Tooth Loss During Supportive Periodontal Care in a Strict Non-surgically Treated Cohort – a Retrospective Data Analysis

Background: This retrospective study aimed to evaluate tooth loss (TL) within a strict non-surgically treated patient cohort after supportive periodontal care (SPC) of 2.5-10.7 years. Methods: Data for non-surgically treated patients were checked for: complete periodontal examination data at baseline (T0), after active periodontal therapy (T1), and after ≥ 2.5 years of SPC (T2); Smoking, diabetes mellitus, age (at least 18 years), plaque and gingival indices, bleeding on probing (BOP), percentage of residual pockets, SPC adherence, and number of SPCs were assessed as risk factors for TL. Results: 132 patients were included (76 female, mean age 56.7±10.3 years), mean T1–T2: 4.5±1.6 years. 26.5% of all patients lost 118 teeth (0.5 teeth/patient, 0.12 teeth/patient/year). Plaque and bleeding parameters: mean plaque control record (PCR): 59.77±28.07%, mean papilla bleeding index (PBI): 47.46±34.12%, mean BOP: 33.46±21.52%. SPC duration (p=0.013) and T2 BOP (p=0.048) were identied as patient-related risk factors for TL. Conclusion: The strictly non-surgical approach within the reported cohort was characterized by elevated BOP, PBI, and PCR scores, possibly highlighting the lack of surgical intervention and regular SPC as negative effect. An apparently low TL rate could be observed. Duration of SPC and BOP (T2) were identied as risk factors for TL.


Introduction
Untreated periodontitis is a chronic in ammatory disease causing progressive attachment loss (1), possibly ending in tooth loss (TL) as true clinical endpoint (2). Studies from the last decades identi ed numerous risk factors for TL, including behavioral factors, such as smoking or lack of adherence to supportive periodontal care (SPC), medical factors, such as diabetes mellitus or the severity of initial periodontal diagnosis (3)(4)(5), and toothrelated factors, such as use as abutment tooth, bone loss, residual periodontal probing depths (PPDs), furcation involvement (FI), and tooth mobility (6-8).
Since the 1990s, established treatment concepts have primarily been based on supra-and subgingival nonsurgical debridement added by oral hygiene instructions and training (9,10). Currently, a three-stage therapy concept has been internationally implemented, which, after the preparatory (step 1) and non-surgical (step 2) phases, provides an optional surgical phase (step 3) before the patient is transferred to lifelong SPC (11,12). In detail, treatment concepts have varied in the last decades, especially regarding whether, when, and which surgical approach or antibiotic drug should be used (10,13,14). Several long-term studies based on combined treatment concepts, including patients who were treated both non-surgically and surgically, if necessary, reported low annual TL rates of 0.09-0.21 teeth/patient up to 25 years (4,6,8,15,16).
The e cacy of reducing PPD of 4-7mm and ≥ 7mm non-surgically was demonstrated early on (17)(18)(19). Whereas ap surgery combined with osteotomy compared to non-surgical treatment for teeth with PPD between 5-6mm exhibited a small average PPD reduction of 0.5mm, other surgical methods failed to show differences after ve years. For PPD ≥ 7mm, the same results were observed after six years (20).
This retrospective cohort study presents results of a strict non-surgically treated patient cohort during active periodontal treatment (APT) followed up for at least 2.5 years of SPC. It aimed to assess TL as the primary outcome variable at the Department for Conservative Dentistry at the University Hospital of Tuebingen (Germany) and evaluate the applied non-surgical concept and expand existing evidence regarding identi ed patient-related factors associated with TL.

Study design
This study is designed as a retrospective cohort study based on data analysis from patients treated between 1999 and 2015 who were identi ed through electronic database research at the Department for Conservative Dentistry at the University Hospital of Tuebingen. As the changeover to the electronic database took place in 1999, previous periodontal treatments were not identi ed. During this period, surgical therapy was not part of the periodontal treatment concept. The study protocol was approved by the University of Tuebingen Ethics committee (reference number 557/2016BO2) and was registered in the German Register of Clinical Trials (URL: https://www.drks.de; ID: DRKS00025110). An informal consent was not required for this type of study.

Inclusion criteria
The inclusion criteria include the following: complete periodontal examination (PPD at six sites/tooth, FI at all furcation sites of multirooted teeth (21), tooth mobility (22)) before start of therapy (baseline, T0) and after completion of APT (strictly non-surgical therapy) and start of SPC (T1); radiographs (panoramic radiographs or a set of periapical radiographs) not older than 12 months at T0; age ≥18 years at start of therapy (T0); no systemic antibiotic treatment during APT; T1-T2 duration of at least 30 months.

Applied treatment concept
Within the period between 1999 and 2015, APT encompassed two appointments of oral hygiene instructions with professional mechanical plaque removal (PMPR), followed by either the concept of Full-Mouth Disinfection (23) or, less often, the use of povidone-iodine (24) simultaneously with subgingival instrumentation. Re-evaluation was performed regularly 3 months after subgingival instrumentation. Periodontal examination (PPD at six sites/tooth, FI at all furcation sites of multirooted teeth, tooth mobility), PMPR, and subgingival instrumentation (at sites with PPD = 4mm with BOP and PPD ≥ 5mm) were conducted. Finally, according to the periodontal risk assessment (PRA) (25), patients were assigned to SPC.

Supportive periodontal care
All treatments were conducted by dentists in collaboration with dental hygienists, dental nurses, or supervised dental students. Moreover, SPC included the following sequence: 1. Plaque control record (PCR (26)) and papilla bleeding index (PBI (27)), 2. oral hygiene remotivation and reinstruction including recommendation of individually tting interdental brushes (Doft, Oesthammar, Sweden) and electronic toothbrushes.
3. PMPR followed by polishing with rotating rubber cups using pumice powder and Cleanic brand polish paste (Kerr GmbH, Biberach an der Riß, Germany) 4. dental and periodontal examination (PPD at six sites/tooth, FI at all furcation sites of multirooted teeth, tooth mobility), 5. subgingival instrumentation at sites with PPD = 4mm with BOP and PPD ≥ 5mm followed by instillation of 1% chlorhexidine gel (Chlorhexamed gel 1% GSK GmbH, Brentfort, UK), uoride gel application using Elmex gelee (CP GABA GmbH, Hamburg, Germany) or Duraphat (Colgate-Palmolive, New York, USA), and . periodontal risk assessment (PRA) to determine the SPC interval until the next appointment.

Patient charts
Periodontal examination charts for T0, T1, and T2 were assessed. For each patient, BOP (%); proportion of teeth with PPD < 5mm, PPD = 5mm, and PPD > 5mm; and the number of missing teeth were documented. Moreover, mean PBI (27) and PCR (26) during SPC period were calculated. Baseline radiographs were assessed to determine the maximum interdental bone loss visually. Furthermore, charts were screened for information on current smoking status (nonsmokers, former smokers (smoking stopped at least 5 years ago), or smokers (25)) and presence of diabetes mellitus. Initial periodontal diagnoses (28) were reclassi ed according to the current classi cation (29), which was performed using maximum baseline PPD, bone loss, presence of diabetes mellitus, smoking status and TL. The grade was assigned based on the bone loss age index and upgraded according to the diabetic and/or smoking status. An SPC frequency of at least 2 visits per year was considered as adherent.

Statistical analysis
The patient was considered a statistical unit. Overall TL during SPC (T1-T2) was considered the primary outcome variable and was calculated by subtracting the number of teeth. All other parameters were considered secondary outcome variables. The descriptive data were calculated as absolute or relative frequencies and mean (± standard deviation). Mean values and frequencies were compared using a paired t-test or chi-square test.
Negative binomial regression analysis was performed to identify factors in uencing TL during SPC. The variables (a) grading, (b) duration of SPC, and (c) relative distribution of PPD at T0 and (d) at T1 exhibited signi cant bivariate correlations with TL during SPC and were consequently put into the model. Third molars were excluded from the data analysis. A signi cance level of 0.05 was assumed. All statistical analyses were performed using computer software (IBM SPSS® Statistics 24 software package, IBM, Chicago, IL, USA).

Results
A total of 573 patient les was screened for eligibility. Thereof 441 were dropped out due to incomplete baseline periodontal status (n = 106), a follow-up period less than 30 months (n = 310), age < 18 years at start of therapy (n = 1) or systemic antibiotic treatment during APT (n = 24) ( Figure 1).

Baseline characteristics
In total, 132 patients (76 females, 56 males) with an average age of 56.7±10.3 years were included in the study. About 27% (n = 36) of all patients were smokers, and 9% (n=12) were suffering from diabetes mellitus. The average duration of SPC was 4.5±1.64 (range: 2.5-10.7) years. All patients showed a stage III periodontitis, most of them in grade B (n = 88, 66.7%).
At start of SPC, patients with TL were older compared to patients without TL (on average 0.5 years older, p=0.071). The relative proportion of smokers was higher when TL occured (p=0.494) as for patients with diabetes (p=0.901). Overall, 93% of patients were identi ed as non-adherent. The mean SPC interval was longer in patients with TL than in those without TL, yet the difference was not statistically signi cant (with TL: 15.55 months; without TL: 12.61 months, p=0.253) (Table 1). Moreover, 7 patients were non-surgically treated with povidoneiodine simultaneously with subgingival instrumentation.

Clinical parameters and tooth loss
Percentage distributions of clinical parameters, PPD, and BOP for each follow-up re-examination and mean PCR and PBI during SPC are presented in Table 2. In all groups, an increase in PPD < 5mm in favor of a decrease in PPD ≥ 5mm from T0-T1 and T0-T2 can be observed for the relative distribution of PPD. Mean BOP and PCR values during SPC were lower in patients without TL. Table 2 Descriptive data for PPD, BOP, mean maximum Boneloss, mean PCR and PBI on patient level according to TL PPD (%) <5 (mean±SD) PPD (%) =5 (mean±SD) PPD (%) >5 (mean±SD)   T0  T1  T2  T0  T1  T2  T0  T1  teeth overall, and three patients with grade A lost 13 teeth overall, which was the highest proportion. The relative proportion of patients with TL increased with a longer SPC period from 20-40% (Table 3).   In general, the study shows the positive effect of a strictly non-surgical therapeutic approach, but also allows the indirect conclusion that better therapeutic results could have been achieved if the international clinical practice guidelines for treatment of stage I-III periodontitis would have been applied (11).
Comparing the annual overall TL rate with studies with similar observation periods, lower to same annual TL rates of 0.06 -0.17 teeth/patient were reported (30)(31)(32). A prospective study over ve years reported a TL rate of 0.12 teeth/patient/year for an adherent subgroup of 96 patients, which is also in line with the overall results of our study. Within the same study, 116 non-adherent patients demonstrated a signi cantly higher TL rate of 0.36 teeth/patient/year (33). This result is threefold higher than the overall ndings in the present study and is comparable to nontreated periodontal patients with a reported periodontal TL rate of 0.33 teeth/patient/year over 40 years (2). However, due to the low number of adherent patients in the present patient cohort, further subanalyses were dispensed with.
Studies with observation periods of 10 years reported annual TL rates of 0.12-0.21 teeth/patient (6, 7, 34-37), and for periods of 17-25 years, annual TL rates of 0.09-0.14 teeth/patient were documented (15,16,38). However, these studies with longer SPC periods are not comparable to the present study due to increasing TL rates within longer observation periods (8, 16). A minority of 7 patients lost 50% of all teeth within the present cohort, which is also concordant with other studies (7, 39-43).
The present study was unable to recon rm some well-known risk factors for TL. The correlation of age with TL and the higher average T1 age for patients with TL (57.1 years) compared to patients without TL (56.5 years) were not statistically signi cant. Generally, age has been con rmed several times as a risk factor for TL during SPC (16, 30,35,39,42). This result might become even clearer through data from a long-term study over 20 SPC adherence was not identi ed as risk factor for TL, which might also result from the low number of adherent patients in the study (44).
Since all patients suffer from stage III periodontitis, the stage itself could not be analyzed as a risk factor for TL. A low number of patients at grade A (3.8%) and a majority at grades B (66.7%) or C (29.5%) was found. Grading was not identi ed as risk factor for TL. Surprisingly patients with grade A or B lost more teeth compared to patients with grade C. An explanation could be that in each group (grade A and B) one single patient lost 11 teeth (A), 9 teeth (B) resp., indicating that this might be a result of a prosthetic planning and not for periodontal reasons. In general, a retrospective determination of reasons for TL is di cult. Especially TL for periodontal, prosthetic, endodontic or restorative reasons highly depends on individual dentists´ decision biased by differences in experience and knowledge of appropriate evidence. To date, there is no uniform de nition for periodontal TL. On the other hand, SPC should primarly prevent TL for periodontal reasons, but not only. We found that maximal bone loss didn´t correlate with TL, which could indicate a high proportion of TL for nonperiodontal reasons within the observed cohort. Bone loss (8, 15,30), smoking (7,16,33,42,45), and diabetes with TL and indeed, this is a high degree of residual gingival and periodontal in ammation, which might result from the low annual SPC frequency mentioned above or the lack of surgical therapy. For BOP at sites ≤ 4mm, an odds ratio (OR) of 1.9-2.1 has been reported, with an increasing OR of up to 43.6 for PPD ≥ 7mm (46). These data might also indicate an increased risk for further TL in a longer observation period within the present cohort.
An oral-optimized healthy diet (47-49) or a paleo-type diet (50) has been shown to reduce periodontal bleeding parameters even in presence of plaque. Diet interventions could be an additional strategy for in ammation control in the future. Currently, more evidence regarding its e cacy is necessary (11). However, no data on nutrition were collected in this study.
In contrast to the SPC interval, the duration of SPC has been shown to correlate with TL. This result is related to the signi cantly higher age of patients with TL, as previously explained, which is in line with previous studies (6, 42). It seems plausible that more teeth are lost the longer the observation period increases. For this reason and the SPC range of 2.5-10.7 years in this cohort, the statistical model was adjusted for the SPC duration.
Overall, the decrease in PPD ≥ 5 mm from T0-T1 and T0-T2 indicates the e cacy of non-surgical therapy. Increased Baseline PPD were not identi ed as signi cant risk factor for TL. As mentioned, this could be another indication that decisions for extraction were predominantly not based on periodontal parameters. Moreover, the results generally indicate higher proportions of residual pockets compared to other ndings reported in both subgroups: a proportion of 3.5% (adherent) and 4.1% (non-adherent) with a PPD of 4 to 5mm, and 0.9% (adherent) and 1.5% (non-adherent) with PPD ≥ 6 mm (33). In contrast to the present study, Costa et al. consequently performed surgical treatment of residual pockets before SPC, resulting in a lower TL rate, which underlines the positive effect of surgical therapy as a complement to a primary non-surgical approach.
Over 11 years, an OR of 9.3 for TL has been reported for residual PPD of 6mm and 37.9 for a PPD ≥ 7mm (46).
Petsos et al. found a 1.5% proportion of sites with PPD ≥ 6mm at T1 and 1.9% at T2 with lower proportions in the group without TL (7). Considering these ndings, the higher proportions of residual pockets at T1 within the present population and the reported OR values for TL, it seems plausible that TL increases within a longer observation period. Recently published guidelines (11,12) recommend a surgical approach in cases with PPD ≥ 6mm. Increased residual pockets, bleeding, and plaque levels in a strict non-surgically treated cohort seem to support these recommendations.
This study has limitations, which should be critically addressed. First, this study has a shorter observation period compared to most recently published studies. Second, due to the lack of documentation of recessions and clinical attachment loss (CAL), no information on CAL development could be reported. Third, two non-surgical approaches were re-examined, possibly leading to a bias. Fourth, due to the retrospective nature of the study, TL in general and for periodontal reasons could not be distinguished, partly as a result of decisions for extraction by dentists in different elds and the high frequency of changing therapists during SPC. Fifth, since all of the patients included suffered from moderate periodontitis at the beginning of therapy, comparability with most studies is limited.

Conclusions
Even if the low TL rate of this cohort with stage III periodontitis patients, which was treated strictly in a nonsurgical way, is comparable with other cohorts that have also been surgically treated if necessary, a comparatively increased gingival and periodontal in ammation status is particularly evident. This possibly highlights the negative effect of the largely lack of adherence and/or the lack of a surgical approach. Duration of SPC and relative proportion of BOP at T2 were identi ed as risk factors for TL.