Association of orthodontic force system and root resorption: A systematic review.

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 databases 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 process, 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 orthodontics has been the determination of the “optimal” force magnitude, which results in the highest rate of tooth movement with minimal iatrogenic side effects.1-4 Still, orthodontically induced inflammatory root resorption (OIIRR) is an undesirable risk of orthodontic treatment.5,6 OIIRR is a biomechanical phenomenon: an association between OIIRR and biologic effects has been shown.5,7-9 It is known that the biologic factors are intrinsic to the patient and, until now, have not been able to be modified.10 Thus, it is essential to identify how the biomechanical orthodontic treatment factors influence OIIRR to minimize the risks and the severity of this phenomenon.11 Orthodontic tooth movement involves a series of biologic reactions after force application, which makes a Postgraduate student, Department of Biomaterials and Oral Biology, School of Dentistry, University of S~ao Paulo, S~ao Paulo, Brazil. b Associate professor, Department of Biomaterials and Oral Biology, School of Dentistry, University of S~ao Paulo, S~ao Paulo, Brazil. c Associate professor, Section of Orthodontics, Department of Dentistry, Faculty of Health Science, Aarhus University, Aarhus, Denmark. Funded by CAPES and CNPq (grant no. BEX 2079-13-5). All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Address correspondence to: Paolo M. Cattaneo, Section of Orthodontics, School of Dentistry, Aarhus University, Vennelyst Boulevard 9, DK-8000 Aarhus, Denmark; e-mail, [email protected]. Submitted, October 2014; revised and accepted, December 2014. 0889-5406/$36.00 Copyright Ó 2015 by the American Association of Orthodontists. http://dx.doi.org/10.1016/j.ajodo.2014.12.026

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teeth vulnerable to root resorption. Already in the 1930s, Schwarz12 proposed that the “optimal” force for tooth movement, characterized by maximal cellular response with maintenance of the vitality of the tissues, should be within the levels of capillary pressure. If the capillary blood pressure is exceeded, this may cause collapse of the capillaries and dysfunction of the blood supply.13 This phenomenon may result in a degradation of the tooth-protecting outer layers of the precementum and its formative layer of cementoblasts; this activates the resorptive activity of the clastic cells. This process leaves the mineralized tooth tissue denuded, triggering inflammatory events, similar to bone resorption, but on the root surface.14,15 Although the severity of OIIRR is mostly clinically insignificant, the literature shows that 1% to 5% of orthodontically treated teeth have severe OIIRR, which is defined as resorption exceeding 4 mm or a third of the original root length.16 A significant reduction in the root length can cause an unfavorable crown-root ratio of the affected teeth. This has great clinical significance, especially when it is coincident with alveolar bone loss or combined with orthodontic retreatment. Apical root loss of 3 mm is equivalent to 1 mm of crestal bone loss, which means that periodontal bone loss will reach a critical stage more rapidly if it is accompanied by OIIRR.17 Regarding orthodontic retreatments, when force is again applied to a tooth with an already traumatized external surface, the onset of resorption will

Roscoe, Meira, and Cattaneo

probably be much more rapid and extensive than that occurring during the primary activation.18 Several reviews,3,16,19-22 systematic reviews,1,23 and a meta-analysis24 have been performed over the years, aiming to elucidate possible treatment-related etiologic factors to guide clinical decisions that will minimize the risks of severe root resorption.23,24 Most authors agree that this biomechanical phenomenon depends on both time and force.5,25-31 The direction of tooth movement32-34 and the loading regimen (continuous vs intermittent forces)31,35-38 also appear to have considerable impact in its occurrence. Yet, until today, no investigators have conducted a systematic review to evaluate the state of the published scientific research on OIIRR, considering the mechanical aspects, the methodologic quality, and the risk of bias. According to the preferred reporting items for systematic reviews and meta-analyses (PRISMA) 2009 checklist, Table I better outlines the questions that will be addressed with reference to participants, interventions, comparisons, outcomes, and study designs (PICOS) in this study. The aims of this systematic review were to assess the scientific literature that has examined root resorption as an outcome of orthodontic treatment and to determine which level of evidence is available to support the association of root resorption with different orthodontic force systems. MATERIAL AND METHODS

This systematic review was performed according to the Cochrane Oral Health Group's Handbook for Systematic Reviews of Interventions (http://ohg.cochrane. org) and was registered with the number CRD42014008912 in the PROSPERO database (http:// www.crd.york.ac.uk/PROSPERO). A computerized systematic search was performed in 3 electronic databases: PubMed, Cochrane, and Embase. For the PubMed and Cochrane databases, we selected the following search sequence of medical subject headings (MeSH) terms: [“orthodontics” AND “root resorption” AND (“biomechanics” or “dental stress analysis”)]. For the Embase database, we selected the following search sequence of Emtree terms: [“orthodontics” AND “tooth root” AND (“biomechanics” OR “dental stress analysis”)]. Hand searches were undertaken to find additional relevant published material that might have been missed in the electronic searches. No restrictions were placed on year, publication status, or language of the articles. The search was performed on December 17, 2013. In the first step of the screening process, titles and abstracts were used to identify full articles concerning the association of root resorption with the mechanical

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aspects of orthodontic treatment with fixed appliances and aligners. The ones that evaluated the risk of root resorption based on genetic factors were not considered relevant for this systematic review. In the second step of the screening process, these full articles were subjected to inclusion and exclusion criteria. The inclusion criteria required the studies to be performed on humans, evaluating root resorption as an outcome of orthodontic treatment, with at least 10 subjects. The exclusion criteria were case reports, case series, reviews, systematic reviews, opinions, studies with questionnaires, and studies where the diagnosis or measurement of OIIRR was performed only on lateral cephalograms or panoramic radiographs. The lowest level of evidence accepted was cohort studies. All studies identified by applying the inclusion and exclusion criteria underwent assessment for validity and data extraction by 2 reviewers (M.G.R. and P.M.C.), who independently examined the studies. The studies that were appropriate to be included were randomized and nonrandomized controlled trials, and cohort studies fulfilling the criteria concerning populations, intervention characteristics, comparison groups, and outcomes as stated in Table I. The reviewers extracted data independently, using specifically designed data-extraction forms. For each included study, qualitative and quantitative information was extracted, including year of publication, experimental and control treatments, numbers and ages of patients, treatment and follow-up durations, method of outcome assessment, authors' conclusions, and all information needed for the methodologic quality evaluation. Any disagreement was discussed to reach a common final decision. If further clarifications were deemed necessary, the authors of the articles were contacted by e-mail. The available literature already includes some scoring systems, which were used as the starting point to develop our methodologic scoring system.24,39-42 Consequently, the remaining articles were scored by the 2 reviewers to analyze study design and conduct, methodologic soundness, and data analysis to answer the research question. This system resulted in the 13 criteria shown in Table II. Concerning study design, time, randomization assignment, control group, sample size, description of the selection criteria for patients, and formulation of the objective of the study were evaluated. Prospective and randomized studies provide the best evidence on the efficacy of health care interventions23; therefore, the time and the randomization process were included in the scoring. The absence of a random assignment could be critical because clinicians with a preconceived notion of what causes root resorption may be biased

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Table I. PICOS format Component Population Intervention Comparison Outcome Study design

Description Clinical studies that involved patients having orthodontic treatment Orthodontic therapy with conventional fixed appliances or aligners 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) OIIRR Randomized and nonrandomized controlled trials, and cohort studies

Table II. Methodologic scoring system Criteria assessed I. Study design (maximum score, 10 points) A. Time B. Randomization C. Control group D. Sample size

Score

Retrospective, 0 point; prospective, 2 points If stated, 1 point If present, 1 point 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 size, the numbers of teeth analyzed in each experimental group were evaluated. Because of the genetic predisposition influence for the onset of OIIRR, large samples were given higher scores to reduce variability.24,43 Importance was given to patient-selection criteria because external factors that might predispose root resorption should be excluded during patient selection. With respect to methodologic soundness, descriptions of appliance types, force magnitudes, radiographic examinations before treatment, and accuracy of the diagnoses and measurement methods of OIIRR were evaluated. Different scores were given if the force magnitude was just stated or controlled by a force measurement device. The radiographic evaluation before the study was also considered in the scoring process because it could detect pretreatment root shortening and eliminate patients who were predisposed to root resorption. The varying degrees of magnification of the radiographs and the limitations of 2-dimensional measurement of a 3-dimensional (3D) phenomenon make light microscopy and plain radiographic methods less accurate than quantitative 3D volumetric evaluations.6,29,44,45 Therefore, these methods were evaluated with lower scores than scanning electron


microscopy (SEM), transmission electron microscopy (TEM), confocal laser scanning microscopy (CLSM), or microcomputed tomography (mCT). Regarding data analysis, we analyzed whether the statistical analysis was appropriate, whether the error of the method was stated, and whether in the data presentation the P value was associated with any measurement of variability, such as confidence interval, range, or standard deviation.42 The methodologic quality scores were reported as percentages of the maximum achievable score (21 points): mean score less than 60% indicates low level of evidence; 60% to 70%, moderate level of evidence; and more than 70%, high level of evidence.41 To account for flaws in design, conduct, analyses, and reporting that might lead to underestimation or overestimation of the true intervention effect (bias), assessments for risk of bias were performed.46 The risk of selection, performance, detection, attrition, and reporting bias of each study was evaluated and classified. Studies were categorized as having a low risk of bias if 4 or more domains were considered adequate, as having a moderate risk of bias if 3 domains were considered adequate, and as having a high risk of bias if 2 or fewer domains were considered adequate.47,48



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

Description Systematic differences between baseline characteristics of the groups that were compared

Relevant domains Sequence generation Allocation concealment

Performance

Blinding of participants and personnel

Detection

Systematic differences between groups in the care that was provided or in exposure to factors other than the interventions of interest Systematic differences between groups in how outcomes were determined

Attrition

Systematic differences between groups in withdrawals from a study

Incomplete outcome data

Reporting

Systematic differences between reported and unreported findings

Selective outcome reporting

Blinding of outcome assessment

The full descriptions of the bias classifications are presented in Table III. The risk of bias across the studies was also assessed. Studies conducted by the same research group were compared to check for similarity between patient characteristics (sex, age, number, and so on). If we detected bias across the studies that might have affected the cumulative evidence, the authors were contacted to clarify or confirm the risk of bias.

score, with a mean score of 72%. Thirteen studies were classified as high (62%), 5 as moderate (24%), and 3 as low (14%) levels of evidence. Eleven studies were considered to have a low risk of bias (52%), 2 had a moderate risk of bias (10%), and 8 were classified as having a high risk of bias (38%). It was not possible to perform a meta-analysis because of the heterogeneous methodologies of these studies.

RESULTS

DISCUSSION

The database search showed 128 articles listed in PubMed, 115 articles in Embase, and 16 articles in Cochrane. Four articles were added after hand searches of the bibliographies of the selected articles and relevant reviews. By using the PRISMA flow diagram, an overview of the article selection process is illustrated (Fig).49 After exclusion of 26 duplicate articles, 237 articles remained. In the first step of the screening process, a further 112 articles were excluded because they were determined to be irrelevant based on the titles and abstracts. In the second step of the screening process, the remaining 125 full-text articles were assessed: 52 articles were excluded because they did not meet the inclusion criteria, and 52 articles were excluded after the application of the exclusion criteria (Fig). Thus, the selection process resulted in 21 full-text articles.5,28-30,37,38,50-64 A summary of the main findings and the data regarding participants, interventions, comparisons, outcomes, study designs (PICOS), and follow-up periods of each study in this systematic review is presented in Table IV. The assessment of the risk of bias across the studies showed that 2 articles were conducted on the same sample of patients (confirmed by e-mail communication from their authors); therefore, these 2 studies were treated as one, and the results were combined.28,29 Most studies (90%) were clinical trials, except for 2 historic cohorts. All articles were published in English between 1982 and 2012. Detailed assessments of the methodologic quality and the risk of bias are shown in Tables V through VIII. Methodologic quality scores ranged from 48% to 86% of the maximum achievable

In spite of many studies investigating the association of root resorption with the mechanical factors of orthodontic treatment, only 21 were considered appropriate for inclusion in this systematic review. An overall quantitative conclusion could not be made because of the heterogeneity of the study designs and their treatment modalities. Moreover, it was not considered relevant to perform a meta-analysis because most studies characterized by similar study designs and methodologies were performed by the same research groups. A metaanalysis with these premises will result in a biased conclusion. Therefore, we preferred to include more studies and perform a qualitative synthesis. Relative to study designs included in this systematic review, 11 studies were randomized controlled trials, 8 were nonrandomized controlled trials, and 2 were historic cohorts. The greatest advantage of randomized controlled trials compared with nonrandomized controlled trials and cohort studies is the random allocation process; nevertheless, cohort studies present the possibility to evaluate large groups of subjects and follow them for longer periods than do randomized controlled trials.65 These 2 aspects are highly desirable in studying OIIRR and therefore justified the inclusion of the 2 cohort studies in this review. Referring to the methodologic quality assessment, the scores ranged from 48% to 86%, with a mean score of 72%, which corresponds to a high evidence level. Studies that performed measurements or diagnoses of OIIRR using only panoramic radiographs or lateral cephalograms were excluded; this certainly contributed to




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

achieving this high score. The reason behind this choice was based on the inherent distortion and magnification problems when measuring the root apex because of superimposition of the incisors on lateral cephalograms,24 and distortion of tooth positions and inclinations on panoramic radiographs.66 These limitations may lead to inaccuracies in OIIRR diagnosis and measurements. Seventeen of the 21 selected studies were performed on premolars (12 evaluated only maxillary premolars5,30,38,50-58; 5 evaluated both maxillary and mandibular premolars28,29,37,59,60). All studies classified as having a high evidence level were performed on premolars. Although they are not the teeth most affected by root resorption, they are the most frequently extracted teeth during orthodontic treatment, often bilaterally. This make it possible to perform randomized controlled trials with a splitmouth design, where detailed information about root resorption can be acquired after tooth extractions using methods of diagnostic such as SEM, TEM, CLSM, and


mCT. In the 4 studies performed on incisors, a high risk of bias was detected.61-64 Moreover, although the theoretical maximum achievable score relative to methodologic soundness is 7, for these studies the actual maximum was 6, since it is not realistic to extract these teeth and apply the most reliable methods of diagnosis (ie, SEM, TEM, CLSM, and mCT). This underlines the limitation of studies on OIIRR when extractions cannot be performed. A significant number of studies did not include a control group, did not clearly describe the selection criteria of patients, or did not perform an adequate radiographic examination before the intervention. In studying OIIRR, comparison of the experimental group with the control group is strongly recommended because it will help to show the actual effect of treatment on root resorption. Yet, 57% of the studies did not include a control group. For ethical and economic reasons, most studies had small samples of patients. Consequently, the authors preferred to include and compare 2 experimental groups, at the


Study Harris et al5 (2006)

Participants Interventions 54 maxillary first PM from Orthodontic therapy with 27 patients (12 M, fixed appliances 15 F); ages, 11.9-19.3 y; (segmented technique) mean, 15.6 y

Study Comparisons Outcomes design RCT, Force levels: low (25 g) vs - Volumetric measurements of the SMD heavy (225 g) vs control (0 g) amount of RR after intrusion forces. - Establishment of the sites where RR is more prevalent.

Follow-up 4 wk

RCT, Force levels: low (25 g) vs - Volumetric SMD heavy (225 g) vs control measurements of the (0 g) extent of RR craters after buccal tipping forces. - Establishment of the sites where RR is more prevalent.

4 wk

54 maxillary first PM from Orthodontic therapy with 27 patients (12 M, fixed appliances (segmented technique) 15 F); ages, 12.5-20 y; mean, 15.3 y and aligners

RCT, Force levels and systems: - Volumetric SMD conventional low (25 g) measurements of the vs conventional heavy amount of RR after (225 g) vs aligner vs buccal tipping forces. control (0 g) - Establishment of the sites where RR is more prevalent.

8 wk

Barbagallo et al30 (2008)

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Chan and Darendeliler28,29 36 maxillary and Orthodontic therapy with (2005, 2006) mandibular PM from 16 fixed appliances patients (10 M, 6 F); (segmented technique) ages, 11.7-16.1 y; mean, 13.9 y

Main findings The 3 force level groups were significantly different. Mean volumes of RR in the light and heavy force groups were about 2 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. More RR in the heavy force group compared with the light and control groups. Although more RR was recorded in the light force group, no statistically significant difference was found between the light and control groups. Buccocervical and lingual-apical surfaces had more RR than the other regions. More RR in the heavy force group compared with the aligner, light, and control groups. The aligner group had similar effects on root cementum as did the light group. More RR was observed was at the buccocervical and lingual-apical regions in all treated teeth.



Table IV. PICOS, follow-up period, and main findings of the studies

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Table IV. Continued Study Outcomes design - Comparison of the NR-CT, effects of stainless SMD steel and superelastic archwires on TM and RR after buccal tipping force.

Participants Interventions 90 maxillary and Orthodontic therapy with mandibular PM from 27 fixed appliances patients (10 M, 17 F); (segmented technique) ages, 10.2-14.5 y; mean, 12.5 y

Comparisons Loading regimen: continuous vs intermittent vs control

Owman-Moll et al38 (1995)

32 maxillary first PM, from Orthodontic therapy with 16 patients (8 F, 8 M); fixed appliances ages 11.8-15.8 y; mean, (segmented technique) 13.9 y

Loading regimen and - Effects of continuous NR-CT, treatment times: and interrupted buccal SMD continuous vs tipping force of the interrupted forces, same magnitude applied for 4 or 7 weeks (50 g), applied for 4 or 7 weeks on the RR occurrence.

4 or 7 wk

Bartley et al50 (2011)

30 maxillary first PM from Orthodontic therapy with 15 patients (7 M, 8 F); fixed appliances ages, 12.75-16.83 y; (segmented technique) mean, 14.3 y

Force system: 2.5 vs 15 of buccal root torque

4 wk

- Volumetric measurements of the amount of RR after buccal root torque.

RCT, SMD

Follow-up 12 wk

Main findings The teeth with the superelastic wire moved significantly more and tipped buccally to a greater degree than 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 resorptions were mainly located on the buccal side, and the apical resorptions on the palatal or lingual side. Areas of RR were found on all experimental teeth. No significant difference of resorption was found between the 2 force systems. No statistically significant differences in RR after the application of either 2.5 or 15 of buccal root torque. More RR at the apical region than at the middle and cervical regions.



Study Weiland37 (2003)

Study

Participants 51

Wu et al

(2011)

King et al52 (2011)

Interventions

Outcomes

Study design

Follow-up

RCT, Force levels: low (25 g) vs - Measurement and SMD heavy (225 g) comparison of the locations, dimensions, and volumes of RR craters after rotational force.

4 wk

30 maxillary first PM from Orthodontic therapy with fixed appliances 15 patients (4 M, 11 F); ages, 12.8-16.11 y; (segmented technique) mean, 14.2 y

Force system: 2.5 vs 15 of distal root tipping

RCT, - Volumetric SMD measurements of the amount of RR after distal root tipping force. - Establishment of the sites where RR is more prevalent.

4 wk

Force levels: low (25 g) vs - Volumetric RCT, heavy (225 g) measurements of the SMD amount of RR after extrusion force. - Establishment of the sites where RR is more prevalent.

4 wk

Force levels: low (25 g) vs - Volumetric heavy (225 g) vs control measurement of RR (0 g) craters after buccal tipping force.

4 wk

20 maxillary first PM from Orthodontic therapy with 10 patients fixed appliances (segmented technique)

RCT, SMD

Main findings More RR in the heavy force group than in the light force group. Greater RR in the compression areas (buccodistal and lingual-mesial surfaces) than in other areas at all levels of the root. Greater RR in teeth that had undergone greater distal root tip bends. Compression of the periodontal ligament caused more RR than tension, which was more pronounced in the apical and cervical thirds of the teeth. Greater RR after heavy forces when compared with light forces. The distal surfaces were more affected than other root surfaces. No significant difference between the cervical, middle, and apical thirds in relation to RR. More RR in the heavy force group than in the light and control groups.

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30 maxillary first PM from Orthodontic therapy with 15 patients (5 M, 10 F); fixed appliances ages, 11.9-16.9 y; (segmented technique) mean, 14.15 y

Montenegro et al53 (2012) 20 maxillary first PM from Orthodontic therapy with 10 patients (3 M, 7 F); fixed appliances ages, 12-18 y; mean not (segmented technique) mentioned

Chan et al54 (2004)

Comparisons



Table IV. Continued

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Table IV. Continued Study Kurol et al

Participants 55

(1996)

Casa et al56 (2006)

Interventions

Comparisons

Outcomes

Study design

Follow-up

Force levels and treatment - Effect of orthodontic NR-CT, SMD times: 50 g applied for 1 force (buccal tipping) to 7 wk vs 0 g (control) and treatment time in RR occurrence and severity. - Comparison of histologic with radiographic findings in detecting RR.

1-7 wk

28 maxillary first PM from Orthodontic therapy with 14 patients; ages, 13fixed appliances 16 y (segmented technique)

Treatment times: 1, 2, 3, or - Appearance and 4 wk vs control distribution of clastic cells during the application of continuous torque over several time periods.

NR-CT, SMD

1-4 wk

Force levels and treatment - Volumetric times: low (25 g) vs measurement of heavy (225 g), applied resorption craters, for 4, 8, or 12 wk after buccal tipping force.

NR-CT, SMD

4, 8, or 12 wk

Paetyangkul et al57 (2011) 54 maxillary first PM from Orthodontic therapy with 36 patients (21 F, fixed appliances 15 M); mean age, 14.9 y (segmented technique)

More than 6 times the RR in all test groups compared with the control group. The RR was mainly located in the apical third of the root. The number of teeth with RR increased with time of force application. The PR failed to show any RR occurrence. Resorption lacunae and clastic cells increased in extent and number with the duration of the force and were found on the cementum surface at the pressure areas. Some signs of cementum repair were also noticed, even with maintenance of the force level. Less RR in the light force group than in the heavy force group. Increased RR from 8-12 weeks of force application with either light or heavy orthodontic forces.



112 maxillary PM from 56 Orthodontic therapy with patients (18 M, 38 F); fixed appliances ages, 10.5-17.5 y; (segmented technique) mean, 13.8 y

Main findings

Study Aras et al58 (2012)

Participants 64 maxillary PM from 32 patients (25 F, 7 M); ages, 12-18 y; mean age, 14.4 y

Interventions Orthodontic therapy with fixed appliances (segmented technique)

Harry and Sims59 (1982)

36 maxillary and Orthodontic therapy with mandibular first PM fixed appliances from 10 patients; ages, (segmented technique) 11-18 y

Study Comparisons Outcomes design RCT, Force system: continuous - Effects of 2 reactivation periods of SMD vs intermittent force, 2 or 3 weekly controlled intermittent reactivations and continuous buccal tipping forces (150 g) on RR and TM.

NR-CT, Force levels and time - Effects of different SMD intervals: 50 g vs 100 g magnitudes and vs 200 g. Intervals of 14, durations of intrusive 35, and 70 d. orthodontic forces on the topography of root surfaces. - Establishment of the sites where RR is more prevalent.

619


Main findings Group of continuous force produced faster TM than intermittent force group. Statistically significant differences 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. 14, 35, and 70 d Surface defects identified with the SEM or macroscopically were not identified on PR. Intrusive forces produced an increase in RR compared with the control teeth. The amount of RR increased with the duration of the force, and to a lesser extent with the magnitude of the activation. More RR was observed at the buccocervical root surfaces and apical thirds of the roots. Follow-up 12 wk



Table IV. Continued

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Table IV. Continued Study design RCT, SMD

Comparisons Outcomes Force levels: low (25 g) vs - Volumetric heavy (225 g) measurement of RR craters after buccal tipping force. - Identification of the sites that might be predisposed to resorption.

Ramanathan and Hofman61 (2009)

49 patients (20 M, 29 F); ages, 9-30.1 y; mean 14.5 y

Appliance types: basal arch vs 3-component arch vs leveling with SWA.

Baumrind et al62 (1996)

Radiographic records of 73 Orthodontic therapy with patients (16 M, 57 F); fixed appliances age, at least 20 y, (edgewise appliance). diagnosed with Class I or II malocclusion

Maxillary central apical - Relationship between incisor displacement vs incisor apical ARR displacement* and ARR.

Historic Variable (1-7 y) cohort

McFadden et al63 (1989)

Radiographic records from Orthodontic therapy with 38 patients; mean age, fixed appliances 13.1 6 1.4 y (bioprogressive technique).

Intrusion vs root shortening

- Relationship between incisor intrusion and root shortening.

Historic 28.8 6 7.4 mo cohort

Deguchi et al64 (2008)

18 patients (2 M, 16 F); Orthodontic therapy with mean ages, 20.7 6 2.5 y fixed appliances (J-hook headgear (edgewise appliance) group) and 21.5 6 3.7 y (implant group)

Appliance types: implant vs J-hook headgear

- Comparison of the NR-CT effects of incisor intrusion, force vector, and amount of RR between implant orthodontics and J-hook headgear.

Orthodontic therapy with fixed appliances (segmented technique and SWA)

- Comparison of the NR-CT extent of RR during different orthodontic TM with 3 techniques.

Follow-up 12 wk

6 mo

7 mo

Main findings Less RR in the light force group than in the heavy force group in both maxillary and mandibular PM. RR greater toward the cervical region on the buccal surfaces and the apical regions on the lingual surfaces. No statistically significant difference in RR among the 3 groups. Association of orthodontic intervention with maxillary incisor RR, even when the position of the tooth was the same on the cephalograms. More RR for retraction displacement than displacements in other directions. Degree of root shortening greater in the maxilla (1.84 mm) than in the mandible (0.61 mm). The most significant factor for occurrence of root shortening was the treatment time. Significantly more RR in the J-hook headgear group than in the implant group after intrusion of the maxillary incisors.

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, straightwire appliance; PR, peripapical radiograph; ARR, apical root resorption. *Directions: retraction, advancement, intrusion, and extrusion.



Study Participants Interventions Paetyangkul et al60 (2009) 40 maxillary and Orthodontic therapy with mandibular first PM fixed appliances from 10 patients (6 F, (segmented technique) 4 M); ages, 12.7-18.2 y; mean age, 14.3 y


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Table V. Study design (maximum score, 10 points) Article Harris et al5 (2006) Chan and Darendeliler28,29 (2005, 2006) Barbagallo et al30 (2008) Weiland37 (2003) Owman-Moll et al38 (1995) Bartley et al50 (2011) Wu et al51 (2011) King et al52 (2011) Montenegro et al53 (2012) Chan et al54 (2004) Kurol et al55 (1996) Casa et al56 (2006) Paetyangkul et al57 (2011) Aras et al58 (2012) Harry and Sims59 (1982) Paetyangkul et al60 (2009) Ramanathan and Hofman61 (2009) Baumrind et al62 (1996) McFadden et al63 (1989) Deguchi et al64 (2008)

Time 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 0 0 2

Randomization 1 1 1 0 0 1 1 1 1 1 0 0 0 1 0 1 0 0 0 0

Control group 1 1 1 1 0 0 0 0 0 1 1 1 0 0 1 0 0 0 0 0

Sample size 3 2 2 4 2 3 3 3 2 2 2 1 2 3 1 3 3 4 4 2

Selection criteria 1 1 1 0 0 1 1 1 1 0 0 0 1 1 0 1 1 1 1 0

Objective 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

Score 9 8 8 8 5 8 8 8 7 7 6 5 6 8 5 8 7 6 6 5

Measurement method of RR 2 2 2 2 2 2 2 2 2 2 2 3 2 2 3 2 1 1 1 1

Score 5 6 4 4 6 4 6 4 6 5 6 5 5 5 7 5 4 3 3 5

Table VI. Methodological soundness (maximum score, 7 points) Article Harris et al5 (2006) Chan and Darendeliler28,29 (2005, 2006) Barbagallo et al30 (2008) Weiland37 (2003) Owman-Moll et al38 (1995) Bartley et al50 (2011) Wu et al51 (2011) King et al52 (2011) Montenegro et al53 (2012) Chan et al54 (2004) Kurol et al55 (1996) Casa et al56 (2006) Paetyangkul et al57 (2011) Aras et al58 (2012) Harry and Sims59 (1982) Paetyangkul et al60 (2009) Ramanathan and Hofman61 (2009) Baumrind et al62 (1996) McFadden et al63 (1989) Deguchi et al64 (2008)

Appliance type 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

Force magnitude 2 2 1 1 2 1 2 1 2 1 2 1 2 2 2 2 1 0 0 2

Radiographic exam BT 0 1 0 0 1 0 1 0 1 1 1 0 0 0 1 0 1 1 1 1

Exam BT, Examination before treatment; RR, root resorption.

expense of including a control group. Nine studies did not report the sample size calculation; the numbers of patients varied from 10 to 73, with 4 studies including only 10 patients. To better score the studies, the numbers of teeth included in each experimental group were considered as well. In the prospective studies, this number varied from 4 to 42 teeth per group (mean, 12 teeth). Regarding the 2 retrospective studies, one evaluated 73 teeth62 and the other 38 teeth.63 The absence of strict

selection criteria and radiographic examinations before the interventions are also critical factors. During a random selection with no previous radiographic analysis, the risk of including patients with signs of previous root resorption or predisposing factors cannot be avoided.67,68 Thirty-three percent of the studies did not clearly describe the selection criteria of the patients, and 43% did not perform appropriate radiographic examinations before the interventions.




622

Table VII. Data analysis (maximum score, 4 points)

Article Harris et al5 (2006) Chan and Darendeliler28,29 (2005, 2006) Barbagallo et al30 (2008) Weiland37 (2003) Owman-Moll et al38 (1995) Bartley et al50 (2011) Wu et al51 (2011) King et al52 (2011) Montenegro et al53 (2012) Chan et al54 (2004) Kurol et al55 (1996) Casa et al56 (2006) Paetyangkul et al57 (2011) Aras et al58 (2012) Harry and Sims59 (1982) Paetyangkul et al60 (2009) Ramanathan and Hofman61 (2009) Baumrind et al62 (1996) McFadden et al63 (1989) Deguchi et al64 (2008)

Error Statistical of the Data analysis method presentation Score 1 1 1 3 1 1 2 4 1 1 1

1 1 0

2 2 2

4 4 3

1 1 1 1 1 1 0 1 1 0 1 1

1 1 1 1 1 0 0 1 1 0 1 0

2 2 2 2 1 1 0 2 2 0 2 2

4 4 4 4 3 2 0 4 4 0 4 3

1 1 1

1 1 1

2 1 2

4 3 4

Although most articles were classified as having a high evidence level, at least 1 type of bias was present in all the studies. For example, for evident reasons, the orthodontists who performed the treatments could not be blinded. On the other hand, the majority of the studies (62%) did not have detection bias. Ten studies had selection bias because the allocation process was not random. Two studies were designed as historic cohorts,62,63 and 8 as nonrandomized controlled trials.37,38,55-57,59,61,64 In the remaining studies, although not clearly stated in the text, on direct request, the randomization process was confirmed by the authors.5,28-30,50-54,58,60 No study had reporting bias, and 1 had attrition bias because the reason for the exclusion of some patients was not reported.62 Twelve split-mouth studies evaluated the influence of the force level on OIIRR in premolars: except for 1 study by Harry and Sims,59 the remaining studies were performed by the same research group. They compared orthodontic light force (25 g) with heavy force (225 g),5,28-30,51,53,54,57,60 light torque (2.5 ) with heavy torque (15 ),50 or light distal tipping (2.5 ) with heavy distal tipping (15 ).52 Buccal tipping was the most studied,28-30,54,57,60 followed by intrusion.5,59 Except for the study by Bartley et al,50 all studies presented a positive correlation between heavy forces and increased root resorption. The influence of appliance designs (conventional fixed appliances and removable


aligners) on root resorption severity was also evaluated: similar results were found between patients treated with aligners and those treated with conventional fixed appliances activated with light forces.30 Still, comparing these results should be done with some caution. First, removable aligners do not apply a continuous, constant force to teeth as fixed appliances do, and it is difficult to control the force level applied. Second, the amount of movement is highly variable and depends on how many hours the patients wore the removable appliances; since it was not possible to determine this, it was not reported.30 The influence of loading regimen (continuous vs intermittent forces) was assessed in 2 articles, and the results are contradictory. Owman-Moll et al38 did not find a significant difference between the 2 systems on root resorption. However, Weiland37 reported significant differences in OIIRR between stainless steel and superelastic archwire systems. These conflicting results might be related to the methods used to study root resorption. Owman-Moll et al only analyzed selected areas using light microscopy, whereas Weiland analyzed root resorption by CLSM, thus enabling a 3D analysis. In support of Weiland's findings, some studies suggest that a pause in tooth movement may allow the resorbed cementum to heal.35,58,69 The influence of treatment time on OIIRR was also assessed. It seems that a positive correlation exists between increased treatment time and increased root resorption. Kurol et al55 showed that starting from the third week, the depth of resorption lacunae increased significantly. Casa et al56 also observed that the severity increased from 1 to 4 weeks of force application. Despite this evidence showing that root resorption depends on time, for 8 of the 10 randomized controlled trials in this systematic review, the maximum period of intervention was only 4 weeks.5,28,29,50-54 The authors justified this choice based on ethical reasons and clinical practicality. When 3 experimental periods were compared (4, 8, and 12 weeks), it was shown that the amount of root resorption increased significantly when 12 weeks of force application was reached. This might be related to the increased osteoclastic activity seen after 8 weeks of force application.57 For future studies, the time factor should be considered. With respect to the location of OIIRR, this seems to be highly dependent on the type of orthodontic movement; yet, after attentive analysis of the loading regimen, it seems that “high-pressure” zones were more susceptible to resorption than “high-tensile” zones. For instance, buccal tipping was associated with resorption mostly on the buccocervical and lingual-apical regions28-30,37; buccal root torque with buccal-apical and palatalcervical regions50; rotation around the long axis of the



623

Table VIII. Evidence level and risk of bias classification Article Harris et al5 (2006) Chan and Darendeliler28,29 (2005, 2006)* Barbagallo et al30 (2008) Weiland37 (2003) Owman-Moll et al38 (1995) Bartley et al50 (2011) Wu et al51 (2011) King et al52 (2011) Montenegro et al53 (2012) Chan et al54 (2004) Kurol et al55 (1996) Casa et al56 (2006) Paetyangkul et al57 (2011) Aras et al58 (2012) Harry and Sims59 (1982) Paetyangkul et al60 (2009) Ramanathan and Hofman61 (2009) Baumrind et al62 (1996) McFadden et al63 (1989) Deguchi et al64 (2008)

Total score and percent 17 (81%) 18 (86%)

Evidence level High High

Selection bias No No

Performance bias Yes Yes

Detection bias No No

Attrition bias No No

Reporting bias No No

Risk of bias Low Low

16 (76%) 16 (76%) 14 (67%) 16 (76%) 18 (86%) 16 (76%) 17 (81%) 15 (71%) 14 (67%) 10 (48%) 15 (71%) 17 (81%) 12 (57%) 17 (81%) 14 (67%) 13 (62%) 12 (57%) 14 (67%)

High High Moderate High High High High High Moderate Low High High Low High Moderate Moderate Low Moderate

No Yes Yes No No No No No Yes Yes Yes No Yes No Yes Yes Yes Yes

Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes

No Yes Yes No No No No No Yes No No No Yes No Yes Yes Yes Yes

No No No No No No No No No No No No No No No Yes No No

No No No No No No No No No No No No No No No No No No

Low High High Low Low Low Low Low High Moderate Moderate Low High Low High High High High

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

tooth with resorption at the boundaries between the buccal and distal surfaces and between the lingual and mesial surfaces51; distal root tipping with more resorption on the distal aspects in the apical and middle thirds and on the mesial aspects in the cervical thirds52; and extrusion movement with more resorption on the distal surfaces.53 Regarding intrusion, the results were not unanimous. In 1 study, more resorption was reported on the mesial and distal surfaces and at the apical thirds of the roots,5 whereas in another study, more resorption was seen at the buccocervical root surfaces and at the apical thirds of the roots.59 The last issue draws the attention to the methods used to assess OIIRR because these seem to influence the detection and amount of OIIRR. For example, in 4 studies evaluating the amount of OIIRR on incisors using periapical radiographs, only apical root resorptions and the extent of root shortening could be detected.61-64 When we looked at the findings of 3 studies comparing the results of assessing OIIRR with either periapical radiographs with SEM59 or periapical radiographs with histologic analysis,38,55 it is clear that periapical radiographs failed to show the real extent of resorption. On the other hand, SEM and histologic analysis cannot be used in a clinical setting because they require tooth extractions. To overcome this problem, some authors suggested that it would be beneficial to use cone-beam computed tomography.70-72 It allows for improved image quality and 3D reconstructions, giving more reliable

measurements.73 Still, no study included in this systematic review used cone-beam computed tomography. To improve the evidence level in OIIRR research, it is suggested that future studies should include control groups, define strict patient inclusion and exclusion selection criteria, and evaluate radiographic material before the interventions. The intended clinical findings should be clearly stated before the start of the investigation, and tests for determining the right sample size, which allows for statistically and clinically significant results, should be performed (adequate power analysis). Proper randomization protocols and blinding of both intervention (when possible) and results assessment must be considered to reduce the risk of bias. From this review, randomized controlled trials when premolars (to be extracted) are studied for OIIRR seem to be the most appropriate design. CONCLUSIONS

1. A high level of evidence is available to support the association of root resorption with orthodontic treatment. 2. 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 times and increased root resorption.




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3. A pause in tooth movement seems to be beneficial in reducing root resorption because it allows the resorbed cementum to heal. 4. The absence of a control group, the selection criteria of patients, and adequate examinations before and after treatment are the most common methodology flaws in studies of OIIRR.

14. 15.

16. 17.

ACKNOWLEDGMENTS

We thank Michel Dalstra for the constructive discussion during the elaboration of the project; Janne Lytoft Simonsen, research librarian of Aarhus University, for help during the computerized searches of the databases; Ali Darendeliler and Victor Arana, who were contacted for clarifications, for answering our questions; and the Brazilian research funding agencies CAPES and CNPq for the grant BEX 2079-13-5.

18.

19.

20.

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