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SYSTEMATIC REVIEW

Association of orthodontic force system


and root resorption: A systematic review
Marina G. Roscoe,a Josete B. C. Meira,b and Paolo M. Cattaneoc
S~ao Paulo, Brazil, and Aarhus, Denmark

Introduction: In this systematic review, we assessed the literature to determine which evidence level supports
the association of orthodontic force system and root resorption. Methods: PubMed, Cochrane, and Embase da-
tabases were searched with no restrictions on year, publication status, or language. Selection criteria included
human studies conducted with fixed orthodontic appliances or aligners, with at least 10 patients and the force
system well described. Results: A total of 259 articles were retrieved in the initial search. After the review pro-
cess, 21 full-text articles met the inclusion criteria. Sample sizes ranged from 10 to 73 patients. Most articles were
classified as having high evidence levels and low risks of bias. Conclusions: Although a meta-analysis was not
performed, from the available literature, it seems that positive correlations exist between increased force levels
and increased root resorption, as well as between increased treatment time and increased root resorption.
Moreover, a pause in tooth movement seems to be beneficial in reducing root resorption because it allows
the resorbed cementum to heal. The absence of a control group, selection criteria of patients, and adequate
examinations before and after treatment are the most common methodology flaws. (Am J Orthod Dentofacial
Orthop 2015;147:610-26)

A
common goal that permeates the practice of or- teeth vulnerable to root resorption. Already in the
thodontics has been the determination of the 1930s, Schwarz12 proposed that the “optimal” force
“optimal” force magnitude, which results in for tooth movement, characterized by maximal cellular
the highest rate of tooth movement with minimal iatro- response with maintenance of the vitality of the tissues,
genic side effects.1-4 Still, orthodontically induced should be within the levels of capillary pressure. If the
inflammatory root resorption (OIIRR) is an undesirable capillary blood pressure is exceeded, this may cause
risk of orthodontic treatment.5,6 OIIRR is a bio- collapse of the capillaries and dysfunction of the blood
mechanical phenomenon: an association between supply.13 This phenomenon may result in a degradation
OIIRR and biologic effects has been shown.5,7-9 It is of the tooth-protecting outer layers of the precementum
known that the biologic factors are intrinsic to the and its formative layer of cementoblasts; this activates
patient and, until now, have not been able to be the resorptive activity of the clastic cells. This process
modified.10 Thus, it is essential to identify how the biome- leaves the mineralized tooth tissue denuded, triggering
chanical orthodontic treatment factors influence OIIRR to inflammatory events, similar to bone resorption, but
minimize the risks and the severity of this phenomenon.11 on the root surface.14,15
Orthodontic tooth movement involves a series of bio- Although the severity of OIIRR is mostly clinically
logic reactions after force application, which makes insignificant, the literature shows that 1% to 5% of
orthodontically treated teeth have severe OIIRR, which
a
Postgraduate student, Department of Biomaterials and Oral Biology, School of is defined as resorption exceeding 4 mm or a third of
Dentistry, University of S~ao Paulo, S~ao Paulo, Brazil.
b
Associate professor, Department of Biomaterials and Oral Biology, School of the original root length.16 A significant reduction in
Dentistry, University of S~ao Paulo, S~ao Paulo, Brazil. the root length can cause an unfavorable crown-root ra-
c
Associate professor, Section of Orthodontics, Department of Dentistry, Faculty tio of the affected teeth. This has great clinical signifi-
of Health Science, Aarhus University, Aarhus, Denmark.
Funded by CAPES and CNPq (grant no. BEX 2079-13-5). cance, especially when it is coincident with alveolar
All authors have completed and submitted the ICMJE Form for Disclosure of Po- bone loss or combined with orthodontic retreatment.
tential Conflicts of Interest, and none were reported. Apical root loss of 3 mm is equivalent to 1 mm of crestal
Address correspondence to: Paolo M. Cattaneo, Section of Orthodontics, School
of Dentistry, Aarhus University, Vennelyst Boulevard 9, DK-8000 Aarhus, bone loss, which means that periodontal bone loss will
Denmark; e-mail, paolo.cattaneo@odontologi.au.dk. reach a critical stage more rapidly if it is accompanied
Submitted, October 2014; revised and accepted, December 2014. by OIIRR.17 Regarding orthodontic retreatments, when
0889-5406/$36.00
Copyright Ó 2015 by the American Association of Orthodontists. force is again applied to a tooth with an already trauma-
http://dx.doi.org/10.1016/j.ajodo.2014.12.026 tized external surface, the onset of resorption will
610
Roscoe, Meira, and Cattaneo 611

probably be much more rapid and extensive than that aspects of orthodontic treatment with fixed appliances
occurring during the primary activation.18 and aligners. The ones that evaluated the risk of root
Several reviews,3,16,19-22 systematic reviews,1,23 and a resorption based on genetic factors were not considered
meta-analysis24 have been performed over the years, relevant for this systematic review. In the second step of
aiming to elucidate possible treatment-related etiologic the screening process, these full articles were subjected
factors to guide clinical decisions that will minimize the to inclusion and exclusion criteria. The inclusion criteria
risks of severe root resorption.23,24 Most authors agree required the studies to be performed on humans, evalu-
that this biomechanical phenomenon depends on both ating root resorption as an outcome of orthodontic
time and force.5,25-31 The direction of tooth treatment, with at least 10 subjects. The exclusion
movement32-34 and the loading regimen (continuous criteria were case reports, case series, reviews, systematic
vs intermittent forces)31,35-38 also appear to have reviews, opinions, studies with questionnaires, and
considerable impact in its occurrence. Yet, until today, studies where the diagnosis or measurement of OIIRR
no investigators have conducted a systematic review to was performed only on lateral cephalograms or pano-
evaluate the state of the published scientific research ramic radiographs. The lowest level of evidence accepted
on OIIRR, considering the mechanical aspects, the was cohort studies.
methodologic quality, and the risk of bias. According All studies identified by applying the inclusion and
to the preferred reporting items for systematic reviews exclusion criteria underwent assessment for validity
and meta-analyses (PRISMA) 2009 checklist, Table I bet- and data extraction by 2 reviewers (M.G.R. and
ter outlines the questions that will be addressed with P.M.C.), who independently examined the studies. The
reference to participants, interventions, comparisons, studies that were appropriate to be included were ran-
outcomes, and study designs (PICOS) in this study. domized and nonrandomized controlled trials, and
The aims of this systematic review were to assess the cohort studies fulfilling the criteria concerning popula-
scientific literature that has examined root resorption as tions, intervention characteristics, comparison groups,
an outcome of orthodontic treatment and to determine and outcomes as stated in Table I. The reviewers ex-
which level of evidence is available to support the asso- tracted data independently, using specifically designed
ciation of root resorption with different orthodontic data-extraction forms. For each included study, qualita-
force systems. tive and quantitative information was extracted,
including year of publication, experimental and control
treatments, numbers and ages of patients, treatment
MATERIAL AND METHODS and follow-up durations, method of outcome assess-
This systematic review was performed according to ment, authors' conclusions, and all information needed
the Cochrane Oral Health Group's Handbook for Sys- for the methodologic quality evaluation. Any disagree-
tematic Reviews of Interventions (http://ohg.cochrane. ment was discussed to reach a common final decision.
org) and was registered with the number If further clarifications were deemed necessary, the au-
CRD42014008912 in the PROSPERO database (http:// thors of the articles were contacted by e-mail.
www.crd.york.ac.uk/PROSPERO). A computerized sys- The available literature already includes some scoring
tematic search was performed in 3 electronic databases: systems, which were used as the starting point to
PubMed, Cochrane, and Embase. For the PubMed and develop our methodologic scoring system.24,39-42
Cochrane databases, we selected the following search Consequently, the remaining articles were scored by
sequence of medical subject headings (MeSH) terms: the 2 reviewers to analyze study design and conduct,
[“orthodontics” AND “root resorption” AND (“biome- methodologic soundness, and data analysis to answer
chanics” or “dental stress analysis”)]. For the Embase the research question. This system resulted in the 13
database, we selected the following search sequence of criteria shown in Table II.
Emtree terms: [“orthodontics” AND “tooth root” AND Concerning study design, time, randomization
(“biomechanics” OR “dental stress analysis”)]. assignment, control group, sample size, description of
Hand searches were undertaken to find additional the selection criteria for patients, and formulation of
relevant published material that might have been missed the objective of the study were evaluated. Prospective
in the electronic searches. No restrictions were placed on and randomized studies provide the best evidence on
year, publication status, or language of the articles. The the efficacy of health care interventions23; therefore,
search was performed on December 17, 2013. the time and the randomization process were included
In the first step of the screening process, titles and in the scoring. The absence of a random assignment
abstracts were used to identify full articles concerning could be critical because clinicians with a preconceived
the association of root resorption with the mechanical notion of what causes root resorption may be biased

American Journal of Orthodontics and Dentofacial Orthopedics May 2015  Vol 147  Issue 5
612 Roscoe, Meira, and Cattaneo

Table I. PICOS format


Component Description
Population Clinical studies that involved patients having orthodontic treatment
Intervention Orthodontic therapy with conventional fixed appliances or aligners
Comparison Mechanical variables of the orthodontic treatment (continuous vs intermittent forces, light vs heavy forces, influence of
tooth movement direction, duration of treatment, and types of orthodontic appliances)
Outcome OIIRR
Study design Randomized and nonrandomized controlled trials, and cohort studies

Table II. Methodologic scoring system


Criteria assessed Score
I. Study design (maximum score, 10 points)
A. Time Retrospective, 0 point; prospective, 2 points
B. Randomization If stated, 1 point
C. Control group If present, 1 point
D. Sample size Number of evaluated teeth per experimental group: \5, 1 point; 5 to #10, 2 points; .10
to #20, 3 points; .20, 4 points
E. Selection criteria If clearly described, 1 point
F. Objective If clearly formulated, 1 point
II. Methodologic soundness (maximum score, 7 points)
A. Appliance type If clearly described, 1 point
B. Force magnitude If stated, 1 point; if controlled by a force measurement device, 2 points
C. Radiographic examination before treatment Periapical radiograph or cone-beam computed tomography, 1 point; other method, 0 point
D. Measurement method of root resorption Periapical radiograph or histological analysis, 1 point; SEM, TEM, CLSM, or mCT, 2 points (if
2 methods were combined, the points were summed)
III. Data analysis (maximum score, 4 points)
A. Statistical analysis Appropriate for data, 1 point
B. Error of the method If stated, 1 point
C. Data presentation If P value stated, 1 point
If any variability measures (standard deviation, confidence interval, or range) stated, 1 point

when obtaining their patient sample. Regarding sample microscopy (SEM), transmission electron microscopy
size, the numbers of teeth analyzed in each experimental (TEM), confocal laser scanning microscopy (CLSM), or
group were evaluated. Because of the genetic predispo- microcomputed tomography (mCT).
sition influence for the onset of OIIRR, large samples Regarding data analysis, we analyzed whether the
were given higher scores to reduce variability.24,43 statistical analysis was appropriate, whether the error
Importance was given to patient-selection criteria of the method was stated, and whether in the data pre-
because external factors that might predispose root sentation the P value was associated with any measure-
resorption should be excluded during patient selection. ment of variability, such as confidence interval, range, or
With respect to methodologic soundness, descriptions standard deviation.42
of appliance types, force magnitudes, radiographic exam- The methodologic quality scores were reported as per-
inations before treatment, and accuracy of the diagnoses centages of the maximum achievable score (21 points):
and measurement methods of OIIRR were evaluated. mean score less than 60% indicates low level of evidence;
Different scores were given if the force magnitude was 60% to 70%, moderate level of evidence; and more than
just stated or controlled by a force measurement device. 70%, high level of evidence.41 To account for flaws in
The radiographic evaluation before the study was also design, conduct, analyses, and reporting that might lead
considered in the scoring process because it could detect to underestimation or overestimation of the true inter-
pretreatment root shortening and eliminate patients who vention effect (bias), assessments for risk of bias were per-
were predisposed to root resorption. The varying degrees formed.46 The risk of selection, performance, detection,
of magnification of the radiographs and the limitations of attrition, and reporting bias of each study was evaluated
2-dimensional measurement of a 3-dimensional (3D) and classified. Studies were categorized as having a low
phenomenon make light microscopy and plain radio- risk of bias if 4 or more domains were considered
graphic methods less accurate than quantitative 3D volu- adequate, as having a moderate risk of bias if 3 domains
metric evaluations.6,29,44,45 Therefore, these methods were considered adequate, and as having a high risk of
were evaluated with lower scores than scanning electron bias if 2 or fewer domains were considered adequate.47,48

May 2015  Vol 147  Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics
Roscoe, Meira, and Cattaneo 613

Table III. Criteria for assessing risk of bias in the studies


Type of bias Description Relevant domains
Selection Systematic differences between baseline characteristics of the groups that  Sequence generation
were compared  Allocation concealment
Performance Systematic differences between groups in the care that was provided or in  Blinding of participants and personnel
exposure to factors other than the interventions of interest
Detection Systematic differences between groups in how outcomes were determined  Blinding of outcome assessment
Attrition Systematic differences between groups in withdrawals from a study  Incomplete outcome data
Reporting Systematic differences between reported and unreported findings  Selective outcome reporting

The full descriptions of the bias classifications are score, with a mean score of 72%. Thirteen studies were
presented in Table III. The risk of bias across the studies classified as high (62%), 5 as moderate (24%), and 3 as
was also assessed. Studies conducted by the same research low (14%) levels of evidence. Eleven studies were
group were compared to check for similarity between pa- considered to have a low risk of bias (52%), 2 had a
tient characteristics (sex, age, number, and so on). If we moderate risk of bias (10%), and 8 were classified as
detected bias across the studies that might have affected having a high risk of bias (38%). It was not possible to
the cumulative evidence, the authors were contacted to perform a meta-analysis because of the heterogeneous
clarify or confirm the risk of bias. methodologies of these studies.

RESULTS DISCUSSION
The database search showed 128 articles listed in In spite of many studies investigating the association
PubMed, 115 articles in Embase, and 16 articles in Co- of root resorption with the mechanical factors of ortho-
chrane. Four articles were added after hand searches of dontic treatment, only 21 were considered appropriate
the bibliographies of the selected articles and relevant for inclusion in this systematic review. An overall quan-
reviews. By using the PRISMA flow diagram, an overview titative conclusion could not be made because of the
of the article selection process is illustrated (Fig).49 After heterogeneity of the study designs and their treatment
exclusion of 26 duplicate articles, 237 articles remained. modalities. Moreover, it was not considered relevant to
In the first step of the screening process, a further 112 perform a meta-analysis because most studies character-
articles were excluded because they were determined ized by similar study designs and methodologies were
to be irrelevant based on the titles and abstracts. In performed by the same research groups. A meta-
the second step of the screening process, the remaining analysis with these premises will result in a biased
125 full-text articles were assessed: 52 articles were conclusion. Therefore, we preferred to include more
excluded because they did not meet the inclusion studies and perform a qualitative synthesis.
criteria, and 52 articles were excluded after the applica- Relative to study designs included in this systematic
tion of the exclusion criteria (Fig). Thus, the selection review, 11 studies were randomized controlled trials, 8
process resulted in 21 full-text articles.5,28-30,37,38,50-64 were nonrandomized controlled trials, and 2 were his-
A summary of the main findings and the data toric cohorts. The greatest advantage of randomized
regarding participants, interventions, comparisons, controlled trials compared with nonrandomized
outcomes, study designs (PICOS), and follow-up periods controlled trials and cohort studies is the random alloca-
of each study in this systematic review is presented in tion process; nevertheless, cohort studies present the
Table IV. The assessment of the risk of bias across the possibility to evaluate large groups of subjects and
studies showed that 2 articles were conducted on the follow them for longer periods than do randomized
same sample of patients (confirmed by e-mail communi- controlled trials.65 These 2 aspects are highly desirable
cation from their authors); therefore, these 2 studies in studying OIIRR and therefore justified the inclusion
were treated as one, and the results were combined.28,29 of the 2 cohort studies in this review.
Most studies (90%) were clinical trials, except for 2 Referring to the methodologic quality assessment,
historic cohorts. All articles were published in English be- the scores ranged from 48% to 86%, with a mean score
tween 1982 and 2012. Detailed assessments of the of 72%, which corresponds to a high evidence level.
methodologic quality and the risk of bias are shown in Studies that performed measurements or diagnoses of
Tables V through VIII. Methodologic quality scores OIIRR using only panoramic radiographs or lateral ceph-
ranged from 48% to 86% of the maximum achievable alograms were excluded; this certainly contributed to

American Journal of Orthodontics and Dentofacial Orthopedics May 2015  Vol 147  Issue 5
614 Roscoe, Meira, and Cattaneo

Fig. Flow diagram with an overview of the article-selection process.

achieving this high score. The reason behind this choice mCT. In the 4 studies performed on incisors, a high risk
was based on the inherent distortion and magnification of bias was detected.61-64 Moreover, although the
problems when measuring the root apex because of su- theoretical maximum achievable score relative to
perimposition of the incisors on lateral cephalograms,24 methodologic soundness is 7, for these studies the
and distortion of tooth positions and inclinations on actual maximum was 6, since it is not realistic to
panoramic radiographs.66 These limitations may lead extract these teeth and apply the most reliable
to inaccuracies in OIIRR diagnosis and measurements. methods of diagnosis (ie, SEM, TEM, CLSM, and mCT).
Seventeen of the 21 selected studies were performed This underlines the limitation of studies on OIIRR
on premolars (12 evaluated only maxillary premo- when extractions cannot be performed.
lars5,30,38,50-58; 5 evaluated both maxillary and A significant number of studies did not include a con-
mandibular premolars28,29,37,59,60). All studies classified trol group, did not clearly describe the selection criteria of
as having a high evidence level were performed on patients, or did not perform an adequate radiographic
premolars. Although they are not the teeth most examination before the intervention. In studying OIIRR,
affected by root resorption, they are the most comparison of the experimental group with the control
frequently extracted teeth during orthodontic group is strongly recommended because it will help to
treatment, often bilaterally. This make it possible to show the actual effect of treatment on root resorption.
perform randomized controlled trials with a split- Yet, 57% of the studies did not include a control group.
mouth design, where detailed information about root For ethical and economic reasons, most studies had small
resorption can be acquired after tooth extractions using samples of patients. Consequently, the authors preferred
methods of diagnostic such as SEM, TEM, CLSM, and to include and compare 2 experimental groups, at the

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Roscoe, Meira, and Cattaneo


Table IV. PICOS, follow-up period, and main findings of the studies
Study
Study Participants Interventions Comparisons Outcomes design Follow-up Main findings
Harris et al5 (2006) 54 maxillary first PM from Orthodontic therapy with Force levels: low (25 g) vs - Volumetric RCT, 4 wk The 3 force level groups
27 patients (12 M, fixed appliances heavy (225 g) vs control measurements of the SMD were significantly
15 F); ages, 11.9-19.3 y; (segmented technique) (0 g) amount of RR after different. Mean
mean, 15.6 y intrusion forces. volumes of RR in the
- Establishment of the light and heavy force
sites where RR is more groups were about 2
prevalent. and 4 times greater than
in the control group.
Mesial-apical and
distal-apical surfaces
had more RR than the
other regions, with no
statistically significant
difference between
them.
Chan and Darendeliler28,29 36 maxillary and Orthodontic therapy with Force levels: low (25 g) vs - Volumetric RCT, 4 wk More RR in the heavy force
(2005, 2006) mandibular PM from 16 fixed appliances heavy (225 g) vs control measurements of the SMD group compared with
patients (10 M, 6 F); (segmented technique) (0 g) extent of RR craters the light and control
ages, 11.7-16.1 y; after buccal tipping groups. Although more
mean, 13.9 y forces. RR was recorded in the
- Establishment of the light force group, no
sites where RR is more statistically significant
prevalent. difference was found
between the light and
control groups.
Buccocervical and
lingual-apical surfaces
had more RR than the
other regions.
Barbagallo et al30 (2008) 54 maxillary first PM from Orthodontic therapy with Force levels and systems: - Volumetric RCT, 8 wk More RR in the heavy force
May 2015  Vol 147  Issue 5

27 patients (12 M, fixed appliances conventional low (25 g) measurements of the SMD group compared with
15 F); ages, 12.5-20 y; (segmented technique) vs conventional heavy amount of RR after the aligner, light, and
mean, 15.3 y and aligners (225 g) vs aligner vs buccal tipping forces. control groups. The
control (0 g) - Establishment of the aligner group had
sites where RR is more similar effects on root
prevalent. cementum as did the
light group. More RR
was observed was at the
buccocervical and
lingual-apical regions in
all treated teeth.

615
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616
Table IV. Continued

Study
Study Participants Interventions Comparisons Outcomes design Follow-up Main findings
Weiland37 (2003) 90 maxillary and Orthodontic therapy with Loading regimen: - Comparison of the NR-CT, 12 wk The teeth with the
mandibular PM from 27 fixed appliances continuous vs effects of stainless SMD superelastic wire moved
patients (10 M, 17 F); (segmented technique) intermittent vs control steel and superelastic significantly more and
ages, 10.2-14.5 y; archwires on TM and tipped buccally to a
mean, 12.5 y RR after buccal tipping greater degree than
force. those moved with the
stainless steel wire. The
teeth moved with the
superelastic wire
showed significantly
more RR, more
resorptive damage
regarding perimeter,
area, and volume of the
lacunae than those
moved with a stainless
steel wire. The cervical
American Journal of Orthodontics and Dentofacial Orthopedics

resorptions were mainly


located on the buccal
side, and the apical
resorptions on the
palatal or lingual side.
Owman-Moll et al38 32 maxillary first PM, from Orthodontic therapy with Loading regimen and - Effects of continuous NR-CT, 4 or 7 wk Areas of RR were found on
(1995) 16 patients (8 F, 8 M); fixed appliances treatment times: and interrupted buccal SMD all experimental teeth.
ages 11.8-15.8 y; mean, (segmented technique) continuous vs tipping force of the No significant
13.9 y interrupted forces, same magnitude difference of resorption
applied for 4 or 7 weeks (50 g), applied for 4 or was found between the
7 weeks on the RR 2 force systems.
occurrence.
Bartley et al50 (2011) 30 maxillary first PM from Orthodontic therapy with Force system: 2.5 vs 15 - Volumetric RCT, 4 wk No statistically significant
15 patients (7 M, 8 F); fixed appliances of buccal root torque measurements of the SMD differences in RR after

Roscoe, Meira, and Cattaneo


ages, 12.75-16.83 y; (segmented technique) amount of RR after the application of either
mean, 14.3 y buccal root torque. 2.5 or 15 of buccal
root torque. More RR at
the apical region than at
the middle and cervical
regions.
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Roscoe, Meira, and Cattaneo


Table IV. Continued

Study
Study Participants Interventions Comparisons Outcomes design Follow-up Main findings
Wu et al51
(2011) 30 maxillary first PM from Orthodontic therapy with Force levels: low (25 g) vs - Measurement and RCT, 4 wk More RR in the heavy force
15 patients (5 M, 10 F); fixed appliances heavy (225 g) comparison of the SMD group than in the light
ages, 11.9-16.9 y; (segmented technique) locations, dimensions, force group. Greater RR
mean, 14.15 y and volumes of RR in the compression
craters after rotational areas (buccodistal and
force. lingual-mesial surfaces)
than in other areas at all
levels of the root.
King et al52 (2011) 30 maxillary first PM from Orthodontic therapy with Force system: 2.5 vs 15 - Volumetric RCT, 4 wk Greater RR in teeth that
15 patients (4 M, 11 F); fixed appliances of distal root tipping measurements of the SMD had undergone greater
ages, 12.8-16.11 y; (segmented technique) amount of RR after distal root tip bends.
mean, 14.2 y distal root tipping Compression of the
force. periodontal ligament
- Establishment of the caused more RR than
sites where RR is more tension, which was
prevalent. more pronounced in the
apical and cervical
thirds of the teeth.
Montenegro et al53 (2012) 20 maxillary first PM from Orthodontic therapy with Force levels: low (25 g) vs - Volumetric RCT, 4 wk Greater RR after heavy
10 patients (3 M, 7 F); fixed appliances heavy (225 g) measurements of the SMD forces when compared
ages, 12-18 y; mean not (segmented technique) amount of RR after with light forces. The
mentioned extrusion force. distal surfaces were
- Establishment of the more affected than
sites where RR is more other root surfaces. No
prevalent. significant difference
between the cervical,
middle, and apical
thirds in relation to RR.
Chan et al54 (2004) 20 maxillary first PM from Orthodontic therapy with Force levels: low (25 g) vs - Volumetric RCT, 4 wk More RR in the heavy force
10 patients fixed appliances heavy (225 g) vs control measurement of RR SMD group than in the light
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(segmented technique) (0 g) craters after buccal and control groups.


tipping force.

617
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618
Table IV. Continued

Study
Study Participants Interventions Comparisons Outcomes design Follow-up Main findings
55
Kurol et al (1996) 112 maxillary PM from 56 Orthodontic therapy with Force levels and treatment - Effect of orthodontic NR-CT, 1-7 wk More than 6 times the RR
patients (18 M, 38 F); fixed appliances times: 50 g applied for 1 force (buccal tipping) SMD in all test groups
ages, 10.5-17.5 y; (segmented technique) to 7 wk vs 0 g (control) and treatment time in compared with the
mean, 13.8 y RR occurrence and control group. The RR
severity. was mainly located in
- Comparison of the apical third of the
histologic with root. The number of
radiographic findings teeth with RR increased
in detecting RR. with time of force
application. The PR
failed to show any RR
occurrence.
Casa et al56 (2006) 28 maxillary first PM from Orthodontic therapy with Treatment times: 1, 2, 3, or - Appearance and NR-CT, 1-4 wk Resorption lacunae and
14 patients; ages, 13- fixed appliances 4 wk vs control distribution of clastic SMD clastic cells increased in
16 y (segmented technique) cells during the extent and number with
application of the duration of the force
continuous torque and were found on the
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over several time cementum surface at


periods. the pressure areas.
Some signs of
cementum repair were
also noticed, even with
maintenance of the
force level.
Paetyangkul et al57 (2011) 54 maxillary first PM from Orthodontic therapy with Force levels and treatment - Volumetric NR-CT, 4, 8, or 12 wk Less RR in the light force
36 patients (21 F, fixed appliances times: low (25 g) vs measurement of SMD group than in the heavy
15 M); mean age, 14.9 y (segmented technique) heavy (225 g), applied resorption craters, force group. Increased
for 4, 8, or 12 wk after buccal tipping RR from 8-12 weeks of
force. force application with
either light or heavy
orthodontic forces.

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Table IV. Continued

Study
Study Participants Interventions Comparisons Outcomes design Follow-up Main findings
Aras et al58 (2012) 64 maxillary PM from 32 Orthodontic therapy with Force system: continuous - Effects of 2 RCT, 12 wk Group of continuous force
patients (25 F, 7 M); fixed appliances vs intermittent force, 2 reactivation periods of SMD produced faster TM
ages, 12-18 y; mean (segmented technique) or 3 weekly controlled intermittent than intermittent force
age, 14.4 y reactivations and continuous buccal group. Statistically
tipping forces (150 g) significant differences
on RR and TM. regarding the amount
of RR between the 2
groups were only
observed in the 3 weekly
reactivation group. RR
decreased when a pause
was given, irrespective
of the timing of
reactivation. Two
weekly reactivations of
continuous orthodontic
force can lead to less RR
than 3 weekly
reactivations.
Harry and Sims59 (1982) 36 maxillary and Orthodontic therapy with Force levels and time - Effects of different NR-CT, 14, 35, and 70 d Surface defects identified
mandibular first PM fixed appliances intervals: 50 g vs 100 g magnitudes and SMD with the SEM or
from 10 patients; ages, (segmented technique) vs 200 g. Intervals of 14, durations of intrusive macroscopically were
11-18 y 35, and 70 d. orthodontic forces on not identified on PR.
the topography of root Intrusive forces
surfaces. produced an increase in
- Establishment of the RR compared with the
sites where RR is more control teeth. The
prevalent. amount of RR increased
with the duration of the
force, and to a lesser
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extent with the


magnitude of the
activation. More RR was
observed at the
buccocervical root
surfaces and apical
thirds of the roots.

619
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620
Table IV. Continued

Study
Study Participants Interventions Comparisons Outcomes design Follow-up Main findings
Paetyangkul et al60 (2009) 40 maxillary and Orthodontic therapy with Force levels: low (25 g) vs - Volumetric RCT, 12 wk Less RR in the light force
mandibular first PM fixed appliances heavy (225 g) measurement of RR SMD group than in the heavy
from 10 patients (6 F, (segmented technique) craters after buccal force group in both
4 M); ages, 12.7-18.2 y; tipping force. maxillary and
mean age, 14.3 y - Identification of the mandibular PM. RR
sites that might be greater toward the
predisposed to cervical region on the
resorption. buccal surfaces and the
apical regions on the
lingual surfaces.
Ramanathan and 49 patients (20 M, 29 F); Orthodontic therapy with Appliance types: basal - Comparison of the NR-CT 6 mo No statistically significant
Hofman61 (2009) ages, 9-30.1 y; mean fixed appliances arch vs 3-component extent of RR during difference in RR among
14.5 y (segmented technique arch vs leveling with different orthodontic the 3 groups.
and SWA) SWA. TM with 3 techniques.
Baumrind et al62 (1996) Radiographic records of 73 Orthodontic therapy with Maxillary central apical - Relationship between Historic Variable (1-7 y) Association of orthodontic
patients (16 M, 57 F); fixed appliances incisor displacement vs incisor apical cohort intervention with
age, at least 20 y, (edgewise appliance). ARR displacement* and maxillary incisor RR,
American Journal of Orthodontics and Dentofacial Orthopedics

diagnosed with Class I ARR. even when the position


or II malocclusion of the tooth was the
same on the
cephalograms. More RR
for retraction
displacement than
displacements in other
directions.
McFadden et al63 (1989) Radiographic records from Orthodontic therapy with Intrusion vs root - Relationship between Historic 28.8 6 7.4 mo Degree of root shortening
38 patients; mean age, fixed appliances shortening incisor intrusion and cohort greater in the maxilla
13.1 6 1.4 y (bioprogressive root shortening. (1.84 mm) than in the
technique). mandible (0.61 mm).
The most significant
factor for occurrence of

Roscoe, Meira, and Cattaneo


root shortening was the
treatment time.
Deguchi et al64 (2008) 18 patients (2 M, 16 F); Orthodontic therapy with Appliance types: implant - Comparison of the NR-CT 7 mo Significantly more RR in
mean ages, 20.7 6 2.5 y fixed appliances vs J-hook headgear effects of incisor the J-hook headgear
(J-hook headgear (edgewise appliance) intrusion, force vector, group than in the
group) and 21.5 6 3.7 y and amount of RR implant group after
(implant group) between implant intrusion of the
orthodontics and maxillary incisors.
J-hook headgear.

PM, Premolars; F, female; M, male; RR, root resorption; NR-CT, nonrandomized controlled trial; RCT, randomized controlled trial; SMD, split-mouth design; TM, tooth movement; SWA, straight-
wire appliance; PR, peripapical radiograph; ARR, apical root resorption.
*Directions: retraction, advancement, intrusion, and extrusion.
Roscoe, Meira, and Cattaneo 621

Table V. Study design (maximum score, 10 points)


Article Time Randomization Control group Sample size Selection criteria Objective Score
Harris et al5 (2006) 2 1 1 3 1 1 9
Chan and Darendeliler28,29 (2005, 2006) 2 1 1 2 1 1 8
Barbagallo et al30 (2008) 2 1 1 2 1 1 8
Weiland37 (2003) 2 0 1 4 0 1 8
Owman-Moll et al38 (1995) 2 0 0 2 0 1 5
Bartley et al50 (2011) 2 1 0 3 1 1 8
Wu et al51 (2011) 2 1 0 3 1 1 8
King et al52 (2011) 2 1 0 3 1 1 8
Montenegro et al53 (2012) 2 1 0 2 1 1 7
Chan et al54 (2004) 2 1 1 2 0 1 7
Kurol et al55 (1996) 2 0 1 2 0 1 6
Casa et al56 (2006) 2 0 1 1 0 1 5
Paetyangkul et al57 (2011) 2 0 0 2 1 1 6
Aras et al58 (2012) 2 1 0 3 1 1 8
Harry and Sims59 (1982) 2 0 1 1 0 1 5
Paetyangkul et al60 (2009) 2 1 0 3 1 1 8
Ramanathan and Hofman61 (2009) 2 0 0 3 1 1 7
Baumrind et al62 (1996) 0 0 0 4 1 1 6
McFadden et al63 (1989) 0 0 0 4 1 1 6
Deguchi et al64 (2008) 2 0 0 2 0 1 5

Table VI. Methodological soundness (maximum score, 7 points)


Article Appliance type Force magnitude Radiographic exam BT Measurement method of RR Score
Harris et al5 (2006) 1 2 0 2 5
Chan and Darendeliler28,29 (2005, 2006) 1 2 1 2 6
Barbagallo et al30 (2008) 1 1 0 2 4
Weiland37 (2003) 1 1 0 2 4
Owman-Moll et al38 (1995) 1 2 1 2 6
Bartley et al50 (2011) 1 1 0 2 4
Wu et al51 (2011) 1 2 1 2 6
King et al52 (2011) 1 1 0 2 4
Montenegro et al53 (2012) 1 2 1 2 6
Chan et al54 (2004) 1 1 1 2 5
Kurol et al55 (1996) 1 2 1 2 6
Casa et al56 (2006) 1 1 0 3 5
Paetyangkul et al57 (2011) 1 2 0 2 5
Aras et al58 (2012) 1 2 0 2 5
Harry and Sims59 (1982) 1 2 1 3 7
Paetyangkul et al60 (2009) 1 2 0 2 5
Ramanathan and Hofman61 (2009) 1 1 1 1 4
Baumrind et al62 (1996) 1 0 1 1 3
McFadden et al63 (1989) 1 0 1 1 3
Deguchi et al64 (2008) 1 2 1 1 5
Exam BT, Examination before treatment; RR, root resorption.

expense of including a control group. Nine studies did selection criteria and radiographic examinations before
not report the sample size calculation; the numbers of the interventions are also critical factors. During a
patients varied from 10 to 73, with 4 studies including random selection with no previous radiographic analysis,
only 10 patients. To better score the studies, the numbers the risk of including patients with signs of previous
of teeth included in each experimental group were root resorption or predisposing factors cannot be
considered as well. In the prospective studies, this num- avoided.67,68 Thirty-three percent of the studies did not
ber varied from 4 to 42 teeth per group (mean, 12 teeth). clearly describe the selection criteria of the patients,
Regarding the 2 retrospective studies, one evaluated 73 and 43% did not perform appropriate radiographic ex-
teeth62 and the other 38 teeth.63 The absence of strict aminations before the interventions.

American Journal of Orthodontics and Dentofacial Orthopedics May 2015  Vol 147  Issue 5
622 Roscoe, Meira, and Cattaneo

aligners) on root resorption severity was also evaluated:


Table VII. Data analysis (maximum score, 4 points)
similar results were found between patients treated with
Error aligners and those treated with conventional fixed appli-
Statistical of the Data ances activated with light forces.30 Still, comparing these
Article analysis method presentation Score
results should be done with some caution. First, remov-
Harris et al5 (2006) 1 1 1 3
Chan and Darendeliler28,29 1 1 2 4 able aligners do not apply a continuous, constant force
(2005, 2006) to teeth as fixed appliances do, and it is difficult to con-
Barbagallo et al30 (2008) 1 1 2 4 trol the force level applied. Second, the amount of move-
Weiland37 (2003) 1 1 2 4 ment is highly variable and depends on how many hours
Owman-Moll et al38 1 0 2 3
the patients wore the removable appliances; since it was
(1995)
Bartley et al50 (2011) 1 1 2 4 not possible to determine this, it was not reported.30
Wu et al51 (2011) 1 1 2 4 The influence of loading regimen (continuous vs
King et al52 (2011) 1 1 2 4 intermittent forces) was assessed in 2 articles, and the re-
Montenegro et al53 (2012) 1 1 2 4 sults are contradictory. Owman-Moll et al38 did not find
Chan et al54 (2004) 1 1 1 3
a significant difference between the 2 systems on root
Kurol et al55 (1996) 1 0 1 2
Casa et al56 (2006) 0 0 0 0 resorption. However, Weiland37 reported significant dif-
Paetyangkul et al57 (2011) 1 1 2 4 ferences in OIIRR between stainless steel and superelas-
Aras et al58 (2012) 1 1 2 4 tic archwire systems. These conflicting results might be
Harry and Sims59 (1982) 0 0 0 0 related to the methods used to study root resorption.
Paetyangkul et al60 (2009) 1 1 2 4
Owman-Moll et al only analyzed selected areas using
Ramanathan and 1 0 2 3
Hofman61 (2009) light microscopy, whereas Weiland analyzed root resorp-
Baumrind et al62 (1996) 1 1 2 4 tion by CLSM, thus enabling a 3D analysis. In support of
McFadden et al63 (1989) 1 1 1 3 Weiland's findings, some studies suggest that a pause in
Deguchi et al64 (2008) 1 1 2 4 tooth movement may allow the resorbed cementum to
heal.35,58,69
Although most articles were classified as having a The influence of treatment time on OIIRR was also
high evidence level, at least 1 type of bias was present assessed. It seems that a positive correlation exists be-
in all the studies. For example, for evident reasons, the tween increased treatment time and increased root
orthodontists who performed the treatments could not resorption. Kurol et al55 showed that starting from the
be blinded. On the other hand, the majority of the third week, the depth of resorption lacunae increased
studies (62%) did not have detection bias. Ten studies significantly. Casa et al56 also observed that the severity
had selection bias because the allocation process was increased from 1 to 4 weeks of force application. Despite
not random. Two studies were designed as historic co- this evidence showing that root resorption depends on
horts,62,63 and 8 as nonrandomized controlled time, for 8 of the 10 randomized controlled trials in
trials.37,38,55-57,59,61,64 In the remaining studies, this systematic review, the maximum period of interven-
although not clearly stated in the text, on direct tion was only 4 weeks.5,28,29,50-54 The authors justified
request, the randomization process was confirmed by this choice based on ethical reasons and clinical
the authors.5,28-30,50-54,58,60 No study had reporting practicality. When 3 experimental periods were
bias, and 1 had attrition bias because the reason for compared (4, 8, and 12 weeks), it was shown that the
the exclusion of some patients was not reported.62 amount of root resorption increased significantly when
Twelve split-mouth studies evaluated the influence 12 weeks of force application was reached. This might
of the force level on OIIRR in premolars: except for 1 be related to the increased osteoclastic activity seen
study by Harry and Sims,59 the remaining studies were after 8 weeks of force application.57 For future studies,
performed by the same research group. They compared the time factor should be considered.
orthodontic light force (25 g) with heavy force With respect to the location of OIIRR, this seems to be
(225 g),5,28-30,51,53,54,57,60 light torque (2.5 ) with highly dependent on the type of orthodontic movement;
heavy torque (15 ),50 or light distal tipping (2.5 ) with yet, after attentive analysis of the loading regimen, it
heavy distal tipping (15 ).52 Buccal tipping was the seems that “high-pressure” zones were more susceptible
most studied,28-30,54,57,60 followed by intrusion.5,59 to resorption than “high-tensile” zones. For instance,
Except for the study by Bartley et al,50 all studies pre- buccal tipping was associated with resorption mostly
sented a positive correlation between heavy forces and on the buccocervical and lingual-apical regions28-30,37;
increased root resorption. The influence of appliance de- buccal root torque with buccal-apical and palatal-
signs (conventional fixed appliances and removable cervical regions50; rotation around the long axis of the

May 2015  Vol 147  Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics
Roscoe, Meira, and Cattaneo 623

Table VIII. Evidence level and risk of bias classification


Total score Evidence Selection Performance Detection Attrition Reporting Risk of
Article and percent level bias bias bias bias bias bias
Harris et al5 (2006) 17 (81%) High No Yes No No No Low
Chan and Darendeliler28,29 18 (86%) High No Yes No No No Low
(2005, 2006)*
Barbagallo et al30 (2008) 16 (76%) High No Yes No No No Low
Weiland37 (2003) 16 (76%) High Yes Yes Yes No No High
Owman-Moll et al38 (1995) 14 (67%) Moderate Yes Yes Yes No No High
Bartley et al50 (2011) 16 (76%) High No Yes No No No Low
Wu et al51 (2011) 18 (86%) High No Yes No No No Low
King et al52 (2011) 16 (76%) High No Yes No No No Low
Montenegro et al53 (2012) 17 (81%) High No Yes No No No Low
Chan et al54 (2004) 15 (71%) High No Yes No No No Low
Kurol et al55 (1996) 14 (67%) Moderate Yes Yes Yes No No High
Casa et al56 (2006) 10 (48%) Low Yes Yes No No No Moderate
Paetyangkul et al57 (2011) 15 (71%) High Yes Yes No No No Moderate
Aras et al58 (2012) 17 (81%) High No Yes No No No Low
Harry and Sims59 (1982) 12 (57%) Low Yes Yes Yes No No High
Paetyangkul et al60 (2009) 17 (81%) High No Yes No No No Low
Ramanathan and Hofman61 (2009) 14 (67%) Moderate Yes Yes Yes No No High
Baumrind et al62 (1996) 13 (62%) Moderate Yes Yes Yes Yes No High
McFadden et al63 (1989) 12 (57%) Low Yes Yes Yes No No High
Deguchi et al64 (2008) 14 (67%) Moderate Yes Yes Yes No No High

*See text for explanation of the combined presentation of these results.

tooth with resorption at the boundaries between the measurements.73 Still, no study included in this system-
buccal and distal surfaces and between the lingual and atic review used cone-beam computed tomography.
mesial surfaces51; distal root tipping with more resorp- To improve the evidence level in OIIRR research, it
tion on the distal aspects in the apical and middle thirds is suggested that future studies should include con-
and on the mesial aspects in the cervical thirds52; and trol groups, define strict patient inclusion and exclu-
extrusion movement with more resorption on the distal sion selection criteria, and evaluate radiographic
surfaces.53 Regarding intrusion, the results were not material before the interventions. The intended clin-
unanimous. In 1 study, more resorption was reported ical findings should be clearly stated before the start
on the mesial and distal surfaces and at the apical thirds of the investigation, and tests for determining the
of the roots,5 whereas in another study, more resorption right sample size, which allows for statistically and
was seen at the buccocervical root surfaces and at the clinically significant results, should be performed
apical thirds of the roots.59 The last issue draws the (adequate power analysis). Proper randomization pro-
attention to the methods used to assess OIIRR because tocols and blinding of both intervention (when
these seem to influence the detection and amount of possible) and results assessment must be considered
OIIRR. For example, in 4 studies evaluating the amount to reduce the risk of bias. From this review, random-
of OIIRR on incisors using periapical radiographs, only ized controlled trials when premolars (to be extracted)
apical root resorptions and the extent of root shortening are studied for OIIRR seem to be the most appropriate
could be detected.61-64 When we looked at the findings design.
of 3 studies comparing the results of assessing OIIRR
with either periapical radiographs with SEM59 or periap-
ical radiographs with histologic analysis,38,55 it is clear CONCLUSIONS
that periapical radiographs failed to show the real 1. A high level of evidence is available to support
extent of resorption. On the other hand, SEM and the association of root resorption with orthodontic
histologic analysis cannot be used in a clinical setting treatment.
because they require tooth extractions. To overcome 2. Although a meta-analysis was not performed, from
this problem, some authors suggested that it would be the available literature, it seems that positive correlations
beneficial to use cone-beam computed exist between increased force levels and increased root
tomography.70-72 It allows for improved image quality resorption, as well as between increased treatment times
and 3D reconstructions, giving more reliable and increased root resorption.

American Journal of Orthodontics and Dentofacial Orthopedics May 2015  Vol 147  Issue 5
624 Roscoe, Meira, and Cattaneo

3. A pause in tooth movement seems to be beneficial study of the same human teeth. Comput Methods Programs Bio-
in reducing root resorption because it allows the re- med 2009;93:155-61.
14. Reitan K. Some factors determining the evaluation of forces in or-
sorbed cementum to heal.
thodontics. Am J Orthod 1957;43:32-45.
4. The absence of a control group, the selection 15. Kvam E. Cellular dynamics on the pressure side of the rat periodon-
criteria of patients, and adequate examinations before tium following experimental tooth movement. Scand J Dent Res
and after treatment are the most common methodology 1972;80:369-83.
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17. Kalkwarf KL, Krejci RF, Pao YC. Effect of apical root resorption on
ACKNOWLEDGMENTS periodontal support. J Prosthet Dent 1986;56:317-9.
18. Katzhendler E, Steigman S. Effect of repeated orthodontic treat-
We thank Michel Dalstra for the constructive discus- ment on the dental and periodontal tissues of the rat incisor. Am
sion during the elaboration of the project; Janne Lytoft J Orthod Dentofacial Orthop 1999;116:642-50.
Simonsen, research librarian of Aarhus University, for 19. Topkara A. External apical root resorption caused by orthodontic
help during the computerized searches of the databases; treatment: a review of the literature. Eur J Paediatr Dent 2011;
12:163-6.
Ali Darendeliler and Victor Arana, who were contacted 20. Zahrowski J, Jeske A. Apical root resorption is associated with
for clarifications, for answering our questions; and the comprehensive orthodontic treatment but not clearly dependent
Brazilian research funding agencies CAPES and CNPq on prior tooth characteristics or orthodontic techniques. J Am
for the grant BEX 2079-13-5. Dent Assoc 2011;142:66-8.
21. Zainal Ariffin SH, Yamamoto Z, Zainol Abidin IZ, Megat Abdul
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