Do fixed orthodontic appliances adversely affect the periodontium? A systematic review of systematic reviews

Do fixed orthodontic appliances adversely affect the periodontium? A systematic review of systematic reviews Sherif A. Elkordy, Leena Palomo, Juan Martin Palomo, and Yehya A. Mostafa This overview aimed to summarize the available systematic reviews that assess the effects of treatment with fixed orthodontic appliances (FOAs) on the periodontium. Unrestricted electronic search of nine databases and additional manual searches were performed up to January 2019. Systematic reviews and meta analyses that assessed the effect of FOAs on the periodontal parameters were included. The methodological quality of the included reviews was evaluated using the A Measurement Tool to Assess Systematic Reviews2 (AMSTAR 2). The initial search yielded 2529 articles from which 19 were included in the current study. AMSTAR 2 scores ranged from critically low to high quality. The quality of evidence ranged from very low to low. The superiority of the periodontal outcomes of self-ligating brackets over conventional brackets could not be proven. The available evidence regarding the effects of FOAs on the periodontium is controversial and of very low quality. The short-term effects of FOAs were temporary worsening the periodontal parameters. Some conclusions regarding the periodontal outcomes of self-ligating brackets could be withdrawn. Future high-quality trials are required. The review was registered at the International prospective register of systematic reviews with registration number CRD42018106662. (Semin Orthod 2019; 25:130–157) © 2019 Elsevier Inc. All rights reserved.

Introduction nhancement of facial and dental aesthetics with preservation of the health and longevity of the masticatory apparatus is a common goal that is shared by the orthodontic and periodontal professions. The number of adult patients seeking orthodontic treatment with fixed appliances has increased steadily in recent decades.1 Additionally, a recent survey identified that 50% of Americans

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Lecturer of orthodontics, Department of Orthodontics, Faculty of Dentistry, Cairo University, Egypt; Associate Professor and Director of DMD Program, Department of Periodontics, School of Dental Medicine, Case Western Reserve University, Cleveland, OH; Professor and Director of Orthodontic Residency, Department of Orthodontics, School of Dental Medicine, Case Western Reserve University, Cleveland, OH; Professor of orthodontics, Department of Orthodontics, Faculty of Dentistry, Cairo University, Egypt. Corresponding author. E-mail addresses: [email protected], [email protected] © 2019 Elsevier Inc. All rights reserved. 1073-8746/12/1801-$30.00/0 https://doi.org/10.1053/j.sodo.2019.05.005

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30 years present with periodontitis.2 The existence of a strong relationship between periodontal and orthodontic treatments; especially in adult patients, triggered the clinicians and researchers from both ends to investigate a variety of questions pertaining to this interconnection. The number of publications evaluating orthodontic and periodontal interactions published in the years (2011 2016) was equal to that of those published in the previous 10 years (2000 2010), which, in turn, almost equals the one of the previous 60 years (1940 2000).3 One of the previous assertions for orthodontic treatment was to prolong the longevity of the individual's dentition through the correction of dental irregularities to allow better oral hygiene and reduce the incidence of gingivitis.4,5 On the contrary, damaging effects of orthodontic treatment on the periodontium were on top of the debatable topics in the dental field. It was stated that fixed orthodontic appliances (FOAs) produce significant clinical attachment loss6 and

Seminars in Orthodontics, Vol 25, No 2, 2019: pp 130 157

Effects of FOAs on the periodontium: A SR of SRs

lead to a shift in the subgingival bacterial microflora and gingival inflammation regardless the oral hygiene level.7 Orthodontic brackets and elastic modules interfere with the effective removal of plaque, thereby increasing the risk of gingivitis.8,9 Selfligating brackets (SLBs) were supported by claims of superiority over the conventional brackets (CBs) regarding the bacterial retention and plaque accumulation.10 Other studies refuted the assumption of improved oral hygiene with SLBs when compared to CBs;11,12 and the controversy is still ongoing. Alternatives to FOAs include clear aligners that could have the advantage of reduced plaque accumulation and improved gingival and periodontal parameters when compared to FOAs.13 The primary studies underpinning the orthodontic periodontal interrelationship suffer from low quality and lack of well-conducted large-scale research. Meanwhile, the number of systematic reviews (SRs) and meta analyses (MAs) focused on the orthodontic periodontal propinquity has rapidly escalated. The results of these reviews are sometimes contradictory, and their validity is highly influenced by their methodology.

Objectives The aim of the current study is to evaluate the methodological quality of the available SRs and MAs investigating the effects of FOAs on the periodontium to offer the clinician a summary of the current evidence and the quality of authentication.

Methods Protocol registration This overview of systematic reviews followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement. The review protocol was registered at the International prospective register of systematic reviews (PROSPERO) with registration number CRD42018106662. Few changes have been made after the protocol registration including the change in the title.

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Information sources, search strategy, and study selection Search strategy The electronic literature search was conducted in databases including PubMed, Embase, Cochrane Library, LILACS, Scopus, Web of science, SCIELO, Ovid, CINAHL via EBSCO in March 2018 and was conducted again in January 2019. No restrictions of language or publication date were applied. The implemented search strategy is presented in Appendix 1. Manual searching was performed in Google scholar, European Journal of Orthodontics, Journal of periodontology, Periodontology 2000, Journal of oral rehabilitation, Journal of clinical and oral investigations, Quintessence Publishing, American Journal of Orthodontics and Dentofacial Orthopedics, the Angle Orthodontist, and Seminars in Orthodontics. Bibliographies of the included full text articles were scanned for relevant studies. Two investigators independently performed and repeated the searches. Unpublished literature was searched electronically at ProQuest and PROSPERO using the terms “orthodontic”, “periodont*”, “systematic review”, “meta-analysis” and “gingiva”. Authors were contacted to identify unpublished or ongoing systematic reviews and to clarify data as required.

Eligibility criteria The selection criteria that were applied for the inclusion of articles in this review are represented in Table 1. After removal of internal and external duplicates, articles were screened based on title and abstract. When titles and abstracts were insufficient to decide, the full text of the article was acquired. Assessment of the reviews for inclusion was performed independently and in duplicate by two investigators. Disagreements regarding study inclusion were resolved by discussion to reach a final consensus

Data items and collection Data extraction sheets were developed, and data were extracted independently by the two investigators. The collected data included: the design of the primary studies; the number of

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Table 1. Eligibility criteria for the included studies in the systematic review. Inclusion criteria

Exclusion criteria

Study design

SR or MA

Design of the primary studies in the SRs

- RCTs - CCTs - Retrospective cohort studies

Quality assessment

Validated tool for quality assessment of primary studies Healthy periodontal patients undergoing fixed appliance therapy

Narrative reviews, commentaries on reviews and duplicate publications. - Animal studies - Case reports - Case series - Expert opinions. No quality assessment

Population

Intervention and comparator

Outcomes

Any type of active fixed appliance therapy that is compared to no treatment or treatment with another orthodontic appliance Include clinical periodontal outcomes.

Patients with periodontal disease or systemic conditions. Subjects having adjunctive periodontal surgeries to fixed appliance therapy Intervention has only removable appliances, fixed retainers Absence of clinical periodontal outcomes.

SR: systematic review. MA: meta-analysis. RCT: randomized controlled trial. CCT: clinical controlled trial.

participants and their grouping, description of the interventions and comparator, the quality of the primary studies, the outcomes, results and conclusions.

Risk of bias/ quality assessment for the included reviews The methodological quality of the included SRs was assessed independently by two reviewers using the A Measurement Tool to Assess Systematic Reviews (AMSTAR 2) checklist.14 The tool has 16 items to which responses are either yes, no, partial yes. The methodological quality was scored as High (Zero or one non-critical weakness), moderate (more than one non-critical weakness), low (One critical flaw with or without non-critical weaknesses), and critically low (more than one critical flaw with or without non-critical weaknesses).

Assessment of the overall quality of evidence across studies The results of the SRs that were shown to have moderate or high quality according to the AMSTAR 2 checklist were used to construct the overall body of evidence for each of the main outcomes using the Grades of Recommendation, Assessment, Development, and Evaluation (GRADE) approach.15 The GRADE profiler was used to evaluate studies for the methodological

quality, risk of bias, directness of evidence, inconsistency, precision of effect estimates, and risk of publication bias. The GRADE result was interpreted as follows: “high quality” ‒ further research is very unlikely to change the confidence in the estimate of effect; “moderate quality” ‒ further research is likely to have an important impact on the confidence in the estimate of effect and may change the estimate; “low quality” ‒ further research is very likely to have an important impact on the confidence in the estimate of effect and is likely to change the estimate; and “very low quality” ‒ very uncertain about the estimate.

Results Study selection and characteristics A total of 2524 articles were initially identified through electronic search, and five articles were obtained through manual searching. Initially, 55 articles met the inclusion criteria and were retrieved in full text. After reviewing the full texts, 36 articles were excluded. The most common reason for exclusion was the narrative nature of the reviews. The list of excluded studies is presented in Appendix 2. We contacted the authors of four studies identified from PROSPERO to check the developing status of their SRs, however they didn’t respond. Finally, nineteen articles were included in the analysis. The

Effects of FOAs on the periodontium: A SR of SRs

detailed literature search process is presented in Fig. 1.

Characteristics of included reviews The data of the included SRs is summarised in Table 2. From the included studies SRs, nine included only qualitative analysis and ten included MAs. Regarding the study designs of the included articles in the reviews, two SRs16,17 included only RCTs, six reviews included cross sectional and non-controlled studies. Seven

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reviews included RCTs and CCTs. Most of the remaining reviews included retrospective and prospective cohort studies. Four reviews assessed the periodontal effects of FOA therapy,18 21 while six studies16,17,22 25 compared between the periodontal outcomes of self-ligating brackets (SLBs) and conventional brackets (CBs). Four reviews quantified the changes in the oral microbiota secondary to FOAs therapy.26 29 Two reviews tried to detect the relation between orthodontic treatment and gingival recession.30,31 Finally, three SRs

Figure 1. PRISMA flow diagram for the study selection process.

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Table 2. Characteristics of included studies. Study (SR/MA)

Number and Design of primary studies

Search strategy

Total number of Intervention participants and grouping

Comparator

Outcomes

Quality of primary studies

Results

Authors’ conclusions

Objectives: to compare between SLBs and CBs regarding; oral hygiene, periodontal parameters, accumulation of S. mutans colonies, prevention of malodour 8 studies (4 in MA) 7 RCTs (3 of them were split mouth) 1 CCT

(May 2016) Medline via Pubmed, CDSR, CENTRAL. Clinicaltrials.gov No language restrictions.

Nascimento et al., 2014 (SR)

6 studies 5 RCTs 1 CCT

(December 2012) 209 CENTRAL; Ovid, PubMed and Bireme no language restrictions

Yang et al., 2016 (SR & MA)

12 studies (8 in MA) (December 2015) RCTs Medline via OVID, No split mouth studies EMBASE via OVID, CENTRAL, World Health Organization International Clinical Trials Registry Platform and the Chinese BioMedical Literature Database 12 studies (8 in MA) (2012- December RCTs 2017) PubMed, 9 parallel Embase, SciELO, Sci3 split mouth enceDirect, LILACS, BBO, Google Scholar and in the CENTRAL Grey literature: SIGLE

Arbildo et al., 2018 (SR and MA)

326 subjects SLB (active and (including split passive) mouth subjects) All patients were adolescents

SLBs

575 SLBs, (active and 311 SLBpassive) treated patients and 264 CB-treated patients

485. SLBs (active and 234 SLBs passive) 251 CBs Age (13.3 21)

CBs (elastomeric or stainless-steel ligatures)

Changes in periodontal or gingival inflammation indices including: (PI), (GI), BOP, (PPD).

Cochrane RoB tool 6 unclear RoB 2 high RoB

After 3 6 months: PI: The mean change in the intervention groups was 0.14 higher GI: The mean change in the intervention groups was 0.06 higher PPD: The mean change in the intervention group was 0.01 higher CBs (5 studies elas- Adhesion and Jadad scale. The increase in oral tomeric and 1 formation of S. All studies had microbiota (S. mutans study metal mutans high quality and Lactobacillus) is ligation) colonies associated with the use of orthodontic appliances with both CBs and SLBs with no differences between them CBs Discomfort Cochrane RoB The results showed Oral hygiene tool 10 studies passive SLB and CB did evaluated unclear risk, 2 not differ significantly through PI or studies low risk in plaque control [MD: ¡0.04, 95% CI bacterial of bias (¡0.30,0.22)]. colonization SLB was not superior over CB in bacterial colonization. CBs

PPD BOP GI PI

Cochrane RoB tool All studies have high ROB

PPD, BOP, GI and PI showed no significant differences between CB, active and passive SL brackets.

There is no evidence to support the claim that SLBs have relevant clinical advantages over CBs regarding the periodontal health in adolescents with bonded brackets

There is no evidence for a possible influence of bracket design (CB or SLBs) over colony formation and adhesion of S. Mutans

SLBs do not outperform CBs in reliving patients’ discomfort or promoting oral hygiene

No differences were detected in the periodontal clinical effect of orthodontic treatment with conventional and self-ligating brackets

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Arnold et al., 2016 (SR and MA)

Table 2 (Continued) Study (SR/MA)

Number and Design of primary studies

Total number of Intervention participants and grouping

Comparator

Longoni et al., 5 studies RCTs (1 par2017 (SR) allel) quasi-RCTs (4; 3 split mouth and 1 parallel)

April 2016 LILACS, PubMed, SCIELO, Science Direct, Scopus, and Google Scholar. Grey literature; Open Grey

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SLBs (active and passive)

CBs (3 studies elas- S. Mutans tomeric and 2 colonization study metal ligation)

Huang et al., 2018 (SR & MA)

September 2016 PubMed, Ovid, Embase, and the Cochrane Library

172; SLB: 43 CB: 77 CG: 62

SLBs, CBs

CBs, untreated control

4 studies (4 in MA) 3 RCTs, 1 CCT

Outcomes

Quality of primary studies MAStARI checklist; 2 low risk, 3 moderate risk of bias

Results

Authors’ conclusions

No difference between S. Mutans in CB and SLB after 3 months by PCR. Stereomicroscope ST Mutans colonization was more in CB than SLBs after 1, 4, 5, 12, and 24 weeks. Oral malodour Cochrane RoB Fixed appliance versus scores, PI, gin- tool; control: gival index 3 unclear Malodour: CBs showed (GI), and peri- 1 high risk of worse scores at the first odontal pocket bias week after bonding depths. only. PI: No difference between CBs and CG at 1 week. At 1 month after bonding; significantly higher PI than control GI: statistically higher in CB only at 1 month after bonding. PPD: No significant changes over the 3month period after bonding. SLB vs. CBs: Malodour scores were better in SLBs than CBs at 1 week. No significant difference in PI and GI.

SL brackets accumulate less S. Mutans than conventional metallic brackets.

FOAs are risk factors for malodour at one week after bonding with SLBs better than CBs. PI was worse one month after bonding.

Effects of FOAs on the periodontium: A SR of SRs

Search strategy

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Table 2 (Continued) Study (SR/MA)

Number and Design of primary studies

Search strategy

Total number of Intervention participants and grouping

Comparator

Outcomes

Quality of primary studies

Results

Authors’ conclusions

Objective: To determine the correlation between gingival recession/ bone height and incisor inclination (labial movement of incisors) in non-growing post-orthodontic patients compared to adult untreated subjects or patients treated with different methodologies. July 2010 Medline, 590 (190 were Fixed appliance PubMed, Embase, CG) with labial moveWeb of Science, ment of incisors Cochrane Database of Systematic Review, CENTRAL

Tepedino et al., 2018 (SR)

June 2017. MEDLINE via PubMed, EMBASE, Scopus, Web of Science, and Cochrane Library. Grey literature: OpenGrey.

2 studies Retrospective

Fixed appliances with no labial movement of incisors

Gingival recession

Custom made Six studies denied an tool for quality increased risk of gingiassessment val recession after labial advancement of mandibular incisors due to orthodontic treatment. One study concluded that lower incisor proclination greater than 10° would inevitably lead to gingival recession. 350 (150 FOAs (non-extrac- Adult untreated Gingival reces- New Castle Recession was signifiuntreated con- tion basis) subjects (1 study) sion and/or Ottawa scale. cantly higher in trol, 26 fixed or patients treated bone height, Moderate qual- treated patients comappliances with with FOAs on and post-treat- ity of studies. pared to that in extraction, 174 extraction basis (1 ment position untreated controls but non-extraction study) of incisors the difference was fixed applianminor and clinically ces) insignificant. Age (22 65) No correlation was found between the final inclination of lower teeth and gingival recession.

There is no association between appliance induced labial tipping and gingival recession. Labial movement of incisors during orthodontic treatment is not contributing to gingival recession

No scientific evidence exists stating that proclination of incisors following orthodontic treatment with fixed appliance increases the risk of gingival recession

Objective: To assess the effect of comprehensive treatment with fixed orthodontic appliances on periodontal outcomes, inflammation indices and clinical attachment levels in adolescent and adult periodontally healthy patients. Bollen 2008 (SR and MA)

12 studies; (8 in MA) 1 RCT, 3 CCT, 8 cross sectional studies excluded studies that assessed periodontal outcomes only at the time of appliance removal.

June 2007 MEDLINE; Web of Science; and the CENTRAL, CDSR, DARE and Health Technology Assessment. Grey literature: Clinicaltrials.gov, ProQuest

1670; 821 inter- Fixed or removable No treatment vention group, appliances 849 in the untreated CGs. Age (12 47)

Alveolar bone loss, PPD, clinical attachment loss, gingival recession and gingivitis.

Cochrane RoB tool for RCTs, New Castle Ottawa scale for NRCTs. All had high risk of bias

Alveolar bone loss: was 0.13 mm (0.07 0.20) greater in the intervention group than controls. PPD: intervention group had pocket depths that were, 0.23 mm (0.15 0.30)

There is an absence of reliable evidence on the positive effects of orthodontic therapy on periodontal status. The available evidence suggested a small mean worsening of

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Aziz et al., 2011 7 studies, all were ret(SR) rospective; 2 had no control group

Table 2 (Continued) Study (SR/MA)

10 studies 7 RCTs (2 of them were split mouth), 3 CCTs

Papageorgiou 9 studies (9 in MA) et al., 2017 (SR prospective non-ranand MA) domized trials

Cerroni et al., 2018 SR

Search strategy

Total number of Intervention participants and grouping

Comparator

July 2016 421, 274: Fixed Orthodontic CENTRAL, Embase, appliances treatment Medline 78 removable appliances 69 untreated control

Untreated patients or patients with different orthodontic treatment

February 2017 Medline via Pubmed, Scopus, Embase, Web of Knowledge, CENTRAL, CDSR, Virtual Health Library Grey Literature: ISRCTN registry

Untreated patients (3 studies only) Other orthodontic treatment

5 studies cohort studies From January 1997 to April 2017 (prospective and retrospective) Pubmed and Cochrane

335; 231 FOAs FOAs 104 untreated CG Age (11.4 42.1)

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Fixed orthodontic NR appliances

Outcomes

Quality of primary studies

Results

Authors’ conclusions

deeper than those of the control groups. Gingival recession: The intervention group had gingival recession 0.03 mm (0.01 0.04) greater than did the control group. BOP Cochrane RoB Patients undergoing GI tool (results orthodontic therapy PI NR) show an increase in PPD BOP, GI and PI CAL The highest inflammatory values were associated with fixed traditional orthodontic treatment Clinical attach- ROBINS-I tool, FOAs were associated ment loss dur- 8 had moder- with a clinical attaching orthodon- ate RoB, 1 had ment loss of 0.11 mm, tic treatment serious RoB which was neither statistically nor clinically significant. Untreated patients showed CAL 0.07 mm Intrusion of anterior teeth was associated with a slight attachment gain of 0.63 mm BOP Customized Long term outcomes: GI quality assess- studies reported no PI ment tool permanent effects on PPD (excluded 3 gingival status and that articles who periodontal values had low tended to normalize 3 quality) months- 2 years after fixed appliance removal.

periodontal status after orthodontic therapy.

The use of orthodontic appliances, particularly fixed appliances, can favour the increase of periodontal tissue inflammation.

Orthodontic treatment with fixed appliances might have little to no clinically relevant detrimental effect on the CAL

Effects of FOAs on the periodontium: A SR of SRs

Verussio et al., 2018 (SR)

Number and Design of primary studies

There is moderate evidence that fixed appliances influence periodontal status. Orthodontic appliances developed generalized plaque accumulation and gingivitis in a short follow-up.

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Table 2 (Continued) Study (SR/MA)

Number and Design of primary studies

Search strategy

Total number of Intervention participants and grouping

Comparator

Outcomes

Quality of primary studies

Results

Authors’ conclusions

Objective: to assess evidence from human studies about qualitative changes in the subgingival microbiota/ plaque induced by orthodontic treatment. Freitas et al., 2014 (SR)

4 studies (1 study prospective longitudinal, 1 study longitudinal, 2 studies NM)

November 2016 PubMed, Cochrane Library, and EMBASE

752 Age 13 36

Fixed orthodontic No control group appliances

Microbial colonization in orthodontic fixed appliances

Customized quality assessment tool (excluded 4 articles who had low quality)

Placement of FOAs increased quantity and quality of oral microbiota. Aa increased in subgingival plaque (2 studies) Aa didn’t increase (1 study) Increased Streptococci (1 study) Fixed orthodontic 3 studies had frequency of MINORS mod- Following FOAs insertreatment with untreated controls, periodontoerate scientific tion, the frequencies of metal brackets and 8 self-controlled pathogen in evidence Pg and Aa showed no bands studies the subgingival significant change, the plaques frequency of Tf significantly increased in short-term (0 3 months). During >6 months observation, the levels of subgingival periodontopathogens exhibited a transient increase but decreased to the pre-treatment levels afterwards. After removal of the FOAs, the 4 periodontopathogens showed no significant difference compared with before removal.

Moderate evidence showed that FOAs influenced the quantity and quality of oral microbiota. This might be a transitional effect that depends on oral hygiene control.

The levels of subgingival pathogens presented temporary increases after FOAs placement and appeared to return to pre-treatment levels several months later. Orthodontic treatment might not permanently induce periodontal disease by affecting the level of subgingival periodontal pathogens.

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Guo et al., 2017 13 studies (4 in MA) (SR & MA) (two CCTs, three cohort studies and eight non-controlled Studies)

May 2012 139 PubMed; Web of Knowledge and Ovid databases. (English language)

Table 2 (Continued) Study (SR/MA)

Number and Design of primary studies

Total number of Intervention participants and grouping

Papageorgiou 24 studies et al., 2018 (SR 3 were RCTs, and MA) 5 were prospective NRCTs, and 16 were nonrandomized studies of unclear design

August 2017 Medline via Pubmed, Scopus, Embase, Web of science, CENTRAL, CDSR, virtual health library, Google Scholar, Grey Literature: ISRCTN registry, ClinicalTrials.gov

1271, only 4 studies had untreated controls

Lucchese et al., 51 studies; (study 2018 (SR) designs were inadequately reported)

October 2017 PubMed, PMC, Scopus, Lilacs, Scielo, Cochrane Trial Library, Web of Science

1863

Comparator

Outcomes

Quality of primary studies

Orthodontic treat- (1) Untreated subment with any jects fixed appliances (2) Other form of orthodontic treatment

Qualitative and quantitative analysis of the subgingival microbiota. Time-points were pre-treatment, shortterm mid-treatment; long term mid-treatment; shortterm post-treatment; longterm posttreatment.

Cochrane’s RoB tool for RCTs, and a checklist based on Downs and Black tool for nonrandomized studies. All studies had high RoB.

Any type of ortho- NR dontic appliance. CBs: (29 studies). SLBs: (8 studies) Lingual brackets (4 studies)

Qualitative change in oral microbiota after FOA insertion. Periodontal parameters as PI, BOP

Results

Authors’ conclusions

The presence of Aa in the subgingival crevicular fluid of orthodontic patients was increased 3 6 months after FOAs insertion compared to untreated patients (RR = 15.54). There was still increased subgingival prevalence of Aa (RR = 3.98) and Tf in orthodontic patients up to 6 months after appliance removal compared to untreated patients. Swedish Coun- Orthodontic appliancil on Technol- ces influence the oral ogy Assessment microbiota with an in Health Care increase in the counts Criteria for of S. mutans and LacGrading tobacillus and in the Assessed Stud- percentage of potenies’ methods. tially pathogenic gram1 study: high negative bacteria. quality. 37 studies: moderate quality. 12 studies: low quality

Insertion of FOAs seemed to be associated with a qualitative change of subgingival microbiota, which reverts to some extent back to normal in the first months after appliance removal

Orthodontic appliances significantly influence the oral microbiota with alterations appearing one month after the start of treatment. Removable appliances had less impact on oral bacteria than fixed ones.

Effects of FOAs on the periodontium: A SR of SRs

Search strategy

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Table 2 (Continued) Study (SR/MA)

Number and Design of primary studies

Search strategy

Total number of Intervention participants and grouping

Comparator

Outcomes

Quality of primary studies

Results

Authors’ conclusions

Objective: to compare periodontal health in patients undergoing orthodontic treatment with clear aligners with that of those undergoing orthodontic treatment with fixed appliances. 7 studies (7 in MA) All were Prospective cohort studies

October 2017 Cochrane Library, EMBASE, PubMed, Medline, Chinese Biomedical Literature Database, CNKI, and Wan Fang Data.

368, 183 Invisalign patients in the invisalign group and 185 patients in the CG

FOA

10 studies; (9 in MA) 3 RCTs, 7 cohort studies

August 2017 PubMed, Web of Science, Cochrane Library, and Embase Grey literature.

427 patients (190 patients used clear aligners, and 237 patients used fixed appliances)

Clear aligners FOA

GI, PI, BOP, PPD

Rossini et al., 2015 SR

173 patients 5 studies (the results of September 2014 4 of them were Pubmed, National 92 with FOA included) Library of Medicine’s 71 with clear

Clear aligners

FOA 1 study had

GI PI, PPD sulcus bleeding index (SBI).

The NewcastleOttawa Scale. All studies were of high quality (more than 7 stars)

GI and PPD: no significant difference between the invisalign group and the CG, at 1,3 and 6 months. PI: Invisalign had a significantly lower PI, at 1 month (OR=¡0.53), 3 months (OR=¡0.69), and 6 months (OR=¡0.91). SBI: Invisalign showed a lower SBI, at 1 month (OR=¡0.44), 3 months (OR=¡0.49), and 6 months (OR=¡0.40) Cochrane RoB Clear aligners Clear aligners were tool for RCTs, were better better for periodontal The Newcastle- than FOA for; health than FOAs and Ottawa Scale PI (MD ¡0.53) might be recomfor non RCTs moderate level mended for patients at 9 studies of evidence high risk of developing medium qual- GI (MD, gingivitis ity, 1 study high ¡0.27) modquality. erate level of GRADE evidence assessment PPD: (MD, ¡0.35) low level of evidence. GI, PI, BOP, A grading sys- A significant decrease PPD tem described of periodontal indices by the Swedish (GI, PBI, BoP and

The meta-analysis indicated that compared with FOAs, patients treated with invisalign had a better periodontal health.

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Lu et al., 2018 (SR and MA)

Periodontal health, as well as quantity and quality of plaque, were

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untreated control group Medline, Embase, aligners CENTRAL, Web of 10 untreated Knowledge, Scopus, control group Google Scholar, and LILACS. 1 RCT, 3 prospective studies

SR: systematic review, MA: meta-analysis, RCT: randomized controlled trial, NRCT: non randomized controlled trials, CCT: clinical controlled trials, SLB: self-ligating bracket, CB: conventional bracket, PI: plaque index, GI: gingival index, PPD: probing pocket depth, BOP: bleeding on probing, SBI: sulcus bleeding index, FOA: fixed orthodontic appliance; CAT: clear aligner therapy; CAL: clinical attachment level, S. mutans: Streptococcus mutans, Aa: Aggregatibacter actinomycetemcomitans, Pg: Porphyromonas gingivalis, Pi: Prevotella intermedia, Tf: Tannerella forsythia, PCR: polymerase chain reaction; CENTRAL: cochrane central register of controlled trials, CDSR: Cochrane Database of Systematic Reviews, ISRCTN: International Standard Randomised Controlled Trial Number, DARE: Database of Abstracts of Reviews of Effects, RoB: risk of bias, MAStARI: Meta-analysis of Statistics Assessment and Review Instrument, MINORS: methodological index for non-randomized studies, CG: control group, 3D: three-dimensional, MD: mean difference, CI: confidence interval, NR: not reported.

better during aligner therapy than during FOA treatments. (moderate evidence) PPD) during CAT was observed in the analyzed sample of patients. Council on Technology Assessment in Health Care. Quality of the collected evidences was moderate (grade B) in all the studies

Authors’ conclusions Search strategy Number and Design of primary studies Study (SR/MA)

Table 2 (Continued)

Total number of Intervention participants and grouping

Comparator

Outcomes

Quality of primary studies

Results

Effects of FOAs on the periodontium: A SR of SRs

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compared the periodontal outcomes of clear aligners with that of FOAs.32 34 The primary and secondary outcomes included the plaque index (PI), gingival index (GI), clinical attachment levels, probing pocket depth (PPD) and bleeding on probing (BOP).

Methodological quality and the quality of evidence in the included reviews The quality of the included reviews was variable; where two reviews were of high quality, eight had moderate, seven showed low quality and two reviews showed critically low quality. The answers to AMSTAR 2 questions for the included SRs are shown in Table 3 and are graphically presented in Fig. 2. The results of the overall quality of evidence using GRADE are summarized in Appendix 3. Forty-four comparisons were assessed, and the quality of the extracted evidence ranged from very low to low.

Effects of intervention The periodontal outcomes of FOA therapy The effects of FOAs on different periodontal parameters including the PI, GI, PPD, BOP, alveolar bone loss and clinical attachment level were assessed by four SRs.18 concluded that FOAs caused a slight worsening of the periodontal status where there was 0.13 mm more alveolar bone loss, 0.23 mm deeper PPD than the control groups.19 stated that FOAs resulted in an increase of the periodontal tissue inflammation, BOP, GI, and PI.21 found that FOAs resulted in a slight change in the clinical attachment level (0.11 mm) which was neither statistically nor clinically significant.20 stated that FOAs developed generalized plaque accumulation and gingivitis in a short follow-up with no evidence of permanent gingival and periodontal changes in the long term.

The relation between orthodontic treatment with FOAs and gingival recession Two SRs30,31 correlated between gingival recession and incisor inclination after FOAs therapy. Both studies agreed that there was no evidence

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Table 3. Quality of the included reviews assessed by the AMSTAR 2 tool. AMSTAR 2 question

Nascimento et al. 2014

Yang et al. 2016

Arbildo et al. 2018

Longoni Huang et al. et al. 2017 2018

Aziz et al. 2011

Tepedino et al. 2018

Bollen 2008

Verussio et al. 2018

Yes

Yes

Yes

No

Yes

No

No

Partial yes

No

Yes

Yes

Yes

Yes

Partial yes

Yes

Guo et al. 2017

Papageorgiou et al. 2018

Lucchese et al. 2018

Lu et al. 2018

Jiang et al. 2018

Yes

No

Yes

Yes

Yes

Yes

No

Yes

Yes

No

No

Yes

Yes

Yes

Yes

No

No

Yes

No

No

Yes

No

No

Yes

Yes

No

No

Partial yes

No

Yes

Yes

Yes

No

Yes

Yes

Yes

Yes

No

Yes

Yes

No

Yes

Yes

Yes

Yes

Partial yes

Partial yes

Partial yes

Partial yes

Yes

Partial yes

Yes

Partial yes

Partial yes

Yes

Partial yes

Partial yes

Yes

Partial yes

Partial yes

Yes

Yes

No

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

No

No

Yes

No

Yes

No

Yes

No

Yes

Yes

No

Yes

Yes

Yes

Yes

Yes

Yes

No

No

No

No

No

Partial yes

No

Yes

No

No

No

Yes

Yes

No

Yes

No

No

yes

No

Yes

Partial yes

Partial yes

Yes

Partial yes

Yes

Partial yes

Yes

Yes

Yes

No

Partial yes

Yes

Partial yes

Partial yes

Yes

Partial yes

Partial yes

Partial Partial yes yes

Partial Partial yes yes

Papageorgiou Freitas et al. 2017 et al. 2014

Rosini et al. 2015

Cerroni et al. 2018

(continued on next page)

Elkordy et al

(1) Did the research questions and inclusion criteria for the review include the components of PICO? (2) Did the report of the review contain an explicit statement that the review methods were established prior to the conduct of the review and did the report justify any significant deviations from the protocol? (3) Did the review authors explain their selection of the study designs for inclusion in the review? (4) Did the review authors use a comprehensive literature search strategy? (5) Did the review authors perform study selection in duplicate? (6) Did the review authors perform data extraction in duplicate? (7) Did the review authors provide a list of excluded studies and justify the exclusions? (8) Did the review authors describe the included studies in adequate detail?

Arnold et al. 2016

Table 3 (Continued) AMSTAR 2 question

Arnold et al. 2016

Nascimento et al. 2014

Arbildo et al. 2018

Longoni Huang et al. et al. 2017 2018

Aziz et al. 2011

Tepedino et al. 2018

Bollen 2008

Verussio et al. 2018

Yes

Yes

Partial yes

No

No

Yes

Papageorgiou Freitas et al. 2017 et al. 2014

Guo et al. 2017

Papageorgiou et al. 2018

Lucchese et al. 2018

Lu et al. 2018

Jiang et al. 2018

Yes

Yes

Yes

Yes

Yes/ Partial yes

Yes

No

No

No

No

Yes

No

Yes

NA

Yes/ No

NA

NA

Yes

No

No

NA

No

NA

NA

Yes

Yes

No

Yes

No

No

Yes

Yes

No

No

Rosini et al. 2015

Cerroni et al. 2018

No

Yes

Yes

No/ Partial yes

Yes

Yes

Partial yes

No

No

No

No

No

No

No

Yes

No

No

NA

Yes

NA

Yes

Yes

NA

Yes

Yes

NA

NA

No

NA

Yes

NA

No

Yes

NA

Yes

Yes

NA

NA

Yes

Yes

No

Yes

Yes

Yes

Yes

No

yes

Yes

No

Yes

Yes

Yes

No

Yes

Yes

Yes

Yes

No

Yes

Yes

Yes

No

143

(continued on next page)

Effects of FOAs on the periodontium: A SR of SRs

(9) Did the review Yes/ Partial No/ Yes authors use a satisfacyes tory technique for assessing the risk of bias (RoB) in individual studies that were included in the review? (10) Did the review No No authors report on the sources of funding for the studies included in the review? (11) If meta-analysis Yes NA was performed did the review authors use appropriate methods for statistical combination of results? (12) If meta-analysis No NA was performed, did the review authors assess the potential impact of RoB in individual studies on the results of the meta-analysis or other evidence synthesis? (13) Did the review Yes No authors account for RoB in individual studies when interpreting/ discussing the results of the review? (14) Did the review Yes No authors provide a satisfactory explanation for, and discussion of, any heterogeneity observed in the results of the review?

Yang et al. 2016

144

Table 3 (Continued) AMSTAR 2 question

Arnold et al. 2016

Yang et al. 2016

Arbildo et al. 2018

NA

No

No

NA

Yes

Yes

Yes

Critically Moderate Moderate low

Longoni Huang et al. et al. 2017 2018

Aziz et al. 2011

Tepedino et al. 2018

Bollen 2008

Verussio et al. 2018

Papageorgiou Freitas et al. 2017 et al. 2014

No

NA

NA

Yes

NA

Yes

Yes

Yes

No

Yes

No

No

Yes

Low

Low

Low Moderate Moderate

Low

High

Guo et al. 2017

Papageorgiou et al. 2018

Lucchese et al. 2018

Lu et al. 2018

Jiang et al. 2018

NA

No

Yes

NA

No

Yes

NA

NA

Yes

Yes

Yes

Yes

Yes

No

No

Yes

Low

Low

Low Moderate

High

Critically Moderate Moderate low

Rosini et al. 2015

Cerroni et al. 2018

Elkordy et al

(15) If they perNo formed quantitative synthesis did the review authors carry out an adequate investigation of publication bias (small study bias) and discuss its likely impact on the results of the review? (16) Did the review No authors report any potential sources of conflict of interest, including any funding they received for conducting the review? Overall review quality Moderate

Nascimento et al. 2014

Effects of FOAs on the periodontium: A SR of SRs

145

Figure 2. Graphic presentation for the answers to AMSTAR 2 questions for the included studies.

of association between the FOAs-induced incisor proclination and gingival recession and that FOAs couldn’t be considered as a risk for gingival recession. On the other hand,18 assessed gingival recession after FOAs and showed that FOAs group had gingival recession 0.03 mm (0.01 0.04) greater than the control group.

The qualitative changes in the subgingival microbiota induced by FOAs Results of the included reviews revealed that placement of FOAs was associated with qualitative and quantitative changes in the oral microbiota. The investigated periodontopathogens included Streptococcus mutans (S. mutans), Aggregatibacter actinomycetemcomitans (Aa), Porphyromonas gingivalis (Pg), Prevotella intermedia (Pi), Tannerella forsythia (Tf) and lactobacilli. Most of the reviews agreed that the

changes started by an increase in the pathogens after FOAs insertion that was transient in nature.

Comparison between SLBs and CBs Results from six SRs16,17,22 25 showed that there were no differences in the PI, GI, PPD, BOP between SLBs and CBs. SLBs did not surpass the CBs regarding the accumulation of bacterial colonies. One SR23 concluded that SLBs showed better malodour scores than CBs.

Comparison between periodontal health in patients undergoing FOAs therapy with those treated with clear aligners Different periodontal parameters were assessed including the PI, GI, PPD, SBI, and BoP. Two SRs33,34 agreed that clear aligners showed a significantly lower PI than FOAs.33 showed that aligners showed a lower GI, and PPD as

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compared to FOAs.32 concluded that the periodontal health, as well as quantity and quality of plaque, were better during aligner therapy than during FOA treatments.

Discussion Multiple SRs assessed the effects of FOAs on the periodontium. Systematic reviews (or overviews) of reviews are a logical and appropriate next step, allowing the findings of separate reviews to be compared and contrasted, providing clinical decision makers with the evidence they need.35 SRs that included animal studies were excluded to avoid the effect of the included animal studies on the final outcomes. Discordance between human and animal studies is well established and is attributed to the failure of the animal models to simulate the clinical disease accurately.36 SRs that included subjects having periodontal disease and/or defects were excluded due to the difference in the reaction of healthy and periodontally compromised subjects to orthodontic treatment.37

Quality of the included reviews The AMSTAR 2 checklist14 is modified from the original AMSTAR tool38 to fit systematic reviews that included both RCTs and non-randomized studies (NRCTs). NRCTs are subject to a range of biases that are either not present or are less noticeable in RCTs and thus require different risk of bias assessments. Responses to AMSTAR2 items do not derive an overall score, unlike the original AMSTAR instrument. It is believed that an overall score may mask critical weaknesses that should diminish confidence in the results of a systematic review.39 According to GRADE, the quality of the extracted evidence ranged from low to very low which shows the increased uncertainty regarding the extracted estimates. The main reason for downgrading the evidence was the high risk of bias inherent in the NRCTs and observational studies. Other reasons for downgrading were the imprecision that resulted from the very wide confidence intervals together with the increased heterogeneity in the reported outcomes that yielded high inconsistency.

Summary of evidence and effects of interventions Regarding the effects of FOAs on the periodontium, the investigated parameters included the PI, GI, PPD, BoP and CAL. Loss of clinical attachment was reported to result from FOAs however, the value was 0.11 mm that, despite being statistically significant, was far from being of clinical importance.21 The same applies for the reported 0.13 mm alveolar bone loss and the 0.23 increased pocket depth.18 Interestingly, intrusion of anterior teeth was associated with a slight attachment gain of 0.63 mm which is in consistence with previous reports that orthodontic intrusion improved the level of clinical attachment.40 Other parameters including PI, GI and BoP showed increased values with FOAs versus controls indicating the periodontal inflammation.19 Long term studies were scarce and failed to prove any permanent long-term effects of FOAs on the periodontal parameters.20 Labial inclination of the lower incisors by FOAs was frequently debated in the literature to result in gingival recession. Two SRs tried to investigate the relationship between gingival recession and incisor proclination and failed to find evidence of association.30,31 On the other hand 0.03 mm of gingival recession was reported with FOAs which is of questionable clinical value.18 It is worth mentioning that gingival recession is a multifactorial condition where many factors are involved. FOAs themselves are not risk factors for gingival recessions however, the injudicious movement of the incisors outside the bone envelope can be a contributing factor.41 Other factors were proven to be more correlated to gingival recession including thin gingival biotype and reduced buccal bone thickness.3,42 The effects of FOAs on the periodontium was also investigated on the microbiological level. The importance of such an assessment is to identify whether FOAs predispose to progression of gingivitis to periodontitis through increasing periodontopathogens in the subgingival environment. Two reviews reported that FOAs resulted in a shift in the composition of the subgingival microbiota that tended to return to near the normal levels few months after appliance removal.21,27 The results from the other two reviews, which were of lower quality, were directed towards a more dramatic change in the subgingival pathogens after FOAs insertion.26,29

Effects of FOAs on the periodontium: A SR of SRs

SLBs are appliances that were claimed to outperform CBs in the treatment efficiency, treatment duration, chairside time and oral hygiene.10,43 Previous SRs concluded that there was no significant difference between CBs and SLBs as regards treatment efficiency and duration.44,45 The results of the reviews included in our study confirmed the plethora of evidence against the superiority of SLBs over CBs. No differences were reported regarding the PI, GI, BoP and PPD. The only reported difference was regarding the malodour scores that were better in the SLBs group however, this was only assessed after one week of appliance insertion. Claims regarding the superiority of SLBs seem to be only supported by the manufacturing companies and their sales representatives and to be interpreted with due consideration of the current scientific knowledge.46 Clear aligners, being removable, are expected to allow for better oral hygiene and superior gingival health than FOAs. This is reflected on the results of the reviews that confirmed the superiority of clear aligners regarding the PI, GI and PPD over the FOAs. However, different aspects regarding the appliance efficiency need to be properly investigated before its routine use as a more hygienic alternative to FOAs. It can be mentioned according to the available evidence, that FOAs cause a temporary worsening of the periodontal parameters that tends to revert after appliance removal. From another perspective, these findings also highlight the utmost importance of giving strict oral hygiene maintenance protocols to patients treated with FOAs. It can be deduced that FOAs are not risk factors of inducing periodontal disease, but they rather provide a transient condition of gingivitis and plaque accumulation.

Strengths and limitations The included SRs suffered from methodological limitations and most of their included primary studies were of cross sectional and retrospective nature. It can be debated that this umbrella review is not currently needed because welldesigned primary studies would be much more timely than SRs at this juncture. However, the benefits of performing a SR of SRs is to help to set implications for future research. It can

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emphasize that we do not need any further SRs underpinning this topic, but research plans should be modified to include well-designed primary studies instead. The evidence retrieved from this systematic review must be taken with caution because the level of evidence ranged from low to very low. A quantitative analysis of the periodontal status before and after treatment would have been meaningful in summarizing the evidence however, because of the substantial methodological heterogeneity in the included SRs, it was not possible. Examples of the methodological flaws in the included SRs included pooling data from adults and adolescents which could affect the accuracy of the estimates. Moreover, the types of FOAs were not specified in all SRs; it is well known that the use of orthodontic bands can adversely affect the periodontium when compared to bondable tubes on the molars.47 Data from patients who were treated with extractions were pooled with those treated on a non-extraction basis. Reporting an aggregate pooled effect might be misleading if there are important reasons to explain the variable treatment effects.48

Conclusions (1) The SRs on the effects of FOAs on the periodontium present a heterogeneous methodological quality. Only two SRs were judged of high quality. The level of the extracted evidence ranged from low to very low. (2) FOAs cause a slight temporary worsening of the periodontal status when compared to control groups. (3) Orthodontic treatment with FOAs might not permanently induce a periodontal disease by affecting the levels of subgingival periodontopathogens. The changes are temporary and revert after the FOAs removal. (4) The relation between treatment with FOAs and the development of gingival recessions is highly debatable and needs further research. The current weak evidence failed to prove an association between the labial inclination of the incisors by FOAs and the incidence of gingival recession. (5) SLBs do not outperform the CBs regarding their periodontal outcomes. Using SLBs

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instead of CBs for the purpose of having better periodontal health is not recommended. (6) The periodontal health is proven to be better with clear aligners in comparison with FOAs.

Implications for research (1) It seems more useful for future research to analyze more homogeneous groups of patients (regarding age, type of malocclusion), appliances, treatment protocols, and means of outcome assessment for studying the effects of FOAs on the periodontium. (2) The complex relationship between the FOAs and the development of gingival recessions still needs to be thoroughly studied. (3) The long-term effects of FOAs on the periodontium need further investigation.

Funding The authors did not receive any funding during performing this systematic review.

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36. Perel P, Roberts I, Sena E, et al. Comparison of treatment effects between animal experiments and clinical trials: systematic review. BMJ. 2007;334(7586):197. 37. Gkantidis N, Christou P, Topouzelis N. The orthodonticperiodontic interrelationship in integrated treatment challenges: a systematic review. J Oral Rehabil. 2010;37 (5):377–390. 38. Shea BJ, Hamel C, Wells GA, et al. AMSTAR is a reliable and valid measurement tool to assess the methodological quality of systematic reviews. J Clin Epidemiol. 2009;62 (10):1013–1020. 39. Greenland S, O’Rourke K. On the bias produced by quality scores in meta-analysis, and a hierarchical view of proposed solutions. Biostatistics. 2001;2(4):463–471. 40. Cardaropoli D, Re S, Corrente G, Abundo R. Intrusion of migrated incisors with infrabony defects in adult periodontal patients. Am J Orthod Dentofacial Orthop. 2001;120(6):671–675. quiz 677. 41. Joss-Vassalli I, Grebenstein C, Topouzelis N, Sculean A, Katsaros C. Orthodontic therapy and gingival recession: a systematic review. Orthod Craniofac Res. 2010;13(3):127– 141. 42. Melsen B, Allais D. Factors of importance for the development of dehiscences during labial movement of mandibular incisors: a retrospective study of adult orthodontic patients. Am J Orthod Dentofacial Orthop. 2005;127(5):552– 561. quiz 625. 43. Damon DH. The rationale, evolution and clinical application of the self-ligating bracket. Clin Orthod Res. 1998;1 (1):52–61. 44. Fleming PS, Johal A. Self-ligating brackets in orthodontics. A systematic review. Angle Orthod. 2010;80(3):575–584. 45. Dehbi H, Azaroual M, Zaoui F, Halimi A, Benyahia H. Therapeutic efficacy of self-ligating brackets: a systematic review. Int Orthod. 2017;15(3):297–311. 46. O’Brien K, Sandler J. In the land of no evidence, is the salesman king. Am J Orthod Dentofacial Orthop. 2010;138 (3):247–249. 47. Al-Anezi SA. The effect of orthodontic bands or tubes upon periodontal status during the initial phase of orthodontic treatment. Saudi Dent J. 2015;27(3): 120–124. 48. Garg AX, Hackam D, Tonelli M. Systematic review and meta-analysis: when one study is just not enough. Clin J Am Soc Nephrol. 2008;3(1):253–260.

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Appendix 1. Search strategy in different databases Database Scopus

PubMed

Web of Science LILACS

CINAHL “EBSCO” SCIELO

ProQuest

Number of hits ALL (orthodont* OR “orthodontic tooth movement” OR “tooth movement” OR bracket OR appliance OR aligner OR invisalign OR braces) AND ALL (periodont* OR gingivitis OR “gingival recession” OR recession OR gingiv* OR periodontium OR “periodontal health”) AND TITLE (“systematic review” OR “meta analysis") ((((((((((((periodont*) OR parodont*) OR perio* OR gingivitis) OR gingival recession) OR recession) OR gingiv* OR periodontium[MeSH Major Topic]) OR periodontal health) OR Periodontics[MeSH Major Topic]))))))) AND ((((((((((orthodont*) OR appliance*) OR aligner) OR orthodontic tooth movement) OR tooth movement) OR bracket*) OR invisalign) OR brace*) OR Orthodontic Appliances[MeSH Major Topic]) OR retain*)) AND (((systematic review[Title/Abstract]) OR meta analysis [Title/Abstract]) OR meta analyses[Title/Abstract]) TS=(orthodont* OR “orthodontic tooth movement" OR “tooth movement" OR bracket OR appliance OR aligner OR invisalign OR braces) AND TS=(periodont* OR gingivitis OR “gingival recession” OR recession OR gingiv* OR periodontium OR “periodontal health”) AND TI=(“systematic review” OR “meta analysis”) (tw:((tw:(othodont*)) OR (tw:(appliance)) OR (tw:(bracket)) OR (tw:(aligner)) OR (tw:(tooth movement)))) AND (tw:((tw:(gingivitis)) OR (tw:(periodontal disease)) OR (tw:(gingival recession)) OR (tw:(periodontium)) OR (tw:(periodont* health)) OR (tw: (periodont*)))) AND (tw:((tw:(systematic review)) OR (ti:(meta analysis)) OR (ti: (meta-analysis)))) TX (periodont* OR parodont* OR perio* OR gingivitis OR “gingival recession” OR periodontium OR “periodontal health”) AND TX (orthodont* OR appliance* OR “orthodontic tooth movement" OR bracket* OR “Orthodontic Appliances”) AND TI (“systematic review” OR “meta analysis”) (periodont* OR parodont* OR perio* OR gingivitis OR “gingival recession” OR periodontium OR “periodontal health” OR gingiva) AND (orthodont* OR appliance* OR “orthodontic tooth movement” OR bracket* OR “Orthodontic Appliances” OR brace* OR “tooth movement”) AND ("systematic review" OR “meta analysis" OR review) (periodont* OR parodont* OR perio* OR gingivitis OR “gingival recession” OR periodontium OR “periodontal health”) AND TX (orthodont* OR appliance* OR “orthodontic tooth movement” OR bracket* OR “Orthodontic Appliances”) AND TI (“systematic review” OR “meta analysis”)

676

447

93

362

383

63

121

Appendix 2. List of excluded studies with reasons Reason for exclusion

Excluded studies

Narrative reviews or commentaries on systematic reviews

(Dersot, 2012), (Ngom, Benoist, Soulier-Peigue, & Niang, 2010), (Antoun, Mei, Gibbs, & Farella, 2017), (van Gastel, Quirynen, Teughels, & Carels, 2007), (Atack, Sandy, & Addy, 1996), (Brignardello-Petersen, 2018), (Shin, 2017) (Gkantidis, Christou, & Topouzelis, 2010), (Najeeb et al., 2017), (Joss-Vassalli, Grebenstein, Topouzelis, Sculean, & Katsaros, 2010), (G€ olz, Reichert, & J€ager, 2011) (Migliorati et al., 2015), (M. Pithon et al., 2017), (M. M. Pithon et al., 2015), (Tang, Sensat, & Stoltenberg, 2016), (Gray & McIntyre, 2008), Kaklamanos and (Kaklamanos & Kalfas, 2008), (Goh, 2007), (Al-Anezi & Harradine, 2012) (Roberto Rotundo et al., 2010), (R Rotundo et al., 2011), (Zasciurinskiene, Lindsten, Slotte, & Bjerklin, 2016) (Al-Moghrabi, Pandis, & Fleming, 2016), (Foz, Artese, Horliana, Pannuti, & Romito, 2012), (Buzatta et al., 2016) (Incerti-Parenti, Checchi, Ippolito, Gracco, & Alessandri-Bonetti, 2016), (Kloukos, Eliades, Sculean, & Katsaros, 2014). (Ata-Ali et al., 2016), (Alhadlaq, 2015), (Kapoor, Kharbanda, Monga, Miglani, & Kapila, 2014), (Perinetti, Primozic, Castaldo, Di Lenarda, & Contardo, 2013) (Korayem, Flores-Mir, Nassar, & Olfert, 2008), (Gon¸c alves Zen
obio et al., 2015), (Magkavali-Trikka et al., 2015), (Somar, Mohadeb, & Huang, 2016) (Bollen, 2008)

Included animal studies Discussed methods of oral hygiene control during fixed appliances therapy only Included patients with periodontal disease and/or periodontal defects Interventions did not include fixed orthodontic appliances Intervention included combined surgical periodontal treatment Did not report periodontal outcomes Discussed implant site development with fixed appliances only Duplicate publication

Effects of FOAs on the periodontium: A SR of SRs

References for the excluded studies Al-Anezi, S. A., & Harradine, N. W. T. (2012). Quantifying plaque during orthodontic treatment: The Angle Orthodontist, 82(4), 748 53. https://doi.org/10.2319/050111-312.1 Al-Moghrabi, D., Pandis, N., & Fleming, P. S. (2016). The effects of fixed and removable orthodontic retainers: a systematic review. Progress in Orthodontics, 17(1), 24. https://doi. org/10.1186/s40510-016-0137-x Alhadlaq, A. M. (2015). Biomarkers of Orthodontic Tooth Movement in Gingival Crevicular Fluid: A Systematic Review. J Contemp Dent Pract, 16(7), 578 587. Antoun, J. S., Mei, L., Gibbs, K., & Farella, M. (2017). Effect of orthodontic treatment on the periodontal tissues. Periodontology 2000, 74(1), 140 157. https://doi.org/10.1111/prd.12194 Ata-Ali, F., Ata-Ali, J., Ferrer-Molina, M., Cobo, T., De Carlos, F., & Cobo, J. (2016). Adverse effects of lingual and buccal orthodontic techniques: A systematic review and meta-analysis. Am J Orthod Dentofacial Orthop, 149(6), 820 829. Atack, N. E., Sandy, J. R., & Addy, M. (1996). Periodontal and microbiological changes associated with the placement of orthodontic appliances. A review. J Periodontol, 67(2), 78 85. Bollen, A. M. (2008). Effects of malocclusions and orthodontics on periodontal health: evidence from a systematic review. J Dent Educ, 72 (8), 912 918. Brignardello-Petersen, R. (2018). Orthodontic treatment with fixed appliances may result in small clinical attachment level loss. Journal of the American Dental Association (1939), 149(4), e70. https://doi.org/10.1016/j.adaj.2017.12.007 Buzatta, L. N., Shimizu, R. H., Shimizu, I. A., Pacheco-Pereira, C., Flores-Mir, C., Taba Jr., M., . . . De Luca Canto, G. (2016). Gingival condition associated with two types of orthodontic fixed retainers: a meta-analysis. Eur J Orthod. https://doi.org/10.1093/ejo/cjw057 Dersot, J.-M. (2012). R
ecession gingivale et orthodontie de l’adulte. Propositions th
erapeutiques fond
ees sur les preuves cliniques. Int Orthod, 10(1), 29 42. Foz, A. M., Artese, H. P. C., Horliana, A. C. R. T., Pannuti, C. M., & Romito, G. A. (2012). Occlusal adjustment associated with periodontal therapy A systematic review. Journal of

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Dentistry, 40(12), 1025 1035. https://doi. org/10.1016/j.jdent.2012.09.002 Gkantidis, N., Christou, P., & Topouzelis, N. (2010). The orthodontic-periodontic interrelationship in integrated treatment challenges: a systematic review. Journal of Oral Rehabilitation, 37 (5), 377 390. https://doi.org/10.1111/j.13652842.2010.02068.x Goh, H. H. (2007). Interspace/interdental brushes for oral hygiene in orthodontic patients with fixed appliances. The Cochrane Database of Systematic Reviews, (3), CD005410. https://doi.org/ 10.1002/14651858.CD005410.pub2 G€ olz, L., Reichert, C., & J€ager, A. (2011). Gingival invagination a systematic review. Journal of Orofacial Orthopedics = Fortschritte Der Kieferorthopadie : Organ/Official Journal Deutsche Gesellschaft Fur Kieferorthopadie, 72(6), 409 20. https://doi.org/10.1007/s00056-011-0046-z Gon¸c alves Zen
obio, E., Carneiro Moreira, R., Villamarin Soares, R., Feres, M., Chambrone, L., & Awad Shibli, J. (2015). A Mixed-Model Study Assessing Orthodontic Tooth Extrusion for the Reestablishment of Biologic Width. A Systematic Review and Exploratory Randomized Trial. International Journal of Periodontics & Restorative Dentistry, 35(1), 19 27. https://doi. org/10.11607/prd.2164 Gray, D., & McIntyre, G. (2008). Does oral health promotion influence the oral hygiene and gingival health of patients undergoing fixed appliance orthodontic treatment? A systematic literature review (Structured abstract). Journal of Orthodontics, 35(4), 262 269. Incerti-Parenti, S., Checchi, V., Ippolito, D. R., Gracco, A., & Alessandri-Bonetti, G. (2016). Periodontal status after surgical-orthodontic treatment of labially impacted canines with different surgical techniques: A systematic review. American Journal of Orthodontics & Dentofacial Orthopedics, 149(4), 463 472. https:// doi.org/10.1016/j.ajodo.2015.10.019 Joss-Vassalli, I., Grebenstein, C., Topouzelis, N., Sculean, A., & Katsaros, C. (2010). Orthodontic therapy and gingival recession: a systematic review. Orthodontics & Craniofacial Research, 13 (3), 127 41. https://doi.org/10.1111/j.16016343.2010.01491.x Kaklamanos, E. G., & Kalfas, S. (2008). Metaanalysis on the effectiveness of powered toothbrushes for orthodontic patients. American

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Journal of Orthodontics and Dentofacial Orthopedics, 133(2), 187.e1-187.e14. Kapoor, P., Kharbanda, O. P., Monga, N., Miglani, R., & Kapila, S. (2014). Effect of orthodontic forces on cytokine and receptor levels in gingival crevicular fluid: a systematic review. Progress in Orthodontics, 15(1), 65. https://doi.org/10.1186/s40510-014-0065-6 Kloukos, D., Eliades, T., Sculean, A., & Katsaros, C. (2014). Indication and timing of soft tissue augmentation at maxillary and mandibular incisors in orthodontic patients. A systematic review. Eur J Orthod, 36(4), 442 449. https:// doi.org/10.1093/ejo/cjt073 Korayem, M., Flores-Mir, C., Nassar, U., & Olfert, K. (2008). Implant site development by orthodontic extrusion A systematic review. Angle Orthodontist, 78(4), 752 760. Magkavali-Trikka, P., Kirmanidou, Y., Michalakis, K., Gracis, S., Kalpidis, C., Pissiotis, A., & Hirayama, H. (2015). Efficacy of Two Site-Development Procedures for Implants in the Maxillary Esthetic Region: A Systematic Review. International Journal of Oral & Maxillofacial Implants, 30(1), 73 94. Migliorati, M., Isaia, L., Cassaro, A., Rivetti, A., Silvestrini-Biavati, F., Gastaldo, L., & Silvestrini-Biavati, A. (2015). Efficacy of professional hygiene and prophylaxis on preventing plaque increase in orthodontic patients with multibracket appliances: A systematic review. European Journal of Orthodontics, 37(3), 297 307. https://doi.org/ 10.1093/ejo/cju044 Najeeb, S., Siddiqui, F., Qasim, S. Bin, Khurshid, Z., Zohaib, S., & Zafar, M. S. (2017). Influence of uncontrolled diabetes mellitus on periodontal tissues during orthodontic tooth movement: a systematic review of animal studies. Progress in Orthodontics, 18(1), 5. https:// doi.org/10.1186/s40510-017-0159-z Ngom, P. I., Benoist, H. M., Soulier-Peigue, D., & Niang, A. (2010). Rapports r
eciproques entre orthodontie et parodontologie. Int
er^ et d'une synergie d'action effective. Orthod Fr, 81(1), 41 58. Perinetti, G., Primozic, J., Castaldo, A., Di Lenarda, R., & Contardo, L. (2013). Is gingival crevicular fluid volume sensitive to orthodontic tooth movement? A systematic review of split-mouth longitudinal studies. Orthodontics & Craniofacial Research, 16(1), 1 19. Pithon, M. M., Sant’Anna, L. I. D. A., Bai~ao, F. C. S., Santos, R. L. D., Coqueiro, R. D. S., & Maia,

L. C. (2015). Assessment of the effectiveness of mouthwashes in reducing cariogenic biofilm in orthodontic patients: A systematic review. Journal of Dentistry, 43(3), 297 308. https://doi.org/10.1016/j.jdent.2014.12.010 Pithon, M., Santanna, L., Baiao, F., Coqueiro, R., Maia, L., & Paranhos, L. (2017). Effectiveness of different mechanical bacterial plaque removal methods in patients with fixed orthodontic appliance: a systematic review and meta-analysis. Biosci. J. Uberl^ a Ndia, 33(2), 537 554. Rotundo, R., Bassarelli, T., Pace, E., Iachetti, G., Mervelt, J., & Pini Prato, G. (2011). Orthodontic treatment of periodontal defects. Part II: A systematic review on human and animal studies. Progress in Orthodontics, 12(1), 45 52. https:// doi.org/10.1016/j.pio.2011.02.008 Rotundo, R., Nieri, M., Iachetti, G., Mervelt, J., Cairo, F., Baccetti, T., . . . Prato, G. P. (2010). Orthodontic treatment of periodontal defects. A systematic review. Progress in Orthodontics, 11 (1), 41 44. https://doi.org/10.1016/j. pio.2010.04.013 Shin, K. (2017). Self-ligating Brackets May Not Have Clinical Advantages Over Conventional Brackets for the Periodontal Health of Adolescent Orthodontic Patients. The Journal of Evidence-Based Dental Practice, 17 (2), 102 104. https://doi.org/10.1016/j. jebdp.2017.03.005 Somar, M., Mohadeb, J. V, & Huang, C. (2016). Predictability of Orthodontic Forced Eruption in Developing an Implant Site: A Systematic Review. Journal of Clinical Orthodontics : JCO, 50 (8), 485 492. Tang, X., Sensat, M. L., & Stoltenberg, J. L. (2016). The antimicrobial effect of chlorhexidine varnish on mutans streptococci in patients with fixed orthodontic appliances: a systematic review of clinical efficacy. International Journal of Dental Hygiene, 14(1), 53 61. https://doi.org/10.1111/idh.12163 van Gastel, J., Quirynen, M., Teughels, W., & Carels, C. (2007). The relationships between malocclusion, fixed orthodontic appliances and periodontal disease. A review of the literature. Australian Orthodontic Journal, 23(2), 121 9. Zasciurinskiene, E., Lindsten, R., Slotte, C., & Bjerklin, K. (2016). Orthodontic treatment in periodontitis-susceptible subjects: a systematic literature review. Clinical and Experimental Dental Research, 2(2), 162 173.

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Effects of FOAs on the periodontium: A SR of SRs

Appendix 3. Quality assessment of the existing evidence using the GRADE tool for the outcomes of the moderate and high-quality reviews Study

Intervention/ Outcome comparator

Arnold et al., 2016

SLBs versus CBs

Yang et al.

Study type Effect estimate

PI after 4 6 MA weeks

MD: 0.09 (95% CI: ¡0.18 0.36)

PI after 3 6 months

MD= ¡0.14 (95% CI: ¡0.31 0.02)

GI after 4 6 weeks

MD: 0.02 (95% CI: ¡0.19 0.22)

GI after 3 6 months

MD: ¡0.02 (95% CI: ¡0.35 0.32)

PPD

MD: ¡0.03 (95% CI: ¡0.17 0.11)

SLBs vs. CBs PI

MA

St mutans

Arbildo et al.

Tepedino et al.

Bollen et al.

SLBs vs. CBs PPD

MD: ¡0.04 (95% CI: ¡0.3 0.22) narrative

MA

SMD= 0.11 (95% CI: ¡0.14, 0.36)

BoP

SMD: ¡0.37 [95% CI: ¡0.77, 0.02]

GI

SMD= 0.59 [95% CI: ¡0.25, 1.43]

PI

SMD: 0.49 [95% CI: ¡0.08, 1.06]

FOA versus Gingival untreated recession controls (1 study) Extraction versus non-extraction (1 study)

SR

Alveolar bone SR loss

Narrative

MD: 0.13 (95% CI: 0.07, 0.20)

Number of participants (studies)

Conclusions

72 (2 studies) No significant difference between SLBs and CBs 105 (3 No significant studies) difference between SLBs and CBs 65 (2 studies) No significant difference between SLBs and CBs 65 (2 studies) No significant difference between SLBs and CBs 65 (2 studies) No significant difference between SLBs and CBs 159 (4 No significant studies) difference between SLBs and CBs 158 (4 No significant studies) difference between SLBs and CBs 243 (5 RCTs) No significant difference between SLBs and CBs 226 (4 RCTs) No significant difference between SLBs and CBs 321 (7 RCTs) No significant difference between SLBs and CBs 361 (8 RCTs) No significant difference between SLBs and CBs 324 (2 One study studies) showed clinically non-significant more recession in FOA group versus untreated controls. The other study showed 0.4 0.8 mm increase in clinical crown length in non-extraction group versus 0.4 1.1 mm in extraction group 254 (3 FOA could probstudies) able show more

GRADE

⨁⨁ LOW a,b ⨁⨁ LOW a,b ⨁⨁ LOW a,b ⨁⨁ LOW a,b ⨁⨁ LOW a,b ⨁ VERY LOW a,c,d ⨁⨁ LOW a,d ⨁ VERY LOW a,b ⨁ VERY LOW a,b,c ⨁ VERY LOW a,b,c ⨁ VERY LOW a,b,c ⨁ VERY LOW d,e

⨁ VERY LOWe (continued)

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(Continued) Study

Intervention/ Outcome comparator

Study type Effect estimate

Number of participants (studies)

FOA versus untreated controls MD: 0.23 (95% CI: 0.15, 0.30)

Gingival recession Attachment loss

Papageorgiou et FOA versus al., 2018 untreated controls

Attachment MA level (comprehensive treatment) Attachment level (intrusion) Prevalence of MA Aa after appliance insertion

Prevalence of Aa after appliance removal

Prevalence of Tf after appliance removal

Jiang et al.

GRADE

alveolar bone loss. PPD

Papageorgiou et FOA versus al., 2017 untreated controls

Conclusions

FOA versus PI in RCTs clear aligners

MA

194 (2 studies)

FOA could probable show more PPD than untreated subjects. MD 0.03 (95% 659 (3 No significant CI: 0.01, 0.04) studies) difference in gingival recession Narrative 449 (3 One study studies) showed 0.11 mm (0.07 0.15) more attachment loss in FOA group. Two studies showed 0.05, 0.06 mm less attachment loss in the FOA group MD: 0.14 mm loss 182 patients There may be lit(95% CI 0.17 mm (2 studies) tle or no attachgain to 0.45 mm ment loss with loss) FOA treatment MD: 0.49 mm gain 20 patients Intrusion with (0.36 mm 0.62 mm (1 study) FOA could probgain) ably allow some attachment gain RR: 15.54 (95% 44 patients Orthodontic CI: 3.19 75.85) (2 studies) patients 3.0 6.0 months after appliance insertion have probably higher subgingival A.a. prevalence than untreated patients RR: 3.98 (95% 166 patients Orthodontic CI: 1.23 12.89) (3 studies) patients 1.0 6.0 months after appliance removal might have higher subgingival A.a. prevalence than untreated patients RR: 2.25 (95% 44 patients Orthodontic CI: 1.41 3.61) (2 studies) patients 0.3 3.0 months after appliance removal might have higher subgingival T.f. prevalence than untreated patients MD: 1.79 (95% 67 (2 RCTs) PI is probably higher in CI: 1.45 2.13) patients with FOA than those

⨁ VERY LOW c,e

⨁ VERY LOWe ⨁ VERY LOW c,d,e

O O O VERY LOW c,g O O LOW e O O O VERY LOW a,b

O O O VERY LOW a,b

O O O VERY LOW a,b



⨁⨁⨁ a MODERATE

(continued)

155

Effects of FOAs on the periodontium: A SR of SRs

(Continued) Study

Lu et al.

Intervention/ Outcome comparator

Study type Effect estimate

PI in observational studies

MD: 0.21 (95% CI: 0.03 0.45)

PI (all studies)

MD: 0.53 (95% CI: 0.20 0.85)

GI

MD: 0.27 (95% CI: 0.17 0.37)

PPD in RCTs

MD: 0.21 (95% CI: 0.77 1.19)

PPD in observational studies

MD: 0.39 (95% CI: 0.03 0.75)

PPD all studies

MD: 0.35 (95% CI: 0.03 0.67)

FOA versus GI 1 month clear aligners

MA

SMD 0.24 (95% CI: ¡0.09 0.57)

PI 1 month

SMD 0.53 (95% CI: 0.18 0.89)

PPD 1 month

SMD 0.39 (95% CI: ¡0.21 0.98)

Sulcus bleeding index at 1 month

SMD 0.44 (95% CI: 0.19 0.7)

Number of participants (studies)

Conclusions

with clear aligners 282 (6 PI is probably studies) slightly higher in patients with FOA than those with clear aligners 349 (8 PI is probably studies) slightly higher in patients with FOA than those with clear aligners 362 (6 GI is probably studies) slightly higher in patients with FOA than those with clear aligners 67 (2 RCTs) There is probably no difference in PPD in patients with FOA and those with clear aligners 240 (5 PPD is probably studies) slightly higher in patients with FOA than those with clear aligners 307 (7 PPD is probably studies) slightly higher in patients with FOA than those with clear aligners 145 (3 There is probably studies) no significant difference in GI after 1 month between FOA and clear aligners. 191 (4 PI after 1 month studies) is probably slightly higher in FOA than clear aligners. 218 (4 There is probably studies) no significant difference in PPD after 1 month between FOA and clear aligners. 258 (5 Sulcus bleeding studies) index after 1 month is probably slightly higher in FOA than clear aligners.

GRADE

⨁ VERY LOW c,e

⨁ VERY LOW c,e

⨁ VERY LOW c,e

⨁ VERY LOW a,b,c

⨁ VERY LOW c,e

⨁ VERY LOW c,e

⨁⨁ LOW e

⨁ VERY LOW c

⨁ VERY LOW b,c

⨁⨁ LOW e

(continued)

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(Continued) Study

Guo et al.

Intervention/ Outcome comparator

Study type Effect estimate

Number of participants (studies)

Conclusions

GRADE

There is probably no significant difference in GI after 6 months between FOA and clear aligners. PI after 6 months is probably slightly higher in FOA than clear aligners. There is probably no significant difference in PPD after 6 months between FOA and clear aligners. Sulcus bleeding index after 6 months is probably slightly higher in FOA than clear aligners. One study showed that there is probably no significant increase in Pg 3 months after FOA insertion versus untreated controls One study showed that there is probably no significant increase in Aa 3 months after FOA insertion versus untreated controls One study showed that there is probably no significant increase in Tf 3 months after FOA insertion versus untreated controls One study showed that there is probably no significant increase in Pi 3 months after FOA insertion versus untreated controls

⨁ VERY LOW b,c,e

GI 6 months

SMD: 0.78 (95% CI: ¡0.05 1.62)

255 (5 studies)

PI at 6 months

SMD 0.91 (95% CI: 0.35 1.47)

301 (6 studies)

PPD at 6 months

SMD 0.38 (95% CI: ¡0.17 to 0.93)

261 (5 studies)

Sulcus bleeding index at 6 months

SMD 0.4 (95% CI: 0.07 0.73)

191 (4 studies)

MD: 0.47 (95% CI: ¡0.12 1.06)

60 (1 study)

Aa 3 months after insertion

MD: 0.004 (95% CI: ¡0.11 0.12)

60 (1 study)

Tf 3 months after insertion

MD: 0.47 (95% CI: ¡0.44 1.38)

60 (1 study)

Pi 3 months after insertion

MD: 0.67 (95% CI: ¡0.31 1.65)

60 (1 study)

FOA versus Pg 3 months MA no treatment after (only 2 insertion studies)

⨁ VERY LOW c,e

⨁ VERY LOW b,c,e

⨁⨁ LOW e

⨁ VERY LOW e,f

⨁ VERY LOW e,f

⨁ VERY LOW e,f

⨁ VERY LOW e,f

(continued)

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Effects of FOAs on the periodontium: A SR of SRs

(Continued) Study

Intervention/ Outcome comparator

Study type Effect estimate

Aa 10 days after appliance removal

Narrative

Pg 10 days after appliance removal

Narrative

Pi 10 days after appliance removal

Narrative

Td 10 days after appliance removal

Narrative

Number of participants (studies)

Conclusions

122 (1 study) One study showed that Aa decreased 10 days after appliance insertion to be similar to the untreated controls 122 (1 study) One study showed that Pg didn’t change 10 days after appliance insertion and is not significantly greater than in untreated controls 122 (1 study) One study showed that Pi didn’t change 10 days after appliance insertion and is not significantly greater than in untreated controls 122 (1 study) One study showed that Td significantly decreased 10 days after appliance insertion to be not significantly greater than in untreated controls

GRADE

⨁ VERY LOW e,f

⨁ VERY LOW e,f

⨁ VERY LOW e,f

⨁ VERY LOW e,f

*The risk in the intervention group (and its 95% confidence interval) is based on the assumed risk in the comparison group and the relative effect of the intervention (and its 95% CI). CI: Confidence interval; MD: Mean difference; SMD: standardized mean difference; DG: downgrade; Aa: Aggregatibacter actinomycetemcomitans; GRADE: Grading of Recommendations Assessment, Development and Evaluation; RR: relative risk; Tf: Tanerrela forsythia; Pg: P. gingivalis; Pi: P. intermedia; Td: T. denticola; FOA: Fixed orthodontic appliance; SLB: self ligating brackets; CB: conventional brackets GRADE Working Group grades of evidence High certainty: We are very confident that the true effect lies close to that of the estimate of the effect. Moderate certainty: We are moderately confident in the effect estimate: The true effect is likely to be close to the estimate of the effect, but there is a possibility that it is substantially different. Low certainty: Our confidence in the effect estimate is limited: The true effect may be substantially different from the estimate of the effect. Very low certainty: We have very little confidence in the effect estimate: The true effect is likely to be substantially different from the estimate of effect. Explanations (a) High and/or Unclear risk of bias in some items. (b) Imprecise due to Wide Confidence interval and inclusion of few studies with limited sample size. (c) High I2 value. (d) Imprecise because data was not pooled. (e) Data from non-randomized studies, retrospective and/or cross-sectional studies. (f) Single study data with small sample size and a wide 95%CI that included no effect.