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ORIGINAL ARTICLE

Predisposing factors for severe incisor root


resorption associated with impacted maxillary
canines
Stella Chaushu,a Karolina Kaczor-Urbanowicz,b Magorzata Zadurska,c and Adrian Beckerd
Jerusalem, Israel, and Warsaw, Poland

Introduction: Severe incisor root resorption (SIRR) associated with impacted maxillary canines is rare but has
important implications. Early diagnosis and treatment are imperative. In this investigation, we aimed to identify
predisposing factors for impacted canine-linked SIRR. Methods: Clinical and radiographic data of 55 consecutive patients (77 canines) with SIRR of 96 incisors were compared with data from 57 consecutive control subjects
(72 canines). The studied variables were age, sex, position of the impacted canine, size of the dental follicle, and
incidence of anomalous lateral incisors. Results: Lateral incisors were more often affected than central incisors,
and bilateral SIRR was common. When each variable was examined separately, SIRR was signicantly associated with female sex, severely mesiodistally displaced and vertically positioned canines in the middle third of
the adjacent incisor root, dental follicles wider than 2 mm, and normal lateral incisors. The multivariate statistical
analysis showed that the risk for SIRR was signicantly higher in female subjects (4.2 times) with enlarged dental
follicles (8.3 times) and normal lateral incisors (5.8 times). Conclusions: SIRR should be carefully screened in
female patients with enlarged dental follicles and normal lateral incisors. A greater degree of canine displacement might also be associated with SIRR. (Am J Orthod Dentofacial Orthop 2015;147:52-60)

arly studies with plain lm radiography indicated


that canine-related incisor root resorption occurs
in approximately 12% of patients.1 Yet the authors were at pains to point out that with plain lm radiography, it was impossible to properly assess the
buccolingual aspects of the incisor roots. With the
advent of more advanced imaging techniques such as
computerized tomography scanning, detectable root
resorption was diagnosed in 38% of resorbed lateral incisors and 9% of central incisors.2 Moreover, from the
study of Walker et al3 using cone-beam computed

a
Associate professor and chair, Department of Orthodontics, Hebrew
University-Hadassah School of Dental Medicine, Jerusalem, Israel.
b
Postgraduate student, International Postgraduate Orthodontic Program,
Department of Orthodontics, Hebrew University-Hadassah School of Dental
Medicine, Jerusalem, Israel.
c
Associate professor and head, Department of Orthodontics, Medical University
of Warsaw, Warsaw, Poland.
d
Clinical associate professor emeritus, Department of Orthodontics, Hebrew
University-Hadassah School of Dental Medicine, Jerusalem, Israel.
All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conicts of Interest, and none were reported.
Address correspondence to: Stella Chaushu, Department of Orthodontics, Hebrew University-Hadassah School of Dental Medicine, PO Box 12272, Jerusalem
91120, Israel; e-mail, drchaushu@gmail.com.
Submitted, February 2014; revised and accepted, September 2014.
0889-5406/$36.00
Copyright 2015 by the American Association of Orthodontists.
http://dx.doi.org/10.1016/j.ajodo.2014.09.012

52

tomography (CBCT), detection capability increased to


67% of cases of which 11% were central incisors and
4% were premolars.3,4
Congenitally missing, small, and peg-shaped maxillary lateral incisors are highly correlated with maxillary
canine palatal impaction.5 Whereas resorption of maxillary incisor roots is a well-recognized phenomenon that
can occur in patients with impacted canines,6-11 these
anomalous lateral incisors with reduced size or
abnormal shape have been reported to be less at risk to
develop severe root resorption, compared with patients
with normally shaped and sized lateral incisors.11
Fortunately, severe incisor root resorption (SIRR)
associated with impacted maxillary canines is rare, but
when is appears, it threatens the long-term survival of
the affected teeth. Early diagnosis and treatment are
imperative to save the affected tooth.12,13 At present,
evidence-based information regarding potential predisposing factors for SIRR is lacking.
The aim of this study was to identify predisposing risk
factors for SIRR associated with impacted maxillary canines.
MATERIAL AND METHODS

The study group included 55 consecutive patients


with impacted maxillary canines and SIRR, and the

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53

Fig 1. A 14-year-old boy with severely resorbed maxillary right lateral incisor associated with canine
impaction: A, panoramic view; B, periapical view; C, transaxial and 3-dimensional CBCT views.

control group included 57 consecutive patients with


impacted maxillary canines without SIRR from the
Department of Orthodontics of the Hebrew University
in Jerusalem, Israel, and the Medical University of Warsaw in Poland and from the private practices of 2 authors
(S.C. and A.B.).
The inclusion criterion for the study group was SIRR
of at least 1 maxillary incisor associated with an adjacent
impacted canine in untreated healthy patients. Diagnosis
of SIRR was made from the available panoramic and periapical radiographs that had been taken earlier with the
intention of commencing orthodontic treatment (Fig 1,
A and B). For most of the patients (75%) in the study
group, CBCT images were also available for examination
(Fig 1, C). CBCT was considered superuous for patients
in whom SIRR could be diagnosed on plain lms alone.
When CBCT was unavailable for a patient, the buccolingual position of the ectopic canine was determined using
the routine tube-shift method and conrmed by the
treating orthodontist or surgeon during surgical exposure. In the control group, CBCT had been available for
all subjects to exclude any signs of root resorption. The
radiographs were examined by 2 authors (S.C. and A.B.)
using an x-ray viewer with standard light intensity.
The CBCT examinations were performed with an iCAT scanner (12-bit; Imaging Sciences International,
Hateld, Pa) with the following parameters: 26.9 seconds
scan time, 120 kV, 5 mA, eld of view size of 13
(height) 3 16 (diameter) cm, and 0.2-mm voxel. The

resultant slice image data were converted to


3-dimensional images in DICOM format, reconstructed
by XoranCat software (version 3.1.62; Xoran Technologies, Inc, Ann Arbor, Mich) and imported to be evaluated
in i-CATVision (2008 version 1.8.1.10; Imaging Sciences
International). The reconstructed image had a 2-mm
slice thickness.
Traditionally, root resorption has been described elsewhere as horizontal shortening of the root.14 The pattern
is different for SIRR associated with impacted maxillary
canines, where the resorption is mostly oblique rather
than horizontal (Fig 2). Root resorption was measured
on the radiographs, and it was considered severe when
it affected more than a third of the length of the root,
but not specically its apical part (Fig 3). The exclusion
criteria for the sample were root resorption of maxillary
incisors less than one third of their expected root length,
root resorption secondary to trauma or pulp pathology,
or the presence of cysts and other pathologies.
The numbers of involved central vs lateral incisors,
and unilateral vs bilateral cases, were recorded.
The associations between SIRR and the following
variables were evaluated: (1) age; (2) sex; (3) buccolingual location: palatally, buccally, or in the line of the
arch; (4) mesiodistal location: sector7 (Fig 4, A); (5)
angulation to the midline14,15 (Fig 4, B); (6) overlap of
the adjacent incisor14,15 (Fig 4, C); (7) vertical crown
height relative to the adjacent incisor root: apical, middle, or coronal16 (Fig 4, D); (8) maximum width of the

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logistic regression analyses with SAS software (version


9.4; SAS Institute, Cary, NC) to calculate odds ratios
and 95% condence intervals. A multivariate regression
model including 9 categorical variables was performed
to identify the signicant factors associated with SIRR.
Only 1 side was included in the bilateral cases on the
advice of the statistician. The inclusion of each side as
a separate case was discounted because the 2 sides are
not independent variables. The side was chosen at
random by the statistician, so that both affected sides
had an equal probability to be included in the analysis.
All statistical tests were 2 sided at a 5 0.05.
RESULTS

Fig 2. CBCT views showing various conguration patterns of SIRR associated with maxillary canine impaction:
A, oblique; B, horizontal. Red arrows indicate the resorption area.

Fig 3. Severely resorbed maxillary left lateral incisor


associated with canine impaction.

canine dental follicle graded in 1-mm intervals (0-1 mm,


grade 1; 1-2 mm, grade 2; 2-3 mm, grade 3; $3 mm,
grade 4); and (9) anomalies of the lateral incisors adjacent to the impacted canines (congenitally missing,
small, or peg-shaped).5
Statistical analysis

The statistical methods for the associations between


each variable and SIRR included chi-square tests and

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In the total study group of 55 patients, there were 96


severely resorbed maxillary incisors69 lateral and 27
central (ratio 2.5:1)a difference that was highly statistically signicant (P 5 0.001; Table I). The most
frequently resorbed tooth associated with maxillary
canine impaction was the maxillary right lateral incisor
(41.6%).
The study group included 22 patients (20 girls, 2
boys) with bilateral impacted canines, and the control
group included 15 bilateral subjects (12 female, 3
male). In the study group among the bilateral impacted
canine patients, 3 (13.6%) had unilateral SIRR.
The control group was older than the study group
(14.2 6 4.7 vs 12.0 6 1.4 years) because of the presence
of 3 adults (.20 years old).
A markedly elevated prevalence of SIRR was associated with maxillary canine impaction in female subjects
(83.6% in the study group vs 54.4% in the control group)
compared with male subjects (16.4% in the study group
vs 45.6% in the control group; P \0.001; Fig 5). When
studied in isolation, the risk of female patients having
SIRR was 4.2 times higher than in males.
In both groups, the prevalence of palatally impacted
canines was higher than that of buccally impacted canines by a ratio just under 2:1 (Fig 6). No statistically signicant differences were seen between the study and
control groups.
In the study group, most canines (64.9%) were
located close to the midline, mainly in sector 5 (35%)
and sector 4 (29.9%) (Fig 7). In the control group, only
a small percentage of the canines were seen in sector 5
(13.9%), with larger percentages in sectors 3 (33.3%)
and 2 (20.8%). The differences between the distributions
of canines were almost statistically signicant
(P 5 0.06). When studied separately, the risk of SIRR
in association with canines positioned in sector 5 was
5.5 and 3.5 times higher than for canines positioned in
sectors 2 and 3, respectively.

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Fig 4. Schematic illustration of the projection of the canine in the panoramic image: A, canine position
in sectors 1 through 5 (the most mesial contour of the crown is taken)7; B, canine angulation to the
midline14,15 (grade 1, 0 -15 ; grade 2, 16 -30 ; grade 3, $31 ); C, canine overlap of the adjacent
incisor root14,15 (grade 1, no horizontal overlap; grade 2, less than half of the root width; grade 3,
more than half, but less than the whole root width; grade 4, complete overlap of root width or more);
D, vertical canine crown height16 (apical, middle, coronal).

Table I. Distribution of SIRR according to the maxil-

lary incisors (N 5 55 patients)


Resorbed maxillary incisor
Right
Right
Left
Left
lateral
central central lateral
Total
No. of teeth (%) 40 (41.6) 18 (18.8) 9 (9.4) 29 (30.2) 96 (100)

In the study group, 68.8% of the impacted canines


were angulated $31 (grade 3), 20.8% of the canines
were between 16 and 30 (grade 2), and 10.4% of the
canines were between 0 and 15 (grade 1) (Fig 8). In
contrast, in the control group, only 40.3% of the canines
were grade 3, 36.1% were grade 2, and 23.6% were
grade 1. The increased prevalence of severely angulated
maxillary canines (grade 3) in association with SIRR was
statistically signicant in comparison with the controls
(P 5 0.02). When this factor was studied in isolation,
the risk of SIRR associated with a canine in sector 3
was about 3 times more than the risk for SIRR in canines
in sectors 1 and 2.

The overlap of the adjacent incisor root was more toward the more extreme end of the grading in the SIRR
group, with 64.9% of impacted maxillary canines exhibiting complete overlap of the adjacent root or beyond
(grade 4) compared with 26.4% in the control group
(Fig 9). Only 14.3% of the canines showed no or less
than half root horizontal overlap (grade 1) in the study
group, compared with 45.8% in the control group, and
the differences were highly statistically signicant
(P 5 0.001). When studied separately, the risks of SIRR
in canines graded 4 were 17.8, 5.8, and 3 times more
than in canines graded 1, 2, and 3, respectively.
In the vertical plane, more than half (62.3%) of the
impacted maxillary canines in the SIRR-affected group
were located in the middle third of the adjacent incisor
root (Fig 10).16 Apically positioned crowns of involved
maxillary canines comprised 15.6%, and coronally positioned crowns, 22.1% of the total. The differences in
the vertical location were highly statistically signicant
(P 5 0.001). The pattern was different in the control
group, with a much higher incidence of coronally positioned crowns (43.1%) and smaller incidences of middle

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Fig 5. Distribution of the SIRR and control groups according to sex.

Fig 6. The buccolingual location of the impacted canines


(palatal, buccal, or in line of the arch) in the SIRR and control groups.
Fig 8. Canine angulation to the midline according to the
study of Stivaros and Mandall.14

Fig 7. Distribution of the impacted canines in sectors, according to the study of Ericson and Kurol.7

(45.8%) and apical canines (11.1%) compared with the


SIRR group (P 5 0.05). When this factor was studied in
isolation, the risk of SIRR was 2.7 times higher for a canine
in the middle third than for a canine positioned coronally.
The dental follicle was graded 4 ($3 mm) in 19.5% of
the canines in the SIRR group (Fig 11). Grade 4 dental
follicles were not observed in any control subject. The
differences were statistically signicant (P 5 0.03).
Grades 3 and 4 dental follicles ($2 mm) were found in
41.6% of the patients in the study group compared
with 8.3% of the subjects in the control group.

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Fig 9. Canine overlap of the adjacent incisor root according to the study of Stivaros and Mandall.14

The patients with congenital absence of the lateral


incisor, but whose central incisor was the affected
tooth, were combined with subjects with anomalous
lateral incisors (Fig 12). In the study group, 20.0% of
the lateral incisors were anomalous (congenitally
missing and peg-shaped), compared with 42.1% in
the control group. Signicantly, 31.6% of the lateral
incisors in the control group were small, whereas no
small lateral incisors with SIRR were found. Because
of the total absence of small lateral incisors, all

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Fig 12. Maxillary lateral incisor anomalies in the SIRR


and control groups.
Fig 10. Distribution of impacted canines in the vertical
plane according to the study of Chaushu et al.16

Table II. Multivariate analysis of effects


Effect
Wald chi-square Probability .chi-square
Age
1.5581
0.2119
Sex
5.0492
0.0246*
Vertical position
0.5261
0.7687
Sector
2.1351
0.7109
Horizontal overlap
2.5120
0.2848
Buccolingual position
1.2401
0.2654
Angulation
2.3445
0.3097
Dental follicle size
10.0736
0.0065*
Anomalous lateral
5.5319
0.0187*
incisors
*Signicant association with SIRR.

DISCUSSION
Fig 11. Dental follicle size in the SIRR and control
groups.

anomalous lateral incisors were grouped together for


the statistical analysis. The risk of SIRR for a normal
lateral incisor was 5.8 times greater than for an anomalous lateral incisor.
The multivariate analysis considered all 9 parameters
together (Table II). The buccolingual position variable
took into account only buccal and palatal canines
because of the small number of in line of the arch canines. Similarly, the anomalous lateral incisors were
grouped together compared with the normal lateral incisors because of the lack of small incisors in the SIRR
group.
The analysis showed that only 3 factors signicantly
discriminated between the groups: sex, dental follicle
size, and anomalous lateral incisors. More specically,
female subjects had a 4.2 times higher risk for SIRR
than did males; dental follicles wider than 2 mm
increased the risk by 8.3 compared with normal dental
follicles; and lateral incisors of normal shape and size
increased the risk for SIRR by 5.8 compared with anomalous lateral incisors.

The etiologic factors underlying root resorption


caused by the neighboring erupting tooth are still unknown. Some authors suggested that the erupting tooth
exerts physical pressure.17-20 Others postulated that the
pressure is caused by the dental follicle and not by the
tooth per se.17 The fact that maxillary lateral incisors
are more affected by SIRR than central incisors, reported
in this study and also in previous studies, partially supports these theories, which are based on the closer intimacy of the canine to the lateral incisor than to the
central incisor.2,20-22
But why the roots resorb in one patient and are intact
in another patient, in whom the canine is identically
situated, remains an enigma.
Our study points toward a multifactorial etiology
including both general systemic factors (sex) and local
factors (aberrant position of the canine, follicle size,
anomalous incisors).
Incisor root resorption associated with impacted
maxillary canines has been reported to occur more in female patients, but the number of affected persons in
that study was inadequate to draw valid conclusions.1
Lai et al20 noted that female subjects seem to be more
affected than males, but their results did not reach statistical signicance. Other authors found no differences

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with regard to sex.18,21,22 However, none of these


investigations restricted their samples to severe cases,
which comprised only 11,21 20,20 24,22 and 4118 teeth
within larger samples. Thus, severe resorption was
largely unrepresented, in contrast to our study (96
teeth). Furthermore, their denition of severe or
resorption through the pulp included subjects whose
resorption was limited to the root apex. If the inclusion
criteria of our study had been applied, their samples
would have been further reduced. It is imperative to
note that canine-related resorption of incisor roots
does not generally shorten the roots in a horizontal
manner but, rather, causes oblique resorption, which is
usually found on the palatal or the labial aspect, depending on the location of the impacted canine.
To the best of our knowledge, this study includes the
largest sample of patients with severe root resorption
linked to impacted canines in the literature. The results
show a denite predilection for SIRR in female subjects
(5:1 ratio, female to male) compared with the control
group (almost a 1:1 ratio). These results regarding the
distribution of the sexes in the control group support
previous ndings from a random population of the
same ethnicity living in the same general area.23 However, in other previous studies, impacted canines were
more frequently found in female subjects than in males;
therefore, it may be claimed that the apparent predilection of root resorption in females merely reects this
imbalance. In studies of orthodontic patient samples,
the ratios of impacted canines in females to males
were 2.3:1 in an American sample,24 2.5:1 in an Israeli
sample,5 and 3:1 in each of Welsh,25 American,26 and
Italian orthodontic samples.27
Thus, the nding reported here of a 5:1 female-tomale ratio of SIRR indicates an obvious afnity for the
condition among female patients, over and above their
apparent naturally occurring predilection for canine
impaction. Although the reasons for this are unknown,
it must be assumed that genetic or hormonal etiologic
factors, as well as girls' earlier skeletal growth spurt,
earlier eruption of canines, and in general earlier dental
development; jaw discrepancies; and root and crown
sexual dimorphism might play signicant roles.
Patients with bilateral maxillary canine impaction
were seen here in considerable numbers (40% in the
study group, 26% in the control group); this has been reported elsewhere.28 However, the fact that 19 of 22
(86.4%) patients exhibited bilateral canine-related
SIRR was surprising. This bilateral pattern further supports a more general, systemic etiology, in addition to
local factors for SIRR.
The control group of consecutive patients was older
than the SIRR group. SIRR will typically be diagnosed

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and treatment initiated at an earlier age than for a patient with routine canine impaction. Furthermore, a signicant proportion of the affected teeth may not survive
into adulthood without treatment.
Local factors can be divided into those related to the
canine (position and size of the dental follicle) and those
related to the size and shape of the affected lateral
incisor.
In this study, a majority of the examined SIRRaffected incisors were associated with palatal impaction;
this was almost double the number with buccal impaction (Fig 6). However, this is similar to the palatal-tobuccal impaction ratio, as can be seen in the control
group and as reported in the literature.27,29-31 Lai
et al20 also found no difference in the prevalence of
root resorption between labial and palatal canines.
In contrast, SIRR was associated with severely horizontally displaced impacted canines that were closer to
the midline and severely mesially angulated canines,
overlapping the lateral incisors. This conrms results published previously.1,7,32 In the vertical plane, the most riskprone canines were those superimposed on the middle
third of the adjacent maxillary incisor root. The fact
that the middle third of the maxillary incisor root is
most commonly resorbed in association with maxillary
canine impaction has already been reported.2,20,32-34 In
their earlier study, using plain lm radiography, Ericson
and Kurol33 found that 82% of the lateral incisors were
resorbed in the middle third and only 13% apically, with
the remainder cervically resorbed. More recent studies
with computerized tomography have conrmed that
maxillary incisor resorption occurs most commonly in
the middle third of the roots.2,20
Our results support the view that pressure from an
enlarged dental follicle may increase the risk for root
resorption. This nding is in contrast to other studies,
which claimed that the existing contact relationship of
the impacted maxillary canine with the lateral incisor
root is critical.19,22 However, our study included only
the most severe cases of root resorption, and this could
be the reason for the apparent conict.
In this sample, SIRR was not seen in any of the
small lateral incisors. This study is consistent with previous studies,5,11 in which anomalous lateral incisors
have been reported to be less likely to develop severe
root resorption, compared with normally shaped and
sized lateral incisors.11,35 One may be permitted to
speculate that in patients with impacted canines, the
normally sized and early developing lateral incisor
root obstructs the deviated eruption path of the
canine and consequently stands a greater chance of
being damaged by resorption.11 Conversely, shorter36
or late developing5 roots of anomalous incisors are

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more easily bypassed and not endangered by the


impacted canines. This nding conrms the results
of a recent study, in which small lateral incisors were
found to be less likely to develop orthodontically
related root resorption.36
When all of these factors were examined together in
the multivariate analysis model, only 1 general factor
(sex) and 2 local factors (enlarged dental follicle and normally sized and shaped lateral incisor) were found to
signicantly increase the risk of SIRR. However, this
might be related to sample size and the number of variables. Future research on larger canine-related SIRR
samples might show that the other factors, which were
signicantly associated when each was studied in isolation, also reach signicance in a multivariate model that
combines them all.
CONCLUSIONS

3
4

The etiology of impacted canine-associated SIRR is


multifactorial, including both systemic and local
factors.
The risk for SIRR is increased in female patients with
enlarged dental follicles and anomalous lateral
incisors.
Lateral incisors are affected more than central incisors, and the chance of bilateral occurrence is high.
SIRR is found in both palatally and buccally
impacted maxillary canines but is associated with
the more severely displaced canines, situated in the
middle third of the adjacent incisor roots.

Screening for SIRR is recommended for all patients


with impacted canines, but especially for female patients
with impacted maxillary canines surrounded by enlarged
follicles and with normally sized and shaped lateral incisors. When one incisor is diagnosed with SIRR in a bilateral impaction, the contralateral incisor should also be
carefully screened. Severely mesially angulated canines
positioned over the middle third of the adjacent incisor
root should also be treated with suspicion.
This information is of major importance for early
diagnosis by the orthodontist, but also for pediatric or
general dentists who are frequently the rst practitioners
to meet the patients, and for surgeons so that they can
plan the most appropriate interdisciplinary treatment.
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