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Long‐term impact of powered toothbrush on oral health: 11‐year cohort study

Abstract Aims This study aimed to assess 11‐year longitudinal effects of powered toothbrush on periodontal health, caries and tooth loss in an adult population. Materials and Methods Participants of Study of Health in Pomerania (SHIP) cohort with dental examinations and interview data at SHIP‐1, SHIP‐2 or SHIP‐3 examinations were included. Mixed‐effects linear regression models were constructed between the exposure (manual versus powered toothbrush) and outcome variables (periodontal status using mean probing depth (PD) and mean clinical attachment loss (CAL), caries status using DMFS and DFS scores, and tooth loss), adjusting for potential baseline covariates. Results Final baseline (SHIP‐1) study sample comprised of 2,819 participants. Powered toothbrush users increased from 18.3% (SHIP‐1) to 36.9% (SHIP‐3); were younger; had significantly less mean PD [β: −0.09 (95% CI: −0.16; −0.02)] and mean CAL [β: −0.19 (95% CI: −0.32; −0.07)] progressions; and had 17.7% less DMFS progression and 19.5% more teeth retained than the manual toothbrushers. Conclusions In the long‐term, powered toothbrush seems to be effective in reducing mean PD and mean CAL progressions, besides increasing the number of teeth retained.

. If an improper technique is detected at a later point of life, it is difficult to modify it (Alcouffe, 1988). Furthermore, the fine motor skills might degrade with ageing and could impair maintaining proper oral hygiene in elderly people (Felder, Reveal, Lemon, & Brown, 1994;Hitz Lindenmüller & Lambrecht, 2011).
Powered toothbrushes (PTB) are advertised as having better biofilm removal capacity than manual toothbrushes (Verma & Bhat, 2004), which was attested by in vitro studies (Hunt, 2002;Schmidt, Zaugg, Weiger, & Walter, 2013). Under clinical settings, they were effective in removing plaque (Rosema, Slot, van Palenstein Helderman, Wiggelinkhuizen, & Van der Weijden, 2016) and tackling gingivitis (Yaacob et al., 2014). However, studies assessing the long-term effectiveness of PTBs on slowing initiation or progression of periodontitis are limited (Dentino et al., 2002;Dörfer, Staehle, & Wolff, 2016;Moritis, Jenkins, Hefti, Schmitt, & McGrady, 2008;Schmalz et al., 2017;Wilson, Levine, Dequincey, & Killoy, 1993); these studies mainly focussed on plaque, calculus or gingivitis. In addition to having employed small sample sizes (maximum of 180 subjects) and short follow-up times ranging from few weeks to a maximum of 3 years, these studies did not include tooth loss as an outcome, which is of paramount importance for patients. A recently published Cochrane review concluded "Powered toothbrushes reduce plaque and gingivitis more than manual toothbrushing in the short and long term. The clinical importance of these findings remains unclear" (Yaacob et al., 2014). Similarly, studies associating PTB usage with caries are limited (Papas et al., 2007;Willershausen & Watermann, 2001). Furthermore, prospective population-based cohort studies assessing the effectiveness of PTBs are unavailable as of now.
Therefore, in this study, we aimed to estimate the longitudinal effects of PTB usage on (a) periodontal health in terms of mean probing depths (PD) and mean clinical attachment loss (CAL), (b) coronal caries experience using decayed, missing and filled surfaces (DMFS) and decayed and filled surfaces (DFS) scores and (c) number of teeth present using 11-year data from the representative population-based cohort, Study of Health in Pomerania (SHIP).

| Study population
The study sample was obtained from the ongoing prospective cohort study (SHIP), which adapted a two-stage cluster design (Keil et al., 1988). The cohort was initiated in 1997-2001 and was followed up after 5 (SHIP-1), 11 (SHIP-2) and 16 years (SHIP-3) (Völzke et al., 2011). Since information about the PTB usage was not available in SHIP-0, we considered the data from SHIP-1 as baseline examination and SHIP-2 and SHIP-3 as the 6-and 11-year follow-ups, respectively. Participants with information on exposure, outcomes and covariates within at least one examination were included in the study. The study started with a sample of 3,300 participants at baseline. The flow of study participants in the study is shown in Figure 1.
The study protocol was approved a priori by the ethics committee of the University of Greifswald, and written informed consent for the interviews, clinical and dental examinations was obtained from all the participants.

| Dental examination
Dental examinations were performed by calibrated and licensed dentists. Initial training was conducted by a periodontist (TK). The intra-rater and inter-rater reliability values are shown in Table S1.
Identical recording protocols were used for all time points. From the dental examination, number of teeth present (full mouth), PD, CAL, DMFS score and DFS score were calculated. Detailed information on the dental examination can be found in the supplementary material.

| Interviews and medical examination
Trained and certified interviewers conducted computer-assisted personal interviews for participants during all the visits to collect information on the exposure and covariates. Participants were asked whether they used powered or manual toothbrush at each time point from SHIP-1 to SHIP-3. Based on the toothbrushing frequency, participants were categorised into irregular (<2 times/day) or regular brushers (≥2 times/day). Classification of covariates considered in the study (educational status at the start of study, smoking status, toothbrushing frequency, dental visit in the last 12 months, periodontal treatment in the last 5 years, diabetes, physical activity and Centers for Disease Control and Prevention/American Academy of Periodontology (CDC/AAP) case definition of periodontitis) are mentioned in Table 1. Body mass index (BMI) was calculated as weight in kg/(height in m) 2 . At baseline (SHIP-1), known diabetic cases, defined as diagnosed cases according to self-reported physician's diagnosis or treatment with anti-diabetic drugs (Anatomical Therapeutic Chemical Classification System code A10), were recorded. Prevalent cases based on information from SHIP-0 were combined with incident cases between SHIP-0 and SHIP-1. Blood samples were drawn at non-fasting status to determine HbA1c levels using HPLC method (Bio-Rad Diamat, Munich, Germany).

Clinical Relevance
Scientific rationale for the study: Powered toothbrushes have been in the market for quite a long time and, their effectiveness has been shown in a number of clinical or observational studies. However, long-term effectiveness of powered toothbrushes in a population-based study has never been performed.
Principal findings: Powered toothbrush users had reduced progression of probing depths and clinical attachment loss.
On the long run, this has been translated into retaining more number of teeth.
Practical implications: Powered toothbrush seems to be an effective (preventive) tool in maintaining oral hygiene.
Therefore, dental practitioners might recommend its usage. number of teeth present. Continuous and categorical variables were compared using Student's t test and chi-square test, respectively. To assess the longitudinal effects of PTB usage on different outcomes, mixed-effects linear regression models over three time points were constructed for each outcome using the entire sample. The time variable was divided by 11, to obtain estimates that reflect the effect of PTB usage 11 years from baseline, which was the time span between SHIP-1 and SHIP-3. All covariates were selected a priori, based on the clinical knowledge. Models were constructed with subject ID and time as random intercept and slope, respectively, so that they took into effect the repeated measurements within subjects at different follow-ups, which denote the multiple levels. The advantage with mixed-effects modelling approach is that it requires complete datasets at each follow-up separately, but not across examinations.

| Statistical analyses
All models were adjusted for baseline (SHIP-1) covariates, such as age, sex, BMI, education, smoking, diabetic status, HbA1c values, frequency of toothbrushing and history of dental visit in the last 12 months. Physical activity was included as additional covariate in the number of teeth present models. Mean PD and CAL models were additionally adjusted for physical activity and history of periodontal treatments during the past 5 years; but the random slope was excluded as the models did not converge. Age was included in the model as a restricted cubic spline with three knots. The adjusted estimates  Analyses were restricted to the following subsets: (a) regular brushers (n = 2,464 at SHIP-1), (b) younger subjects (25-55 years, n = 1,617) and (c) younger regular brushers (n = 1,403). After initial analyses, participants were stratified based on the CDC/AAP case definition of periodontitis to observe if the severity of periodontal disease had an influence on the association with PTB, and all models were repeated. Furthermore, sensitivity analyses were performed on the entire sample models by including subjective influence on oral hygiene, inter-dental aids usage, screening for preventive medicine and cancer or preventive dental screening (Table S5). Additionally, to avoid over-adjustment, we performed directed acyclic graphs (DAGs) for each outcome spectrum (periodontitis, caries and no. of teeth present) (Textor, Hardt, & Knüppel, 2011). DAGs for each outcome resulted in adjusting for age, sex, education, toothbrushing frequency, dental visit in the last 12 months and history of periodontal treatment within the last 5 years ( Figure S1). Thereafter, models were constructed adjusting for these variables under each outcome. The recommendations of the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines for observational studies were applied for reporting (von Elm et al., 2014).

| Baseline characteristics
A total of 2,819 participants with mean age of 52.1 ± 14.4 years were included in the model (Table 1). PTB users were younger (46.3 years) than the MTB users (53.4 years). PTB users fared well in education, toothbrushing frequency, dental visit in the last 12 months, diabetic TA B L E 1 Baseline characteristics (SHIP 1) for participants present in the final model

| Association between PTB usage and periodontal measures
After adjustment, PTB usage was significantly associated with reduced mean PD and mean CAL progression in the entire sample as well as all subsets (Table 3). "PTB usage" denotes the effect of PTB usage on dependent variable for time = 0 (baseline/SHIP-1). Time

| Association between PTB usage and caries
With respect to caries, PTB users had lower DMFS and DFS scores throughout the study period (Table 2). On further exploring the data after adjustment (

| Association between PTB usage and number of teeth present
PTB users also had significantly less number of teeth lost over 11-year follow-up, indirectly leading to more number of teeth present (  Published short-term studies on PTB usage showed better plaque control and reduced gingivitis, but the present longitudinal study showed for the first time that these effects are likely to get translated into reduced progression of PD and CAL. Also, more retained teeth speak in favour of a clear tangible health benefit of PTB.

| D ISCUSS I ON
The main strength of the present study is that prospective data from a population-based cohort with a follow-up time of 11 years have been analysed. Our study had the benefit of extensive dental data in terms of surface-level periodontal measures and caries data.
We identified and adjusted for commonly observed covariates such as age, sex, BMI, education, smoking, diabetic status, HbA1c values, toothbrushing frequency and history of dental visits, in addition to periodontal treatment history and physical activity in some models.
Our study also had its share of limitations. It might be argued that PTB users were younger in age, with better education, and oral health awareness, in addition to having better physical activity. However, the associations observed in this study were not lost even after adjusting for all the relevant factors, although residual confounding cannot be excluded. Furthermore, when the entire sample models were additionally adjusted for subjective influence on oral hygiene, inter-dental TA B L E 3 Results from mixed-effects linear models evaluating the effects of powered toothbrush usage on rates of change in oral health parameters   aids usage, screening for preventive medicine and cancer or preventive dental screening, none of these variables failed to elicit significant effect on the estimates. To avoid over-adjustment, based on the information from DAGs, models were adjusted only for age, sex, education, toothbrushing frequency, dental visits in the last 12 months and history of periodontal treatment within the last 5 years. This conservative approach did not alter any of our results (Table S6).
Periodontal and caries examinations were recorded using halfmouth basis, which might not reflect the absolute values, although it has less bias in comparison with full-mouth method (Tran et al., 2016). Furthermore, caries was recorded only on cavitation level.
Leaving out non-cavitated caries lesions would have under-represented the caries burden in this study. Information on PTB usage was obtained only through a simple question with binomial answer possibility. In addition to usage of PTB in combination with MTB, differentiation between different types of PTB, that is oscillatory vs. vibratory, battery-powered vs. electric, sonic vs. ultra-sonic, was not measured, especially when there were studies reporting differences among them (Deacon et al., 2010;Rosema et al., 2016).
However, the differences between the different types of PTB are not well studied, and more focus in this direction is needed.
Because it is not plausible to perform a long-term randomized controlled trial to test the effectiveness of PTBs over MTBs, evidence from well-designed population-based cohorts/practice-based research is relevant for the dental community.
Although the effectiveness of PTB on periodontitis has been well documented in the literature (Forrest & Miller, 2004;de Jager, Rmaile, Darch, & Bikker, 2017;Yaacob et al., 2014), the evidence arriving from long-term studies is limited (Ainamo, Xie, Ainamo, & Kallio, 1997;Dentino et al., 2002;Dörfer, Joerss, & Wolff, 2009;Dörfer et al., 2016). In a 12-month longitudinal study, Ainamo et al. (1997) found PTBs to be effective in controlling gingivitis in terms of reducing bleeding on probing, but they were not significantly better in removing plaque. Dörfer et al. (2016) performed a randomized study with the longest follow-up time of 3 years, in which they did not find any significant differences in PD and CAL progression between PTB and MTB users with pre-existing recessions >2 mm.
However, as shown in a recent meta-analysis (Yaacob et al., 2014), the use of a PTB results in less supragingival plaque, which in consequence prevents or decreases the magnitude of gingivitis. An improved oral hygiene has an effect on preventing the transition from gingivitis to periodontitis rather than the progression of periodontitis (Hellström, Ramberg, Krok, & Lindhe, 1996;Ramseier et al., 2017;Schätzle et al., 2004). In line with this observation, we could see that PTB had a distinct effect in reducing the PD and CAL progression in subjects affected with no/mild or moderate periodontitis, whereas the subjects with severe periodontitis did not benefit from the better oral hygiene through PTB usage (Hellström et al., 1996). Although the magnitude of change in PD and CAL among subjects with severe periodontitis was in line with the moderate periodontitis subjects, the effects were not significant, presumably due to the reduced sample size. Furthermore, it could be observed that the mean age of the PTB users was significantly lower than the MTB users. In addition to oral hygiene, progression of the periodontal disease in elderly people is influenced by many other factors (Lamster, 2016), which might not be counteracted by toothbrushing alone. Ramseier et al. (2017)  periodontitis, further loss of attachment and ultimately tooth loss.
Our data may be interpreted that subjects using a PTB experience less attachment loss, which after 11-year follow-up resulted on average 0.36 more teeth than the MTB users. Furthermore, subjects with no/mild periodontitis had 0.19 more teeth retained than their MTB counterparts.
To our knowledge, the number of studies assessing the relationship between caries and PTB is rare. In an interventional study among drug-induced xerostomia patients (N = 80) with a follow-up time of 1 year, Papas et al. (2007) recorded a significant reduction of root caries among PTB users. Willershausen and Watermann (2001) performed an interventional study (N = 40) with a 3-year follow-up on elementary school children, but did not observe any benefit of PTB on caries prevalence. A systematic review conducted on seven studies assessing influence of oral hygiene in the absence of fluoride on dental caries concluded "Personal oral hygiene in the absence of fluorides has failed to show a benefit in terms of reducing the incidence of dental caries" (Hujoel, Hujoel, & Kotsakis, 2018).
In line with this argumentation, lack of association between PTB usage and DFS seems plausible. However, PTB usage was associated with less DMFS progression, and this was due to the influence from the M-component, which is a predominant feature in the elderly population.
There has been a significant association of PTB usage with more number of teeth retained in the entire sample and in the regular brushers' subset. Based on this, it is evident that the PTB usage on the long run helps in preventing tooth loss and maintaining the number of teeth in the oral cavity. From this study, it could be seen that the TA B L E 4 Results from mixed-effects linear models evaluating the effects of powered toothbrush usage on rates of change in periodontitis models stratified by CDC/AAP definition Note: All models were adjusted for baseline covariates, such as, age, sex, education, smoking, BMI, diabetic status, HbA1c values, toothbrushing frequency, dental visit in the last 12 months, physical activity and history of periodontal treatment in the last 5 years. Subject ID was constructed as random intercept. Abbreviations: β: beta coefficient; 95% CI: 95% confidence interval. CDC/AAP: Centers for Disease Control and Prevention/American Academy of Periodontology. PD: probing depth; CAL: clinical attachment loss; DMFS: decayed, missing, filled surfaces; DFS: decayed, filled surfaces. PTB usage: Effects of powered toothbrush usage on dependent variable for time = 0 (baseline/SHIP-1). Time (per 11-year increase): Rate of change for manual toothbrush user over 11-year follow-up period. Interaction: Exposure-dependent (PTB versus MTB) difference in the rates of change over 11-year follow-up period. a Models were performed without the inclusion of random slope.
PTB usage may have a long-term protective effect on the oral health in general. It could also be seen that there has been a gradual increase in the usage of PTB over time. The reasons for this might be increased advertisements and dentist recommendations. German Oral Health Study showed that recently there has been an increase in the usage of inter-dental cleaning aids (Jordan & Micheelis, 2016). This, in addition to increased PTB usage as observed in the SHIP cohort, reflects the increased awareness of German population towards oral hygiene.

| CON CLUS ION
From the results in this study, it could be seen that the PTB usage has a long-term protective effect on the oral health in terms of reduced probing depths, clinical attachments and number of teeth lost.
Based on this, it seems that the PTB usage in the long run helps in maintaining the number of teeth in the oral cavity and reducing the progression of periodontal disease burden.

ACK N OWLED G EM ENTS
The authors thank the study participants and all contributions to the SHIP data collection by dental and medical examiners, technicians, interviewers and assistants.

CO N FLI C T S O F I NTE R E S T S
Prof. Dr. Thomas Kocher had received grants from Procter and Gamble Co. to pay the salary for a scientist for 6 months, which did not have any influence on the study design, data analysis and interpretation of the results. The authors declare no potential conflicts of interest with respect to the authorship and publication of this article, and this includes financial interests.