Association Between Root Resorption and Tooth Development: A Quantitative Clinical Study

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ORIGINAL ARTICLE

Association between root resorption and


tooth development: A quantitative
clinical study
Xinyi Li, Jingchen Xu, Yuanyuan Yin, Ting Liu, Le Chang, Zhaomeng Tang, and Song Chen
Chengdu, Sichuan, China

Introduction: The aim of this study was to verify less resorption of incompletely developed roots compared with
those that were fully developed during the same orthodontic treatment and to test the value of the amount of
external apical root resorption for predicting tooth development. Methods: A sample of 524 patients aged
10-15 years was selected following the inclusion criteria. For each subject, pretreatment and posttreatment dig-
ital panoramic and lateral radiographs were collected, and tooth development was determined from each radio-
graph. Through calculations, the amount of root resorption was assessed by a created and scientific approach
for large-scale application using radiographs with only 8 measurement indexes for each patient. Other basic
information and treatment parameters regarded as possible risk factors were also collected from
standardized recordings or radiographs. The root length between the groups or in the single group were
compared with t tests and correlation analyses. Linear univariate and multivariate regression analyses were
used to test identify predictors for root resorption and to develop a prediction model. Results: There was a sta-
tistically significant difference in the amount of root resorption with tooth development before correction
(P \0.001) as well as after correction (P 5 0.002). There was a statistically significant correlation (P \0.001)
but no difference between pretreatment and posttreatment root length in the immature tooth group because
of less root resorption. In the multivariate analyses, tooth development (P\0.001), treatment duration, apex hor-
izontal movements, apex vertical movements, and previous orthodontic treatment were included in the final
model as risk factors, and tooth development had the highest beta value. Conclusions: There is an association
between root resorption and tooth development, and tooth development is an important predictor of
root resorption. Patients with immature teeth are at a much lower risk of apical root resorption. (Am J Orthod
Dentofacial Orthop 2020;157:602-10)

E
xternal apical root resorption (EARR) is an inevi- affected in most cases of mild EARR, orthodontic treat-
table side effect of orthodontic treatment.1,2 ment should be suspended in some cases of severe EARR,
Whereas external root resorption occurs from all and it is important for the practitioner to identify the
directions, EARR of teeth shows only apical resorption, dominant factors for the development of EARR to be
which is characterized by root shortening.3 EARR is esti- able to adjust treatment to manage this adverse effect.
mated to occur in 80%-90% of orthodontic patients.4,5 According to our previous study,6 EARR was a multifac-
Although tooth survival and normal function are not torial problem, and several potential genetic and clinical
risk factors were reported. The common consensus is
that the type and the amount of orthodontic force7-14
From the State Key Laboratory of Oral Diseases, National Clinical Research Center
for Oral Diseases, Department of Orthodontics, West China Hospital of Stomatol- were considered as the main causes of EARR in
ogy, Sichuan University, Chengdu, Sichuan, China. treatment factors.15,16 As for patient characteristics, ge-
All authors have completed and submitted the ICMJE Form for Disclosure of Po- notype,17-19 sex, nutrition, amount of apical
tential Conflicts of Interest, and none were reported.
This study was supported by funds from the National Natural Science Founda- displacement,20-22 and malocclusion type21,23 can also
tion of China (number 81671021). initiate and induce root resorption.
Address correspondence to: Song Chen, Department of Orthodontics, West China Previous studies also found that increased ages coin-
Hospital of Stomatology, Sichuan University, Section 3, No. 14, Renmin South
Road, Chengdu, Sichuan, 610041 China; e-mail, songchen882002@hotmail. cided with more root resorption20,23-25 indicating older
com. people are more vulnerable.26 However, physiological
Submitted, August 2019; revised and accepted, November 2019. age, which many studies used, was unable to accurately
0889-5406/$36.00
Ó 2019 by the American Association of Orthodontists. All rights reserved. reflect root development, which was more likely to asso-
https://doi.org/10.1016/j.ajodo.2019.11.011 ciate with root resorption. Thus, considering whether the
602
Li et al 603

tooth was fully developed as inclusion and exclusion Radiographs of insufficient quality, films not displaying
criteria can be simple for observers to increase repeat- the entire root, impacted teeth, and incomplete orthodon-
ability and reproducibility. The stages of dental maturity tic records were excluded.
can be assessed by methods such as Demirjian's and The tooth development of each radiograph was
Haavikko's.27,28 In addition, open or closed apical determined by 2 observers independently according to
foramina may play a vital role in root resorption. It has Moorrees and Kent,35 and Moorrees et al.36 The ob-
been suggested that there is a contact between the servers were blinded to sample information, and they
root and the alveolar bone causing EARR and a relation- repeated the procedures twice in a 3-week interval.
ship between EARR and pulp,23,29 and the apical The within-observer repeatability and reproducibility
foramina connect the pulp and alveolar bone. Because of the 2 observers were evaluated using intraclass corre-
the pulp vessels are the branches of alveolar bone vessels, lation coefficients (ICCs).37 Then the included cases were
orthodontic forces can stretch or damage apical vessels, further divided into an immature tooth (IT) group and a
decrease blood flow, and cause pulpal disturbances.30-32 mature tooth (MT) group. Because the maxillary incisors
An unclosed apical foramina, indicating more free space usually showed more EARR than any other teeth in
and adequate blood supply, may help relieve pressure several studies,2,38 all maxillary central incisors of which
and maintain balance. the apexes had not completely formed both before and
To reliably assess the amount of EARR in a patient is after treatment were viewed as IT cases, and those of
the major obstacle in such clinical studies. It had been which the apexes had completely formed both before
widely reported that root length change could be consid- and after treatment were viewed as MT cases (Fig 1).
ered as evidence of EARR, and 2-dimensional images The basic information and treatment parameters of
were mainly used for measuring root shortening, but un- each included patient were collected, including initial
desirable errors may occur when aligning the images age, sex, history of trauma, history of earlier orthodontic
taken at different times.33,34 Thus, both digital pano- treatment or endodontic treatment, extraction decision,
ramic radiographs and lateral radiographs were involved and treatment period, which were possible factors for
in this assessment, and the quantitative measurements root resorption.
that have small changes in the images taken at different Then several lengths and angulations were measured
times were selected. Through calculations, the reduced using the same program on the pretreatment and post-
root length can be obtained and compared before and treatment radiographs for each patient. The reference
after orthodontic treatment. points and lines for measurements are shown in
Therefore, the purpose of this investigation was to Figure 2. Before treatment, the lengths of the crowns
verify the following hypothesis during clinical experi- and roots on the lateral radiographs were C1L0 and
ence: There is an association between root resorption R1L0 , and the lengths of the crowns and roots on the
and tooth development, and patients with immature panoramic radiographs were C1P0 and R1P0 . The magnifi-
teeth will undergo less root resorption. cations of the lateral and panoramic radiographs were VL
and Vp. Respectively, the real lengths of the crowns and
roots on the lateral radiographs were C1L and R1L, and
MATERIAL AND METHODS
the real lengths of the crowns and roots on the pano-
This longitudinal retrospective study was approved by ramic radiographs were C1P and R1P. The minimum scale
the ethical board of West China Hospital of of the rules on the lateral radiographs were d1, and the
Stomatology involving all subjects who accepted ortho- real minimum scale was d (d 5 10 mm). The angulations
dontic treatment from 2015 to 2018. Patients were of the maxillary central incisors on the lateral radio-
selected according to the following inclusion criteria: graphs were q1. Similarly, the lengths and angulations
aged 10-15 years during the entire treatment, both digital on the posttreatment radiographs were C2L0 , R2L0 , C2P0 ,
panoramic and lateral radiographs before and after treat- R2P0 , VL, Vp, C2L, R2L, C2P, R2P, d2, d, and q2. Attention
ment, the Frankfort plane of the radiographs parallel to should be paid to the crown and root lengths that
the floor, good occlusal finishing, and periapical radio- were measured differently compared with those that
graphs. All patients were treated the standard fixed– were calculated by measuring the distance from the
straight wire appliances with 0.022 3 0.028-in slots and maxillary central incisal edge to the midpoint of the
general archwire sequences of 0.016-in nickel-titanium line. In the panoramic radiographs, the highest point
to 0.019 3 0.025-in stainless steel. All radiographs were of cementoenamel junction (CEJ) was determined, and
taken and scanned on the same machine at West China the crown lengths were the distance from the incisal
Hospital of Stomatology with the same setting used. edge to the highest point, whereas the root lengths

American Journal of Orthodontics and Dentofacial Orthopedics May 2020  Vol 157  Issue 5
604 Li et al

Fig 1. Grouping methods of included cases: A, immature tooth group, all maxillary central incisors
apexes had not completely formed both before and after treatment; B, mature tooth group, all maxillary
central incisors apexes had completely formed both before and after treatment.

Fig 2. The reference points and lines for measurements: A, on pretreatment lateral radiographs, the
lengths of crowns and roots were C1L0 and R1L0 , the real lengths of crowns and roots were C1L and
R1L, the minimum scale of the rules were d1 and the real minimum scale was d, the angulations of
the maxillary central incisors were q1, and the magnifications were VL; Similarly, the lengths and angu-
lations on the posttreatment lateral radiographs were C2L0 , R2L0 , VL, C2L, R2L, d2, d, and q2; B, on pre-
treatment panoramic radiographs, the lengths of crowns and roots were C1P0 and R1P0 , the real lengths
of crowns and roots on the panoramic radiographs were C1P and R1P, and the magnifications were Vp;
Similarly, the lengths and angulations on the posttreatment lateral radiographs were C2P0 , R2P0 , Vp, C2P,
R2P; C, the anterior and posterior CEJ points in the lateral radiographs are the highest point of CEJ in
the panoramic radiographs.

were the distance from the highest point to the root where Vp can be presented as
apices.
C1P 0 C1P 0 C1P 0 C1P 0
Through the following calculations, the quantitative VP 5 5 5 0 5 0
C1P C1L 3sin q1 C1L C1L
measurements that had small changes in the images 3sin q1 3sin q1
taken at different times were selected. R1L can be pre- VL d1 =d
sented as
Therefore,
R1P R1P 0 =VP
R1L 5 5 R1P 0 3C1L 0 3d
sin q1 sin q1 R1L 5
C1P 0 3d1

May 2020  Vol 157  Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics
Li et al 605

Similarly, R2L can be presented as added 0.18 mm per year during ages 10-13 years to the
0 0 amount of root resorption as the correction.
R2P 3C2L 3d
R2L 5 Two observers were required to measure all subjects
C2P 0 3d2 of 50 patients selected randomly again in a 3-week in-
Therefore, the root resorption R is terval, and the average errors were determined by intra-
R1P 0 3C1L 0 3d R2P 0 3C2L 0 3d observer and interobserver comparison using ICCs.
R5 
C1P 0 3d1 C2P 0 3d2
Eventually, the quantitative measurements selected Statistical analysis
to assess the amount of EARR were only C1P0 , R1P0 , The basic data were summarized using means, stan-
C1L0 , d1, C2P0 , R2P0 , C2L0 , and d2 for each patient (Fig 3). dard deviations, and frequencies. Normal distribution of
In addition, apical displacement is also a main risk the variables was verified with Kolmogorov-Smirnov
factor for root resorption. According to the study by Mir- tests, and all variables showed a normal distribution.
abella and Artun,39 in lateral radiographs, pretreatment Initial intergroup data were compared using t test and
overjet and the horizontal movement of the incisal chi-square test. Associations of tooth development and
edge during treatment (Dx) and pretreatment overbite EARR between IT and MT groups were analyzed using
and the vertical movement of the incisal edge during independent-samples t tests, and a comparison of pre-
treatment (Dy) were measured; therefore, the horizontal treatment and posttreatment in each single group was
(Dx0 ) and vertical (Dy0 ) movements of the apex could be evaluated using paired-samples t tests and correlation
calculated. The proximity of the central incisor roots to analyses. The statistical significance was P \0.05.
the palatal cortical bone were scored both before and af- Linear regression analyses were used to test identify
ter treatment. predictors for root resorption. After univariate regres-
Without any other similar study, Xu and Baumrind40 sion, stepwise multiple regressions with forward selec-
found that the root growth of patients aged 7-10 years tion were used to develop a prediction model.
was rapid, whereas that of patients aged 10-13 years was Variables with the lowest P value were successively
slow with a total growth of 0.54 mm in 3 years, and the entered into the model if their effects were significant
root length after age 13 years was stable. Therefore, we at P \0.05.

Fig 3. The quantitative measurements selected to assess the amount of EARR: A, C1P0 , R1P0 , C1L0 , and
d1 were measured in the pretreatment lateral and panoramic radiographs of a patient; B, C2P0 , R2P0 ,
C2L0 , and d2 were measured in the posttreatment lateral and panoramic radiographs of the same pa-
tient.

American Journal of Orthodontics and Dentofacial Orthopedics May 2020  Vol 157  Issue 5
606 Li et al

RESULTS
Table II. Measurements of EARR in OA group and CA
The intraobserver repeatability of tooth development group (t test)
was high for both observers (ICC 5 0.998 and 0.999),
Open apex Closed apex
and the reproducibility of the 2 observers was also group, n 5 259 group, n 5 265
high (ICC 5 0.855). The intraobserver and interobserver Variable mean (SD) mean (SD) P value
reproducibility of measurements were all high (all C1P0 (mm) 10.57 (2.01) 10.61 (1.83) 0.802
ICC .0.8). R1P0 (mm) 14.73 (2.90) 14.61 (2.53) 0.619
This study included 259 patients in the IT group and C1L0 (mm) 12.19 (1.08) 12.07 (1.08) 0.185
d1 (mm) 10.80 (0.55) 10.75 (0.52) 0.282
265 patients in the MT group. The average ages, sex, his-
C2P0 (mm) 10.09 (1.74) 10.25 (1.62) 0.274
tory of trauma, history of earlier orthodontic treatment R2P0 (mm) 14.34 (2.72) 13.45 (2.48) \0.001*
or endodontic treatment, extraction decision, the ortho- C2L0 (mm) 11.84 (0.97) 11.69 (1.02) 0.069
dontic treatment duration, and the horizontal and verti- d2 (mm) 10.61 (0.57) 10.53 (0.57) 0.113
cal apex movements of the 2 groups were presented Pretreatment root 16.00 (3.24) 15.62 (2.56) 0.146
length (mm)
below, respectively. Initial intergroup data comparisons
Posttreatment root 16.07 (3.10) 14.71 (2.77) \0.001*
(t and chi-square tests) are shown in Table I. length (mm)
The digital panoramic and lateral radiographs of all Root resorption (mm) 0.07 (3.25) 0.91 (2.73) \0.001*
subjects were used for assessing EARRs. Table II and Root resorption after 0.20 (3.26) 1.01 (2.72) 0.002*
Figure 4 show the amount of EARR in the 2 groups, indi- correction (mm)
cating that the IT group has less root resorption than the OA, open apex; CA, closed apex; SD, standard deviation; C1P0 ,
MT group before correction (P \0.001) as well as after the crown lengths on pretreatment panoramic radiographs; R1P0 ,
the root lengths on pretreatment panoramic radiographs; C1L0 , the
correction (P 5 0.002), which are both statistically sig-
crown lengths on pretreatment lateral radiographs; d1, the rule
nificant. The pretreatment and posttreatment root minimum scale on pretreatment lateral radiographs; C2P0 , the crown
lengths in the single group were also compared in lengths on posttreatment panoramic radiographs; R2P0 , the
Table III. root lengths on posttreatment panoramic radiographs; C2L0 , the
Univariate linear regression showed that extraction crown lengths on posttreatment lateral radiographs; d2, the rule
minimum scale on posttreatment lateral radiographs.
decision (P \0.05), treatment duration (P \0.01), the
*Statistically significant at P \0.05.
horizontal movements of the apex (P \0.05), and tooth
development (P \0.01) were associated with the
Root resorption after correction 5 1.599 1 1.09
amount of root resorption after correction. The multi-
(tooth development) 1 0.06 (duration) 1 0.46 (horizon-
variate analyses detected an association between root
tal movement) 1 0.75 (vertical movement)  5.21 (pre-
resorption and possible factors. Tooth development
vious orthodontic treatment)
(P \0.001), treatment duration (P \0.001), apex hori-
zontal movements (P \0.001), apex vertical movements
DISCUSSION
(P \0.05), and previous orthodontic treatment
(P\0.05) were included in the final model as risk factors In this study, we investigated EARR associated with
(Table IV) with r2 5 0.83. The amount of root resorption tooth development, rather than physiological age. It is
after correction could therefore be predicted with this easier for observers to determine the achievement of
formula: tooth development to increase repeatability and

Table I. Initial intergroup data comparison (t test and chi-square test)


Open apex group, n 5 259 Closed apex group, n 5 265
Variable mean (SD) mean (SD) P value
Initial age (y) 11.47 (0.89) 12.67 (0.99) \0.001*y
Duration (mo) 26.92 (9.03) 25.40 (8.84) 0.052y
Overjet reduction (mm) 1.80 (2.35) 1.25 (1.63) 0.002*y
U1-SN reduction ( ) 4.14 (9.46) 3.10 (7.61) 0.166y
Sex \0.001*z
Male 141 79
Female 118 186

SD, standard deviation.


*Statistically significant at P \0.05; yt test; zchi-square test.

May 2020  Vol 157  Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics
Li et al 607

Fig 4. Comparison of EARR in the IT group and MT group.

reproducibility in large-scale application. The EARR was protrudes to root, and the mesial or distal curve pro-
evaluated using both digital panoramic radiographs and trudes to crown. To match C1L and C1P, C2L, and C2P,
lateral radiographs for low costs and high follow-up rate, R1L and R1P, R2L, and R2P, a common division straight
which is more accurate based on quantitative measure- line of crown and root should be determined on the
ments selected through scientific calculations. For labial and proximal surfaces. Because the anterior and
example, because the apical point on the lateral radio- posterior CEJ points in the lateral radiographs are the
graphs was not clear, the root length on the lateral radio- highest point of CEJ in the panoramic radiographs, the
graphs (R1L0 and R2L0 ) was replaced by other division line can be obtained by connecting the anterior
measurements. The angulations of the maxillary central and posterior points or crossing the highest points, and
incisors on the lateral radiographs (q1 and q2) were the crown or root length can be measured from the line
greatly impacted by the subjective position of the SN to the incisal edges or root apices. Therefore, the crown
plane and had considerable changes measured at and root lengths were measured more accurately, which
different times, therefore they were removed during cal- was different from other studies. Thus, the results are
culations. Eventually, after the calculations, only C1P0 , more accurate and reliable as the high intraobserver
R1P0 , C1L0 , d1, C2P0 , R2P0 , C2L0 , and d2 need to be measured and interobserver ICCs showed.
for each patient. The 8 measurements are clear and sim- Special attention was dedicated to having an IT
ple to determine on radiographs to increase repeatability group and MT group with similar characteristics, such
and reproducibility in large-scale application. Moreover, as initial age, sex distribution, history of trauma, history
the CEJ is not a straight line, as the labial or lingual curve of earlier orthodontic treatment or endodontic

Table III. Intragroup data comparison of root length (correlation analysis and t test)
Correlation analysis
t test
Variable Pretreatment, mean (SD) Posttreatment, mean (SD) r P value P value
Root length of OA group 16.00 (3.24) 16.07 (3.10) 0.474 \0.001* 0.715
Root length after correction of OA group 16.00 (3.24) 15.79 (3.12) 0.475 \0.001* 0.319
Root length of CA group 15.62 (2.56) 14.71 (2.77) 0.476 \0.001* \0.001*

SD, standard deviation; OA, open apex; CA, closed apex.


*Statistically significant at P \0.05.

American Journal of Orthodontics and Dentofacial Orthopedics May 2020  Vol 157  Issue 5
608 Li et al

Table IV. Results of univariate and multivariate regression analyses with forward selection using root resorption after
correction (mm) as the dependent variables
Univariate Multivariate

Variable (unit) B P value B (SE) Beta P value


Initial age (y) 0.20 0.10
Sex (male/female) 0.26 0.33
Trauma (yes/no) 1.49 0.23
Previous orthodontic treatment (yes/no) 3.36 0.12 5.21 (2.10) 0.11 \0.05*
Endodontic treatment (yes/no) 0.09 0.98
Extraction (yes/no) 0.54 \0.05*
Duration (mo) 0.05 \0.01* 0.06 (0.01) 0.16 \0.001*
Pretreatment overjet (mm) 0.05 0.44
Pretreatment overbite (mm) 0.02 0.69
Horizontal movement (Dx') (mm) 0.44 \0.05* 0.46 (0.13) 0.15 \0.001*
Vertical movement (Dy') (mm) 0.67 0.09 0.75 (0.38) 0.08 \0.05*
Pretreatment proximity to palate (yes/no) 0.53 0.76
Posttreatment proximity to palate (yes/no) 1.77 0.19
Apex closure (yes/no) 0.811 \0.01* 1.09 (0.26) 0.18 \0.001*
SE, standard error.
*Statistically significant at P \0.05.

treatment, extraction decision, treatment duration, and that the incisor roots in the IT group will undergo less
the horizontal and vertical apex movements, because resorption.
these factors may contribute to root resorption (Table There are 3 possible outcomes in moving an IT—
I). Although the treatment time does not seem to be achieve normal length, be stunted (no further growth),
associated with root resorption as most studies have or real root shortening. To discuss these possibilities, in-
indicated, there was a significant difference between tragroup data of root length were compared in Table III.
initial age and sex distribution in the groups because The pretreatment root length was statistically signifi-
tooth development is closely related to age and happens cantly correlated with the posttreatment root length in
earlier in female patients. There was also significant dif- the IT group, but there was no statistical significance be-
ference between the horizontal and vertical apex move- tween them, which can be explained by the compensa-
ments, showing that the IT group had more incisor tion of root growth or the small amount of root
torque changes or bodily movement, but in the later resorption. To find the reason, another paired-samples
investigation, the IT group had less root resorption, t test was conducted to compare the pretreatment root
which is different from previous discoveries and indi- length and posttreatment root length after correction
cates the immature teeth can resist the root resorption. of the IT group, and the result was the same, indicating
Root resorption was carefully compared between the that it was because the root resorption was little in the
IT group and MT group and between each quantitative cases with immature teeth. Therefore, a tooth with an
measurement (Table II). All single measurements IT will suffer little real root shortening but not be
including C1P0 , R1P0 , C1L0 , d1, C2P0 , R2P0 , C2L0 , and d2 stunted. In addition, there was statistically significantly
had no statistical significance showing similar character- correlation and difference between pretreatment and
istics of the 2 groups. Pretreatment root length had no posttreatment root length, showing more root resorp-
statistical significance, but posttreatment root length tion in the MT group.
had statistical significance and root resorption, which Because EARR is a multifactorial problem, linear
indicates that there is an association between root regression analyses were used to test identify predictors
resorption and tooth development. However, most pre- for root resorption (Table IV). According to the multivar-
vious studies ignored the problem of root growth, and iate analyses, we also confirmed our hypothesis that pre-
few have determined the amount of root growth. dictability of apical orthodontic root resorption increases
Although the result in this study will be similar regardless when tooth development is considered. Although the
of the root growth amount, we added 0.18 mm per year apical movement (horizontal or vertical), treatment
during ages 10-13 years to posttreatment root length as duration, and previous orthodontic treatment were
the correction. After correction, there was also signifi- also the risk factors for EARR, aligning with previous
cant difference between root resorption, proving again studies,41-43 the beta value of tooth development was

May 2020  Vol 157  Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics
Li et al 609

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