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Accepted: 29 October 2017

DOI: 10.1111/jcpe.12835

RANDOMIZED CLINICAL TRIAL

Orthodontic treatment simultaneous to or after periodontal


cause-­related treatment in periodontitis susceptible patients.
Part I: Clinical outcome. A randomized clinical trial

Eglė Zasčiurinskienė1,2  | Nomeda Basevičienė3 | Rune Lindsten2,4 | 


Christer Slotte5,6,* | Henrik Jansson2,5 | Krister Bjerklin4

1
Department of Orthodontics, Medical
Academy, Lithuanian University of Health Abstract
Sciences, Kaunas, Lithuania Aim: To compare two treatment strategies regarding the effect of orthodontic treat-
2
Centre For Oral Health, School of Health and
ment on periodontal status in patients with plaque-­induced periodontitis.
Welfare, Jönköping University, Jönköping,
Sweden Subjects and Methods: This was a randomized clinical trial. Fifty periodontal patients
3
Department of Dental and Oral were randomly assigned to the test or control groups according to periodontal treat-
Pathology, Medical Academy, Lithuanian
ment timing. All patients received supra-­and subgingival debridement following base-
University of Health Sciences, Kaunas,
Lithuania line examination. Control group patients received cause-­related periodontal treatment
4
Department of Orthodontics, Institute for before the start of orthodontic treatment and which was performed simultaneous to
Postgraduate Dental Education, Jönköping,
Sweden orthodontic treatment for the test group patients.
5
Department of Periodontology, Institute for Results: No difference between the test and control groups was found regarding
Postgraduate Dental Education, Jönköping, change of clinical attachment level (CAL) after periodontal–orthodontic treatment.
Sweden
6 Fewer sites with initial pocket depth (PD) of 4–6 mm healed after periodontal–ortho-
Department of Biomaterials, Institute
for Clinical Sciences, Sahlgrenska dontic treatment in the test group (20.5%, IQR = 11.9%) in comparison with controls
Academy, University of Gothenburg,
(30.4%, IQR = 27.1%) (p = .03). Anterior teeth [OR 2.5] and teeth in male patients [OR
Göteborg, Sweden
1.6] had a greater chance for PD improvement ≥2 mm. Total periodontal–orthodontic
Correspondence
treatment duration was significantly longer for the control group (p < .01).
Eglė Zasčiurinskienė, Department of
Orthodontics, Lithuanian University of Health Conclusions: Both groups showed a gain of CAL and a reduction in sites with PD ≥
Sciences, Kaunas, Lithuania.
4 mm. Orthodontic treatment, simultaneously to the periodontal treatment, could be
Email: eglezas@gmail.com
used in the routine treatment of patients with plaque-­induced periodontitis.

KEYWORDS
clinical attachment level, gingival recession, orthodontic treatment, periodontal treatment,
periodontitis, pocket depth

1 | INTRODUCTION successfully performed (Badersten, Nilveus, & Egelberg, 1981, 1984;


Periodontitis is described as a result of an imbalance of the oral mi- Becker et al., 2001; Deas, Moritz, Sagun, Gruwell, & Powell, 2016;
crobiota, in the dento-­gingival area, and the host response leading Isidor & Karring, 1986; Kaldahl, Kalkwarf, Patil, Dyer, & Bates, 1988;
to inflammation and destruction of the periodontium in susceptible Ramfjord et al., 1987; Sanz, Alonso, Carasol, Herrera, & Sanz, 2012).
individuals (Berglundh & Donati, 2005; Flemmig, 1999). To reduce As a consequence of plaque-­
induced periodontitis, patients
microorganisms, both non-­surgical and surgical therapies have been with increased numbers of teeth showing attachment loss also have

*Deceased February, 2016.

J Clin Periodontol. 2018;45:213–224. wileyonlinelibrary.com/journal/jcpe   © 2017 John Wiley & Sons A/S. |  213
Published by John Wiley & Sons Ltd
214      | ZASČIURINSKIENĖ et al.

pathological migration of anterior teeth, decreased posterior bite


height and worsened smile aesthetics (Brunsvold, 2005; Johal & Ide,
Clinical Relevance
1999). The latter is the most common reason for patients seeking
Scientific rationale for the study: Two treatment strategies
treatment.
regarding the effect of orthodontic tooth movement on
Some clinical studies have shown that orthodontic treatment
periodontal status in patients with plaque-­induced perio-
may be effective in intruding and replacing the migrated max-
dontitis were tested in this trial.
illary incisors (Artun & Urbye, 1988; Cardaropoli, Re, Corrente,
Principal findings: Combined periodontal–orthodontic treat-
& Abundo, 2001, 2004; Corrente, Abundo, Re, Cardaropoli, &
ment resulted in about 1/4 of sites with CAL gain despite
Cardaropoli, 2003; Melsen, 2001). The use of orthodontic tooth
the periodontal treatment timing. Significantly more sites
movement after conventional periodontal therapy in periodontally
with initial PD 4–6 mm healed where periodontal treatment
involved patients has been described in a number of case reports in
was performed before orthodontic treatment.
the past years (Agarwal et al., 2014; Fukunaga, Kuroda, Kurosaka,
Practical implications: Combined periodontal–orthodontic
& Takano-­Yamamoto, 2006; Janson, Janson, & Murillo-­Goizueta,
treatment showed a gain of CAL and a reduction in sites
2011; Nakamura, Gomi, Oikawa, Tokiwa, & Sekiya, 2013; Pinho,
with PD 4 
mm. Simultaneous periodontal–orthodontic
Neves, & Alves, 2012). However, the effect of orthodontic treat-
treatment could be used in the routine treatment of patients
ment on periodontal tissues, the risks and benefits of orthodontic
with plaque-­induced periodontitis.
tooth movement in the patients with periodontal pathology is con-
troversial and lacking sufficient scientific evidence (Zasciurinskiene,
Lindsten, Slotte, & Bjerklin, 2016). Therefore, it is not clear if it
2 | MATERIALS AND METHODS
could be used as a routine treatment protocol in periodontally in-
volved dentitions.
2.1 | Subjects
Tooth movement in reduced, but healthy periodontium may
improve attachment level, and conversely, in active periodontal This trial was performed according to the Declaration of Helsinki
cases, orthodontic treatment may cause further progression of guidelines. Approval by the Regional Ethical Review Board in Kaunas,
periodontal destruction (Ericsson, Thilander, Lindhe, & Okamoto, Lithuania, and informed consent from the patients were obtained. All
1977; Melsen, 2001; Melsen, Agerbaek, Eriksen, & Terp, 1988 patients were given oral and written information about the study de-
Wennstrom, Lindhe, Sinclair, & Thilander, 1987). These studies led sign and their right to withdraw from the study at any time without
to the knowledge that periodontal treatment should be performed negative effect on their future treatment.
first.
The aim of the present randomized clinical trial was to compare
2.1.1 | Selection criteria
two treatment strategies regarding the effect of orthodontic tooth
movement on periodontal status in patients with plaque-­induced peri- The selection period lasted from 2010 to 2015. Occlusion, function
odontitis. The secondary aim was to evaluate differences in treatment and aesthetics were evaluated for all individuals with plaque-­induced
duration. periodontitis, who were consecutively attending the Department of
The null hypothesis tested was that no statistically significant dif- Dental and Oral Pathology, Lithuanian University of Health Sciences
ference could be demonstrated between the test and control groups (LUHS) and two private clinics in Kaunas, Lithuania. Patients having
assessing clinical attachment level (CAL) change after combined peri- malocclusion were consulted by orthodontist (EZ) and selected for the
odontal–orthodontic treatment. trial according to inclusion and exclusion criteria (Table 1).

T A B L E   1   Inclusion and exclusion criteria

Inclusion criteria Exclusion criteria

• >25 years of age; • any systemic disease (e.g. diabetes) or medication that would
• good general health status; influence treatment;
• a minimum of six anterior teeth present; • periodontal treatment in the previous 2 years;
• periodontitis experience and marginal bone loss at ≥3 teeth and more • pregnant or lactating women;
than 1/3 of the root length (assessed by panoramic radiographs); • smokers (>5 cigarettes/day);
• ≥3 teeth with bleeding on probing (BoP), pocket depth (PD) ≥4 mm • failure to comply to oral hygiene instructions provided or/and to keep
and loss of clinical attachment level (CAL) ≥4 mm (assessed by clinical to regular study appointments.
examination);
• malocclusion that needs orthodontic treatment.
ZASČIURINSKIENĖ et al. |
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consecutively. Clinicians and patients were not blinded due to the de-
2.2 | Trial design
sign of this research. Patients who dropped out of the study (n = 2)
This was a randomized, controlled, parallel, open-­label clinical trial. were replaced by additional patients, but no later than January 2015
The CONSORT (consolidated standards of reporting trials) guidelines (Figure 1).
for clinical trials were followed (Moher et al., 2012; Pandis, 2013). All trial patients received oral hygiene instructions (OHI) and pro-
fessional oral hygiene (POH) (Figure 2).
Test group: Twenty-­five patients started orthodontic treatment
2.2.1 | Randomization and allocation concealment
with conventional straight-­wire mechanics directly after POH. Non-­
After consultation by orthodontist, selected patients were offered the surgical therapy and subsequent periodontal surgery in sites showing
treatment with fixed orthodontic appliances. The patients who con- probing depth (PD) ≥6 mm that bled on probing were performed after
sented to undergo orthodontic treatment were randomly assigned orthodontic alignment and levelling phases had been finished.
into either the intervention test group (periodontal treatment simul- Control group: Twenty-­five patients received cause-­related non-­
taneous to orthodontic treatment) or the control group (periodontal surgical therapy with subsequent periodontal surgery in sites show-
treatment before orthodontic treatment) (Figure 1). Randomization ing PD ≥6 mm that bled on probing, before orthodontic treatment.
was performed immediately after baseline examination according to Orthodontic treatment was applied as in the test group (Figure 2).
a computer-­generated randomization list. All patients were numbered Changes in periodontal status were compared between the groups.

F I G U R E   1   Flow chart of trial patients


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216       ZASČIURINSKIENĖ et al.

F I G U R E   2   Flow chart of trial procedures

examination. The result was assessed after 2 weeks. In cases with BoP
2.3 | Periodontal treatment (PT)
> 30%, POH was repeated.

2.3.1 | Professional oral hygiene


2.3.2 | Cause-­related periodontal treatment
POH treatment including the removal of supra-­and subgingival cal-
culus by ultrasonic instrumentation supplemented with hand instru- Non-­surgical therapy was performed under local anaesthesia at dif-
ments was performed for every study patient following baseline ferent time points (Figure 2). Treatment was scheduled in four weekly
ZASČIURINSKIENĖ et al. |
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visits. Patients had to rinse with a 0.12% chlorhexidine solution twice vacuum-­pressured retainers were provided for the night time for un-
daily during this phase. limited period of time.

2.3.3 | Periodontal surgery 2.5 | Clinical examination


Modified Widman flap surgery was scheduled and performed in Standardized clinical measurements at all time points for every trial
sites showing PD ≥6 mm that bled on probing, following SRP at the patient were performed by the same investigator (EZ). Measurements
3-­month follow-­up visit. All patients were prescribed mouth rinsing were recorded on forms designed for the trial. The measurements
with a 0.12% chlorhexidine solution twice daily during the surgical were performed at all sites around each tooth with a manual peri-
phase and for two weeks following surgery (American Academy of odontal probe (Hu-­Friedy PCP-­UNC 15, Chicago, IL, USA). Only the
Periodontology 2011). No antibiotics were prescribed for the ad- deepest measurement was recorded for each of the four sites: mesial
ditional effect of periodontal treatment. However, antibiotics in (M), buccal (B), distal (D) and lingual (L). To decrease measurement bias
Lithuania are easily accessible and often used to treat other diseases of the clinical parameters, every clinical examination was recorded on
as in many parts of the world. a separate record form at every time point. Periodontal assessments
The application of active orthodontic forces for the test group was before and after OT were performed only for teeth that were ortho-
postponed 2–4 weeks after periodontal surgery. dontically moved.
T0: Baseline examination. All participants were given a baseline ex-
amination including the following measurements:
2.3.4 | Supportive periodontal treatment
OHI (including interproximal brushing) was performed continuously • Visible plaque index (VPI): counted by the presence of visible dental
throughout all treatments for both groups (Figure 2). POH was con- plaque along the gingival margin at four sites (M-B-D-L) of each
tinuously maintained at 3–6 month intervals by a dental hygienist dur- tooth and expressed as a percentage of examined sites within each
ing OT. subject (Ainamo & Bay, 1975).
• Bleeding on probing (BoP): measured after probing to the base of
the pocket.
2.4 | Orthodontic treatment (OT)
• Pocket depth (PD): measured from the gingival margin to the bot-
Orthodontic treatment with straight-­wire appliance was performed in tom of the pocket at four sites (M-B-D-L) and recorded to the near-
the Orthodontic Department of LUHS and two private clinics by one est millimetre.
of the authors (EZ). • Gingival recession (REC): measured as a distance from the cemen-
Good oral hygiene with a full-­mouth plaque score <25% was as- to-enamel junction (CEJ) to the gingival margin at four sites (M-B-
sured before the start of OT (Lang & Tonetti, 2003). D-L) and recorded to the nearest millimetre.
After baseline examination and POH, the decision was made about • Clinical attachment level (CAL): measured as a distance from the
the teeth that needed to be moved in each patient. This depended bottom of the pocket to cement–enamel junction and recorded in
on the number of teeth present, the severity of malocclusion of each millimetres at four sites (M-B-D-L).
patient, planned/existing neighbouring implants and/or prosthetic
restorations. T1: Pre-orthodontic examination. All patients were examined before
Self-­
ligating brackets with MBT (McLaughlin, Bennett, Trevisi), OT start with all and the same measurements: VPI, BoP, PD, REC and
prescription (3M Unitek Orthodontic Products; Monrovia, CA, USA) CAL.
and 0.022-­inch slot were used. Aesthetic brackets (Clarity™ SL) were T2: Post-orthodontic examination (study end point). All patients were
used for maxillary anterior segment to fulfil the aesthetic requirements examined the day of bracket debond: VPI, BoP, PD, REC and CAL.
of the trial patients according to individual needs. Initial levelling and Changes in periodontal status were compared between time
alignment were performed using round, nitinol heat-­activated arch- points T0, T1, T2 in both groups.
wires (3M Unitek Orthodontic Products; Monrovia, CA, USA). The
inter-­dental enamel reduction technique was used in crowded cases
2.5.1 | Examination during OT
where needed. Intrusion and retrusion of maxillary and/or mandibular
anterior teeth were provided in flared incisor cases. Space closure was Every 3 to 6 months: BoP, PD.
performed using rectangular or round stainless steel wires. Anchorage,
where needed, was ensured with microscrews or temporary crowns
2.6 | Radiographic examination
on implants.
Following active OT, the fixed appliances were removed and a The enrolled study patients were examined with panoramic radio-
fixed (multistrand wire) orthodontic retainer for maxillary and man- graphs before PT for diagnostic purpose—evaluation of alveolar bone
dibular anterior teeth was applied for all patients and Hawley or status.
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For the assessment of reproducibility of measurements made by


2.7 | Outcomes
two investigators, the interclass correlation coefficient (ICC) and “con-
Gain in CAL was chosen as the primary response variable to judge sistency type” were used. Intra-­class reproducibility (EZ) was calcu-
the effectiveness of the treatment (Page & DeRouen, 1992; Savage, lated with “absolute agreement” type.
Eaton, Moles, & Needleman, 2009). Secondary outcomes included (i) In all analyses, a p value <.05 was considered significant.
PD reduction; (ii) REC development, (iii) treatment duration.

2.8.3 | Calibration
2.7.1 | Data management
Calibration of the investigator (EZ) was performed twice (with 1-­year
Data analyses were based on the patient as the unit of measure. CAL interval) during the experimental period by recording measurements
gain was evaluated by the millimetre change. Measurement analysis of same half mouth of each of three patients by periodontologist (NB)
included sites that had CAL ≥4 mm and expressed as median value and orthodontist (EZ). Examiners were blinded to each other. CAL at
of the assessed registrations within each subject in test and control four sites of 30 teeth was examined. A total of 120 repeated measure-
groups at time points corresponding to T0 and T2. ments were evaluated.
CAL and PD changes in patient level were also evaluated in the The repeated measurements were made twice at the same visit
subgroup analysis. Sites were classified as follows: <4 mm, 4–6 mm with 30-­min intervals for intra-­class reproducibility for the author EZ.
and >6 mm. Sites that had changed CAL and PD class during treatment The analysis showed high interclass agreement (0.95; 95% CI:
phases T0–T1, T1–T2 and T0–T2 were analysed. 0.92, 0.96; p = .0001) and intra-­class agreement (0.93; 95% CI: 0.87,
Analysis was performed also at tooth level for PD change from T0 0.95; p = .0001).
to T2. Only sites PD ≥4 mm were included. PD change was measured
for every tooth number according to FDI World Dental Federation
3 | RESULTS
system. PD change T0–T2 was grouped (<2 and ≥2 mm) according to
median value of 2 mm. Teeth were also grouped as anterior (central
3.1 | Participant flow
incisors, lateral incisors, canines) and posterior (premolars, molars).
Two age groups (≤35 and >35 years) were also created (Demmer & The present trial was conducted between 2010 and 2016.
Papapanou, 2010). PD change of ≥2 mm as dependent variable was The flow chart of trial patients and the reasons for exclusion are
used in multivariate binary logistic regression analysis model. presented in Figure 1.
In total 50 selected patients, 25 in the test and 25 in the control group
started periodontal–orthodontic treatment. After two withdrawn and
2.8 | Statistical analysis
two replaced patients, 50 patients completed the trial and were finally
evaluated. Reasons for dropout are shown in the flow diagram (Figure 1).
2.8.1 | Sample size
The CAL difference of 1.0 mm was considered to be of clinical impor-
3.2 | Baseline data
tance between the test and control groups. To be able to detect a clin-
ically meaningful difference in mean CAL of 1.0 mm between groups, The baseline demographic and clinical data for both groups are
standard deviation of 1.0 mm, with a power of 90% and an alpha-­level shown in Table 2. There were no significant differences between
at 0.05, 22 patients were needed in each group. To compensate for the test and control treatment groups. One patient in each group
dropouts, twenty-­five patients were recruited in each group. smoked ≤5 cigarettes per day. Both of them stopped smoking during
the treatment.
Majority of included patients showed reduced posterior height of
2.8.2 | Statistical method
the occlusion with proclined anterior teeth (80%). Most of them had
Statistical data analysis was performed using SPSS 20.0 program spacing in the upper and/or lower teeth and/or over-­eruption of inci-
package (SPSS Inc, Chicago, IL). sors. Nineteen (38%) patients had flared maxillary incisors. Dental mal-
Every data set was tested for normality by Shapiro–Wilk test. occlusions according to angle classification are described in Table 2.
Statistical analyses to compare two independent variables were con-
ducted using Student’s t test or Mann–Whitney U test.
3.3 | Adverse events
Wilcoxon signed-­ranks test was used for dependent variables.
A chi-­square test was used to compare the proportions of categor- One maxillary central incisor developed severe apical root resorption
ical variables between the groups. more than 1/3 of the root. Due to reduced bone level and extensive
To determine correlation between variables, Spearman’s coeffi- apical root resorption, this tooth was deemed for extraction after OT.
cient was used. One maxillary central incisor developed severe external root re-
Logistic regression analysis was performed to determine odds ratio sorption with extension to the pulp. This tooth was vital, resulted in
(OR) predictive values. CAL gain with PD <4 mm and was left for follow-­up.
ZASČIURINSKIENĖ et al. |
      219

T A B L E   2   Comparison of baseline parameters between test and T A B L E   2   (Continued)


control group patients included in the trial
Variable Test n = 25 Control n = 25 p value

Variable Test n = 25 Control n = 25 p value % teeth BoP

Teeth for ortho tx (n) 479 520 .8 Median (IQR) 95.7 (78.9, 100) 100 (77.5, 100) .4

Maxillary incisors (n) 90 95 CAL, clinical attachment level; PD, probing depth; REC, gingival recession;
Maxillary canines (n) 45 48 BoP, bleeding on probing; IQR, interquartile range; ortho tx ,orthodontic
treatment.
Maxillary premolars (n) 59 66

Maxillary molars (n) 41 48

Mandibular incisors (n) 87 94 3.3.1 | CAL change after periodontal–orthodontic


Mandibular canines (n) 46 48 treatment (T0–T2)
Mandibular premolars (n) 72 83 No difference in CAL change was found between test and control pa-
Mandibular molars (n) 39 38 tients. Twenty-­two (88%) patients in every group resulted in CAL gain.
n teeth with PD≥ 4 mm The values are presented in Table 3.
Mean (SD) 13.2 (5.70) 15.8 (5.96) .1

Age (years)
3.3.2 | T0–T1: Pre-­orthodontic treatment phase
Mean (SE) 47.31 (1.62) 43.49 (2.27) .2

Treated both arches n (%) 21 (84) 23 (92)


No difference in the median % of CAL change was found between test
and control groups. The overview of calculated values for comparison
Treated lower arch n (%) 2 (8) 1 (4) .4
is seen in Table 4.
Treated upper arch n (%) 2 (8) 1(4)
There was a significant difference in mean duration of the ini-
Sex n (%) 16 (64%) women 19 (76%) women
.4 tial (pre-­orthodontic) treatment phase between the test and control
9 (36%) men 6 (24%) men
groups (Table 5).
Smokers ≤5 cig/day n (%) 1 (0.04) 1 (0.04) .8

Dental malocclusion

Angle I 11 10
3.3.3 | T1–T2: Orthodontic treatment phase
Angle II 10 10 .7 Mean 20.6 (95% CI: 18.19; 22.93, range 7–28) teeth in the test group
Angle III 4 5 and 20.84 (18.47; 23.21, range 9–28) were incorporated in ortho-
Mean CAL of sites ≥4 mm dontic appliances (p = .8). Mean OT time did not differ between the
mm (95% CI) 5.28 (5.07, 5.49) 5.24 (5.02, 5.47) .6 groups (Table 5).

% sites CAL ≥4 mm


No difference in CAL change was observed between the test and
control groups after OT. The median % changes of sites for CAL, PD
Mean (SD) 47.6 (18.3) 53.5(19.7)
and REC are seen in Table 4.
Median (IQR) 45.7 (34.1, 57.1) 57.9 (36.5, 70.6) .2

Min–Max 25.0–84.5 17.5–82.1

Mean PD of sites ≥4 mm 3.3.4 | T0–T2: Whole periodontal–orthodontic


mm (95% CI) 4.99 (4.77, 5.22) 4.97 (4.80, 5.15) .9 treatment
% sites PD ≥4 mm Total periodontal–orthodontic treatment duration was signifi-
Mean (SD) 37.4 (17.2) 44.9 (18.4) cantly longer for the control group with mean time difference found
Median (IQR) 32.1 (24.0, 46.8) 48.2 (33.5, 59.5) .1 4.05 ± 1.59 months (Table 5).
Min–Max 14.5–77.1 9.82–82.1 A significant difference between the groups was found in median
Mean REC of sites ≥1 mm % of sites that changed to the lower disease group of PD (Table 4). This

(mm) 95% CI 1.57 (1.27, 1.86) 1.53 (1.24, 1.82) .9


difference was observed in sites with baseline PD of 4–6 mm, which
after combined treatment became <4 mm (Table 6).
% sites REC ≥1 mm
Tooth level analysis of PD change T0–T2 showed no significant
Mean (SD) 21.32 (17.73) 27.46 (19.77)
difference between different teeth and was mean 2.72 (SD 1.25) mm.
Median (IQR) 28.0 (7.7, 42.3) 13.8 (6.5, 35.9) .3
Univariate binary logistic regression analysis revealed statistically
Min–Max 0–80.7 0–66.7
significant association between PD improvement ≥2 mm and tooth
% sites plaque group (anterior/posterior) [OR 2.6; 95% CI: 2.03, 3.211, p = .001],
Median (IQR) 66.7 (46.2, 75.0) 65.9 (55.0, 80.3) .7 sex [OR 1.7; 95% CI: 1.29–2.12, p = .001], age group (≤35/>35 years)
[OR 1.4; 95% CI: 1.03–1.78, p = .03]. Analysis showed multicol-
(continues)
linearity between sex and age group (r = .327, p < .001). Multivariate
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220       ZASČIURINSKIENĖ et al.

T A B L E   3   Comparison of clinical
Test patients n = 25 Control patients n = 25
p attachment level (CAL) change between
Variable T0 T2 T0 T2 value test and control group patients before (T0)
and after (T2) periodontal–orthodontic
CAL (mm) (sites ≥4 mm) treatment
Mean (95% CI) 5.28 (5.07, 5.49) 4.85 (4.67, 5.01) 5.24 (5.02, 5.47) 4.81 (4.59, 5.04)
Median (IQR) 5.18 (4.85; 5.64) 4.83 (4.49; 5.11) 5.15 (4.84; 5.58) 4.70 (4.37; 5.05)
Min–Max 4.61–6.39 4.18–5.78 4.51–6.75 4.17–6.17
p = .0001** p = .0001**
CAL CHANGE (mm) (sites ≥4 mm)
Mean (95% CI) 0.44 (0.25, 0.62) 0.38 (0.18, 0.58)
Median (IQR) 0.40 (0.20, 0.59) 0.49 (0.12, 0.62) .59*
Min–Max −0.47 to 1.84 −1.34 to 1.02
CAL LOSS (mm) n = 3 n = 3
(sites ≥4 mm)
Mean −0.21 −0.58
Median −0.14 −0.35 .70*
Min–Max −0.47 to 0.02 −1.34 to 0.06
CAL GAIN (mm) n = 22 n = 22
(sites ≥4 mm)
Mean (95% CI) 0.51 (0.38; 0.64) 0.52 (0.35; 0.70)
Median (IQR) 0.50 (0.32; 0.66) 0.42 (0.27; 0.67) .50*
Min -­Max 0.08–1.2 0.08–1.84

CAL, clinical attachment level; IQR, interquartile range.


*Mann–Whitney U test.
**Wilcoxon signed-­ranks test.

binary logistic regression analysis (overall percentage of the model The change of sites with PD ≥4 mm was observed in both groups in
72.8%) revealed higher odds ratio for PPD improvement by ≥2 mm every treatment phase (Table 4). At the end (T0–T2), there were more
for anterior teeth [OR 2.5; 95% CI: 1.97–3.11, p = .0001] and teeth sites that changed PD class (healed) in the control than in the test group
in male patients [OR 1.6; 95% CI: 1.18–1.97, p = .001]. (Tables 4 and 6). Classified PD analysis showed that this difference was
As no difference in CAL change (Tables 3 and 4) after combined mainly in sites with initial PD of 4–6 mm (Table 6). This could probably
periodontal–orthodontic treatment was found between test and con- be explained by more sites with PD 4–6 mm at T0 in the control group.
trol patients, the null hypothesis was accepted. The method we used to classify pockets could also influence the re-
sult that PD of 4–6 mm remained in the same class. The pockets that
initially were 6 mm could heal to 4 mm, but we could not see that as
4 |  DISCUSSION they remained in the limits of the same class. However, deep periodon-
tal pockets (>6 mm) at T0 showed similar improvement in both groups
The present trial shows the overall favourable results of periodontal– (Table 6). Nearly half of them healed to the “healthy” status (<4 mm).
orthodontic treatment of patients with plaque-­induced periodontitis. In previous studies that were performed on periodontal patients, PD
To the best of our knowledge, the present study is the first RCT, reduction was also observed (Cardaropoli et al., 2001; Corrente et al.,
which is designed to analyse two different timings of PT in combina- 2003; Han, 2015; Re, Corrente, Abundo, & Cardaropoli, 2000).
tion with OT in patients with plaque-­induced periodontitis. Previously The multivariate binary logistic regression analysis showed greater
published clinical studies (Cardaropoli et al., 2001; Corrente et al., 2003; chance for PD improvement by ≥2 mm in anterior teeth and teeth
Melsen, 2001; Melsen, Agerbaek, & Markenstam, 1989; Re, Cardaropoli, in male patients. As mentioned before, 80% of patients had baseline
Abundo, & Corrente, 2004) evaluated OT effect on attachment appara- proclination of anterior teeth. So, anterior teeth were intruded and
tus, when surgical PT was completed 1–2 weeks before OT. retruded and this could influence difference in soft tissue response
(Figure 3).
Gingival recession is a common consequence of periodontal and
4.1 | Main findings
orthodontic treatment (Becker et  al., 2001; Lindhe, Socransky, Nyman,
The main clinical finding of the present trial was CAL gain observed in & Westfelt, 1987; Renkema, Fudalej, Renkema, Kiekens, & Katsaros,
both groups, in spite of the timing of the PT (Tables 3 and 4). CAL gain 2013). In the present trial, more sites resulted in REC in the control
was also reported in a study by Corrente et al. (2003), where intrusion group at T0–T1, and part of them improved during OT (Table 4). This
was used to replace migrated maxillary incisors. could happen due to orthodontic movements, as shown in earlier
ZASČIURINSKIENĖ et al. |
      221

T A B L E   4   Difference between the test and control group patients for changes during T0–T1 (initial periodontal treatment), T1–T2
(orthodontic treatment) and T0–T2 (total treatment) for clinical attachment level (CAL), pocket depth (PD) according to the baseline values
<4 mm, 4–6 mm, >6 mm, development of gingival recessions (REC), reduction in plaque and bleeding on probing (BoP)

Initial periodontal treatment T0–T1 Orthodontic treatment T1–T2 Total treatment T0–T2

Median (Q1–Q3) % Median (Q1–Q3) % Median (Q1–Q3) %


Group sites p value sites p value sites p value

CAL gain Control 6.3 (2.5–14.8) 14.1 (9.7–21.7) 25.0 (18.1–30.7)


.09 .23 .5
Test 4.0 (0–10.6) 17.0 (14.2–21.2) 23.2 (15.3–28.0)
CAL no change Control 93.4 (85.2–96.8) 83.3 (74.9–89.3) 73.2 (67.9–80.9)
.07 .47 .5
Test 96.1 (89.4–100) 82.1 (78.9–84.3) 76.9 (71.1–82.9)
CAL loss Control 0 1.0 (0–2.8) 1 (0–2.2)
.04 .1
Test 0 0 (0–1.7) 0 (0–1.3)
PD reduced Control 31.0 (14.8–45.6) 7.5 (4.3–14.6) 36.4 (24.9–51.2)
.002 .03 .05
Test 8.3 (1.6–23.2) 13.4 (9.8–18.7) 25.0 (16.7–36.5)
PD no change Control 69.0 (54.4–85.3) 86.6 (83.5–94.1) 62.0 (48.8–74.0)
.002 .29 .04
Test 91.7 (76.8–98.5) 85.9 (81.4–89.2) 75.0 (63.5–83.3)
PD increased Control 0 1.4 (0–2.8) 0 (0–1.1)
.001 .2
Test 0 0 (0–0.6) 0
REC Control −27.7 (−40.1 to −5.1) 4.2 (−2.5 to 10.8) −20.2 (−40.0 to −5.3)
development .003 .01 .2
Test −4.2 (−13.8 to 0) −3.6 (−7.4 to 4.4) −10.9 (−20.5 to −1.3)
PLAQUE Control 54.2 (41.0–65.5) 2.6 (−1.2 to 9.4) 57.1 (43.1–71.8)
reduction .74 .69 .9
Test 51.4 (41.6–62.2) 4.2 (0–10.1) 57.1 (45.3–68.7)
BoP reduction Control 73.7 (62.1–82.2) 4.8 (−1.9 to 12.1) 76.2 (68.1–85.2)
.04 .01 .7
Test 60.9 (46.1–76.8) 11.1 (6.4–16.7) 81.0 (66.7–86.0)

CAL, clinical attachment level; PD, pocket depth; REC, gingival recession; BoP, bleeding on probing; Q1, the first quartile; Q3 ,the third quartile; control
group n = 25, test group n = 25; p value by Mann–Whitney U test.

studies (Cardaropoli et al., 2001; Melsen, 2001; Melsen et al., 1989; The cooperation between one orthodontist (EZ) and ten periodon-
Re et al., 2004). For the test group, fewer sites developed REC during tologists was needed to perform the present trial. This can be a limita-
the initial PT. But the changes went in the opposite direction during tion but also a strength because it was possible to carry out the trial
OT with an increase in sites with recession development. This could in a reasonable time (6 years), and we were not dependent on a single
be related to the PT being performed simultaneous to OT for this periodontologist.
group. After T0–T2, there was no significant difference in median % Due to the absence of studies with comprehensive OT in patients
of sites with REC development between the groups (Table 4). with plaque-­induced periodontitis, especially RCTs, we were not able
Mean OT duration was similar for both groups and is in agreement to compare our findings.
with the findings of a recent review article, where the average com-
prehensive OT time was 20 months (Tsichlaki, Chin, Pandis, & Fleming,
2016). Based on the results of the present trial, total treatment time was 5 | CONCLUSIONS
significantly longer for the control group patients (Table 5). This differ-
ence for the control group was due to the longer PT phase before OT. If Both groups showed gain of clinical attachment level (CAL) and re-
the treatment duration is important for the patient, based on the find- duction in sites with probing depth (PD) ≥4 mm. No difference in
ings of this trial, final PT may be postponed and performed during OT. REC development between the two groups was observed. Total

T A B L E   5   Treatment time (months) for initial periodontal treatment, orthodontic treatment and total treatment

Initial periodontal Orthodontic treatment T1–T2 Total treatment T0–T2


treatment T0–T1 (months) (months) (months)

Group n Mean ± SE 95% CI p value Mean ± SE 95% CI p value Mean ± SE 95% CI p value

Test 25 1.38 ± 0.18 1.02 1.74 20.30 ± 1.22 17.78 22.83 21.68 ± 1.23 19.15 24.21
.0001 .57 .01
Control 25 4.56 ± 0.35 3.84 5.28 21.17 ± 0.88 19.36 22.98 25.73 ± 1.00 23.66 27.80

CI, confidence interval; p value by Student t test.


222      | ZASČIURINSKIENĖ et al.

T A B L E   6   Distribution of different pocket depth (PD) classes (<4 mm, 4–6 mm, >6 mm) in control (n = 25) and test (n = 25) patients at
registrations before (T0) and after (T2) combined periodontal–orthodontic treatment. Also change of PD class from T0 to T2

T0 T2 T0 and T2 T0–T2

% Sites % Sites % Sites


PD level change
PD (mm) Group Median (Q1–Q3) Median (Q1–Q3) (mm) Group Median (Q1–Q3) p value*

Control 51.8 (40.6–66.5)


<4 and <4a .13
Control 51.8 (40.6–66.5) 90.6 (84.1–95.7) Test 62.5 (50.5–74.0)
<4 Control 0 (0–1.1)
<4 and 4–6b .14
Test 69.4 (54.7–76.4) 93.8 (87.7–95.3) Test 0
Control -­
<4 and >6b -­
Test -­
Control 30.4 (18.8–45.9)
4–6 and <4c .03
Control 40.9 (26.8–50.0) 9.4 (4.3–15) Test 20.5 (13.6–25.5)
4–6 Control 6.5 (2.8–10.7)
4–6 and 4–6a .29
Test 26.4 (19.8–33.7) 6.0 (3.9–11.5) Test 4.5 (2.8–7.2)
Control -­
4–6 and >6b -­
Test -­
Control 1.3 (0–5.0)
>6 and <4c .52
Control 4.0 (1.0–8.7) 0 Test 1.1 (0–2.9)
>6 Control 1.2 (0–6.1)
>6 and 4–6c .69
Test 3.6 (1.1–6.7) 0 Test 2.0 (0–3.1)
Control -­
>6 and >6a -­
Test -­

PD, pocket depth; Q1, the first quartile; Q3, the third quartile; control group n = 25; test group n = 25; T0, baseline; T2, after total treatment.
a
No change.
b
Increase.
c
Decrease.
*p value by Mann–Whitney U test.

(a) (f)

(b)

(c)

(d)

(e)

F I G U R E   3   Treatment progress of Angle II-­1 patient with plaque-­induced periodontitis baseline (a), after periodontal treatment (b), during
orthodontic treatment (c, d) and after treatment (e) with straight-­wire mechanics and microimplant used for anchorage. Periapical radiograph at
baseline (f)
ZASČIURINSKIENĖ et al. |
      223

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4811714
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