Journal of Public Health Dentistry .

ISSN 0022-4006

Association of environmental tobacco smoke and snacking

habits with the risk of early childhood caries among
3-year-old Japanese children
Yoshimi Nakayama, DDS, PhD1,2; Mitsuru Mori, MD, PhD2
1 Hokkaido Tomakomai Public Health Center, Tomakomai, Hokkaido, Japan
2 Department of Public Health, Sapporo Medical University School of Medicine, Sapporo, Japan

Keywords
environmental tobacco smoke; early childhood
caries; snacking habits.
Correspondence
Dr. Yoshimi Nakayama, Hokkaido Tomakomai
Public Health Center, 2-2-21 Wakakusa town,
Tomakomai-shi, Hokkaido 053-0021, Japan.
Tel.: 81-144-34-4168; Fax: 81-144-34-4177;
e-mail: nakayama.
yoshimi@pref.hokkaido.lg.jp. Yoshimi
Nakayama is with the Hokkaido Tomakomai
Public Health Center. Yoshimi Nakayama and
Mitsuru Mori are with the Department of
Public Health, Sapporo Medical University
School of Medicine.
Received: 3/3/2014; accepted: 12/19/2014.
doi: 10.1111/jphd.12085
Journal of Public Health Dentistry 75 (2015) 157162

Abstract
Objectives: The aim of this study was to investigate the association of environmental
tobacco smoke (ETS) and other risk factors with early childhood caries (ECC) in
3-year-old Japanese children by a cross-sectional study.
Methods: Study subjects were 1,801 children aged 3 years old. The self-administered
questionnaire was completed by parents or guardians of the children. The survey
contents included such things as if there was a smoker in the home, snack times, the
kinds of snacks consumed more than or equal to four times a week, the kinds of
drinks consumed more than or equal to four times a week, parents brushing their
childs teeth daily, and the use of fluoride toothpaste. We obtained the number of
decayed, missing, or filled teeth per person (dmft) from the dental examinations.
Logistic regression analysis was performed to estimate odds ratio of ECC.
Results: The average number of decayed, missing and filled teeth (dmft index)
was 1.00. The prevalence of dental caries was 22.4 percent. There was at least
one smoker in the homes of 1,121 subjects (62.2 percent). After excluding items
of multicollinearity, the results of multivariate analysis were as follows: drinking
or eating sweets after dinner, irregular snack times, frequent intake of chocolate,
frequent intake of sugar-sweetened gum, frequent intake of isotonic
drink, and maternal smoking were significantly associated with the risk of
ECC.
Conclusions: This study suggests that there is a significant correlation between ETS
from family members and snacking habits and ECC.

Introduction
Early childhood caries (ECC) is one of the most prevalent
chronic diseases among children. Heretofore, ECC has been
shown to result from the transmission of bacteria from
mother to child (1), daily habits such as oral hygiene practice, feeding habits, snacking habits, and socioeconomic
status (2-5). Recently, it was suggested that children exposed
to environmental tobacco smoke (ETS) also have an
increased risk of dental caries in the deciduous dentition
(6-14). Aligne et al. (7) reported that an elevated serum
cotinine level was significantly associated with an increased
risk of both decayed and filled teeth of US children from 4
to 11 years old. Shenkin et al. (8) reported that US children
from 4 to 7 years old residing in homes with regular
smoker had a higher prevalence of caries compared with
2015 American Association of Public Health Dentistry

nonregular/nonsmoking homes. Tanaka et al. (13) reported

that ETS exposure at home was associated with an increased
prevalence of dental caries among 3-year-old Japanese children. In children, ETS exposure has been shown to be particularly associated with such issues as upper and lower
respiratory tract infections, middle-ear disease, bronchitis,
and sudden infant death syndrome (15). Furthermore, some
previous studies (6-8) suggested that ETS was significantly
associated with ECC even after socioeconomic status was
controlled. However, because the association between ETS
and ECC has been poorly studied, the process remains
incompletely understood.
The aim of this study was to investigate the association
between ETS from family members and other risk factors and
ECC in 3-year-old Japanese children by a cross-sectional
study.
157

Tobacco smoke and childhood caries

Methods
Subjects
The study was conducted in one city and four towns in the
east Iburi region, located in the center part of Hokkaido, the
northernmost island of Japan. The population of the east
Iburi region was 215,233 persons. The total number of subjects aged 3 years old in the east Iburi region was 1,879 people.
Among them, 1,801 children (95.8 percent, male: 908, female:
893) received a dental examination from April 2012 to March
2013. The age in months of subjects was between 36 and 47
months.
This study was approved by the Ethical Committee of
Sapporo Medical University.

Y. Nakayama and M. Mori

decayed (non-cavitated or cavitated lesions), missing (due to

caries), or filled tooth surfaces in any primary tooth in children from birth through 71 months of age (1). Risk factors for
the prevalence of ECC were evaluated using univariate and
multivariate analysis by employing the logistic regression
model as previous studies (6-11,14). The odds ratios (ORs)
and their 95 percent confidence intervals (95 percent CIs)
were estimated with regard to risk factors for ECC. Before the
multivariate logistic regression analysis was conducted, we
evaluated multicollinearity among the variables by the Spearmans rank correlation test. Tests of statistical significance
were based on a two-sided P-value, and the -error was set at
the 5 percent level. The SAS system (ver. 9.2; SAS Institute,
Cary, NC, USA) was employed for the analysis.

Method of survey

Results

The self-administered questionnaire was completed by

parents or guardians of the children before dental examination. After the questionnaire was completed, the data were
checked by hygienists or public health nurses.
The survey contents contained items such as whether a
smoker resided in the home, the number of smokers in the
home, snack times, kinds of snacks (fruits or vegetables,
cheese or yogurt, snack foods, ice cream, candy, chocolate,
sugar-sweetened gum, sugarless gum, pudding or jelly, Japanese cracker, bread, cake, and cookies) eaten more than or
equal to four times a week, kinds of drinks (milk, Japanese tea
or water, isotonic drink, juice, soda, and lactic acid drink)
consumed more than or equal to four times a week, parents
brushing their childs teeth daily, and use of fluoride toothpaste. Our study did not investigate socioeconomic status.

The dmft index was 1.00 (standard deviation = 2.61). The

prevalence of dental caries was 22.4 percent (404/1,801).
Table 1 shows prevalence of dental caries in the study subjects
according to ETS. There was at least one smoker in the homes
of 1,121 subjects (62.2 percent).
Table 2 shows a crude OR with 95 percent CI for
ECC. Drinking or eating sweets after dinner sometimes
(OR = 2.01, 95 percent CI: 1.52-2.67) or everyday
(OR = 3.06, 95 percent CI: 2.31-4.05), parents brushing their
childs teeth less frequently (OR = 2.09, 95 percent CI: 1.492.93), irregular snack times (OR = 2.01, 95 percent CI: 1.592.53), frequent intake of ice cream (OR = 1.37, 95 percent CI:
1.08-1.72), frequent intake of chocolate (OR = 1.67, 95
percent CI: 1.33-2.09), frequent intake of sugar-sweetened
gum (OR = 2.48, 95 percent CI: 1.63-3.78), frequent intake of
sugarless gum (OR = 1.51, 95 percent CI: 1.02-2.23), less frequent intake of Japanese crackers (OR = 0.66, 95 percent CI:
0.52-0.84), less frequent intake of milk (OR = 0.61, 95 percent
CI: 0.49-0.76), frequent intake of isotonic drinks (OR = 1.92,
95 percent CI: 1.36-2.70), frequent intake of juice
(OR = 1.52, 95 percent CI: 1.22-1.91), frequent intake of soda
(OR = 2.18, 95 percent CI: 1.48-3.21), frequent intake of

Examination
The dental examinations were carried out at the municipal
examination site by some dentists of a local dental clinic with
a dental mirror under artificial light. They used the explorer
when appropriate. The childrens teeth were not dried. We
obtained dmft (number of decayed, missing, and filled teeth
per person) from this dental examination. The dentists were
given detailed criteria for performing the examination but
were not specifically trained as to ensure standardization of
their examinations. In Japan, when children reach 3 years old,
the municipality in which the family currently resides sponsors a physical examination that includes a dental examination, measurement of height and weight, and an interview
survey with parents or guardians regarding the childs health
by the Maternal and Child Health Act.

Analyses
We defined ETS as at least one smoker residing in the home.
ECC has been defined as the presence of one or more
158

Table 1 Prevalence of Dental Caries in the Study Subjects According to

ETS

ETS
Yes
No
Total

Number of
subjects

dmft index

Prevalence
of ECC

1,121
642
1,763*

1.27 (SD = 2.98)

0.53 (SD = 1.69)
1.00 (SD = 2.61)

26.9%
14.6%
22.5%

* 38 subjects were lacking in ETS data.

dmft index, the average number of decayed, missing, or filled teeth; ECC,
early childhood caries; ETS, environmental tobacco smoke; SD, standard
deviation.

2015 American Association of Public Health Dentistry

Y. Nakayama and M. Mori

Tobacco smoke and childhood caries

Table 2 Odd Ratios (ORs) and 95% Confidence Intervals (CIs) of ECC with Univariate Logistic Regression Analysis
Variables

dmft 1

dmft = 0

OR (95%CI)

Application of 2% sodium fluoride solution: 3 times per 3 years

2 times per 3 years
Use of fluoride toothpaste: Everyday or sometimes
Never
Drinking or eating sweets after dinner: Never
Sometimes
Everyday
Frequency of parents brushing childs teeth: Everyday
Sometimes or never
Complete mastication: Good
Bad
Snack times: Regular
Irregular
Consuming vegetable or fruits: No
Yes
Consuming cheese or yogurt: No
Yes
Consuming snack food: No
Yes
Consuming ice cream: No
Yes
Consuming candy: No
Yes
Consuming chocolate: No
Yes
Consuming cookies: No
Yes
Consuming cake: No
Yes
Consuming sugar-sweetened gum: No
Yes
Consuming sugarless gum: No
Yes
Consuming pudding or jelly: No
Yes
Consuming Japanese crackers: No
Yes
Consuming bread: No
Yes
Drinking milk: No
Yes
Drinking isotonic drinks: No
Yes
Drinking juice: No
Yes
Drinking soda: No
Yes
Drinking lactic acid drinks: No
Yes
Drinking water or Japanese tea: No
Yes
Smoker in family: Absence
Presence
Smoking father: Absence
Presence
Smoking mother: Absence
Presence
Smoking grandparent: Absence
Presence
Smoking parent: Absence
Presence
Number of smokers in family: No smoker
One smoker
Two smokers
Three smokers

57
298
232
165
107
131
156
335
59
334
57
160
219
217
179
223
173
169
227
241
155
257
139
181
215
390
6
366
30
357
39
357
39
288
108
278
118
310
86
187
208
339
56
212
183
350
45
304
91
86
309
94
302
167
229
246
150
323
73
300
96
94
169
115
18

255
1,019
820
566
661
402
315
1,279
108
1,120
237
771
526
731
644
775
600
583
792
935
440
881
494
803
572
1,332
42
1,294
80
1,317
58
1,282
93
935
440
838
537
1,104
270
490
895
1,275
110
884
501
1,308
77
1,149
236
171
1,214
548
819
690
677
1,101
266
1,175
192
1,163
204
548
544
230
45

1.00 (reference)
1.31 (0.96-1.79)
1.00 (reference)
1.03 (0.82-1.29)
1.00 (reference)
2.01 (1.52-2.67)
3.06 (2.31-4.05)
1.00 (reference)
2.09 (1.49-2.93)
1.00 (reference)
0.81 (0.59-1.10)
1.00 (reference)
2.01 (1.59-2.53)
1.00 (reference)
0.94 (0.75-1.17)
1.00 (reference)
1.00 (0.80-1.26)
1.00 (reference)
0.99 (0.80-1.24)
1.00 (reference)
1.37 (1.08-1.72)
1.00 (reference)
0.97 (0.76-1.22)
1.00 (reference)
1.67 (1.33-2.09)
1.00 (reference)
0.49 (0.21-1.16)
1.00 (reference)
1.33 (0.86-2.05)
1.00 (reference)
2.48 (1.63-3.78)
1.00 (reference)
1.51 (1.02-2.23)
1.00 (reference)
0.80 (0.62-1.02)
1.00 (reference)
0.66 (0.52-0.84)
1.00 (reference)
1.13 (0.86-1.49)
1.00 (reference)
0.61 (0.49-0.76)
1.00 (reference)
1.92 (1.36-2.70)
1.00 (reference)
1.52 (1.22-1.91)
1.00 (reference)
2.18 (1.48-3.21)
1.00 (reference)
1.46 (1.11-1.92)
1.00 (reference)
0.51 (0.38-0.68)
1.00 (reference)
2.15 (1.67-2.78)
1.00 (reference)
1.40 (1.12-1.75)
1.00 (reference)
2.52 (1.98-3.22)
1.00 (reference)
1.38 (1.03-1.86)
1.00 (reference)
1.82 (1.39-2.40)
1.00 (reference)
1.81 (1.37-2.39)
2.92 (2.13-3.99)
2.33 (1.29-4.20)

dmft: total number of decayed, missing, or filled teeth.

2015 American Association of Public Health Dentistry

159

Tobacco smoke and childhood caries

Y. Nakayama and M. Mori

Table 3 Adjusted Odd Ratios (ORs) and 95% Confidence Intervals (CIs)
of ECC with Multivariate Logistic Regression Analysis
Variables

OR (95% CI)

Drinking or eating sweets after

dinner: Never
Sometimes
Everyday
Frequency of parent brushing childs
teeth: Everyday
Sometimes or never
Snack times: Regular
Irregular
Consuming ice cream: No
Yes
Consuming chocolate: No
Yes
Consuming sugar-sweetened gum: No
Yes
Consuming sugarless gum: No
Yes
Consuming Japanese crackers: No
Yes
Drinking milk: No
Yes
Drinking isotonic drinks: No
Yes
Drinking juice: No
Yes
Drinking soda: No
Yes
Drinking lactic acid drinks: No
Yes
Drinking water or Japanese tea: No
Yes
Smoking father: Absence
Presence
Smoking mother: Absence
Presence
Smoking grandparent: Absence
Presence

1.00 (reference)

P-value

1.61 (1.18-2.20)
1.68 (1.19-2.37)
1.00 (reference)

0.0027
0.0035

1.23 (0.83-1.82)
1.00 (reference)
1.42 (1.10-1.84)
1.00 (reference)
0.92 (0.71-1.21)
1.00 (reference)
1.38 (1.07-1.78)
1.00 (reference)
2.01 (1.27-3.19)
1.00 (reference)
1.45 (0.93-2.28)
1.00 (reference)
0.78 (0.60-1.02)
1.00 (reference)
0.83 (0.64-1.07)
1.00 (reference)
1.47 (1.00-2.17)
1.00 (reference)
1.06 (0.81-1.38)
1.00 (reference)
1.28 (0.82-1.98)
1.00 (reference)
1.20 (0.88-1.64)
1.00 (reference)
0.73 (0.52-1.02)
1.00 (reference)
1.07 (0.83-1.38)
1.00 (reference)
1.91 (1.43-2.54)
1.00 (reference)
1.10 (0.78-1.53)

0.3121
0.0075
0.5615
0.0118
0.0031
0.1033

Discussion

0.0704

The present study found that ECC was significantly associated with the existence of smokers in the home. In particular, maternal smoking was significantly associated with a
higher prevalence of dental caries, and the number of
smokers in a family was significantly associated with the risk
of ECC. The mother may influence her child more strongly
than other family members, as the mother is likely to spend
a longer time with the child. The percentage of children age
less than or equal to 5 years old in daycare in Japan was 32.2
percent by data from the Ministry of Health, Labour and
Welfare of Japan. Our results confirmed those of other
studies showing an effect of ETS exposure at home on
dental caries (6-14).
Causes that influenced ETS exposure at home on pediatric
dental caries are considered to be as follows: First, Preston
et al. (16) reported that ETS can reduce concentrations of
ascorbates in children, even when the amount of exposure to
ETS is minimal. Vnnen (17) reported that decreased
vitamin C levels have been associated with the growth of cariogenic bacteria. Lindemeyer et al. (18) reported that tobacco
enhances the growth of cariogenic streptococci in vitro. ETS
exposure may increase cariogenic streptococci in the oral
cavity of infants. Second, Leory et al. (10) reported that children raised by parents who smoked, brushed their teeth less
frequently, received less help with tooth brushing, and consumed more in between meals and nightly beverage may have
had poor oral hygiene and were more likely to have dental
caries. However, we found a relationship between ETS exposure at home and ECC even after controlling for oral hygiene
and snacking habits in this study.
Additionally, a transmission of streptococcus mutans from
smoking mothers to their children may be considered an
impact of maternal smoking on pediatric dental caries.
Shinga et al. (19) reported that pregnant females who had

0.1475
0.0497
0.6672
0.2747
0.2389
0.0644
0.6145
<0.0001
0.5951

lactic acid drinks (OR = 1.46, 95 percent CI: 1.11-1.92), and

less frequent intake of water or Japanese tea (OR = 0.51, 95
percent CI: 0.38-0.68) were significantly associated with the
risk factors of ECC. Existence of smokers in the home
(OR = 2.15, 95 percent CI: 1.67-2.78), paternal smoking
(OR = 1.40, 95 percent CI: 1.12-1.75), maternal smoking (OR = 2.52, 95 percent CI: 1.98-3.22), parental smoking
(OR = 1.82, 95 percent CI: 1.39-2.40), grandparental
smoking (OR = 1.38, 95 percent CI: 1.03-1.86), and the
number of smokers in the family (one smoker: OR = 1.81, 95
percent CI: 1.37-2.39, two smokers: OR = 2.92, 95 percent CI:
2.13-3.99, three smokers: OR = 2.33, 95 percent CI: 1.294.20) were significantly associated with the risk of ECC.
As shown in Table 3, the multivariate analysis included the
significant variables found by univariate analysis, after
160

excluding items of multicollinearity. Drinking or eating

sweets after dinner sometimes (OR = 1.61, 95 percent CI:
1.18-2.20) and everyday (OR = 1.68, 95 percent CI: 1.192.37), irregular snack times (OR = 1.42, 95 percent CI: 1.101.84), frequent intake of chocolate (OR = 1.38, 95 percent
CI: 1.07-1.78), frequent intake of sugar-sweetened gum
(OR = 2.01, 95 percent CI: 1.00-2.17), frequent intake of isotonic drinks (OR = 1.47, 95 percent CI: 1.00-2.17), and
maternal smoking (OR = 1.91, 95 percent CI: 1.43-2.54) were
significantly associated with the risk of ECC.
Also, we conducted a multivariable analysis using variables
for the number of smokers in a family instead of variables for
a smoking mother, father, and grandparent. The number of
smokers in a family (P for trend, P < 0.001) was significantly
associated with the risk of ECC (not shown in table).

2015 American Association of Public Health Dentistry

Y. Nakayama and M. Mori

more cariogenic streptococci in their mouth were more likely

to have smoking habits than those who had less cariogenic
streptococci.
In multivariate analysis, frequent drinking or eating of
sweets after dinner, irregular snack times, and frequent intake
of chocolate, sugar-sweetened gum, and isotonic drinks were
significantly associated with ECC. The results of this study
were in accordance with several previous studies (3,10,13,2023). Leroy et al. (10) reported by multivariable analysis that
drinks at nights had a significant, positive association with
visible caries in 3-year-old. Schluter et al. (22) reported that
children snacking or drinking prior to bed displayed an
increased OR of fillings and/or extraction to those neither
snacking nor drinking before bed in 4-year-old children.
Tanaka et al. (13) reported that two or more between-meal
snacks per day was positively associated with dental caries
among 3-year-old children. Ibrahim et al. (21) reported in a
longitudinal study that irregular snacking was associated
with dental caries. Sankeshwari et al. (23) reported that significant correlation were obtained concerning sucrose exposure between meals and the total frequency of sucrose
exposure to the risk of ECC. Features of our study, which have
been less common in other studies, investigated the association between the content of snacks with ECC in detail. Leroy
et al. (10) and Hanioka et al. (11) reported that ETS was significantly associated with ECC adjusted for snacks, drinks,
and oral hygiene, such as tooth brushing, among 3-year-old
children, which is similar to our study. However, they did not
investigate the contents of snacks or drinks in detail, which we
did.
In this study, a reduced frequency in parents brushing their
childs teeth was not significantly associated with ECC in the
multivariate analysis. Prakash et al. (3) reported in a crosssectional study that the prevalence of caries in children who
practiced tooth brushing by themselves contained a significantly higher risk of dental caries than in children who
brushed under parental supervision. Ibrahim et al. (21)
reported in a longitudinal study that brushing without the
mothers assistance by the age of 2.5-years-old put 3.5-yearold children at high risk of developing caries.
There were some limitations to our study. First, our
results were unable to identify the cause of ECC in the
cross-sectional study. Furthermore, a study such as a cohort
study is necessary to establish the relationship between ECC
and ETS. Second, our study did not investigate socioeconomic status. Several studies (2-5) reported on the impact
of socioeconomic status on ECC. Preschool children, especially those living in low socioeconomic situations, are susceptible to dental caries, perhaps owing to poorer nutrition,
less emphasis on health behaviors, and insufficient access to
dental care (2). Third, the data on dental caries used in the
present study were gathered during routine examinations by
dentists at local dental clinics. The dentists were given
2015 American Association of Public Health Dentistry

Tobacco smoke and childhood caries

detailed criteria for performing the examination but were

not specifically trained so as to ensure standardization of
their examinations.
In conclusion, this study suggests that there is a significant
relationship between ECC and the existence of smokers in the
home (in particular, maternal smoking and number of
smokers) even after controlling for snacking habits. Furthermore, we found that there is a significant relationship
between ECC and snacking habits such as irregular snack
times, frequent drinking, or eating sweets after dinner.

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2015 American Association of Public Health Dentistry