International Journal of

Environmental Research
and Public Health

Article
Association between Household Exposure to
Secondhand Smoke and Dental Caries among
Japanese Young Adults: A Cross-Sectional Study
Hikari Saho 1, * , Ayano Taniguchi-Tabata 2 , Daisuke Ekuni 1 , Aya Yokoi 2 ,
Kouta Kataoka 1 , Daiki Fukuhara 2 , Naoki Toyama 1 , Md Monirul Islam 1 ,
Nanami Sawada 1 , Yukiho Nakashima 2 , Momoko Nakahara 1 , Junya Deguchi 1 ,
Yoko Uchida-Fukuhara 1 , Toshiki Yoneda 1 , Yoshiaki Iwasaki 3 and Manabu Morita 1
1 Department of Preventive Dentistry, Okayama University Graduate School of Medicine, Dentistry and
Pharmaceutical Sciences, Okayama 700-8558, Japan; [email protected] (D.E.);
[email protected] (K.K.); [email protected] (N.T.);
[email protected] (M.M.I.); [email protected] (N.S.);
[email protected] (M.N.); [email protected] (J.D.);
[email protected] (Y.U.-F.); [email protected] (T.Y.); [email protected] (M.M.)
2 Department of Preventive Dentistry, Okayama University Hospital, Okayama 700-8558, Japan;
[email protected] (A.T.-T.); [email protected] (A.Y.); [email protected] (D.F.);
[email protected] (Y.N.)
3 Health Service Center, Okayama University, Okayama 700-8530, Japan; [email protected]
* Correspondence: [email protected]; Tel.: +81-86-235-6712




Received: 19 October 2020; Accepted: 17 November 2020; Published: 20 November 2020


Abstract: The long-term effects of secondhand smoke (SHS) on dental caries among Japanese young
adults remain unclear. The purpose of this cross-sectional study was to evaluate whether household
exposure to SHS is associated with dental caries in permanent dentition among Japanese young
adults. The study sample included 1905 first-year university students (age range: 18–19 years)
who answered a questionnaire and participated in oral examinations. The degree of household
exposure to SHS was categorized into four levels according to the SHS duration: no experience (−),
past, current SHS < 10 years, and current SHS ≥ 10 years. Dental caries are expressed as the total
number of decayed, missing, and filled teeth (DMFT) score. The relationships between SHS and
dental caries were determined by logistic regression analysis. DMFT scores (median (25th percentile,
75th percentile)) were significantly higher in the current SHS ≥ 10 years (median: 1.0 (0.0, 3.0))
than in the SHS—(median: 0.0 (0.0, 2.0)); p = 0.001). DMFT ≥ 1 was significantly associated with
SHS ≥ 10 years (adjusted odds ratio: 1.50, 95% confidence interval: 1.20–1.87, p < 0.001). Long-term
exposure to SHS (≥10 years) was associated with dental caries in permanent dentition among Japanese
young adults.

Keywords: secondhand smoke; dental caries; permanent dentition; young adult

1. Introduction
Secondhand smoke (SHS), known as environmental tobacco smoke, is a combination of mainstream
smoke exhaled by a smoker and sidestream smoke released by the lighted end of a cigarette. As SHS
does not pass through a filter, it contains higher concentrations of harmful components than smoke
that is inhaled through a cigarette [1,2]. Thus, SHS is related to diseases including coronary heart
disease [3,4], stroke [5], lung cancer [6,7], and dental caries [8].

Int. J. Environ. Res. Public Health 2020, 17, 8623; doi:10.3390/ijerph17228623 www.mdpi.com/journal/ijerph
Int. J. Environ. Res. Public Health 2020, 17, 8623 2 of 9

Dental caries is one of the most prevalent infectious diseases. It is defined as the localized
destruction of tooth tissue by bacterial action [9]. A recent systematic review [8] suggested an association
between SHS and dental caries in both primary and permanent dentitions of children and adolescents.
As a mechanism, nicotine promotes the growth of the cariogenic bacterium Streptococcus mutans [10].
In addition, SHS causes respiratory tract inflammation [11] and indirectly causes mouth breathing/dry
mouth. SHS causes histological changes in salivary glands and salivary composition [12], so caries
are more likely to occur by the change in saliva flow rate and function (e.g., self-cleaning action and
buffering action against acid). However, compared to available evidence about the effects of SHS on
deciduous teeth of children [13], little is known about the long-term effects (≥10 years) of SHS on the
permanent dentition of Japanese adolescents and/or young adults (aged > 15 years).
In Japan, tobacco smoke is restricted by the Health Promotion Act. The revised law [14] has
encouraged authorities of public places such as hospitals, schools, municipal offices, and restaurants to
take the lead in implementing smoking restrictions and in preventing SHS for non-smokers, especially
in populations younger than 20 years. However, household exposure to SHS is not regulated. Therefore,
it is important to explore the effects of household SHS and to prevent household exposure to SHS.
Here, we focused on the effects of household exposure to SHS among Japanese adolescents
and young adults. In this study, we hypothesized that household exposure to SHS is a risk factor
for dental caries in permanent dentition among Japanese young adults. Therefore, the aim of this
cross-sectional study was to evaluate whether household exposure to SHS is associated with dental
caries in permanent dentition among Japanese young adults.

2. Materials and Methods

2.1. Study Population

In this cross-sectional study, data were collected from first-year university students who answered
the questionnaire and underwent oral examinations at the Health Service Center of Okayama University
in April 2019. The inclusion criteria were young adults between 18 and 19 years of age. The exclusion
criteria for analysis were: (i) aged ≥20 years, (ii) being a current smoker, and/or (iii) providing incomplete
data. We estimated the sample size using G*Power version 3.1 statistical software (Universität Kiel,
Kiel, Germany). We hypothesized an odds ratio of 1.3 by logistic regression analysis by referring to
a past study [8] with a power of 80% and a two-sided significance level of 5%. Thus, we needed to
include a minimum of 386 participants.

2.2. Ethical Procedures and Informed Consent

This study protocol was approved by the Ethics Committees of Okayama University Graduate
School of Medicine, Dentistry and Pharmaceutical Sciences and Okayama University Hospital (no. 1060).
Verbal and written informed consent to participate in the study were provided by all selected participants.
The study’s reporting conforms to STROBE guidelines (Table S1).

2.3. Questionnaire
The questionnaires addressed age, sex, daily frequency of tooth brushing, use of dental floss,
regular dental checkups, consumption frequency of sugar-sweetened snacks and/or soft drinks,
experience of topical fluoride application, knowledge about dietary education, and household exposure
to SHS. The following factors were evaluated by yes or no answers: use of dental floss [15], regular dental
checkups [15], experience of topical fluoride application [16], and knowledge of dietary education [17].
Daily frequency of tooth brushing (≤1 time, 2 times, or ≥3 times) [15] and consumption frequency
of sugar-sweetened snacks and/or soft drinks (never, 1 or 2 times per day, or ≥3 times per day) [18]
were evaluated in the form of ternary answers. Questions on household exposure to SHS included
two parts: (i) Does anyone in your household smoke? (current smokers, past smokers, or no smokers)
and (ii) If there are any smokers in your household, have you been exposed to SHS for greater than or
Int. J. Environ. Res. Public Health 2020, 17, 8623 3 of 9

equal to 10 years? (yes or no) based on the previous decision to a 10-year threshold for the exposure
categories [19]. Household exposure to SHS was then categorized into four levels: (i) no experience of
SHS, SHS −; (ii) past experience of household exposure, past SHS; (iii) current household exposure
to SHS < 10 years, current SHS < 10 years; and (iv) current household exposure to SHS ≥ 10 years,
current SHS ≥ 10 years.

2.4. Oral Examination

Nine qualified dentists (D.E., A.T.-T., H.S., A.Y., T.Y., N.T., Y.U.-F., D.F., and K.K.) conducted oral
examinations. The World Health Organization diagnostic criteria for dental caries experience [20] were
used to evaluate decayed, missing, and filled teeth (DMFT). Oral hygiene status was evaluated by
visually inspecting selected teeth based on the Debris Index-Simplified (DI-S) [21]. A modified version
of the Index of Orthodontic Treatment Need [22] was used to evaluate malocclusion. The presence
of an orthodontic appliance in the oral cavity was visually checked. Qualified dentists repeatedly
practiced DMFT scoring and malocclusion evaluation in five volunteers for two weeks. For the oral
examination, intra- and inter-agreement were good (Kappa statistic > 0.8).

2.5. Statistical Analyses

The normality of data was investigated by the Shapiro–Wilk test. We did not confirm the normal
distribution of each value. The Kruskal–Wallis test and Dunn test with Bonferroni correction were
used to compare DMFT scores by SHS status. The chi-squared test or Mann–Whitney U test was used
to examine the difference between groups with (DMFT ≥ 1) and groups without (DMFT = 0) dental
caries. The association between dental caries (DMFT ≥ 1) and independent variables that are risk
factors of dental caries was analyzed using logistic regression. Independent variables were selected
when the p-value was <0.20 for the chi-square test or unpaired t-test in each variable and were based
on previous studies because it has been suggested that potential confounders should be eliminated
only if p > 0.20 to prevent residual confounding [23]. All analyses were performed using SPSS® 21.0 J
software (IBM Japan Ltd., Tokyo, Japan). Significant differences were considered to exist at p < 0.05.

3. Results
A total of 2241 participants answered the questionnaire and underwent oral examinations in 2019.
Of these students, 336 students were excluded for the following reasons: (i) being aged ≥ 20 years
(n = 114), (ii) being a current smoker (n = 4), and (iii) providing incomplete data (n = 218). Finally,
1905 participants (85.0%) were analyzed.
The characteristics of the participants are shown in Table 1. Overall, 1101 (57.8%) participants
were men. The median (25th percentile, 75th percentile) DMFT score was 0.0 (0.0, 2.0). For SHS
status, 438 (23.0%) participants answered that they experienced long-term household exposure to
SHS (≥10 years).
Figure 1 compares DMFT scores by household exposure to SHS (box-plot). DMFT scores in the
SHS ≥10 years category (median: 1.0 (0.0, 3.0)) were significantly higher than those in the SHS − group
(median; 0.0 (0.0, 2.0)) (p = 0.001).
Table 2 shows the comparison between the DMFT = 0 and DMFT ≥ 1 groups. The DMFT ≥ 1
group included 884 (46.4%) participants. Significant differences in daily frequency of tooth brushing
and household exposure to SHS were observed between the two groups (p < 0.05 for all).
In Table 3, logistic regression analysis revealed that the risk of DMFT ≥1 was significantly
associated with use of an orthodontic appliance (odds ratio (OR), 1.45; 95% confidence interval (CI),
1.02–2.07, p = 0.039), daily frequency of tooth brushing (≤1 time) (OR, 1.76; 95% CI, 1.22–2.54, p = 0.002),
and household exposure to SHS ≥ 10 years (OR, 1.50; 95% CI, 1.20–1.87, p < 0.001). Significant
associations between the other variables and DMFT ≥ 1 were not observed.
Int. J. Environ. Res. Public Health 2020, 17, 8623 4 of 9

Table 1. Characteristics of participants (n = 1905).

Median
(25th percentile,
Variable
75th percentile)
or n (%)
Age (years) 18.0 (18.0, 18.0)
Sex Male 1101 (57.8)
DMFT 0.0 (0.0, 2.0)
Decayed teeth 0.0 (0.0, 0.0)
Missing teeth 0.0 (0.0, 0.0)
Filled teeth 0.0 (0.0, 2.0)
Int. J. Environ. Res. Public Health 2020, 17, x 4 of 10
DI-S 0.2 (0.0, 0.7)
Malocclusion Yes 673 (35.3)
Use of orthodontic appliance ≥3 times
Yes 313 (7.1)
135 (16.4)
DailyUse of dental
frequency flossbrushing
of tooth ≤1Yestime 554(10.3)
197 (29.1)
Regular dental checkups 2Yes
times 632 (73.2)
1395 (33.2)
Consumption frequency of sugar- ≥3 times 313 (16.4)
Use of dental floss Never
Yes 637(29.1)
554 (33.4)
sweetened snacks and/or soft drinks
Regular dental checkups Yes 632 (33.2)
Consumption frequency of sugar-sweetened 1 time per day 930 (48.8)
2 times Never
per day 637
246(33.4)
(12.9)
snacks and/or soft drinks
≥3 1times
time per
per day
day 930
92(48.8)
(4.8)
Experience of topical fluoride application 2 times
Yes day
per 246 (12.9)
1253 (65.8)
≥3 times per
Knowledge about dietary education Yes
day
695 (36.5)
92 (4.8)
Household
Experience exposure
of topical to SHS
fluoride application − (no experience)
Yes 1112 (58.4)
1253 (65.8)
Knowledge about dietary education Past
Yes 315(36.5)
695 (16.5)
Household exposure to SHS Current−<10(no years 40 (2.1)
1112 (58.4)
experience)
Current ≥10 years 438 (23.0)
Past 315 (16.5)
DMFT, decayed, missing and filled teeth; DI-S, Debris Index-Simplified;
Current <10 SHS, secondhand smoke.
40 (2.1)
years
Figure 1 compares DMFT scores by household exposure to ≥10
Current SHS (box-plot). DMFT scores in the
438 (23.0)
years
SHS ≥10 years category (median: 1.0 (0.0, 3.0)) were significantly higher than those in the SHS − group
DMFT,
(median; 0.0 (0.0,decayed,
2.0)) (p missing and filled teeth; DI-S, Debris Index-Simplified; SHS, secondhand smoke.
= 0.001).

SHS −
N = 1112

Figure 1.
Figure Comparison of
1. Comparison of DMFT
DMFT by by the
the presence/absence
presence/absence of of household
household exposure
exposure toto secondhand
secondhand
smoke. DMFT scores were significantly higher in the current SHS ≥ 10 years than those
smoke. DMFT scores were significantly higher in the current SHS ≥ 10 years than those in the in the SHS
SHS −.−.
Kruskal–Wallis test and Dunn test with Bonferroni correction. DMFT, decayed, missing and
Kruskal–Wallis test and Dunn test with Bonferroni correction. DMFT, decayed, missing and filled filled teeth;
SHS, secondhand
teeth; smoke.smoke.
SHS, secondhand

Table 2 shows the comparison between the DMFT = 0 and DMFT ≥ 1 groups. The DMFT ≥ 1
group included 884 (46.4%) participants. Significant differences in daily frequency of tooth brushing
and household exposure to SHS were observed between the two groups (p < 0.05 for all).

Table 2. Differences in variables between DMFT = 0 and DMFT ≥1 groups.

a
DMFT = 0 DMFT ≥ 1 p-Value b,
Int. J. Environ. Res. Public Health 2020, 17, 8623 5 of 9

Table 2. Differences in variables between DMFT = 0 and DMFT ≥1 groups.

DMFT = 0 DMFT ≥ 1
Variables a p-Value b, c
n = 1021 n = 884
Sex Male 602 (59.0) 499 (56.4) 0.268
Female 419 (41.0) 385 (43.6)
DI-S 0.2 (0.0, 0.7) 0.3 (0.0, 0.7) 0.134
Malocclusion Yes 360 (35.3) 313 (35.4) 0.946
Use of orthodontic appliance Yes 62 (6.1) 73 (8.3) 0.064
Daily frequency of tooth brushing ≤1 time 89 (8.7) 108 (12.2) 0.014
2 times 749 (73.4) 646 (73.1)
≥3 times 183 (17.9) 130 (14.7)
Use of dental floss Yes 292 (28.6) 262 (29.6) 0.619
Regular dental checkups Yes 330 (32.3) 302 (34.2) 0.395
Consumption frequency of
Never 350 (34.3) 287 (32.5) 0.420
sugar-sweetened snacks and/or soft drinks
1 or 2 times per day 627 (61.4) 549 (62.1)
≥3 times per day 44 (4.3) 48 (5.4)
Experience of topical fluoride application Yes 670 (65.6) 583 (66.0) 0.880
Knowledge about dietary education Yes 372 (36.4) 323 (36.5) 0.963
Household exposure to SHS − (no experience) 636 (62.3) 476 (53.8) 0.002
Past 159 (15.6) 156 (17.6)
Current <10 years 18 (1.8) 22 (2.5)
Current ≥10 years 208 (20.4) 230 (26.0)
a Data are expressed as median (25th percentile, 75th percentile) or n (%). b Mann–Whitney U test, as appropriate.
cChi-squared test, as appropriate. DMFT, decayed, missing and filled teeth; DI-S, Debris Index-Simplified; SHS,
secondhand smoke.

Table 3. Logistic regression analysis when independent variables were selected based on the p-value
(<0.20) by the chi-square test or Mann–Whitney U test.

Independent Variables ORs 95% CIs p-Value

DI-S 1.11 0.87–1.42 0.402
Use of orthodontic appliance No Ref.
Yes 1.45 1.02–2.07 0.039
≥3 times Ref.
Daily frequency of tooth brushing 2 times 1.24 0.97–1.60 0.089
≤1 time 1.76 1.22–2.54 0.002
Household exposure to SHS − (no experience) Ref.
Past 1.31 1.01–1.68 0.039
Current <10 years 1.72 0.91–3.25 0.095
Current ≥10 years 1.50 1.20–1.87 <0.001
Ref., reference group; DI-S, Debris Index-Simplified; SHS, secondhand smoke; OR, odds ratio; CI, confidence interval.

4. Discussion
In this study, we hypothesized that household exposure to SHS is a risk factor of dental caries
in permanent dentition among Japanese young adults. To the best of our knowledge, this is the first
study to show the long-term effects (≥10 years) of household exposure to SHS on dental caries of
permanent dentition among Japanese young adults between the ages of 18 and 19. This study found
that household exposure to SHS ≥10 years is associated with dental caries (OR, 1.50; 95% CI, 1.20–1.87,
p < 0.001). The findings of this study support those of a previous meta-analysis [8] that indicated an
association between caries in permanent dentition and postnatal exposure to SHS in children and
adolescents (OR, 1.30; 95% CI, 1.25–1.34, p < 0.001).
Our results suggest that household exposure to SHS should be considered in the prevention of
dental caries in young adults. Avoiding exposure to SHS is meaningful not only for the prevention
of systemic diseases but also for dental caries. Therefore, an early-stage approach should be used to
minimize household exposure to SHS and to prevent dental caries before children enter university.
Int. J. Environ. Res. Public Health 2020, 17, 8623 6 of 9

Increasing evidence supports a causal role for SHS in caries formation [24]. A cross-sectional
study showed that children exposed to SHS had a higher prevalence of dental caries, higher salivary
levels of cariogenic bacteria (e.g., Streptococcus mutans and Lactobacillus), lower salivary pH, lower flow
rate, and lower buffering capacity than non-exposed children [24]. Furthermore, a review suggested
that saliva from household members, such as parents or grandparents, affects the bacteria responsible
for dental caries’ formation in their children/grandchildren [25]. An in vitro study showed that nicotine
promoted S. mutans growth [12]. Therefore, children who live with a family member who smokes may
be more likely to be transmitted these bacteria [12]. As SHS is known to increase respiratory tract
inflammation and cause respiratory illnesses including asthma and allergic rhinitis [11], it can indirectly
cause mouth breathing and thus result in dry mouth by an effective decrease in saliva. In addition,
an animal study found that histological changes in salivary glands were observed, and decreases in total
protein amount, amylase activity, and peroxidase activity in saliva were detected among SHS-exposed
rats compared to non-exposed rats [12]. Saliva, acting as a buffering agent against acid, physically
removes debris from tooth surfaces and has immunological and bacteriostatic properties [26]. Therefore,
SHS may reduce the protective properties of saliva against dental caries. Other cross-sectional studies
suggested an association between SHS and vitamin C in dental caries of children [27,28]. SHS is
associated with decreased serum vitamin C levels [27], which, in turn, are associated with the growth of
cariogenic bacteria [28]. Taken together, SHS could promote dental caries through effects on cariogenic
bacteria and salivary condition.
In this study, the major component of DMFT score was filled teeth. Since DMFT means the past
experiences of caries, the present effect of SHS on caries remains unclear. Only 156 students (8.2%) had
one or more decayed teeth in the present study population. We analyzed the impact of SHS on decayed
teeth to investigate the present effect of SHS on dental caries. As a result, we found no significant
relationship between SHS and decayed teeth (data not shown). Thus, the present effect of SHS on
present decayed teeth in this age group may be minor.
Our results showed that use of an orthodontic appliance is one of the risk factors for dental
caries. This finding supports those of a recent review that suggested an association between use of an
orthodontic appliance and the risk of dental caries [29]. Thus, clinicians should educate young adults
about the susceptibility to dental caries and should educate young adults with orthodontic appliances
about careful tooth cleaning practices.
Our results also showed that daily frequency of tooth brushing one or fewer times is a risk
factor for dental caries. A cohort study showed that higher brushing frequency is associated with
lower decayed and filled surface increases among participants aged 9, 13, and 17 years in the United
States [30]. These findings suggest that more frequent fluoride exposure from dentifrice and mechanical
disruption of cariogenic biofilms contribute to caries prevention.
We did not identify significant associations between dental caries experience and other risk
factors. No significant difference in sex was found between DMFT = 0 and DMFT ≥ 1 groups.
Some reviews [31–33] suggested effects of sex difference on dental caries. However, there was
heterogeneity and further investigation is needed. No significant difference in DI-S was found between
DMFT = 0 and DMFT ≥ 1 groups in this study. As we could not investigate oral hygiene status in the
full mouth and fundamental differences in dental plaque ecology as a risk of dental caries [34], careful
attention is needed regarding the interpretation of these results. Similar to results of our previous
study [17], frequent consumption of sugar-sweetened snacks and/or soft drinks was not associated
with dental caries. The effects of sugar consumption on dental caries may be low among young adults.
We found no association between the experience of topical fluoride application and dental caries.
One potential reason for this lack of association may be because we only investigated the experience
of topical fluoride application, not the frequency and period. Moreover, the cutoff value (DMFT = 0
and DMFT ≥ 1) may have affected these results. The lack of associations with these established dental
caries risk factors in the present study should be considered a limitation when evaluating all other
reported study findings, including those for SHS.
Int. J. Environ. Res. Public Health 2020, 17, 8623 7 of 9

There are some limitations associated with the present study. First, all participants were enrolled
from a single institution. The percentages of participants who brush their teeth more than one time per
day and who experienced topical fluoride application and a DMFT score reported in this study were
superior to data reported from a national survey in Japan (89.7% vs. 77.0%, 65.5% vs. 62.5%, and 1.6
vs. 3.1, respectively) [35]. Therefore, extrapolating these results to the general Japanese population
might be limited. Second, salivary/serum cotinine level [36], salivary flow rate [24], salivary buffering
capacity [24], salivary pH [24], and salivary levels of cariogenic bacteria (e.g., Streptococcus mutans
and Lactobacillus) [24] were not examined in this study. We did not investigate other qualitative
assessments (e.g., number of cigarettes smoked per day, smoking location, and number of smokers)
for SHS because we focused on the period of exposure to SHS. These factors might have affected our
results. Third, we did not consider possible confounders such as different household situations before
entrance, social capital [37] or socioeconomic status [38]. Future studies are needed to assess the effects
of these factors. Fourth, we did not include daily use of toothpaste with fluoride in our questionnaires,
although fluoride is one of the most important factors for the prevention of caries. In 2015, the market
share of toothpaste with fluoride in Japan was 91% [39]. Thus, we assumed that most students in
this study use toothpaste with fluoride. Fifth, we did not include the frequency of food in general
in our questionnaires, although we focused on consumption frequency of sugar-sweetened snacks
and/or soft drinks. Finally, a causal relationship could not be shown because this was a cross-sectional
study. Therefore, a cohort study is needed to identify SHS as a direct risk factor for the development of
dental caries.

5. Conclusions
In conclusion, we found that long-term exposure to household SHS (≥10 years) was associated
with dental caries in permanent dentition of Japanese young adults between 18 and 19 years of age.
Our results suggest that household exposure to SHS should be taken into consideration in prevention
of dental caries in young adults, although further investigation is needed to confirm the association.

Supplementary Materials: The following are available online at http://www.mdpi.com/1660-4601/17/22/8623/s1,

Table S1: STROBE Statement.
Author Contributions: Conceptualization, H.S., A.T.-T., D.E., and M.M.; methodology, H.S. and A.T.-T.; validation,
A.T.-T., D.E., and M.M.; formal analysis, H.S.; investigation, D.E., A.T.-T., H.S., A.Y., T.Y., N.T., Y.U.-F., D.F.,
and K.K.; resources, M.M.; data curation, M.M.I., N.S., Y.N., M.N., and J.D.; writing—original draft preparation,
H.S.; writing—review and editing, all authors; project administration, Y.I., and M.M. All authors have read and
agreed to the published version of the manuscript.
Funding: This study was self-supported.
Conflicts of Interest: The authors declare no conflict of interest.

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