Abstract
Periodontal diseases (PD) are complex, multifactorial disorders. Effective daily plaque control promotes gingival/periodontal health. Recent meta-analyses and other reviews have found inconclusive evidence to support that tooth flossing promotes gingival/periodontal health. Ideally, the claim should have been that, “at present, we do not have high-quality evidence from well-designed randomized clinical trials (RCTs) to determine whether flossing lowers the risk for periodontal diseases.” Rather than “not proven to be effective,” the lay public may now think that flossing is “almost entirely unhelpful and/or unnecessary.” How does the dental community communicate the nuances of this topic? Herein, we examine the key structural issues underlying this area of research. We assert that effective flossing between specific teeth can promote gingival/periodontal health. Further, we explore the nuances of for whom this may be true and untrue, why our evidence is lacking and what can be done to clarify the effectiveness of flossing on clinical outcomes.
Keywords: flossing, oral hygiene, periodontal diseases, interpreting evidence, self-report, behavior change
Introduction
A majority of oral health care providers in the United States of America probably still recommend flossing and likely believe that effective tooth flossing can promote gingival and periodontal health. And yet, by examining recent Cochran Reviews (CRs)1, 2 and meta-reviews3, 4, the media and lay public has begun to seriously question whether flossing should be performed at all. Is such a conclusion potentially flawed? We would argue that at the very least, this conclusion is premature and maybe fundamentally inaccurate. Here is why:
POOR QUALITY EVIDENCE: Even the authors of the recent CRs examining flossing state that “The trials [used in their review of flossing] were of poor quality and conclusions must be viewed as unreliable.”1 While technically the evidence for flossing is weak, more importantly the methodology and rigor of the studies examining flossing effectiveness are also weak. The latter statement appears not to be stressed enough.
LIMITED SCOPE OF RESEARCH QUESTIONS ADDRESSED: CR’s, the primary source of the media reasoning, use only a handful of all available RCTs to answer very narrow questions. For example, the CR’s examined RCTs that studied tooth brushing and flossing versus flossing alone at 1, 3 and 6 months and using only plaque and gingival indices as outcomes (i.e., surrogate endpoints instead of long-term measures of periodontitis) 1.
LIMITED EVIDENCE/ OTHER AVAILABLE EVIDENCE: CRs focus solely on RCTs (a small percent of all types of studies), and not all questions can be easily or, at times, ethically be addressed by RCTs (e.g., randomizing people to not brush their teeth). Focusing on CRs and a limited number of RCTs that were based upon low-quality evidence at the expense of the complete body of evidence may be limiting and could be viewed as selectively interpreting findings out of context. As well, there is a plethora of evidence (albeit from studies that are not RCTs) to support that regular effective flossing can promote gingival and periodontal health. If the current “best evidence” is of admittedly low-quality, how can we trust conclusions based upon these data? As well, the FDA classifies floss as a Class I device, meaning it has the lowest risk and no mandate for manufacturers to perform evaluative studies5, 6. This may help explain the lack of more extensive research in this area.
SELF-REPORTED DATA: The CRs examining flossing are based on RCTs that rely on patient self-reported assessments of flossing behavior. Notably missing from these studies is both independently verified patient frequency of flossing and, importantly, reliable assessments of the quality of patients’ flossing 7.
INTERPRETATION OF REPORTED FINDINGS: Guidelines are not well established for how dental clinicians should interpret CRs within the context of other evidence, especially when such findings are applied to a specific patient’s unique clinical presentation.
As with the implementation of almost all health behaviors, there are many nuances that scientists and practitioners must understand and address in order to conduct rigorous research and/or adequately advise individual patients in a clinical setting. For example: which individuals need to floss? How often? Does one need to floss all their teeth? At what level of skill does one need to floss (i.e. average or expert skill level)? To what degree can one’s flossing skill be improved? Also, PD are multifactorial disorders; there are numerous and complex risk factors for PD as well as many different phenotypes8, 9 or classifications of PD. Further, not all risk factors are under a person’s control. Is the dental research community and the media taking a single prevention modality (e.g., flossing) out of the context of its multifactorial causation10, 11? When we do not consider factors such as patient skill level and frequency of tooth brushing behavior, level of motivation, specific type of PD, genetic predisposition, medical status and socio-economic factors—then, are we being, well, just too reductionistic?
While previously we addressed the issue of whether flossing could help protect against dental caries7, in this article we extend the focus of this piece to include emphasis on point #3, mentioned earlier, to support that, for most people, effective flossing (see YouTube video12) and/or interproximal cleaning can promote gingival and periodontal health.
First, let us take a step back and re-frame the utility of flossing from another perspective. To further highlight the central issues, we will ask and answer a series of questions. We chose this question and answer format in order the specifically highlight the issues central to our argument and our point of view. Using this approach, we will “unpack” the recent media story (Saint Louis, New York Times (NYT), Aug 2, 2016) that was, at best, suspicious of flossing to prevent PD. As well, the European Federation of Periodontology (EFP) recent reports have recommend interdental brushes and essentially stopped short of endorsing flossing, but suggested it could have some value in limited circumstances13, 14.
Question (Q1A) The media report (Saint Louis, NYT, Aug 2, 2016), suspicious of flossing, was based on what evidence? (Q1B) What about the recent EFP reports13, 14?
Answer (A1) The primary source information was a CR that itself was based on 16 studies, all RCTs, in which the authors found little evidence to support flossing as being an effective preventative practice; however, the caveat is that the authors also clearly stated that: “The trials [RCTs used in their review] were of poor quality and conclusions must be viewed as unreliable”1. (A1B) Much like the primary CR, the analyses and reviews cited by the EFP 13, 14 also had significant methodological limitations7 (also see discussion of limitations later question #6 of 10 Critical Questions to Establish the Effectiveness of Flossing).
(Q2) Is there reasonable evidence from studies other than RCTs (described later, see question #5 of 10 Critical Questions to Establish the Effectiveness of Flossing) to inform us on the usefulness of flossing?
(A2) Yes, but we would need to critically evaluate and integrate these studies into logical conclusions which would also have significant limitations. Therefore, herein we have tried to pinpoint the most critical limitations of the current evidence in hopes that they can be addressed in future research.
(Q3) How can we establish guidelines for whom dental flossing is clinically meaningful?
(A3) We would need new studies that: i) use a valid and reliable measure of tooth brushing and flossing skill7, ii) thoroughly characterize research participants at study entry (assess all relevant clinical and socio-demographic characteristics) and identify critical variables (quantify/verify daily oral hygiene behaviors; identify the type/extent/severity of PD at study entry) as well as potential confounding variables and/or covariates (i.e., age, number of teeth, risk factors for PD, access to and prior use of oral health care services), and then iii) implement next-generation sequential multiple assignment randomized trials (SMART Studies) 15, 16 that follow and assess participants longitudinally and, based upon assessment of clinical outcomes at pre-determined time points, allow multiple randomizations per study participant15, 16. The use of randomized longitudinal, intra-individual designs in which patients are matched based upon similar baseline characteristics, would allow for more thorough assessment of the nuances and confounding factors that we believe may previously have comprised the outcomes of flossing effectiveness studies. Such SMART studies could even be coupled with a split mouth study design to help determine the requisite level of oral hygiene self-care for a given person with a specific baseline presentation. Findings from such studies could help provide guidelines for oral health providers to address the needs of specific individuals that present in a clinical setting.
Background/Overview
To fully address flossing in the context of PD, there are a number of important topics that need to be understood in some detail. We will ask a series of question and answer them in paragraph form. These questions include: 1) What is PD? 2) How do we define PD? 3) Is it Fair to Say There Are Phenotypes of PD? If so, Why Does it matter? 4) Does lack of plaque control contribute to PD? 5) Does effective flossing promote gingival and periodontal health? 6) How are systematic reviews and meta-analyses a source of controversy? 7) Do multi-level influences of PD add complexity to longitudinal studies? 8) Flossing vs. the use of inter-dental brushes(IDB)—do we know all we need to know yet? 9) How can an objective measure of tooth brushing and flossing help clarify this topic? 10) How can SMART studies help us gain clarity on the utility of flossing?
10 Critical Questions to Establish the Effectiveness of Flossing
1) What is PD?
Periodontal diseases (PD) are comprised of gingivitis and periodontitis17.PD are multifactorial disorders that involve inflammation-mediated destruction of tooth-supporting tissues and bone. Influenced by genetic predisposition, lifestyle and environmental factors14—PD is played out in an ongoing interaction between the dental biofilm and the host’s immune system. Both gingivitis and periodontitis develop in response to bacterial biofilms (also termed “dental plaque”). Dental plaque is a dynamic microbial biofilm/ecosystem that contains hundreds of bacterial species18. The biofilm initiates with adherence of certain bacteria, such as Streptococcus species, to oral surfaces that contain saliva. Then, later-colonizing species attach to the primary-colonizing bacteria. In the absence of established oral hygiene for 2–3 weeks, individuals can develop gingival inflammation19. Gingivitis does not always evolve into periodontitis20; however, periodontitis is always preceded by gingivitis21. According to Kinane and Attstrom, 2005, gingivitis and periodontitis are on a continuum of the same inflammatory disease17.
Whether an individual develops periodontitis depends on the host’s susceptibility to elicit an inflammatory response when dental plaque has accumulated on teeth at and below the gingival margin. This predisposition is in part governed by genetic factors as well as and behavioral factors such as smoking22, nutrition14 and medical illnesses such as diabetes 23, HIV-related immunosuppression24 and other factors 23.
2) How do we define PD?
Past research studies have used various definitions or classifications of PD25–27. This factor alone can influence study findings and complicate comparing findings across studies. Presently, investigators can help address the issue of how to define /classify PD by using multiple definitions, which can allow for greater comparison across studies.
3) Is it Fair to Say There Are Phenotypes of PD? If so, Why Does it Matter?
It is now recognized that there are distinct phenotypes of cancer28 and obesity29. Based on the work by Offenbacher et al, 2007 and 20088, 9, one can also argue that there are phenotypes of PD within a population. Using a sample size on nearly 6,768 patients, Offenbacher et al (2007) developed new clinical categories of gingivitis and PD representing distinct biological phenotypes; these were based on distinct patterns of biofilm composition, humoral antibody response, and local inflammatory mediator levels thus characterizing the biology of the biofilm–gingival interface (BGI). The five BGI clinical conditions, each reflecting different underlying biological phenotypes, were defined using varying levels of probing depths (PDs) and sites with bleeding on probing (BOP)8, 9. The BGI clinical categories are clearly different from the more established or “traditional” definitions of periodontitis that focus on clinical attachment loss (CAL)—perhaps because it was developed with an intent of examining a periodontal-systemic link. Recently, a longitudinal intervention study by using an HIV+ cohort found that biologically-based BGI classification differentiated baseline profiles of PD and changes over time in levels of PD 30 better than traditional measures such as the American Academy of Periodontology (AAP) 26 and the Centers for Disease Control with the American Academy of Periodontology (CDC/AAP)31 which focus on CAL. Such results suggest that the BGI system may have utility in longitudinal studies of flossing/interproximal cleaning.
If indeed there are phenotypes of PD, then baseline characterization of PD is critical because it is possible that the individual/group-level natural progression and/or response to treatment may differ across phenotypes. This could be an important consideration for sampling. Lumping all subjects into one definition of PD (e.g., those based on CAL) may, however, lead to misclassification which can limit the reliability and/or generalizability of research findings.
4) Does the Lack of Plaque Control Contribute to PD?
Unremoved dental plaque can lead to gingival tissue irritation/inflammation which may then also promote PD. In a classic naturalistic study by Loe et al, 1986, a caries-free cohort study of male Sri-Lankan tea workers were followed longitudinally32. Individuals in this cohort did not perform oral hygiene and had no treatment or prevention of oral diseases. Across 15 years, 8% had rapid progression of PD (aggressive periodontitis), 81% had moderate progression (chronic periodontitis) and 11% had no progression of PD (they were healthy without prevention)32. Tooth loss increased with severity of periodontitis. Findings from this study suggest that, in the absence of oral health prevention and dental treatment, most people developed at least moderate PD32.
Conversely, Lang et al, 1973 demonstrated that plaque removal by tooth brushing, coupled with effective interproximal plaque removal at least once every 24 hours, can prevent the onset of gingivitis33. As well, effective interproximal oral hygiene helps to reduce the extent and severity of PD, and (if also coupled with effective scaling and root planing, when indicated) may even help halt the progression such oral diseases34.
5) Does Effective Flossing Promote Gingival and Periodontal Health?
There are a number of cross-sectional and longitudinal (non-RCT) studies that conclusively support the utility of effective flossing to promote oral health. Walsh and Heckman (1985) reported that patients using dental floss had decreased bleeding on probing (BOP)35. Graves et al. (1989) found that tooth brushing reduced interproximal bleeding by 35% but the use of dental floss further decreased bleeding by 67%36. Lang et al (1995) examined 319 individuals and found that those subjects who exhibited acceptable flossing ability had less plaque and calculus, shallower pocket depths, and less attachment loss than those with unacceptable flossing skill; in regression analyses, brushing thoroughness, flossing ability and frequency, and dental visit frequency were predictors of lower levels of plaque, gingivitis, and calculus37. Barendregt et al (2002) determined that flossing as the sole form of oral hygiene was effective in preventing the development of gingival inflammation and reducing the level of dental plaque38. Lewis et al, (2004) longitudinally examined 55 adults with gingivitis or slight chronic periodontitis, and found at 12 weeks that plaque scores and bleeding were reduced in the group randomized to flossing as compared to a group that used a toothpick-holder39. Crocombe et al, 2012, obtaining data from the National Survey of Adult Oral Health 2004–06, found that regular interdental cleaning was associated with better oral hygiene outcomes (lower levels of dental plaque and gingivitis); however, there was no significant association between regular interdental cleaning and clinical attachment loss40, suggesting potentially that non-behavioral factors (i.e., host predisposition) may have a greater influence on CAL.
6) How Are Systematic Reviews and Meta- Analyses a Source of Controversy?
Recent findings from meta-analyses and systematic reviews have raised questions as to the effectiveness of flossing1–4. In a meta- analysis- by Sambunjak et al. (2011) the authors reported some evidence from 12 studies that flossing in addition to tooth brushing reduces gingivitis compared to tooth brushing alone. They determined that “there is weak, very unreliable evidence from 10 studies that flossing plus tooth brushing may be associated with a small reduction in plaque at 1 and 3 months”1.
In a more recent consensus report drawing off meta-reviews and systematic reviews, Chapple et al, 2015, asked : “Does daily interproximal cleaning in addition to tooth brushing reduce gingival inflammation and does it also reduce interproximal plaque levels compared to tooth brushing alone?”13 The authors found that there is “very inconsistent/weak evidence for an adjunctive effect of interproximal cleaning to brushing, either due to a lack of efficacy (flossing) or a lack of evidence from appropriate clinical investigations”13. Interestingly, they found limited evidence that IDB use (or other interproximal cleaning) reduced gingival inflammation. The reasons for this, according to Chapple et al, 2015, may be related to the limitations of the gingival indices used, the variability of outcome measures used (i.e., gingival inflammation vs. plaque) or the variability of study designs13. As stated earlier, to this list we would also add not having a measure of oral hygiene skills7.
Further, in the report by Chapple et al, 2015, no RCTs were identified which assessed whether individual sites without attachment loss and no signs of gingival inflammation (healthy sites) would benefit from daily interproximal plaque control13. Thus, it is unknown whether effective flossing (in sites initially too small to use IDBs) can help maintain healthy and tight gingival margins around teeth—that is, maintain a first line of defense against PD.
7) Do Multi-Level Influences of PD Add Complexity to Longitudinal Studies?
Other host and environmental factors may influence the progression on PD over time. Such factors include genetic predisposition, personal level factors (diet, smoking status home care, medical conditions) the access to and use of oral health care services, and, more recently, even epigenetic factors41. Collecting accurate data on such variables can be an important consideration for longitudinal studies. Given the advent of electronic medical records, large-scale, multi-site naturalistic databases could be used to collect and analyze findings to strengthen the evidence base—provided that variables are consistently defined, measured and updated on regular and ongoing basis.
8) Flossing vs. the Use of IDB—do we Know all we Need to Know Yet?
Recently, the EFP, citing a lack of evidence, did not endorse flossing to prevent dental caries and gingivitis; instead, they advocated the use of interdental brushes (IDBs), citing greater current evidence14. We question whether endorsing IDB use, at the almost complete expense of flossing, may be premature. We addressed this topic in relation to dental caries previously with a focus on the low quality of the studies, lack of a measure of oral hygiene skill and self-reported data7. Further, studies comparing flossing with IDB use tended to exclude teeth/interproximal sites that were too narrow for appropriate IDB cleaning (i.e., more appropriate for flossing) which further stacks the deck for more favorable results for IDB use. Granted, flossing is technically difficult; however, these studies may indicate that, in general, participants found IDBs easier to use and thus used them more regularly than those in the flossing group (who were given minimal or no instruction on effective flossing).
9) How can an Objective Measure of Tooth Brushing and Flossing Help Clarify This Topic?
We are establishing the reliability and validity of a new provider-observed measure, the oral hygiene skills mastery (OHSIM)7. The OHSIM measures central components of tooth brushing and flossing skills. Once provisionally established to be reliable and valid measure, OHSIM can be added to future studies on the topic of flossing to add methodological rigor. Interestingly, in preliminary analyses (n=67) tooth brushing skill is highly correlated with flossing skill (using Pearson correlation, rho=0.46, p<0.001; Vernon et al, unpublished data)—suggesting that tooth brushing skill may be a critical confounding variable in studies of interproximal cleaning. Or, what if flossing, directly or indirectly, enhances tooth brushing skill over time—could that yield powerful long-term effects? Even a small effect over a long period of time could make a substantial difference in oral health.
10) How can SMART studies help us gain clarity on the utility of flossing?
Sequential Multiple assignment randomized trails (SMART) employ Adaptive Treatment Strategies (ATS) and allow researchers the opportunity to individualize treatment based on how people respond clinically to a series of pre-defined treatment options; thus, subjects are randomized to different interventions at multiple points in the study 15.In essence, SMART studies allow for multiple RCTs to be conducted at the intra-individual level and within the confines of a singular study. For example, a primary tailoring variable (e.g., type and level of oral hygiene care) can be modified using ATS if there is a lack of a clinical response by a pre-defined time period15, 16. OHSIM could be used in SMART studies to potentially yield more valid and reliable findings regarding flossing. In addition to SMART design implementation, future such studies could also employ digital technologies that help to monitor patient behaviors such as tooth brushing (e.g., “smart” tooth brushes)42, 43 to measure frequency and duration of time spent brushing. By combining SMART design and current technological innovations, researchers will better be able to address traditional data biases inherent to self-reported information.
Conclusion
In sum, the current state of evidence for flossing effectiveness as it pertains to PD is weak and underdeveloped. PD is a complex disorder with many factors contributing to it. Understanding the relative clinical value of flossing/interdental cleaning will require a thorough, nuanced, well designed44 and methodologically valid approach. Finally, interpreting the currently available “evidence” in all its forms (i.e., varying type of studies, different study designs and varying measures used) is not well delineated11. In other words, this is a complicated research question. How best to communicate this complexity in a simple manner to the lay public may also be yet another question in search of an answer. Given the importance of prevention in oral health promotion, we have developed a set of plain language guidelines that providers may consider to promote patients’ effective cleaning between their teeth. These suggestions (See Tables 1, 2 and 3) are based upon the development of OHSIM, existing health behavior change theory and previously published work on oral health coaching by our group 45, 46.
Table 1.
|
Table 2.
Main point: Merely giving information alone (i.e., “telling” a person to floss or clean between their teeth) is unlikely to change a person’s behavior47.
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Adapted from Vernon and Howard, 201546
Table 3.
|
Adapted from Vernon and Howard, 2015 46
Acknowledgments
This work was funded by the National Institutes of Health: R21 DE023740 and had no involvement in writing this manuscript. Conflict of interests: None.
Abbreviations
- AAP
American Academy of Periodontology
- ADA
American Dental Association
- ATS
Adaptive Treatment Strategies
- BGI
Biofilm–Gingival Interface
- BOP
bleeding on probing
- CDC/AAP
the Centers for Disease Control with the American Academy of Periodontology
- CAL
clinical attachment loss
- CR
Cochran Reviews
- EFP
European Federation of Periodontology
- FDA
Food and Drug Administration
- IDB
inter-dental cleaning devices, inter-dental brushes
- NYT
New York Times
- OHSIM
Oral Hygiene Skills Mastery
- PD
periodontal diseases
- RTC
randomized clinical trials
- SMART
Sequential Multiple Assignment Randomized Trials
Contributor Information
Lance T. Vernon, Case Western Reserve University School of Dental Medicine, Department of Pediatric Dentistry and Community Dentistry; 10900 Euclid Avenue, Cleveland, Ohio USA 44106-4905.
Dr. Andre Paes, Case Western Reserve University School of Dental Medicine, Department of Periodontology, 10900 Euclid Avenue, Cleveland, Ohio USA 44106-4905
Jason D. Seacat, Western New England University, Department of Psychology, 1215 Wilbraham Road, Springfield, MA 01119.
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