ORIGINAL ARTICLE

Vertical alveolar growth in subjects with

infraoccluded mandibular deciduous molars
Caroline Dias,a Luciane Quadrado Closs,b Vania Fontanella,c and Fernando Borba de Araujod
Canoas and Porto Alegre, Rio Grande do Sul, Brazil
Introduction: Our objective was to compare vertical alveolar growth in areas adjacent to infraoccluded deciduous molars with growth in areas of deciduous molars and normal occlusion for a period of at least 1 year by
using digital subtraction radiography. Methods: This case-control study included 40 pairs of panoramic
radiographs of growing patients with infraoccluded deciduous molars and 40 pairs of radiographs of patients
without infraoccluded deciduous molars. One radiograph at baseline was obtained at diagnosis, and the other
at least 1 year later. The subjects and the controls were matched according to chronologic age and time
interval between the 2 radiographs. The 2 groups were compared with regard to vertical alveolar growth and
vertical tooth movement. Measurements were assessed by using nonparametric tests (Mann-Whitney and
Friedman) and a multiple comparison test. Signicance was set at 5%. Results: A statistically signicant difference was observed between the groups with regard to vertical alveolar growth measured on the bone crest between the rst permanent molars and second premolars. Conclusions: Vertical alveolar growth between the
rst permanent molar and the second premolar adjacent to the infraoccluded teeth was smaller than in areas
adjacent to teeth with normal occlusion. (Am J Orthod Dentofacial Orthop 2012;141:81-6)

ental ankylosis, also called teeth in infraocclusion, is commonly found in deciduous and transitional dentitions, with a prevalence ranging
from 8% to 14% in patients aged 6 to 11 years; severity
is usually mild (61.3%) or moderate (30.4%).1-5
Deciduous teeth are more commonly affected than
permanent teeth, especially the rst and second
deciduous molars.4-7
When there is infraocclusion, growth and development of the alveolar bone are affected, with a consequent
reduction in bone height, thus precluding eruption of the
affected tooth that remains in infraocclusion.8,9 Early
diagnosis of the infraocclusion is essential for the
establishment of effective preventive measures or
treatment planning, including invasive procedures,
always associated with adequate follow-up.4
a
Postgraduate student, Department of Orthodontics, School of Dentistry, Universidade Luterana do Brasil, Canoas, Rio Grande do Sul, Brazil.
b
Assistant professor, Department of Orthodontics, School of Dentistry, Universidade Luterana do Brasil, Canoas, Rio Grande do Sul, Brazil.
c
Assistant professor, Department of Oral Radiology, School of Dentistry, Universidade Luterana do Brasil, Canoas, Rio Grande do Sul, Brazil.
d
Associate professor, Department of Pediatrics, School of Dentistry, Universidade
Federal do Rio Grande do Sul, Porto Alegre, Brazil.
The authors report no commercial, proprietary, or nancial interest in the products or companies described in this article.
Reprint requests to: Caroline Dias, Marcelo Gama, 1249. Porto Alegre/RS, Brazil;
e-mail, carolinedias@terra.com.br.
Submitted, September 2010; revised and accepted, June 2011.
0889-5406/$36.00
Copyright ! 2012 by the American Association of Orthodontists.
doi:10.1016/j.ajodo.2011.06.037

Radiographic investigation is often recognized as an

important diagnostic method in the follow-up of patients with infraoccluded teeth. It allows detection of
an ankylosed area based on the absence of continuity
of the periodontal ligament in the region where the cementum fuses with the alveolar bone.10,11 Moreover,
digital subtraction of panoramic radiographs has been
successfully used to evaluate the behavior of implants,
periapical lesions, and condylar alterations. This
method allows evaluation of small changes by the
superimposition of 2 radiographs, as shown in
previous studies.12-15
No scientic evidence or research data are available
conrming the relationship between infraocclusion
of deciduous molars and vertical alveolar growth
abnormalities in areas adjacent to the affected teeth.
Therefore, the objective of this study was to compare
vertical alveolar growth in areas adjacent to infraoccluded deciduous molars with areas of deciduous molars
with normal occlusion for at least 1 year, based on
measurements obtained with digital subtraction radiography.
MATERIAL AND METHODS

The study protocol was approved by the Research

Ethics Committee at Universidade Federal do Rio Grande
do Sul in Brazil (protocol number 05/08). Pairs of panoramic radiographs of 80 patients in the transitional
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82

Fig 1. A and B, subject with mild infraocclusion (clinical

and panoramic images).

Fig 2. A and B, subject with moderate infraocclusion

(clinical and panoramic images).

dentition, aged 6 to 9 years, and with the rst permanent

molars having at least one third of root formation, were
selected from the les in the Department of Orthodontics and Pediatric Dentistry of the School of Dentistry.
Half of the radiographic image pairs (n 5 40) were obtained from patients who had infraoccluded deciduous
molars (group 1, subjects) and the other half (n 5 40)
from age-matched patients without infraocclusion
(group 2, controls).
Inclusion criteria for group 1 were infraocclusion affecting at least 1 mandibular deciduous molar and the
availability of 2 panoramic radiographs obtained within
a time interval of at least 12 months, one at diagnosis
(baseline, T1) and the other at least 1 year later (T2). After
initial clinical examinations of the patients by 2 experienced examiners (a pedodontist [C.D.] and an orthodontist [L.C.]) for submergence of the deciduous molars,
intraoral photographs and study models were evaluated
to diagnose infraoccluded second deciduous molars. Infraocclusion was considered to be mild when the occlusal
surface of the tooth was approximately 1 mm below the
occlusal plane (line drawn between the rst molar and the
canine) and moderate when the occlusal surface of the
tooth and both marginal crests were at the same level
or slightly below the contact point with the adjacent

teeth (Figs 1 and 2). Measurements were recorded to

the nearest tenth of a millimeter with a digital caliper (Mitutoyo Digimatic, Mitutoyo, Hampshire, United Kingdom). Two independent investigators (C.D. and L.C.)
made space measurements, and the average of the 2
measurements was used in the analysis. The sample included 18 teeth with moderate infraocclusion and 22
with mild infraocclusion.
Patients undergoing treatment with systemic medications or with a history of growth disorders, such as gigantism, nanism (abnormally small size or stature),
cleidocranial dysostosis, and ectodermal dysplasia,
among others, were excluded from the sample. Patients
needed to have their mandibular rst permanent molars
fully erupted and normally shaped. Deciduous molars
had to have at least a third of their root length with no
mobility. Subjects with dental anomalies of number
and form in the deciduous dentition were also excluded
from the sample.
The control patients were matched to each subject
based on chronologic age and time interval between
the T1 and T2 radiographs.
The mean ages were 8.0 6 1.2 years in group 1 and
8.1 6 1.2 years in group 2. The mean time intervals between the 2 radiographs comprising the pairs were 27.3

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Fig 3. A, Lines marked along the crest of the ridge from the mandibular rst permanent molar to the
mandibular permanent canine, and B, points marked on the cusp tips of permanent teeth.

6 17.9 months in group 1 and 25.8 6 13.4 months in

group 2.
The radiographs were digitized with a resolution of
150 dpi at 8 bits and saved as jpg les, divided into
left and right sides. Measurement points were marked
on the digital copies of the T1 and T2 images by a previously trained examiner (C.D.). For the assessment of vertical tooth movement, the cusp tips of the rst
permanent molar, second premolar, rst premolar, and
permanent canine were marked with points (Fig 3, A).
For the assessment of vertical alveolar growth, lines
were marked along the crest of the ridge from the permanent rst molar up to the permanent canine of each
hemi-arch in each image (Fig 3, B).
Each radiographic image pair was assessed by the
same examiner (C.D.), previously calibrated in a pilot
study. Briey, 10 images were selected, superimposed,
and measured 3 times by the same examiner. The intraclass correlation coefcient showed excellent agreement among the 3 measurements (ri 5 0.947;
P \0.001).
With the digital subtraction radiography method
and Photoshop (version 7.0; Adobe, San Jose, Calif),
the 2 images obtained from each patient at T1 and
T2 were superimposed (Fig 4). Vertical and horizontal
adjustments (sliding and rotating 1 image on another)
were made based on the cortical border of the mandible
and the mesiodistal diameter of the rst permanent
molar.
Vertical tooth movement and vertical alveolar growth
were measured in millimeters, to an accuracy of 0.1 mm,

by using the digital ruler tool in Adobe Photoshop, as the

distance between the points previously marked on the
cusp tips and on the bone crest of each image, respectively. Growth and movement were expressed as the difference in the distance between the reference points
marked on the T1 and T2 images. Measurements made
after superimposition of the 2 images aimed to prevent
possible errors in the measurements of the 2 images of
the same patient.
Statistical analysis

Measurements obtained in the 2 groups were assessed and compared by using nonparametric tests
(Mann-Whitney and Friedman), as well as a multiple
comparison test. Nonparametric tests are used for small
samples and are not based on normal distribution. The
Mann-Whitney test, a nonparametric counterpart to
the independent samples t test, was used when at least
1 ordinal dependent variable was not assumed to be normally distributed. The Friedman test was used for independent variables with 2 or more levels and when at least
1 dependent variable was not assumed to be normally
distributed. Signicance was set at 5%.
RESULTS

The Table shows the results from groups 1 and 2.

There were no statistically signicant differences between the groups with regard to vertical tooth movement. However, in the assessment of vertical alveolar
growth, a statistically signicant difference was

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Fig 4. Digital subtraction radiography: superimposed

images.

observed in the area of the rst permanent molar and

second premolar.
By using the Friedman test and a multiple comparison test, statistically signicant differences were observed for vertical tooth movement in all sites assessed
in the control group; these differences were progressively smaller from the permanent canine toward the
molar, as expected. In the subject group, however, no
differences were observed in the measurements obtained
for the rst and second premolars; the movement observed in the premolars was signicantly smaller compared with the permanent canine and greater than that
observed in the rst permanent molar. When assessing
vertical alveolar growth, no differences were detected
between the sites in either group.
DISCUSSION

This study was designed to assess the vertical alveolar

growth patterns often observed in clinical practice in association with infraoccluded deciduous molars, by using
digital subtraction radiography. This imaging technique
has been studied and used since the 1980s for various diagnostic and clinical applications, and consists of inverting gray levels and assigning 50% of transparence to the
upper layer. Because the images do not have the sharpness usually observed in radiographs, the structures of interest were marked on the image pair.12 Reproducibility of
the subtraction method has already been demonstrated
for repetition of linear and gray-level measurements on
the same superimposed images and also for repetition
of the whole subtraction process from the beginning.16
Evaluation of alveolar bone loss, caries, periapical lesions,
and external root resorption are some of the most frequent applications of digital subtraction radiography.17

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Originally, the sample was planned to include patients with unilateral infraoccluded deciduous molars,
so that different growth disorders affecting the same patient could be investigated. However, during sample selection, most patients were found to have infraocclusion
of deciduous molars in both hemi-arches; therefore, we
decided to change the study design and establish a subject group with bilateral infraocclusion (group 1) and
a control group without infraocclusion (group 2). Radiographic image pairs from both groups were matched
based on chronologic age and time interval between
the T1 and T2 radiographs.
In patients with moderate or severe ankylosis, growth
abnormalities can be clearly detected on the occlusal
plane of areas with infraoccluded teeth because of the
extrusion of antagonist teeth. Another common nding
was local open bite, caused by an arrest in alveolar
growth in the region. In our sample, however, most patients were classied as having mild or moderate infraocclusion, and there were few occurrences of tooth
extrusion and local open bite. A greater number of abnormalities related to both occlusion and alveolar
growth would probably be found if more patients with
moderate or severe infraoccluded teeth were evaluated.
Ankylosis is the main cause of infraoccluded deciduous molars. There are 2 main theories aimed at explaining the etiology of ankylosis: one focuses on local
clinical ndings, and the other on genetics.5 According
to the rst theory, changes to the local metabolism of
the periodontal ligament could provoke fusion of the alveolar bone and the cementum, leading to ankylosis.4 In
turn, some authors have assessed family members of patients with infraocclusion and suggested the involvement of a genetic mechanism, and studies with
monozygotic twins have shown that genetics do play
a role in the etiology of secondary retention of deciduous molars.18
The best way to identify ankylosis is by assessing decient interproximal growth of the alveolar bone in areas
adjacent to affected teeth.3 In our sample, a statistically
signicant difference was observed in vertical alveolar
growth between the rst permanent molar and the second premolar, suggesting decient alveolar bone growth
in areas adjacent to the infraoccluded tooth. One could
question why the rst permanent molars were used as
a reference for image superimposition. There is consensus in the literature that geometric alignment of an image pair for subtraction improves the detection of small
changes.19,20
Vertical alveolar growth adjacent to infraoccluded
teeth is slower in older children; a growth rate of
0.5 6 0.3 mm per year has been reported.8 Vertical alveolar growth variations observed between the rst

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Table. Comparison of vertical alveolar growth and vertical tooth movement (in mm)
Group 1 (subjects)
Measurement and site
Vertical tooth movement
First molar
Second premolar
First premolar
Canine
Vertical alveolar growth
Distal molar
Between rst molar
and second premolar
Between second premolar
and rst premolar
Mesial rst premolar

Group 2 (controls)

Median

25th
percentile

75th
percentile

Mean
rank

Median

25th
percentile

75th
percentile

Mean
rank

2.4
6.7
9.3
14.4

1.5
4.5
5.3
10.3

3.6
9.3
12.3
21.8

1.22c
2.28b
2.74b
3.76a

3.0
6.6
10.3
13.9

1.6
4.2
5.6
8.1

4.2
9.4
16.4
23.3

1.22d
2.19c
2.88b
3.72a

0.184
0.903
0.167
0.652

2.4
2.0

1.9
1.2

2.9
2.9

2.51a
2.28a

2.6
2.4

1.6
1.9

4.7
4.0

2.71a
2.55a

0.111
0.009*

2.1

1.5

3.4

2.43a

2.4

1.3

4.0

2.34a

0.404

2.7

1.6

3.8

2.79a

2.4

1.5

3.9

2.40a

0.733

P is the minimum signicance level (nonparametric Mann-Whitney test). Different letters indicate signicant differences (nonparametric Friedman
test complemented by multiple comparison test); signicance was set at 5%.
*Statistically signicant difference observed in the area of the rst permanent molar and second premolar.

permanent molar and the second premolar in this study

ranged from 0.2 to 4.8 mm (mean, 2.2 6 1.2 mm) in
group 1 (subjects) and from 0.7 to 10.6 mm (mean,
3.1 6 2.2 mm) in group 2. The mean bone crest growth
observed in the period assessed (26.1 6 15.8 months)
was similar to that in the study by Kurol and Koch,8
who reported approximately 40% more growth in the
control group compared with the study group. The absence of statistically signicant differences in terms of
vertical alveolar growth in each group can probably be
explained by the small sample size and the great heterogeneity of the sample.
Late extraction of infraoccluded teeth results in additional risks for the alveolar bone.1 Early tooth extraction
is indicated when adjacent teeth are inclined toward the
affected tooth and with space loss, inadequate position
of the permanent successor tooth bud associated with
deciduous root resorption, and severe infraocclusion.
With severe infraocclusion of the deciduous molars,
poor bone development is expected; therefore, tooth extraction is usually the treatment of choice.21 However,
a previous study in adults demonstrated that patients
with congenitally missing premolars have a great chance
that the retained deciduous molars will survive.22
When adequate periodontal support is available, restoration of infraoccluded deciduous molars might be an
option, with the benet of maintaining occlusal balance.6 The occlusal surface of the affected tooth is usually restored with the aim of minimizing occlusal
misalignment and reestablishing occlusion and interproximal contact.23
One important contribution of our study was to
show that, in addition to the applications already

described for digital subtraction radiography, this imaging technique can also be used to quantitatively
evaluate panoramic radiographs commonly obtained
in clinical practice.12-17
Radiographic follow-up should be used for clinical
monitoring and to dene the best moment to intervene
when necessary, to prevent growth arrest in the areas
adjacent to ankylosed teeth. A long-term follow-up
study with our sample would be interesting to assess
other clinical outcomes and to investigate whether abnormal bone growth patterns will affect the permanent
occlusion.
CONCLUSIONS

Our ndings showed that vertical alveolar growth

between the rst permanent molar and the second premolar adjacent to infraoccluded teeth was less than in
areas adjacent to teeth with normal occlusion. Subtraction radiography seems to be an effective method for assessing the absence of vertical alveolar bone growth.
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