D Mean SD Mean SD Mean SD Mean SD AB AC AD BC BD CD Age (years) 6.70 2.99 6.19 2.67 5.49 2.31 5.94 2.58 NS NS 0.03 NS NS NS NS AD (mm) 4.30 2.83 4.03 2.55 3.81 2.67 3.11 2.38 NS NS NS 0.01 NS 0.03 NS CD (mm) 4.94 3.039 4.84 3.3 4.22 2.92 3.76 2.74 NS NS NS 0.03 NS 0.04 NS Sagittal measurements SNA (°) 81.49 4.32 81.72 3.78 80.61 3.39 79.25 3.98 0.02 NS NS 0.03 0.074 0.004 NS SNB (°) 77.05 4.31 77.06 3.45 75.46 2.84 73.26 3.88 0.000 NS NS 0.000 0.004 0.000 0.002 ANB (°) 4.45 2.19 4.68 2.16 5.14 2.68 5.98 2.38 0.03 NS NS 0.009 NS 0.008 NS Overjet (mm) 3.18 2.186 2.65 2.01 2.55 1.99 2.81 1.89 NS NS NS NS NS NS NS Vertical measurements LFH (%) 55.85 1.76 56.83 1.76 58.02 2.12 59.18 1.65 0.000 0.009 0.000 0.000 0.000 0.000 0.02 PP-H (°) )6.24 3.03 )6.19 3.19 )8.46 3.16 )10.94 2.38 0.000 NS 0.001 0.000 0.000 0.003 0.000 MP-SN (°) 33.68 3.35 37.72 3.37 41.30 2.93 46.62 3.73 0.000 0.000 0.000 0.000 0.000 0.000 0.000 PP-MP (°) 25.72 1.82 29.79 1.23 33.91 1.25 39.31 2.66 0.000 0.000 0.000 0.000 0.000 0.000 0.000 Overbite (mm) 1.87 1.88 1.09 2.44 0.58 1.75 )0.67 1.74 0.000 NS 0.000 0.000 NS 0.000 0.001 6 Orthod Craniofac Res 2012 Macari et al. Airway clearance and long-face characteristics
  • 7. Dental relations ranged from normal occlusion with adequate overjet ⁄ overbite to malocclusions with one or more of the following characteristics: posterior crossbite, overjet, distoclusion, open bite, anterior crossbite. Discussion This study yielded important contributions re- ported for the first time because the significant number of children < age 6 years (most of whom are below 5 years – Fig. 1) allowed the description of very early stages of morphologic alteration. Association between nasal obstruction and facial dysmorphology Many differences between younger and older age groups could be related to the effect of normal growth of the nasopharynx leading to increase in airway clearance (11). Other ameliorations with age include decreases in the lower face height and in the postero-inferior tilt of the palatal plane (Table 1). However, both age groups include important characteristics ascribed to hyperdiver- gence (MP-SN, PP-MP), suggesting that this pat- tern on average would persist. Chosen at more than one SD of the total sample average and exceeding the one SD of normative data, Group D possessed, at statistically significant levels, the most severe airway obstruction (AD and CD), and the most severely associated characteristics of the long-face syndrome, both skeletal (LFH, PP-H, MP-SN) and dental (overbite), as well as man- dibular retrognathism (SNB) (Table 3). While hy- perdivergence occurred less in group 2 (n = 12) than in group 1 (n = 19), percentages were simi- lar: 15.78 and 15.32%, respectively (Table 2). The findings suggest that facial dysmorphology develops in a sequential process, apparently starting in structures closest to the obstruction namely the maxilla, which tilted postero-inferi- orly as gauged by the inclination of the palatal plane, with a maximal tilt ()8.41°) in the younger group, mostly between 4 and 4.9 years ()8.9°), compared to the Caucasian norm [PP-H = 0° ± 2.5° (19)]. The oropharyngeal space is a primary entity that influences the position and behavior of the surrounding soft tissues, which in turn shape the associated skeletal units (20). Impingement on the oropharyngeal space leads to adaptive reorgani- zation of adjacent structures, the long-face syn- drome representing the extreme expression of prolonged functional disturbance. Conversely, any degree of adaptive morphologic change may result in a level of restoration of nasal breathing. As adaptation to either total or partial airway obstruction is an individual response to preserve the oropharyngeal matrix, the occlusal variation from normal relation to different malocclusions is not surprising. Similar variations were found in experimental animal studies whereby the nostrils of monkeys were obstructed to induce oral res- piration (21). Longitudinal data are not available on normal growth of the distances AD and CD, which in- creased between ages 4.3 years (Group 1 average) and 8.79 years (Group 2 average) by 50% (4.78– 3.19 = 1.59 mm) and 45% (5.54–3.83 = 1.71 mm), respectively (Table 1). In contrast, longitudinal data on a corresponding hard tissue measure- ment, such as the distance between PNS and hormion (at the bottom of the spheno-occipital synchondrosis), indicate an increase of nearly 13% (14% in males, 12% in females) between ages 4 and 9 years (22). The seemingly smaller percent- age increase in the hard tissue parallel to AD and CD would suggest that the soft tissue airway clearance improved at a proportion greater than the underlying skeletal structures. Given that the skeletal distance is nearly 24 mm at younger ages (range: 23–26 mm) (22, 23), 13% would corre- spond to approximately 3 mm. The 1.6–1.7 mm (45–50%) improvement in AD or CD is less than the skeletal change, notwithstanding the fact that the skeletal data were derived from individuals who did not necessarily have mouth breathing, the prevailing condition of the children in this study. Clinical implications Primary care physicians often delay or oppose removal of the adenoids because these tissues contribute to immunological defenses and are Orthod Craniofac Res 2012 7 Macari et al. Airway clearance and long-face characteristics
  • 8. expected to decrease in size around adolescence (15). Medical and craniofacial characteristics are not competitive reasons for adenoidectomy. Medical reasons may dictate the surgery without craniofacial alterations having risen to the pri- mary cause of the surgery. Yet, nasal airway obstruction, of any etiology, has the potential to severely affect only craniofacial morphology, jus- tifying intervention. Stating that adenoids lead to mouth breathing primarily in children with a small nasopharynx, Linder-Aronson advocates adenoidectomy in these children (15, 16), but this recommendation is not tested in clinical trials. Our research indi- cates that the children in group D, who combined both the severe vertical pattern (beyond 1 SD) and the smallest distances between the adenoid and soft palate (AD and CD), are probably the likeliest candidates for adenoidectomy for reasons that include facial dysmorphology. The deviant fea- tures were present below and above age 6 years. These data would suggest that: 1 – decreased airway clearance in the presence of dysmorphol- ogy would warrant adenoidectomy, at least for the cohort already exhibiting severe characteristics of long-face syndrome least affected by orthodontic treatment (e.g. gummy smile in conjunction with anterior open bite and overerupted posterior teeth); 2 – the optimal timing of the surgery should be before age 6 years. The average age of the children in group D below age 6 years was 4.37 years, ranging from 3 to 6 years (Table 2). Perhaps this age bracket should be considered for future research on optimal timing of early ade- noidectomy. A later surgery, such at the average age of group 2 (8.79 years), would not lead to reversal of the dysmorphology. In a 6-year longitudinal study (12) in which adenoidectomy was recommended for 26 children with nasal obstruction, half had surgery within the first year of diagnosis (age 9.1 ± 2 years), and the other half served as con- trols (9.4 ± 1.5 years). The results indicated that adenoidectomy may change the breathing pattern without a significant effect on malocclusion and facial type. The suspicion of enlarged adenoids as the pre- dominant reason for the diagnosed mouth breathing may be questioned in at least the chil- dren with wider airway clearance (groups A, B, C) unless other obstructions justify intervention. Upon evaluation of the x-rays of these children, tonsillar and ⁄ or inferior turbinate hypertrophy was documented when present. The former is readily diagnosed clinically, and the latter is best confirmed with endoscopy. The referring pediat- ric otolaryngologist followed up on these findings, having requested the cephalograph to image the adenoid as the only or combined cause of mouth breathing for a complete diagnosis and a com- prehensive treatment plan. A clear differentiation between the effects of enlarged tonsils and hypertrophied adenoids is not available in the literature. When either enlarged adenoids, tonsils, or both block nasal breathing, the effect on facial morphology is commonly thought to include characteristics toward the long- face syndrome. However, in his pioneering description of the Class III malocclusion, Angle relates its early origin, at or before the age of emergence of the permanent first molars, solely to enlarged tonsils Ôand the habit of protruding the mandibleÕ to afford Ôrelief in breathing.Õ (24) Research is needed to discern these possibilities. Research considerations The study supports findings from systematic re- views that AD best reflects the status of airway clearance in a two-dimensional record (9). Three- dimensional imaging of nasopharyngeal space and structures may yield more accurate informa- tion (25), but their potential association with mouth breathing still requires quantitative assessments of respiration. A cause-and-effect relationship between nasal airway obstruction and dysmorphology is both difficult and unethical to investigate with longi- tudinal radiation in children with untreated obstruction (26). The difficulty in recruiting nor- mally breathing children with normal occlusion, particularly between the ages of 2 and 5 years, who would be subjected to cephalometric radiation, precluded the inclusion of a control group. Also, defining normal ÔnasalÕ respiration is questionable in the absence of objective assessment, which 8 Orthod Craniofac Res 2012 Macari et al. Airway clearance and long-face characteristics
  • 9. remains difficult to obtain in younger children. Although no matched controls were available, the stratification on vertical pattern discriminated between the children with long-face syndrome characteristics and those with less severe or no dysmorphology. Research, particularly longitudinal, is needed to formulate definitive projections of irreversible changes that would warrant the timely early adenoidectomy. Conclusions In a study that included for the first time a sig- nificant number of children early in childhood (ages 2–6 years), initial stages of morphologic alteration from nasal obstruction were described. Narrowing of the posterior pharyngeal airway by enlarged adenoids apparently leads to a sequen- tial process of morphologic alteration, starting with the closest structure (maxilla), and encom- passing variable occlusal changes. Facial adjust- ments were more severe with greater airway obstruction (group D). These findings suggest early clearance of the nasal passageway to avert, arrest, or reverse facial alterations in the most severely affected children. Guidelines must be defined for early adenoid- ectomy in relation to facial morphology, not- withstanding the medical imperatives for the surgery. Research to determine such guidelines should be based on the premise that optimal conditions may include severe airway obstruction at age < 6 years in individuals on track to develop irreversible characteristics of the long-face syndrome. A set dysmorphology is difficult to resolve with increasing age. While primary care physicians do not readily accept the tenet that prevention of craniofacial dysmorphology represents an indi- cation for adenoidectomy (and ⁄ or tonsillectomy), the potential craniofacial problems and associ- ated difficulty in treatment (including eventual orthognathic surgery) cannot be dismissed and require due attention. Clinical relevance We evaluated the cephalometric relationship be- tween nasopharyngeal obstruction by adenoid hypertrophy and facial morphology in children referred by the otolaryngologist. Long-face syn- drome characteristics are difficult to treat back to normal in late childhood. Decreased airway clearance in children with most severe hyperdi- vergent features suggests removing obstacles to nasal respiration early (age < 6 years), laying the ground for more longitudinal research. References 1. Schendel SA, Eisenfeld J, Bell WH, Epker BN, Mishelevich DJ. The long face syndrome: vertical maxillary ex- cess. Am J Orthod 1976;70:398–408. 2. Trotman CA, McNamara JA Jr, Dib- bets JM, van der Weele LT. Associa- tion of lip posture and the dimensions of the tonsils and sagittal airway with facial morphology. Angle Orthod 1997;67:425–32. 3. Vig KWL. Nasal obstruction and facial growth: the strength of evidence for clinical assumptions. Am J Orthod Dentofacial Orthop 1998;113:603–11. 4. Leiter JC, Baker GL. Partitioning of ventilation between nose and mouth: the role of nasal resistance. Am J Orthod Dentofacial Orthop 1989;95: 432–8. 5. Ovsenik M, Farcnik FM, Korpar M, Verdenik I. Follow-up study of functional and morphological mal- occlusion trait changes from 3 to 12 years of age. Eur J Orthod 2007;29:523–9. 6. Ovsenik M. Incorrect orofacial func- tions until 5 years of age and their association with posterior crossbite. Am J Orthod Dentofacial Orthop 2009;136:375–81. 7. Fujimoto S, Yamaguchi K, Gunjigake K. Clinical estimation of mouth breathing. Am J Orthod Dentofacial Orthop 2009;136:630.e1-7; discussion 630–1. 8. Bitar MA, Macari AT, Ghafari JG. Correspondence between subjective and linear measurements of the palatal airway on lateral cephalomet- ric radiographs. Arch Otolaryngol Head Neck Surg 2010;136:43–7. 9. Major MP, Flores-Mir C, Major PW. Assessment of lateral cephalometric diagnosis of adenoid hypertrophy and posterior upper airway obstruc- tion: a systematic review. Am J Orthod Dentofacial Orthop 2006;130: 700–8. 10. Bahadir O, Caylan R, Bektas D, Bahadir A. Effects of adenoidectomy in children with symptoms of adenoidal hypertrophy. Eur Arch Otorhinolaryngol 2006;263:156–9. 11. Linder-Aronson S, Woodside DG, Lundstrom A. Mandibular growth direction following adenoidectomy. Am J Orthod 1986;89:273–84. 12. Gu¨ray E, Karaman AI. Effects of ade- noidectomy on dentofacial structures: Orthod Craniofac Res 2012 9 Macari et al. Airway clearance and long-face characteristics
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