The clinical benefits of orthodontic treatment to pathologically migrated teeth: A systematic review

184 © Australian Society of Orthodontists Inc. 2019 Introduction: The present systematic review aimed to assess the evidence related to the periodontal benefits of orthodontic treatment of pathologically migrated teeth in combination with periodontal therapy with or without a regenerative procedure. Methods: Electronic databases (PubMed, Embase and Cochrane) were searched up to March 21, 2019. Selection criteria included human studies in which pathologically migrated maxillary teeth were repositioned with orthodontic fixed appliances after periodontal therapy. Clinical trials not reporting a quantitative measurement of clinical attachment gain were excluded. Results: The search strategy identified 90 relevant articles. After selection according to the inclusion/exclusion criteria, 15 articles qualified for the final analysis of which five were clinical trials and 10 were case series or reports. Five studies could be classified as providing a moderate level of evidence (33%), while 10 were classified as low levels of evidence (67%). None of the studies were classified as providing a high-level of evidence, Conclusions: Based on the limited available evidence, orthodontic treatment had a fundamental role in the resolution of anterior pathologic tooth migration. Gains were seen in clinical attachment levels with accompanying improved aesthetic and functional final results. However, it was not possible to make any recommendations regarding the use of a specific regenerative procedure to improve the clinical results obtained by a combination of periodontal and orthodontic therapies. The most recurrent sources of bias were the absence of a control group and limited adequate examinations before and after treatment. (Aust Orthod J 2019; 35: 184-194)


Introduction
Pathologic tooth migration (PTM) is defined as tooth displacement resulting from the disruption of forces that maintain teeth in a normal position with reference to the underlying skeleton. 1 The prevalence of PTM is high in periodontal patients, ranging from 30% to 56%. 2 Because of its significant negative impact with regard to a patient's self-esteem, a malocclusion generated from PTM is often the main motivation for adult patients to seek periodontal and orthodontic therapy. 2 Progressive spacing of the incisors is the most evident sign of a pathological change in the position of the teeth, and the minor spacing (< 1 mm) in the anterior teeth that sometimes occurs in the acute periodontal stages can be partially or completely reversed after conventional or surgical periodontal therapy. 3 However, moderate and severe cases require orthodontic intervention not only to correct, but also to prevent the aggravation of the PTM. It is well known that occlusal trauma and periodontitis can be mutually exacerbated in PTM, resulting in greater loss of attachment, extrusion, and mobility of the displaced teeth. 4 The control of intrusion and torque during anterior tooth retraction and intrusion are the major concerns during orthodontic correction of PTM. 5,6 Although TREATMENT OF PATHOLOGIC TOOTH MIGRATION these procedures are considered normal and not challenging when performed on teeth without severe alveolar bone loss, they can be a challenge when dealing with periodontally compromised dentitions. 6,7 A proper sequence of treatment planning when dealing with a periodontally compromised dentition should always be preceded by periodontal therapy, as the risk of periodontal breakdown when dental plaque control and periodontal health are not adequate is much higher. 6 Special attention should be given to the presence of angular bony defects, since these defects present a significantly higher risk of additional bone and tooth loss when compared with horizontal bone defects. 8 The possible clinical benefits of orthodontic treatment in the management of infrabony defects are still a matter of debate. Although several clinical trials 5,[9][10][11][12][13][14][15][16] and reviews 6,17,18 have been performed to investigate the effects of orthodontic treatment on periodontal defects, there are still unanswered questions related to the biomechanical aspects of moving a tooth with a reduced periodontium. In addition, the optimal timing of orthodontic treatment after periodontal therapy is unknown, as is the advantage of adding regenerative procedures during therapy.

Objectives
The aim of the present systematic review was to evaluate the published scientific research on orthodontic movement to correct pathologic tooth migration by considering the clinical and radiographic findings, the biomechanical aspects, the methodologic quality, and the risk of bias. The focused question was: "What are the clinical benefits of orthodontic treatment in the correction of pathologically migrated teeth?" The possible advantage of adding a regenerative procedure during periodontal therapy was also investigated, as well as the optimal timing of orthodontic treatment after therapy. 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 (PICO) in this study.

Protocol and registration
This systematic review was prepared according to the Cochrane Oral Health Group's Handbook for Systematic Reviews of Interventions (http://ohg. cochrane.org) and was registered with the number CRD42015027068 in the PROSPERO database (http://www.crd.york.ac.uk/PROSPERO).

Eligibility criteria
Two reviewers independently screened titles and abstracts for eligible papers. Subsequently, full-text papers that fulfilled the eligibility criteria were identified and included for assessment. The inclusion criteria required the studies to be in English, conducted on humans, and evaluating orthodontic intrusion using fixed appliances to correct pathologic tooth migration of maxillary anterior teeth. The results should have been evaluated by clinical quantitative measurements and by radiographic exams before and after treatment. The exclusion criteria were reviews, studies on suprabony defects, studies on furcation defects, studies on posterior teeth and studies on implants or prosthetic treatment.
No study mentioned the term 'aggressive' in the case reports. Considering that aggressive periodontitis, in its local and generalised form, is usually associated with first molars and incisors, and normally occurs at the age of puberty, it was considered that the studies included in the present review described chronic periodontitis. The primary outcome measure was the gain in clinical attachment level, because it is a highly sensitive diagnostic tool and it is the primary outcome variable used in studies of periodontal patients. 19 The secondary outcomes included changes in probing depth and in alveolar bone area.

Information sources, search strategy, and study selection
Computerised and manual searches were performed in three electronic databases: PubMed, Cochrane, and Embase. The databases were searched for studies conducted in the period up to and including March 21, 2019. The structured search strategy was designed to include any published paper that evaluated the clinical effects of orthodontic intrusion on patients with pathologic tooth migration and/or infra-bony defects. The electronic search strategy included the following terms and combinations: (orthodontics OR orthodontic) AND ((Pathologic tooth migration) OR "angular defect" OR "angular defects" OR "Infrabony defect" OR "Infrabony defects" OR "Infra-bony defect" OR "Infra-bony defects" OR "Intrabony defect" OR "Intrabony defects" OR "Intra-bony defect" OR "Intra-bony defects" OR "Infraosseous defect" OR "Infraosseous defects" OR "Intraosseous defect" OR "Intraosseous defects").

Data items and collection
The reviewers extracted data independently, using specifically designed data-extraction forms. For each included study, qualitative and quantitative information was extracted, including the year of publication, the numbers and ages of patients, treatment types and durations, method of outcome assessment, the authors' conclusions, and all information needed for the methodologic quality evaluation. Any disagreement was discussed to reach a common final decision.
Considering the lack of randomised clinical trials and the small number of clinical trials evaluating the benefits of orthodontic treatment related to PTM, case series and case reports were also included in this review.

Risk of bias/quality assessment in individual studies
The methodologic scoring system was based on a previous systematic review 20 and on a methods guide for assessing the risk of bias of individual studies in systematic reviews, 21 which are described in Table  II. The methodologic quality scores were reported as percentages of the maximum achievable score (19 points for clinical studies and 17 points for case reports or series). A mean score less than 60% indicated a low level of evidence; 60% to 70%, a moderate level of evidence; and more than 70%, a high level of evidence. The scoring system was adapted to include the evaluation of case series and case reports in a way that the scores were based on each study design. When some topics could not be reported due to an inherent limitation of that type of study (for example: the use of control group and statistical analysis in a case series or case report), that topic was marked as not applicable. This approach allowed a fair quality assessment when case reports are included in a Systematic Review. 21 The assessments for risk of bias were also performed, including an evaluation of the risk of selection, detection, attrition, and reporting biases for each study. As case reports were included in the present study, and as no RCTs were available, performance bias was not evaluated. Studies were categorised as having a low risk of bias if three or more domains were considered adequate, as having a moderate risk of bias if two domains were considered adequate, and as having a high risk of bias if only one domain was considered adequate.

Results
A total of 90 articles were identified by the electronic and manual search. The PRISMA flow diagram 22 reports the overview of the article's selection process ( Figure 1). In the first step of the screening process, 45 articles were excluded because they were determined to be irrelevant based on their titles and/or abstracts. The remaining 45 full-text articles were re-assessed, of which 24 articles were excluded because of failure to meet the inclusion criteria, and four articles were excluded after the application of the exclusion criteria.
After the selection process, 17 full-text articles were included. By careful reading and comparison of the authors' name and the sample studied, it was found that the same sample of patients was repeated in two articles. This was confirmed by an email from the authors of these studies. Therefore, in both cases the two articles were treated as one article and consequently the results were combined. The final number of studies included in this review was 15 ( Figure 1).
A summary of the main findings and data of the selected studies is reported in Table III (studies on orthodontic treatment and periodontal therapy without a regenerative procedure) and Table IV (studies on orthodontic treatment and periodontal therapy with a regenerative procedure). Detailed assessments of the methodologic quality and the risk of bias are reported in Tables V through VIII.

Discussion
The present discussion is divided into two main topics, describing firstly the mechanical and temporal aspects of orthodontic treatment and, secondly, the benefits of regenerative procedures during periodontal therapy.
The intrusion and retraction of the incisors is usually the logical solution to correct anterior pathologically migrated teeth, in relation to causative, aesthetic, and functional perspectives. 5,6 However, orthodontists need to be aware of the altered biomechanical conditions when dealing with periodontally compromised dentitions. Firstly, the centre of resistance in periodontally reduced teeth moves to a more apical position as progressive alveolar bone loss occurs. This requires specific adjustments in the torque-force ratio in order to avoid a larger moment and an uncontrolled tooth displacement during force application. 7 Secondly, the reduced bone levels and the smaller periodontal ligament volumes will cause the orthodontic forces to be distributed over a smaller surface area. 23 The increased loads could, therefore, give rise to greater bone loss. Thirdly, the increased loads may also cause or accelerate root resorption.
Considering that excessive forces represent one of the main treatment-related aetiologic factors of root resorption, 20 the control of force levels has clinical significance in patients with alveolar bone loss. The present review has focused on a study of orthodontic intrusion, because this movement is usually associated with an increased risk of root resorption, independently of the orthodontic technique applied. 24 This is an obvious biomechanical consequence of incisor root shape. Given the tapered, essentially coneshaped structure of the roots, pressure from the axial component of orthodontic forces will be maximised at the root apex. 25 Twelve of the 15 studies included in the present review applied a segmented technique to intrude the pathologically migrated teeth, 5,9,10,13-16,26-30 and three used a continuous straight-wire appliance. 11,12,31 Six studies did not report the force values applied, and in the remaining nine studies, the forces ranged from 10 to 20 g per tooth. Although there is no evidence identifying the optimal force level in orthodontics, a recent study using a finite element method suggested a force reduction of approximately 30% in periodontally reduced teeth. 7 This reduction would avoid loads exceeding the levels that normally develop in a healthy periodontium. Three articles reported a lack of significant root resorption after orthodontic treatment, but the remaining articles did not evaluate this problem.
Relative to the optimal timing of orthodontic treatment after a pre-orthodontic phase of periodontal therapy, most studies preferred to initiate orthodontic treatment shortly after therapy. The orthodontic movement was initiated seven to 14 days after the periodontal surgery in seven studies 5,9,10,15,26,32,33 and after one month in one study. 30 Two articles (both related to a regenerative procedure) reported a delayed orthodontic start of one year after surgery. 28,31 The other articles did not report the time it took to initiate the orthodontic treatment after periodontal therapy. Given the heterogeneous methodologies applied in the studies, a direct comparison of the results was not possible, and therefore there was an inability to  Table III. Results of studies on orthodontic treatment and periodontal therapy without a regenerative procedure.
determine which of the two strategies produced the best outcome. However, several experimental studies have shown the advantages of early orthodontic tooth movement after periodontal therapy, such as the favourable effects on the restraint of epithelial apical down-growth, a decrease pocket depth and an enhancement in healing of bony defects. 34,35 The clinical and radiological findings of the studies present significant positive effects of the orthodontic treatment on the gain of clinical attachment.
Ten studies (four clinical trials, 5,9,10,15 five case reports 11,12,16,29,30 and one case series 13 ) evaluated the effects of orthodontic treatment after a course of traditional periodontal therapy, with or without surgery (Table III), and six studies 14,26-28,30,31 evaluated the effects of orthodontic treatment after periodontal therapy following a regenerative procedure (   no regenerative procedure, the gain in clinical attachment obtained after orthodontic treatment ranged from 3 to 8 mm, with a reduction in probing depth values ranging between 2 to 4.4 mm. The results reported by the studies that applied a regenerative procedure during periodontal therapy were similar. The increase in clinical attachment levels varied from 2 to 6 mm, with a reduction in probing depths values ranging from 2.8 to 6 mm. Although a direct comparison of these results cannot be performed, it appears that the addition of a periodontal regenerative procedure during the periodontal therapy did not provide additional clinical benefits to the orthodontic treatment in relation to clinical attachment gain. However, recent systematic reviews have provided evidence that the use of a regenerative procedure can result in additional clinical improvements in tissue attachment and probing depth compared with those obtained by periodontal therapy that applied only open flap debridement. 36,37 The former procedure seems to have a higher potential to heal via the formation of new cementum, new periodontal ligament, and new alveolar bone, while the latter usually leads to minimal or no bone infill and the formation of a long junctional epithelium in the treatment of infra-bony defects. Considering that the attachment between the newly regenerated tissue and the root surface cannot be examined without a biopsy of the treated teeth, further controlled clinical trials are required to clarify this topic.
In reference to the methodologic quality assessment, the scores ranged from 29% to 68%, with a mean score of 45%, which corresponds to a low evidence level. Interestingly, if only the clinical trials are considered, the mean methodologic quality score is 65%, which corresponds to a moderate evidence level. Considering the lack of randomised clinical trials and the small number of clinical trials evaluating the benefits of orthodontic treatment to PTM, case series and case reports were also included in the present review. Despite their limitations, case series and case reports comprise a large part of the evidence base in health sciences and are generally accepted as clinical guidelines by clinicians when dealing with complex cases. Moreover, the inclusion of these reports assists to strengthen the credibility of the present review.
No study achieved a high evidence level, and almost all were considered to have a moderate risk of bias. Some reasons for these results are obvious. For example, the orthodontists who performed the treatments could not be blinded. The blinding of outcome assessment was also not possible because none of the studies included in the present review evaluated a control   NA: not applicable group without orthodontic treatment. This would be the only way to quantify the possible additional benefits of correcting the malpositioned teeth after the control of the periodontal disease.
It is important to emphasise that the orthodontic correction of pathologically migrated teeth may not only increase tissue attachment levels, but also improve the aesthetic and functional aspects of the occlusion. The orthodontic treatment in these cases has a profound impact on patient appearance, which also indirectly increases the patient´s motivation. Moreover, the repositioning of teeth can improve access for cleaning, re-establishes incisal guidance, improves lip-seal and reduces non-axial loading which can act as an important co-factor, along with a dental biofilm, to accelerate periodontal destruction. 38,39