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DENTOALVEOLAR SURGERY

What Are the Risk Factors for External


Root Resorption of Second Molars
Associated With Impacted Third
Molars? A Cone-Beam Computed
Tomography Study
Melek Tassoker, DDS, PhD
Purpose: In relation to an impacted third molar, which is the most frequently impacted tooth, external
root resorption (ERR) or dental caries can be seen on the distal surface of the adjacent second molar. The
purpose of this study was to investigate the risk factors for ERR in second molars associated with impacted
third molars using cone-beam computed tomography (CBCT).
Materials and Methods: In this cross-sectional study, the presence of ERR on the adjacent second molar
was investigated retrospectively on sagittal and axial CBCT slices of patients who underwent CBCT exam-
ination for diagnostic reasons (surgical removal of third molars, orthodontic assessments, and so on) be-
tween 2013 and 2017 at the Necmettin Erbakan University Faculty of Dentistry, Konya, Turkey. The
primary outcome variable was ERR (yes or no). Predictor variables included demographic (age and gender)
and radiographic (impacted tooth angulation and tooth type) parameters. Given that there are multiple
observations per patient (1 to 4 impacted teeth), 1 third molar per patient was selected at random for study
inclusion. Statistical analysis was performed using descriptive statistics, the Mann-Whitney U test, and the
Pearson c2 test. Logistic regression analysis was used to determine the risk factors for ERR in second molars.
The Cohen k test was used to test intraobserver agreement. The significance level was set at P < .05.
Results: Two hundred patients were analyzed, and of the 200 impacted third molars evaluated, 42 (21%)
showed ERR. The severity of resorption increased with aging (P < .05). Logistic regression analysis indi-
cated that tooth type and inclination of the third molars could predict the occurrence of ERR associated
with an impacted third molar (P < .05).
Conclusions: Mesioangular and horizontal inclinations and impacted mandibular third molars posed a
greater risk of ERR lesions in adjacent second molars than other inclinations (distoangular and vertical)
and maxillary third molars.
Ó 2018 American Association of Oral and Maxillofacial Surgeons
J Oral Maxillofac Surg 77:11-17, 2019

Third molars are the most frequently impacted teeth. If the adjacent second molar should be considered when
they are not impacted, they generally erupt between 17 making such a decision.5,6 In relation to an impacted
and 21 years of age.1 Removing or extracting a third molar, external root resorption (ERR) or dental
third molar has been discussed for many years, but caries can be seen on the distal surface of the
prophylactically removing an asymptomatic third molar adjacent second molar.7-9 This type of resorption
might not be an easy decision.2-4 The harmful effect on emerges owing to the pressure from the impacted

Assistant Professor, Department of Oral and Maxillofacial Necmettin Erbakan University, 42050 Konya, Turkey; e-mail:
Radiology, Faculty of Dentistry, Necmettin Erbakan University, dishekmelek@gmail.com
Konya, Turkey. Received March 19 2018
Conflict of Interest Disclosures: None of the authors have any Accepted August 19 2018
relevant financial relationship(s) with a commercial interest. Ó 2018 American Association of Oral and Maxillofacial Surgeons
Address correspondence and reprint requests to Dr Tassoker: 0278-2391/18/30988-1
Department of Oral and Maxillofacial Radiology, Faculty of Dentistry, https://doi.org/10.1016/j.joms.2018.08.023

11
12 EXTERNAL ROOT RESORPTION OF MOLARS

tooth.8,9 This pressure causes inflammation and triggers sons (surgical removal of third molars, orthodontic as-
the resorption via clastic cells.10 sessments, and so on) presenting with at least 1
Two-dimensional radiographic studies conducted impacted third molar to the Department of Oral and
with panoramic and periapical radiographs have re- Maxillofacial Radiology, Faculty of Dentistry, Necmet-
ported a low prevalence of ERR in second molars tin Erbakan University, between 2013 and 2017.
(0.3-7%).8,9 Because of image distortion related to The inclusion criteria were as follows: patients
their projective geometry, their diagnostic value is aged 18 years or older, eruption of all teeth except
quite low.11 On the other hand, cone-beam computed the third molar(s), and at least 1 impacted third
tomography (CBCT) provides 4.3 times greater detec- molar. The exclusion criteria were as follows:
tion of ERR than panoramic radiographs.4 This system completely erupted third molars with cystic or tu-
is free of overlapping and provides 3-dimensional (3D) mor lesions associated with impacted teeth; third
multiplanar imaging with a low radiation dose and molars with evidence of root development that is
high spatial resolution.11 Using conventional less than two thirds; second molars with severe
computed tomography scanning instead of CBCT for carious lesions, crowns, or distal restorations; or
routine analysis of impacted teeth is not justifiable demonstration of any artifacts.
given the higher radiation exposure.4
The position of the impacted tooth predisposes the
adjacent tooth to ERR or dental caries.12 In the litera- STUDY VARIABLES
ture, horizontal and mesioangular impactions were
The primary outcome variable was ERR (yes or no).
found to be related to a higher frequency of ERR in
Predictor variables included demographic (age and
second molars because of larger contact surfaces or
gender) and radiographic (impacted tooth angulation
the presence of a gap.4,9
and tooth type) parameters.
It is difficult to diagnose ERR until periapical inflam-
mation or pulpitis occurs.4,8,11 Its progress is generally
asymptomatic.11 In a recent study, the impaction rate
of third molars was found to be 54.1% in the Turkish DATA COLLECTION METHODS
population.13 Considering such a high prevalence of The patients were divided into 3 age groups (18 to
third molar impaction, it is necessary to identify the 24, 25 to 34, and 35 to 50 years). The presence of
risk factors for ERR and to implement preventive mea- ERR on the adjacent second molar was investigated
sures.11 Very few studies have addressed these issues. on sagittal and axial CBCT slices by the same radiolo-
The purpose of this study was to assess the ERR of gist. The CBCT scans were acquired using a 3D Accui-
second molars associated with impacted third molars tomo 170 machine (Morita, Kyoto, Japan).
using CBCT. We hypothesized that impacted third We used the diagnosis of ERR according to Al-
molars with different inclinations (mesioangular, Khateeb and Bataineh.14 The observation of ‘‘a clear
distoangular, horizontal, or vertical) and different loca- loss of substance in the root of adjacent
tions (mandibular or maxillary) would have an impact second molar teeth due to direct contact between it
on the risk of ERR in adjacent second molars. The spe- and impacted third molar’’ was diagnosed as ERR.
cific aim of this study was to investigate the risk factors Once detected, ERR was categorized according to its
for ERR in second molars associated with impacted location (cervical, middle root third, and apical root
third molars using CBCT. third) (Figs 1-3) and severity (slight, moderate, and
severe) (Figs 4-6).9 According to Ericson et al,15 ERR
involving less than half the dentin thickness was
Materials and Methods
scored as slight; ERR involving at least half the dentin
STUDY DESIGN was scored as moderate; and ERR involving the pulp
To address the research purpose, we designed and cavity was scored as severe.
implemented a cross-sectional study. The study was The differential diagnosis between dental caries and
performed with the approval of the Necmettin Erba- ERR was based on radiologic appearance. If there
kan University Faculty of Dentistry Research Ethics was a clear gap between the second molar and the
Committee (decision No. 2017/12). Furthermore, the dental crown of the third molar and radiolucency
analysis was performed according to the stipulations showed irregular morphology, the diagnosis was
laid out by the Declaration of Helsinki. dental caries.11
The inclination of the third molars was determined
using the classification of Winter16 (vertical, horizon-
STUDY SAMPLE tal, mesioangular, or distoangular). Two weeks later,
The study population was composed of all patients examinations were repeated, and these showed good
who underwent CBCT examination for diagnostic rea- intraexaminer agreement.
MELEK TASSOKER 13

FIGURE 1. Sagittal cone-beam computed tomography section FIGURE 3. Sagittal cone-beam computed tomography section
showing external root resorption (arrow) in cervical region. showing external root resorption (arrow) in apical root third region.
Melek Tassoker. External Root Resorption of Molars. J Oral Maxil- Melek Tassoker. External Root Resorption of Molars. J Oral Maxil-
lofac Surg 2019. lofac Surg 2019.

DATA ANALYSIS and standard deviation values were calculated. Data


Given that there are multiple observations per were tested for normality using the Shapiro-Wilk
patient (1 to 4 impacted teeth), one third molar per test. Normality was violated, and differences in mean
patient was selected at random for study inclusion, age between the 2 genders were analyzed by the
and analysis of 200 patients (200 teeth) was per- Mann-Whitney U test. The Pearson c2 test was used
formed. All statistical analysis was performed using for categorical variables. In addition, logistic regres-
SPSS software (version 21; IBM, Armonk, NY). Mean sion analysis was used to determine the risk factors
for ERR in second molars. Intraexaminer reliability
was tested with the Cohen k test. The k coefficient
was interpreted as being poor (0), slight (0.01 to
0.20), fair (0.21 to 0.40), moderate (0.41 to 0.60), sub-
stantial (0.61 to 0.80), or almost perfect (0.81 to 1.0)
according to Landis and Koch.17 Statistical significance
was assumed for P < .05.

FIGURE 2. Sagittal cone-beam computed tomography section FIGURE 4. Slight external root resorption lesion on axial cone-
showing external root resorption (arrow) in middle root third region. beam computed tomography slice.
Melek Tassoker. External Root Resorption of Molars. J Oral Maxil- Melek Tassoker. External Root Resorption of Molars. J Oral Maxil-
lofac Surg 2019. lofac Surg 2019.
14 EXTERNAL ROOT RESORPTION OF MOLARS

results of the initial examination were tabulated. The


overall frequency of ERR was 21% (42 teeth).
The severity of resorption increased with aging
(P < .05). Most slight ERR lesions were found in the
group aged 18 to 24 years. Severe ERR lesions were
only seen in the groups aged 25 to 34 years and 35
to 50 years (Table 1). Logistic regression analysis indi-
cated that age and gender could not predict the occur-
rence of ERR associated with an impacted third molar
(P > .05) (Table 1). There was no statistically signifi-
cant relationship between gender and the presence
and severity of ERR (P > .05). Of the 42 ERR lesions,
24 were seen in female patients and 18 in
male patients.
Logistic regression analysis indicated that tooth type
could predict the occurrence of ERR associated with
FIGURE 5. Moderate external root resorption lesion on sagittal an impacted third molar (P < .05) (Table 1). ERR was
cone-beam computed tomography slice. more prevalent in mandibular second molars than
Melek Tassoker. External Root Resorption of Molars. J Oral Maxil- maxillary second molars, and the risk of ERR was
lofac Surg 2019. about 4 times greater in mandibular molars than in
maxillary molars (P < .05). The distribution of ERR
Results regarding tooth type is presented in Table 1.
We evaluated 200 impacted third molars in 200 pa- There was a statistically significant relationship be-
tients. Of the 200 patients, with a mean age of tween the impaction position of third molars and the
27.26  8.60 years (age range, 18 to 50 years), 118 presence of ERR (P < .05). ERR was seen in an
were women and 82 were men. The mean age of extremely low number of cases of distoangular and
male patients (29.11  9.27 years) was higher than vertical molars. The mesioangular and horizontal posi-
that of female patients (25.97  7.90 years) (P = .018). tions of third molars were found to be more at risk of
The k test showed excellent intraobserver values for ERR (Table 1). As indicated in Table 1, the distoangular
the repeated ERR observations (k = 0.96, P < .05). The and vertical inclinations of impacted third molars pre-
sented less risk of ERR on second molars (P < .05).
The cross tabulation of severity and localization of
ERR is shown in Table 2. The cervical region in
mandibular second molars and the middle third region
in maxillary second molars were most affected by ERR.

Discussion
This study aimed to investigate the risk factors for
ERR in second molars associated with impacted third
molars. The impacted teeth may be related to some
pathologic conditions, such as pericoronitis, dental
caries, bone loss, odontogenic cysts or tumors,
swelling, cheek ulcerations, or ERR of adjacent teeth.4
ERR is not rare and may penetrate into the pulp, which
can lead to inflammation.8,11,18 The extraction of
impacted third molars removes the mechanical stress
from second molars, and the inflammatory process
ends. In cases of bacterial invasion into the pulp,
endodontic treatment is required.19 Our study indi-
cated that mesioangular and horizontal inclinations
FIGURE 6. Severe external root resorption lesion on axial cone-
of impacted third molars were more at risk of being
beam computed tomography slice. associated with ERR than other impaction positions.
Melek Tassoker. External Root Resorption of Molars. J Oral Maxil- This finding reinforces the theory of previous
lofac Surg 2019. studies.4,5,11,20-24 One of our patients who had ERR
MELEK TASSOKER 15

Table 1. RESULTS OF REGRESSION ANALYSIS OF ALL STUDIED VARIABLES (200 PATIENTS, 200 TEETH)

ERR Severity, n

Variable No. of Patients OR (95% CI) P Value ERR Presence, n Slight Moderate Severe

Age
18-24 yr 100 1 (reference) 17 16 1 0
25-34 yr 57 1.70 (0.83-3.47) .143 15 10 2 3
35-50 yr 43 1.44 (0.65-3.22) .366 10 4 1 5
Gender
Male 82 1 (reference) 18 11 1 6
Female 118 0.92 (0.52-1.65) .902 24 19 3 2
Tooth type
Upper right second molar 40 1 (reference) 3 2 0 1
Upper left second molar 38 0.78 (0.26-2.36) .670 2 1 0 1
Lower left second molar 62 4.35 (1.93-9.80) <.001* 19 15 1 3
Lower right second molar 60 4.09 (1.80-9.28) .001* 18 12 3 3
Angulation of third molar
Mesioangular 124 1 (reference) 27 20 3 4
Distoangular 20 0.17 (0.03-0.78) .023y 2 1 0 1
Horizontal 35 1.65 (0.78-3.49) .190 12 8 1 3
Vertical 21 0.03 (0.01-0.71) .023y 1 1 0 0
Total 200 42 30 4 8
Abbreviations: CI, confidential interval; ERR, external root resorption; OR, odds ratio.
* The significance level is P < .01.
y The significance level is P < .05.
Melek Tassoker. External Root Resorption of Molars. J Oral Maxillofac Surg 2019.

on a maxillary second molar is described in Figures 7 uated only completely unerupted third molars, re-
and 8 before and after tooth removal. ported that the apical third region of the adjacent
Examination of ERR on the root surface, especially second molar was most affected by ERR. The ERR le-
in the early stages, requires 3D imaging. In a recent sions most commonly detected in the cervical region
study, CBCT and panoramic radiography were of the second molars were associated with partially
compared and the 2 methods corresponded in only erupted third molars because of their susceptibility
4.3% of cases.4 The overall prevalence of ERR was to inflammation.9,10
21% in our study, which was higher than that in previ- Our study showed that the risk of ERR was about 4
ous reports by Nitzan et al10 and Enabulele and Ob- times greater in mandibular molars than in maxillary
uekwe,21 both of whom used periapical radiographs molars and a greater number of ERR lesions (37 teeth)
to find ERR prevalence rates of 8% and 4.7%, respec- were found in the mandible than in the maxilla (5
tively. These 2-dimensional methods can cause misin- teeth). This result was in accordance with other
terpretation of the images because of overlapping studies conducted using panoramic radiographs,18
and distortion.11 Al-Khateeb and Bataineh14 found periapical radiographs,10 and CBCT scans.4 This can
that ERR lesions on second molars were present in be explained by the complex eruption process of
only 0.3% of cases when using panoramic radiography. mandibular third molars.
Oenning et al4 reported that the prevalence of ERR One limitation of this study was the correct distinc-
was 22.88% when using CBCT images, and this was tion of ERR lesions from dental caries, as other
corroborated by the findings of our study. It should researchers previously reported.4 The presence of a
be noted that the bias of sample selection (unerupted gap between the second and third molars that leads
or partially erupted third molars)5 or a different defini- to food retention may actually suggest dental caries,
tion of ERR14 could yield different results. especially in cases of partially erupted third mo-
The findings of this study, which evaluated both lars.4,7,25 Enabulele and Obuekwe21 indicated that
partially erupted and unerupted third molars, showed second molars with cervical resorption had direct
that the cervical region in mandibular second molars tooth-to-tooth contact with the impacted third molar
and the cervical and middle third regions in maxillary whereas most second molars with distal caries did
second molars were most affected by ERR. In contrast not have tooth-to-tooth contact. Another limitation
to the results of this study, Nemcovsky et al,5 who eval- of our study was using only radiologic diagnosis for
16 EXTERNAL ROOT RESORPTION OF MOLARS

Table 2. CROSS TABULATION OF SEVERITY AND


LOCALIZATION OF 42 TEETH WITH ERR

Severity of Cervical, Middle Root Apical Root


ERR n Third, n Third, n

Upper right second molar


Slight 1 1 0
Moderate 0 0 0
Severe 0 1 0
Maxilla 1 2 0
total
Upper left second molar
Slight 1 0 0
Moderate 0 0 0
Severe 0 0 1
Maxilla 1 0 1
total
Lower left second molar
Slight 10 5 0
Moderate 1 0 0
Severe 2 1 0 FIGURE 7. Cone-beam computed tomography examination of
Mandible 13 6 0 external root resorption in apical root third of second molar before
total extraction.
Lower right second molar Melek Tassoker. External Root Resorption of Molars. J Oral Maxil-
Slight 9 3 0 lofac Surg 2019.
Moderate 2 1 0
Severe 2 0 1
Mandible 13 4 1
total
Abbreviation: ERR, external root resorption.
Melek Tassoker. External Root Resorption of Molars. J Oral Maxil-
lofac Surg 2019.

ERR and not correlating radiology with clinical find-


ings. To provide better scientific evidence for this
study, direct visualization of ERR after tooth extraction
and histopathologic analysis could be useful.
Age was not found to be a risk factor for ERR in our
research. This was inconsistent with the findings of
Wang et al,11 who reported that being over the age
of 35 years was an independent risk factor for ERR. A
cross-sectional study cannot provide full insight into
age as a risk factor, as older individuals may have had
their third molar teeth with ERR extracted earlier
in life.26
Some controversial studies have suggested that men
are more susceptible to the development of ERR than
women, which researchers explained as a difference
in sex hormones.8,10 However, gender was not found
to be a predictive parameter for ERR in our study.
This study showed that there was a tendency to-
ward moderate and severe resorption in older patients
whereas slight ERR lesions tended to be seen in FIGURE 8. Second molar resorption in same patient shown in
younger individuals. This finding is not unexpected Figure 7 after removal of teeth.
because root resorption progresses over time.11,27,28 Melek Tassoker. External Root Resorption of Molars. J Oral Maxil-
The eruptive tooth movement continues, and lofac Surg 2019.
MELEK TASSOKER 17

mechanical pressure on second molars stimulates the 11. Wang D, He X, Wang Y, et al: External root resorption of the sec-
ond molar associated with mesially and horizontally impacted
progression of ERR formation.11
mandibular third molar: Evidence from cone beam computed to-
Within the limitations of this study, age and gender mography. Clin Oral Invest 21:1335, 2017
were not found to be independent risk factors for 12. Akarslan ZZ, Kocabay C: Assessment of the associated symp-
toms, pathologies, positions and angulations of bilateral occur-
ERR in second molars. Mesioangular and horizontal ring mandibular third molars: Is there any similarity? Oral Surg
inclinations and impacted mandibular third molars Oral Med Oral Pathol Oral Radiol Endod 108:e26, 2009
posed a greater risk of ERR lesions in adjacent 13. Topkara A, Sari Z: Investigation of third molar impaction in
Turkish orthodontic patients: Prevalence, depth and angular
second molars than other inclinations (distoangular positions. Eur J Dent 7:94, 2013
and vertical) and maxillary third molars. Whether 14. Al-Khateeb TH, Bataineh AB: Pathology associated with
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