Abstract
The purpose of this study was to evaluate the associations between interdental cleaningbehavior and the prevalence of caries and periodontal disease and numbers of missingteeth, with data from the National Health and Nutrition Examination Survey (2011 to 2012and 2013 to 2014). Analysis included the following parameters: interproximal clinicalattachment level (iCAL) ≥3 mm, interproximal probing depth (iPD) ≥4 mm, number of coronaland interproximal caries, number of missing teeth, ≥1 surfaces with coronal caries, andperiodontal profile classes (PPCs). Chi-square was used for bivariate associations.Associations of interdental cleaning with outcomes were assessed with multiple linearregression and generalized logit regression, adjusting for age, race, sex, diabetes,smoking, education, dental visits, and sugar consumption. Nonusers had a significantlyhigher percentage of sites with iCAL ≥3 mm and iPD ≥4 mm as compared with individuals whoused interdental cleaning devices (P < 0.0001). Individuals with ahigher frequency of cleaning (4 to 7×/wk) had a significantly lower extent of sites withiCAL ≥3 mm as compared with lower-frequency cleaning (1 to 3×/wk; P ≤0.05). Interdental cleaning users showed lower numbers of coronal caries, interproximalcoronal caries, and missing teeth as compared with nonusers (P <0.0001). Nonusers had 1.73-times (95% confidence interval, 1.53 to 1.94) higher odds forhaving ≥1 surfaces of coronal caries as compared with interdental cleaning users,regardless of the weekly frequency. Individuals were less likely to be in diseased PPCs ifthey were interdental cleaning users. Low-frequency cleaners (1 to 3×/wk) hadsignificantly greater odds (1.43; 95% confidence interval, 1.08 to 1.88) to have severedisease (PPC-G) versus health (PPC-A) than were high-frequency cleaners (4 to 7×/wk).Interdental cleaning users showed lower levels of periodontal disease and caries and lowernumbers of missing teeth. Higher frequency of interdental cleaning was correlated withincreased periodontal health. Individuals with severe periodontal disease could showadditional oral health benefits by increasing cleaning frequency. The data support the useof interdental cleaning devices as an oral hygiene behavior for promoting health.
Keywords: biofilm(s), caries, oral hygiene, periodontal disease(s)/periodontitis, preventive dentistry, dental hygiene
Introduction
Periodontal disease and dental caries are multifactorial diseases that comprise 3 maincomponents: a susceptible host, enabling environmental factors, and the presence of oraldysbiosis (Chapple et al. 2017).Globally, severe periodontitis affects 9% to 11% of the world’s adult population (Eke et al. 2012; Kassebaum et al. 2014). Untreated caries in permanentteeth was the most prevalent condition evaluated for the entire Global Burden of DiseasesStudy 2010 (Marcenes et al.2013). If either disease is left untreated, tooth loss may be an undesirable outcome,which can lead to reduced quality of life (Haag et al. 2017).
A plethora of in vitro, in vivo, clinical, and epidemiologic studies since the 1960sdemonstrated that microorganisms in the oral biofilm play a fundamental role in caries andperiodontal disease (Loe et al.1965; Beck and Drake1975; Listgarten et al.1975; Hunt et al. 1992;Guggenheim et al. 2004; Socransky and Haffajee 2005; Curtis et al. 2011; Hajishengallis et al. 2012; Jiao et al. 2013; Teles et al. 2013; Takahashi 2015; Sanz et al. 2017). Therefore, oral hygieneinstructions that include removal of biofilm by the use of toothbrushing and interdentalcleaning (i.e., flossing and other methods) are cited in most dental education and dentalhygiene programs. These recommendations are supported by several dental professional groups,including the American Dental Association, the National Institute of Dental and CraniofacialResearch, the Centers for Disease Control and Prevention (CDC), the American Academy ofPeriodontology, the World Health Organization, and the European Federation ofPeriodontology. While abundant literature supports a role of the microbial oral biofilm inthe development of caries and periodontal disease, direct evidence that flossing isassociated with a lower number of caries and less periodontal disease in the adultpopulation is still considered weak (Sambunjak et al. 2011). It is important to clarify that the weak evidence shouldnot be interpreted as evidence of a lack of effect (as previously interpreted by some mediaoutlets). The absence of evidence clearly differs from evidence of an absence of effect, asrecently reported (Glick 2017).The categorization of the evidence as weak is mostly due to small sample sizes or studydesign. In fact, flossing is generally related to less caries and periodontal inflammation.In adults, flossing in addition to toothbrushing reduces gingivitis (Sambunjak et al. 2011). For children, flossingreduces interproximal caries risk by 40% (Hujoel et al. 2006). To increase the strength ofdata, many authors suggested the need for randomized controlled trials on interdentalcleaning. However, there are a variety of issues in conducting such studies: 1) potentialethical issues in assigning people who currently perform interdental cleaning into anoncleaning regimen, 2) length of a study required for diseases to develop, and 3)difficulties in detecting early interdental caries lesions (Ismail 2004; Sambunjak et al. 2011). Until an adequate trial isdone, secondary analysis and retrospective studies may produce the best availableevidence.
Therefore, the purpose of this study was to estimate the prevalence of oral disease andmissing teeth among interdental cleaning users and nonusers. We hypothesized thatinterdental cleaning users would have fewer sites with periodontal disease, lower carieslevels, and diminished number of missing teeth.
Methods
Publically available data from the National Health and Nutrition Examination Survey(NHANES; 2011 to 2012 and 2013 to 2014) were used for this study. The cycles were selectedper the availability of the full mouth examination and dental utilization questionnaire(used as a covariate). NHANES is a survey that has released data on a 2-y cycle since 1999to represent the civilian, noninstitutionalized population of the United States. Data from6,891 adults (≥30 years old) were available from the survey. Pregnant women and individualswho had partial oral examinations were excluded from the analysis. Technical details of thesurvey, including sampling design and data collection protocols, can be accessed at the CDCwebsite. All NHANES protocols that generated the data used in this study were approved bythe CDC’s National Center for Health Statistics Ethics Review Board (Institutional ReviewBoard equivalent). Since the current study analyzed public use data, an additional researchethics review was not necessary for our analysis. The question used for addressinginterdental cleaning in both surveys was “Aside from brushing your teeth with a toothbrush,in the last 7 days, how many days did you use dental floss or any other device to cleanbetween your teeth?” (OHQ.870). To evaluate the effect of interdental cleaning in oraldisease and tooth loss, the following parameters were selected per the available clinicaldata: interproximal clinical attachment level (iCAL) ≥3 mm, interproximal probing depth(iPD) ≥4 mm, number of coronal and interproximal caries, number of missing teeth, ≥1surfaces with coronal caries, and periodontal profile class (PPC; Morelli et al. 2017). Seven distinct PPCs forindividuals were utilized: health (PPC-A), mild disease (PPC-B), high gingival index(PPC-C), tooth loss (PPC-D), posterior disease (PPC-E), severe tooth loss (PPC-F), andsevere periodontal disease (PPC-G; Fig.1). The PPC system differs from the traditional clinical case status indices thathave been used, including the CDC–American Academy of Periodontology and Europeanclassifications. The PPCs were given monikers, or names, based on the dominant clinicalfeature of the teeth in that class, which uses detailed clinical measures at the toothlevel, including periodontal measurements, gingival recession, crowns, and tooth loss.
Statistical Analysis
Pearson chi-square test was used to compare demographic variables between interdentalcleaning users and nonusers (P ≤ 0.05). Interdental cleaning wascategorized as nonusers, low-frequency users (1 to 3×/wk), and high-frequency users (4 to7×/wk). Multiple linear regression—adjusted for race, sex, age, diabetes, smokingeducation, and dental visits—compared clinical parameters based on interdental cleaningbehavior. For caries and tooth loss, data were adjusted for sugar consumption. Generalizedlogit model (95% confidence interval [95% CI]) evaluated the odds of being in each PPCaccording to interdental cleaning behavior.
Results
Demographics and Clinical Characterization
NHANES is a nationally represented data set to assess the health and nutrition status ofadults and children in the United States. Table 1 shows the demographics and clinicalcondition of the individuals included in this study, as stratified by nonusers andinterdental cleaning users. Sixty-nine percent of individuals reported using some type ofinterdental cleaning. Mean age was statistically different between groups (52.5 and 51.8 yfor nonusers and interdental cleaning users, respectively). The main differences betweengroups were that interdental cleaning users were more likely than nonusers to be women,have higher education, be never smokers, and have regular dental utilization. Otherwise,owing to the large sample size, statistically significant while less pronounceddifferences were that users tended to be Caucasians (and less likely to be AfricanAmericans) and nondiabetic as compared with nonusers.
Table 1.
Characteristics of the Study Population Stratified on Interdental Cleaning Behavior(N = 6,891).
Interdental Cleaning, n(%) | |||
---|---|---|---|
Nonusers (0×/wk) | Users (≥1×/wk) | P Value | |
Individuals | 2,141 (31) | 4,750 (69) | |
Age, y, mean ± SD | 52.5 ± 14.7 | 51.8 ± 14.0 | 0.02 |
Race | |||
African Americans | 531 (24.8) | 1,002 (21.1) | |
Caucasians | 778 (36.3) | 1,989 (41.9) | |
Other | 832 (38.9) | 1,759 (37.0) | <0.0001 |
Sex | |||
Female | 882 (41.2) | 2,628 (55.3) | |
Male | 1,259 (58.8) | 2,122 (44.7) | <0.0001 |
Diabetes | |||
Diabetic | 310 (14.5) | 582 (12.3) | |
Nondiabetic | 1,831 (85.5) | 4,168 (87.8) | <0.0001 |
Smoker | |||
Current | 529 (24.7) | 741 (15.6) | |
Former | 522 (24.4) | 1,188 (25.0) | |
Never | 1,090 (50.9) | 2,816 (59.4) | <0.0001 |
Education | |||
Basic | 710 (33.2) | 752 (15.8) | |
Intermediate | 521 (24.4) | 954 (20.1) | |
Advance | 907 (42.4) | 3,043 (64.1) | <0.0001 |
Dental utilization | |||
Regular | 914 (44.0) | 2,975 (63.0) | |
Irregular | 1,164 (56.0) | 1,748 (37.0) | <0.0001 |
Sugar consumption, g/da | |||
≤25 | 126 (6.5) | 201 (4.5) | |
>25 | 1,825 (93.5) | 4,230 (95.5) | 0.001 |
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a
n = 6,382 (information not available for all individuals).
Interdental Cleaning and Oral Disease
On average, nonusers had a significantly higher percentage of sites with iCALs (≥3 mm)and iPDs (≥4 mm) as compared with interdental cleaning users (P <0.0001, Table 2). Individualswho used interdental cleaning devices 4 to 7×/wk also showed a significant lowerpercentage of sites with iCAL ≥3 mm compared with individuals who used devices 1 to 3×/wk(P = 0.04; Table2). A trend for significance was observed for 4 to 7×/wk, showing fewer sites bypercentage with high iPDs (≥4 mm; P = 0.07). The patterns of iCAL and iPDaccording to frequency of interdental cleaning are shown in the AppendixFigure.
Table 2.
Clinical Parameters of Periodontal Disease, Caries, and Number of Missing Teethaccording to Interdental Cleaning Behavior (n = 6,797).
Parameter, Mean (SE) | |||||
---|---|---|---|---|---|
Group: Interdental Cleaning Behavior | iCAL ≥3 mm, % Sites | iPD ≥4 mm, % Sites | Coronal Caries, n | Interproximal Caries, n | Missing Teeth, n |
A: Nonusers | 30.6 (0.53) | 5.77 (0.24) | 1.12 (0.04) | 0.62 (0.03) | 9.53 (0.13) |
B: Interdental cleaning users (1 to 3×/d) | 22.8 (0.58) | 4.37 (0.26) | 0.72 (0.05) | 0.37 (0.03) | 7.60 (0.14) |
C: Interdental cleaning users (4 to 7×/d) | 21.3 (0.44) | 3.77 (0.20) | 0.76 (0.04) | 0.43 (0.02) | 7.32 (0.10) |
P value | |||||
Overall | <0.0001 | <0.0001 | <0.0001 | <0.0001 | <0.0001 |
A vs. B | <0.0001 | <0.0001 | <0.0001 | <0.0001 | <0.0001 |
A vs. C | <0.0001 | <0.0001 | <0.0001 | <0.0001 | <0.0001 |
B vs. C | 0.04 | 0.07 | 0.59 | 0.14 | 0.11 |
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Data adjusted for race, sex, age, diabetes, smoking, education, and dentalutilization. Caries, interproximal caries, and number of missing teeth were alsoadjusted for sugar consumption.
iCAL, interproximal clinical attachment level; iPD, interproximal probingdepth.
For evaluating caries and tooth loss, the data were further adjusted for the amount ofsugar consumption. Interdental cleaning users showed significantly lower numbers ofcoronal caries and interproximal caries as compared with nonusers (P <0.0001; Table 2). Nosignificant difference in the number of coronal caries and interproximal coronal carieswas found between the cleaning frequency categories. When the numbers of missing teethwere evaluated, nonusers had significantly more missing teeth than interdental cleaningusers, with no difference observed between interdental cleaning frequencies.
Finally, we evaluated the effect of interdental cleaning in disease outcome byconsidering ≥1 caries in coronal surfaces and 7 distinct PPCs (A to G; Morelli et al. 2017). When dentalcaries was used as an outcome, noninterdental cleaners had 1.73 (95% CI, 1.53 to 1.94)times higher odds for having ≥1 surfaces of coronal caries as compared with interdentalcleaners regardless of the weekly frequency. For periodontal conditions, our analysis ofthe distribution of individuals among the 7 PPCs shows that the majority of interdentalcleaning users (>60%) were healthy individuals (PPC-A; Fig. 2). Interdental cleaning users had significantlylower odds to be in a disease category relative to health, regardless of whether thecleaning frequency was 1 to 3×/wk or 4 to 7×/wk; an exception was for mild diseasecategory and flossing 1 to 3×/wk, which nonetheless showed a similar trend (Fig. 3A). Interdental cleaning userswith a frequency of 1 to 3×/wk had significantly greater odds to have severe disease(PPC-G) versus health than individuals who cleaned 4 to 7×/wk (1.43; 95% CI, 1.08 to 1.88;Fig. 3B). Together, the datashow that individuals who use interdental cleaning devices have a lower percentage ofinterproximal clinical parameters of periodontal disease, a lower number of cariouslesions (teeth), and fewer missing teeth.
Discussion
In this representative cross-sectional sample of U.S. adults aged ≥30 y, interdentalcleaning was significantly associated with decreased periodontal disease measurements, lesscaries, and increased numbers of present teeth. Extent of iCAL ≥3 mm was lower forindividuals with a higher cleaning frequency (4 to 7×/wk vs. 1 to 3×/wk). Individuals wereless likely to be in all periodontal disease categories of the PPC system if they wereinterdental cleaners than if they were noninterdental cleaners. Individuals with a lowinterdental cleaning frequency were more likely to have severe periodontal disease (PPC-G)versus health than individuals with a high cleaning frequency. These results further supportthe evidence that interdental cleaning is associated with less oral disease.
The data indicate that the benefits of a high interdental cleaning frequency may existsince individuals who reported performing interdental cleaning 4 to 7×/wk showedsignificantly less interproximal periodontal disease (Table 2). The conclusion of our results are differentfrom a recent analysis of the NHANES data set by Cepeda et al. (2017), in which a higher frequency ofcleaning was not associated with less disease. Note that the approach used to evaluate thedata was distinct. First, we divided our cleaning frequency into 1 to 3×/wk and 4 to 7×/wk,as opposed to 0 to 1×/wk, 2 to 4×/wk, and ≥5×/wk. The outcomes utilized in the analysis werealso different. Cepeda and collaborators used the CDC definition of periodontal disease(Eke et al. 2012) and includedmild, moderate, and severe periodontitis into 1 category of disease. The outcomes used inthe present study include iCAL ≥3 mm (percentage sites), iPD ≥4 mm (percentage sites), andthe PPC system for periodontal disease classification (Morelli et al. 2017). A probing depth ≥4 mm and aclinical attachment level ≥3 mm were previously used as indicator variables for periodontalpathologic features (Moss et al.2009; Akinkugbe et al.2017). For the present study, we selected only the interproximal region as theoutcome of interest, since the main question was addressing the effect of interproximalcleaning behavior. This approach also differs from the approach used by Cepeda et al. (2017) and could assistin explaining the different results. In addition, analysis based on a new periodontaldisease classification (i.e., PPC) demonstrated that individuals with a high interdentalcleaning frequency were less likely to have severe disease (PPC-G; Morelli et al. 2017) than individuals with a lowinterdental cleaning frequency. Therefore, the periodontal status of an individual may alsoinfluence the oral health benefit achieved by increased cleaning frequency. Theseindividuals have not only disease but also an average of 25 teeth present in their oralcavity. As such, they may be likely to have more teeth at risk for disease and could have agreater benefit from interdental cleaning.
The effect of flossing on interproximal caries was evaluated in a review of 6 trials with808 children, which found a 40% risk reduction with professional flossing (Hujoel et al. 2006). In the adultpopulation, no study evaluating the effect of flossing on caries was identified (Hujoel et al. 2006; Sambunjak et al. 2011). In accordanceto Hujoel and collaborators(2006), our study shows that interdental cleaning is associated with a lower numberof interproximal carious lesions. No review evaluating the effect of interdental cleaning onthe number of teeth was identified.
A weakness of this study relates to the potential influence of important caries-relatedfactors, including brushing frequency and fluoride exposure (Chapple et al. 2017; Hujoel and Lingström 2017; Jepsen et al. 2017). The NHANES data set does notinclude brushing information for the adult population used in the present study. Fluoridewas not included in the adjustment, since the available data include only a small number ofindividuals (NHANES, 2011 to 2012, 2013 to 2014; n = 27 total). However,the study was adjusted for other important confounding factors, such as sugar consumption,diabetes, education, and dental visits, which are known to affect the development of caries(Chapple et al. 2017).Fermentable carbohydrates (which include sugars) are considered the most relevant commondietary risk factor for both diseases (Chapple et al. 2017) and, therefore, an important factor to be considered foradjustment in our analysis. We adjusted our analysis to the amount of sugar consumptionbased on the World Health Organization recommendation of 25 g/d. Because the high intake ofsugar in the United States was well-documented in a previous analysis of the NHANES data set(Ervin and Ogden 2013; Powell et al. 2016), the expectationwas that individuals who did interdental cleaning would show lower oral disease levels evenafter data adjustment for sugar consumption. Accordingly, the consumption of sugar did notsignificantly modify the results observed.
Since this is a cross-sectional study, it does not allow analysis of the direct effect ofinterdental cleaning in oral health outcomes but instead allows identification ofassociations with disease based on the selected oral health behavior. However, this studyallowed analysis of a large sample that is representative of the U.S. population. Multiplefactors hinder the development of a randomized controlled trial for evaluating the effect ofinterdental cleaning on caries and periodontal disease, including assigning individuals to agroup that would not conduct interdental cleaning. The significant amount of literaturesupporting the importance of microorganisms in disease provides sufficient justification fornot assigning individuals to a noninterdental cleaning regimen. Therefore, secondaryanalysis and retrospective studies of large samples may produce the best available evidenceto directly support the beneficial effects of interdental cleaning.
In summary, our study found that interdental cleaning was associated with less periodontaldisease, decreased coronal and interproximal caries, and fewer missing teeth. A higherfrequency of interdental cleaning (4 to 7×/wk) was associated with less interproximalperiodontal disease. Some disease categories may have improved oral health benefits from ahigher frequency of interdental cleaning. Together, the data support the use of interdentalcleaning devices as an oral hygiene behavior for promoting health.
Author Contributions
J.T. Marchesan, contributed to conception, design, and data analysis, drafted themanuscript; T. Morelli, contributed to conception, design, and data analysis, criticallyrevised the manuscript; K. Moss, J.S. Preisser, A.F. Zandona, S. Offenbacher, contributed todata analysis, critically revised the manuscript; J. Beck, contributed to conception anddesign, critically revised the manuscript. All authors gave final approval and agree to beaccountable for all aspects of the work.
Supplementary Material
Supplementary material
DS_10.1177_0022034518759915.pdf (214.5KB, pdf)
Footnotes
A supplemental appendix to this article is available online.
The authors declare no conflicts of interest with respect to the authorship and/orpublication of this article.
The authors thank the following funding agencies for their support:National Institute of Dental and Craniofacial Research (NIDCR) K01 DE027087-01 to J.T.M.,NIDCR K23 DE025093 to T.M., and NIDCR R01 DE023836 to S.O.
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Supplementary Materials
Supplementary material
DS_10.1177_0022034518759915.pdf (214.5KB, pdf)