Secondhand smoke and incidence of dental caries in deciduous teeth among children in Japan: Population based retrospective cohort study

Abstract

Study question Does maternal smoking during pregnancy and exposure of infants to tobacco smoke at age 4 months increase the risk of caries in deciduous teeth?
Methods Population based retrospective cohort study of 76 920 children born between 2004 and 2010 in Kobe City, Japan who received municipal health check-ups at birth, 4, 9, and 18 months, and 3 years and had information on household smoking status at age 4 months and records of dental examinations at age 18 months and 3 years. Smoking during pregnancy and exposure of infants to secondhand smoke at age 4 months was assessed by standardised parent reported questionnaires. The main outcome measure was the incidence of caries in deciduous teeth, defined as at least one decayed, missing, or filled tooth assessed by qualified dentists without radiographs. Cox regression was used to estimate hazard ratios of exposure to secondhand smoke compared with having no smoker in the family after propensity score adjustment for clinical and lifestyle characteristics.
Study answer and limitations Prevalence of household smoking among the 76 920 children was 55.3% (n=42 525), and 6.8% (n=5268) had evidence of exposure to tobacco smoke. A total of 12 729 incidents of dental caries were observed and most were decayed teeth (3 year follow-up rate 91.9%). The risk of caries at age 3 years was 14.0% (no smoker in family), 20.0% (smoking in household but without evidence of exposure to tobacco smoke), and 27.6% (exposure to tobacco smoke). The propensity score adjusted hazard ratios of the two exposure groups compared with having no smoker in the family were 1.46 (95% confidence interval 1.40 to 1.52) and 2.14 (1.99 to 2.29), respectively. The propensity score adjusted hazard ratio between maternal smoking during pregnancy and having no smoker in the family was 1.10 (0.97 to 1.25).
What this study adds Exposure to tobacco smoke at 4 months of age was associated with an approximately twofold increased risk of caries, and the risk of caries was also increased among those exposed to household smoking, by 1.5-fold, whereas the effect of maternal smoking during pregnancy was not statistically significant.
Funding, competing interests, data sharing This study was supported by a grant in aid for scientific research 26860415. The authors have no competing interests or additional data to share.

Full text

thebmj 
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2015;351:h5397  doi: 10.1136/bmj.h5397
RESEARCH
1
open access
Department of Pharmaco-
epidemiology, Graduate School
of Medicine and Public Health,
Kyoto University, Yoshida-
Konoe-cho, Sakyo-ku, Kyoto
606-8501, Japan
Correspondence to: KKawakami
kawakami.koji.4e@kyoto-u.ac.jp
Additional material is published
online only. To view please visit
the journal online (http://dx.doi.
org/10.1136/bmj.h5397)
Cite this as: BMJ ;:h
doi: 10.1136/bmj.h5397
Accepted: 22 September 2015
Secondhand smoke and incidence of dental caries in deciduous
teeth among children in Japan: population based retrospective
cohort study
Shiro Tanaka, Maki Shinzawa, Hironobu Tokumasu, Kahori Seto, Sachiko Tanaka, Koji Kawakami
ABSTRACT
STUDY QUESTION
Does maternal smoking during pregnancy and
exposure of infants to tobacco smoke at age 4 months
increase the risk of caries in deciduous teeth?
METHODS
Population based retrospective cohort study of 76 920
children born between 2004 and 2010 in Kobe City,
Japan who received municipal health check-ups at
birth, 4, 9, and 18 months, and 3 years and had
information on household smoking status at age
4months and records of dental examinations at age
18months and 3 years. Smoking during pregnancy and
exposure of infants to secondhand smoke at age
4months was assessed by standardised parent
reported questionnaires. The main outcome measure
was the incidence of caries in deciduous teeth, dened
as at least one decayed, missing, or lled tooth
assessed by qualied dentists without radiographs.
Cox regression was used to estimate hazard ratios of
exposure to secondhand smoke compared with having
no smoker in the family aer propensity score
adjustment for clinical and lifestyle characteristics.
STUDY ANSWER AND LIMITATIONS
Prevalence of household smoking among the 76 920
children was 55.3% (n=42 525), and 6.8% (n=5268)
had evidence of exposure to tobacco smoke. A total of
12 729 incidents of dental caries were observed and
most were decayed teeth (3 year follow-up rate 91.9%).
The risk of caries at age 3 years was 14.0% (no smoker
in family), 20.0% (smoking in household but without
evidence of exposure to tobacco smoke), and 27.6%
(exposure to tobacco smoke). The propensity score
adjusted hazard ratios of the two exposure groups
compared with having no smoker in the family were
1.46 (95% condence interval 1.40 to 1.52) and 2.14
(1.99 to 2.29), respectively. The propensity score
adjusted hazard ratio between maternal smoking
during pregnancy and having no smoker in the family
was 1.10 (0.97 to 1.25).
WHAT THIS STUDY ADDS
Exposure to tobacco smoke at 4 months of age was
associated with an approximately twofold increased
risk of caries, and the risk of caries was also increased
among those exposed to household smoking, by
1.5-fold, whereas the eect of maternal smoking during
pregnancy was not statistically signicant.
FUNDING, COMPETING INTERESTS, DATA SHARING
This study was supported by a grant in aid for scientic
research 26860415. The authors have no competing
interests or additional data to share.
Introduction
Dental caries is a continuing problem worldwide.
Among all causes of disability adjusted life years
evaluated in the Global Burden of Disease 2010 Study,
the global prevalence of untreated caries was the high
-
est, with no decreasing trends between 1990 and 2010,
and its global burden is ranked 80th.
1
In developed
countries, the prevalence of caries in deciduous teeth
remains high (20.5% in children aged 2 to 5 years in the
United States
2
and 25.0% in children aged 3 years in
Japan),
3
and established measures for caries preven-
tion in young children is limited to sugar restriction,
oral fluoride supplementation, and fluoride varnish.
4
The cause of caries involves various physical, biologi-
cal, environmental, and lifestyle factors—for example,
cariogenic bacteria, inadequate salivary flow, insucient
exposure to fluoride, and poor oral hygiene,
5
and the cru-
cial event in the clinical course is the initial acquisition of
Streptococcus mutans. However, the ecacy of caries pre
-
vention by chlorhexidine, which eectively eliminates
Smutans, is inconclusive. Randomised controlled trials
in adults and school children have shown that chlorhex
-
idine is not eective, and the American Dental Associa-
tion does not recommend its use.
6
However, a two year
randomised controlled trial of 334 preschool children
aged 4 and 5 years found a small but significant reduc
-
tion of dental caries in deciduous teeth with chorhexi-
dine use.
7
S mutans is usually transmitted from mothers
and possibly from cross infection among children in
nursery environments.
8
The risk of acquisition is partic-
ularly high from 19 to 31 months of age, referred to as a
window of infectivity.
9
Therefore the eects of preventing
or delaying the acquisition of S mutans before or during
the window of infectivity remain unknown.
WHAT IS ALREADY KNOWN ON THIS TOPIC
The prevalence of caries in deciduous teeth in developed countries remains high
Established measures for caries prevention in young children is limited to sugar
restriction, oral fluoride supplementation, and fluoride varnish
Cross sectional studies have suggested associations between exposure to
secondhand smoke and caries in deciduous and permanent teeth, but data from
cohort studies are limited to one study in Sweden
WHAT THIS STUDY ADDS
Exposure to tobacco smoke at 4 months of age was associated with an
approximately twofold increased risk of caries in deciduous teeth
The risk of caries was also increased by 1.5-fold among those exposed to smoking in
the household, whereas the eect of maternal smoking during pregnancy was not
statistically signicant
Although these ndings cannot establish causality, they support extending public
health and clinical interventions to reduce secondhand smoke

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Secondhand smoke may directly influence teeth and
microorganisms.
10
The adverse eects of secondhand
smoke include inflammation of the oral membrane and
impaired salivary gland function
11
and a decrease in
serum vitamin C levels
12
as well as immune dysfunction.
Children exposed to passive smoking also have lower
salivary IgA levels and higher levels of sialic acid with
higher activity.
12
Sialic acid enhances agglutination of S
mutans, leading to the formation of dental plaque and
caries.
13
In addition to the direct eects of secondhand
smoke, inhibition of the morphology and mineralisa
-
tion of dental hard tissue in the ospring of rats
exposed to passive smoking was also reported.
14
The
global prevalence of those exposed to secondhand
smoke is estimated to be 40% of children and more than
30% of non-smokers.
15
Cross sectional studies have sug-
gested associations between secondhand smoke and
caries in deciduous and permanent teeth,
10
16-18
ut data
from cohort studies are limited to the registry of 18 142
teenagers in Sweden.
19
In that study, maternal smoking
during early pregnancy and exposure to secondhand
smoke from mothers were linked to an increased risk of
increments in caries during the ages of 13 to 19 years,
whereas these associations may be confounded by
unmeasured lifestyle factors such as tooth brushing.
20
Hence it is still uncertain whether a reduction in the
prevalence of exposure to secondhand smoke among
children would contribute to caries prevention. We
investigated maternal smoking status during pregnancy
and before the window of infectivity as risk factors for
the incidence of caries in deciduous teeth in a cohort of
76 920 Japanese children, taking lifestyle factors of the
children into consideration.
Methods
Settings and study design
The Kobe Ospring Study was designed as a population
based retrospective cohort study using records of
municipal health check-ups in Kobe City, Japan. In
Japan, health check-ups are mandatory for women of
childbearing potential and children up to 3 years old
according to the Maternal and Child Health Act.
21
We
had access to deidentified data on health check-ups
from 31 March 2004 to 1 April 2014 after approval by the
Planning and Coordination Bureau of Kobe.
Kobe City is the sixth largest city in Japan, with a pop
-
ulation of about 1.5 million, and is the capital city of
Hyogo Prefecture on the southern side of the main
island of Japan. According to vital statistics for 2013
there were 90 216 births in Kobe between 2004 and 2010
(see supplementary figure 1). All women of childbearing
age and children from pregnancy to 3 years of age resid
-
ing in Kobe City participated in the health check-up pro-
gramme. We included children who were born between
2004 and 2010 with available information on associated
smoking at age 4 months and records of dental exam
-
inations at 18 months and 3 years. In the study protocol,
we estimated the cohort size based on the annual num
-
ber of participants, but the sample size calculation
based on statistical considerations was not relevant
owing to the retrospective design of the study.
Patient involvement
There was no direct patient involvement in this study.
The datasets used for analysis did not include names
and identity numbers of citizens.
Measurements
The health check-up programme in Kobe City consisted of
completing a standardised pregnancy notification form,
neonatal health check-ups, and advice provided during
home visits and health check-ups of infants at ages 4, 9,
and 18 months and 3 years at healthcare centres of ward
oces or designated clinics. Personal and physical data
on pregnancy provided by the mother included maternal
age at birth, planned and actual date of delivery, height,
body weight, occupation, birth order and gestational age
of the infant, and multiple births. Personal, physical, and
laboratory data from the infant’s birth to 3 years of age
included gestational age at birth; abnormalities during
pregnancy and at delivery; body weight; height; head and
chest circumference; physical, neurological, ophthalmo
-
logical, and dental examinations; hearing tests; urinary
protein level; and occult blood by a dipstick test.
Information on lifestyle factors was based exclusively
on information from standardised parent reported ques
-
tionnaires, which mothers were required to fill out at
every health check-up. Exposure to secondhand smoke
from pregnancy to 3 years of age was assessed as: mater
-
nal smoking during pregnancy (never, former, or current
smoker), daily number of cigarettes smoked during
pregnancy, presence of smokers in the household during
pregnancy, smoking status of parents and family mem
-
bers when the infant was 4 months of age (non-smoker,
smoking away from child, or smoking in front of child),
and presence of smokers in the family at 9 months, 18
months, and 3 years. Information on third hand smoke
was not available. In the current analysis we defined
household smoking as smoking by family members in
the household when the infant was 4 months old, and
we defined exposure to tobacco smoke as smoking by
family members in front of the infant at age 4 months.
Other lifestyle factors included the number of family
members in the household; people involved in parent
-
ing and childcare; use of a babysitter or nursery; mental
status of the mother, assessed by a picture face scale
with five levels from a smile to a tearful face; frequency
of alcohol consumption during pregnancy; sleeping
hours or sleep duration of the child; dietary habits of the
child, such as breast feeding and bottle feeding and fre
-
quency of eating sweets and drinking juice; and oral
care, such as tooth brushing alone or by parents.
Assessment of dental caries
Qualified dentists assessed the oral conditions of the
children at 18 months and 3 years of age through visual
examination and not radiography. They classified each
tooth into one of seven types: normal, decayed, miss
-
ing, filled, treated by diammine silver fluoride, observa-
tion required, or treated by a dental sealant. We counted
teeth treated by diammine silver fluoride as well as
decayed teeth as decayed. Incidence of dental caries
was defined as the occurrence of at least one decayed,

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missing, or filled tooth. Other records of dental exam-
inations included the caries activity test (0 to 4 points,
4 points indicating most active), presence of plaque,
abnormal conditions of soft tissues and occlusion, and
treatment with fluoride varnish.
Statistical analysis
The primary outcome was time to the first incidence of
caries in deciduous teeth. Secondary outcomes were the
first incidence of caries in mandibular or maxillary ante
-
rior teeth or molars and numbers of decayed, missing, or
filled teeth at 18 months and 3 years, using the DMF
(decayed, missing, filled) index. We used the dierence
between birth date and the first date of assessment when
dental caries was diagnosed as failure time, and the dif
-
ference between birth date and the last date of assess-
ment (18 months if assessment at 3 years was not done) as
censored time. The Kaplan-Meier method was used to
estimate the risks of caries at 3 years of age. We expressed
the eects of secondhand smoke on the incidence of car
-
ies as hazard ratios with 95% confidence intervals, esti-
mated by Cox regression adjusted for a linear term of the
propensity score. The proportional hazards assumption
was confirmed with log-negative log graphs. We com
-
pared the numbers of decayed, missing, or filled teeth
using mixed models adjusted for a linear term of the pro
-
pensity score. For each infant we calculated the propen-
sity score, defined as the conditional probability of a child
being exposed to secondhand smoke at 4 months of age
given several confounders (see box), using logistic regres
-
sion and single mean imputation for missing covariates.
Sensitivity analyses
We performed four sensitivity analyses: Cox regression
analysis restricted to first born singletons, which
accounts for the eects of clustering of children within
the same family; Cox regression analysis excluding chil
-
dren with a propensity score below the first centile and
above the 99th centile, which ensures strict overlap of
propensity scores of dierent groups; and Cox regression
analysis further adjusting for the covariates of number of
teeth at 9 months, fluoride varnish treatment at 18
months and 3 years, tooth brushing alone at 18 months
and 3 years, tooth brushing by parents at 18 months and
3 years, bottle feeding at 4 months and 9 months, baby
food intake at 9 months, age at start of baby food, fre
-
quency of eating sweets at 18 months and 3 years, eating
sweets irregularly at 18 months and 3 years, and drinking
juice every day at 18 months and 3 years, which adjusts
for post-exposure covariates as potential confounders;
and exponential regression analysis handling the time to
event data as interval censored, which accounts for the
fact that time to events were not known exactly.
All reported probability values were two sided, and
we considered P<0.05 to be statistically significant. An
academic statistician conducted all analyses using SAS
software version 9.4 (SAS Institute, Cary, NC).
Results
The database of the health check-up programme in
Kobe City consisted of records of 145 318 participants in
the health check-up programme in Kobe City between
2004 and 2014. We initially identified 82 543 infants
born between 2004 and 2010 who received a health
check-up at 4 months of age. Information about expo
-
sure to smoking at 4 months was available for 82 409
(99.8%) children and the records of a dental examina
-
tion were available for 76 920 (93.2%) of these children
(see supplementary figure 1). Thus the analysis popula
-
tion used for time to event analysis consisted of the
76 920 children. Background characteristics diered
significantly for mother’s age, smoking and alcohol
consumption, gestational week, and birth weight
between those included and excluded in this analysis.
The dierences were, however, generally small (see
supplementary table 1).
Tables 1 and 2 describe the baseline characteristics
and lifestyles of the 76 920 children, categorised into
three groups according to details of family smoking at
age 4 months: family members did not smoke, family
members smoked away from the infant; and infant
was exposed to secondhand smoke. Prevalence of
smoking in the household (family members who
smoked when the infant was 4 months old) was 55.3%
(42 525/76 920), and most smokers were the fathers (see
supplementary table 2). Among them, 5268 (6.8%)
children had evidence of exposure to tobacco smoke—
that is, at least one family member smoked in their
Potential confounders
Maternal factors
• Maternal age at birth
• Alcohol consumption during pregnancy
• First birth
• Multiple birth
• Pre-eclampsia
• Anaemia
• Threatened abortion
• Gestation weeks
• Caesarean section
• Vacuum extraction
• Mental status four months post partum
Infant factors
• Birth year of child
• Sex of child
• Nuchal cord
• Asphyxia
• Jaundice and transfusion
• Convulsion
• Incubator
• Oxygen inhalation
• Weight at birth
• Height at birth
• Head circumference at birth
• Chest circumference at birth
• Bottle feeding
Other factors
• People involved in parenting
• Support by family, friends, and neighbours

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presence. Prevalence of household smoking at age 3
years in the three groups was 4.9%, 68.4%, and 76.2%,
respectively (see supplementary table 2). The mothers
of children who were exposed to smoking tended to be
younger, and around 25% of those whose infants were
exposed to secondhand smoke during pregnancy
(table 1). Abnormalities at delivery, gestational age,
and birth weight did not dier significantly across the
three groups (table 1). More than 99% of children
received fluoride varnish at 18 months. Four month old
children with family members who smoked had their
teeth brushed less frequently by themselves or by
Table  | Background data on   infants according to smoking status of family members and exposure to tobacco smoke at  months of age. Values
are numbers (percentages) unless stated otherwise
Characteristics
Not exposed to secondhand
smoke(n= )
Exposed to only household
smoking(n= )
Exposed to tobacco
smoke(n=)
Mean (SD) maternal age at delivery (years)* 32.5 (4.2) 30.5 (4.9) 30.0 (5.2)
Maternal age ≥35 years* 6 8 92 (27.5) 4743 (18.1) 6 4 0 (17. 8)
Maternal smoking during pregnancy* 2062 (8.4) 6176 (24.1) 879 (25.0)
Maternal alcohol consumption during pregnancy:*
Occasional 4 410 (17. 9) 4242 (16.6) 725 (20.7)
Daily 147 (0.6) 147 (0.6) 37 (1.1)
Girl 51 151 (48.7) 55 402 (48.7) 7828 (48.6)
First birth* 40 060 (45.7) 12 144 (49.7) 1002 (30.3)
Multiple birth* 275 (1.1) 205 (0.8) 18 (0.5)
Pre-eclampsia 777 (2.3) 970 (2.6) 148 (2.8)
Anaemia 3653 (10.6) 3935 (10.6) 556 (10.6)
Threatened abortion 3822 (11.1) 4073 (10.9) 586 (11.1)
Gestational weeks:†
22-27 54 (0.2) 67 (0.2) 10 (0.2)
28-36 1978 (5.9) 2160 (6.0) 271 (5.4)
36-43 31 212 (93.9) 33637 (93.8) 4762 (94.4)
Mean (SD) birth weight (g) 3008.9 (418.8) 2995.8 (416.6) 3026.1 (415.4)
*Data missing for 33% of infants.
†Data missing for 4% of infants.
Table  | Characteristics of   children according to smoking status of family members and exposure to tobacco smoke at  months of age. Values
are numbers (percentages) unless stated otherwise
Characteristics
Not exposed to secondhand
smoke(n= )
Exposed to only household
smoking(n= )
Exposed to tobacco
smoke(n=)
Mean (SD) No of teeth at 9 months 3.5 (2.2) 3.6 (2.2) 3.6 (2.2)
Treated by fluoride varnish at 18 months 29 783 (99.4) 31 758 (99.3) 4246 (99.1)
Tooth brushing:
Own self at 18 months 27 370 (80.2) 28 884 (78.3) 3817 (73.5)
Own self at 3 years 27 781 (87.7) 29 847 (87.0) 4034 (83.2)
Parents at 18 months 26 175 (76.7) 26 365 (71.4) 3368 (64.8)
Parents at 3 years 28 497 (90.0) 29 100 (84.8) 3661 (75.5)
Plaque present:
18 months 7045 (20.7) 8320 (22.6) 140 6 (2 7. 2)
3 years 4924 (15.7) 6450 (19.0) 1175 (24.5)
Feeding method:
Bottle at 4 months 13 456 (39.9) 17 163 (47.4) 2696 (52.8)
Bottle at 9 months 12 136 (35.9) 14 972 (41.3) 2160 (43.0)
Baby food at 9 months 31 334 (92.7) 33 187 (91.6) 4462 (88.8)
Mean (SD) age at start of baby food (months) 5.6 (0.8) 5.4 (0.8) 5.4 (0.9)
Mean (SD) frequency of eating sweets at 18 months (daily) 1.5 (0.6) 1.5 (0.6) 1.6 (0.7)
Mean (SD) frequency of eating sweets at 3 years (daily) 1.5 (0.6) 1.5 (0.6) 1.6 (0.6)
Consumption of sweets:
Irregularly at 18 months 9743 (28.3) 12 568 (33.7) 2009 (38.1)
Irregularly at 3 years 10 106 (29.4) 12 344 (33.1) 1896 (36.0)
Daily juice consumption:
18 months 12 424 (36.3) 16 964 (45.9) 2553 (49.1)
3 years 13 291 (42.0) 16 870 (49.2) 2428 (50.1)
Use of babysitter or nursery:
4 months 592 (1.7) 740 (2.0) 160 (3.0)
18 months 8071 (23.6) 9420 (25.5) 1629 (31.4)
3 years 13 915 (44.0) 15 806 (46.2) 2511 (51.8)
*1% to 14% of infants had missing data on each item.

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parents. The frequency of eating sweets was similar
across the three groups, but exposure to smoke was
associated with higher proportions of bottle feeding,
drinking juice every day, and use of a babysitter or
nursery (table 2).
Of the 76 920 children, 70 711 (91.9%) attended a den
-
tal examination at 3 years of age. There were significant
dierences in mother’s age, child’s sex, first born sta
-
tus, and maternal anaemia at delivery between those
who were followed for three years and those who were
not, including smoking status at four months (see sup
-
plementary table 3). Overall, 12 729 cases of dental car-
ies were observed, with 12 579 related to decayed teeth.
The mean DMF index (the numbers of decayed, miss
-
ing, or filled teeth) was 0.06 (2.5 centile: 0, median: 0,
97.5 centile: 0) at age 18 months and 0.61 (2.5 centile: 0,
median: 0, 97.5 centile: 6) at age 3 years. Unadjusted
three year risks of caries calculated by the Kaplan-Meier
method were 18.0% in total and 14.0% for infants in
households where no family members smoked, 20.0%
when family members smoked away from infants, and
27.6% when infants were exposed to tobacco smoke at
age 4 months (table 3). The propensity score adjusted
hazard ratios of having family members who smoked
away from or in front of children compared with having
no smoker in the family were 1.46 (95% confidence
interval 1.40 to 1.52, P<0.01) and 2.14 (1.99 to 2.29,
P<0.01), respectively. Similar associations were
observed for dierent sites (mandibular or maxillary,
anterior teeth or molars). Sensitivity analysis indicated
Table  | Propensity score analysis of exposure to secondhand smoke at age  months and incidence of caries
Variables
Not exposed to
secondhand
smoke(n=)
Exposed to only household
smoking (n= )
Exposed to tobacco smoke
(n=)
Hazard ratio (% CI) P value Hazard ratio (% CI) P value
Incidence of any caries (unadjusted) (%): 4453 (14.0*) 6925 (20.0*) 1351 ( 2 7.6* )
Unadjusted Ref 1.54 (1.48 to 1.61) < 0.01 2.35 (2.19 to 2.52) < 0.01
Propensity score adjusted† Ref 1.46 (1.40 to 1.52) < 0.01 2.14 (1.99 to 2.29) <0.01
Sensitivity analysis‡ Ref 1.71 (1.56 to 1.87) <0.01 2.92 (2.48 to 3.43) < 0.01
Sensitivity analysis§ Ref 1.46 (1.40 to 1.52) <0.01 2.13 (1.99 to 2.29) <0.01
Sensitivity analysis¶ Ref 1.32 (1.24 to 1.40) <0.01 1.77 (1.58 to 1.98) < 0.01
Sensitivity analysis** Ref 1.40 (1.35 to 1.46) <0.01 1.94 (1.83 to 2.07) <0.01
Incidence of caries in maxillary anterior teeth (unadjusted) (%): 2882 (9.0*) 4602 (13.3*) 892 (18.2*)
Crude Ref 1.55 (1.47 to 1.62) < 0.01 2.24 (2.07 to 2.43) < 0.01
Propensity score adjusted† Ref 1.48 (1.41 to 1.56) <0.01 2.10 (1.94 to 2.28) <0.01
Sensitivity analysis‡ Ref 1.71 (1.57 to 1.87) <0.01 2.94 (2.49 to 3.45) <0.01
Sensitivity analysis§ Ref 1.46 (1.40 to 1.52) <0.01 2.14 (2.00 to 2.30) <0.01
Sensitivity analysis¶ Ref 1.32 (1.24 to 1.41) < 0.01 1.77 (1.58 to 1.99) <0.01
Sensitivity analysis** Ref 1.45 (1.38 to 1.52) <0.01 1.99 (1.84 to 2.15) <0.01
Incidence of caries on maxillary molars (unadjusted) (%): 1361 (4.3*) 2297 (6.7*) 478 (9.8*)
Crude Ref 1.60 (1.49 to 1.71) <0.01 2.43 (2.18 to 2.71) <0.01
Propensity score adjusted† Ref 1.51 (1.41 to 1.62) <0.01 2.23 (2.00 to 2.49) < 0.01
Sensitivity analysis‡ Ref 1.71 (1.56 to 1.87) <0.01 2.95 (2.50 to 3.48) <0.01
Sensitivity analysis§ Ref 1.46 (1.40 to 1.53) <0.01 2.16 (2.01 to 2.32) < 0.01
Sensitivity analysis¶ Ref 1.32 (1.24 to 1.40) <0.01 1.78 (1.59 to 2.01) <0.01
Sensitivity analysis** Ref 1.49 (1.39 to 1.60) <0.01 2.16 (1.94 to 2.40) <0.01
Incidence of caries on mandibular anterior teeth (unadjusted) (%): 287 (0.9*) 494 (1.4*) 112 (2.3*)
Crude Ref 1.60 (1.38 to 1.85) <0.01 2.58 (2.07 to 3.22) <0.01
Propensity score adjusted† Ref 1.50 (1.29 to 1.74) <0.01 2.36 (1.88 to 2.95) <0.01
Sensitivity analysis‡ Ref 1.71 (1.57 to 1.87) <0.01 2.96 (2.51 to 3.50) <0.01
Sensitivity analysis§ Ref 1.47 (1.40 to 1.53) <0.01 2.17 (2.01 to 2.33) <0.01
Sensitivity analysis¶ Ref 1.32 (1.24 to 1.41) < 0.01 1.79 (1.59 to 2.01) <0.01
Sensitivity analysis** Ref 1.50 (1.30 to 1.75) 0.89 2.35 (1.88 to 2.94) <0.01
Incidence of caries on mandibular molars (unadjusted) (%): 2062 (6.5*) 3666 (10.7*) 768 (16.0*)
Crude Ref 1.72 (1.62 to 1.82) <0.01 2.70 (2.47 to 2.95) <0.01
Propensity score adjusted† Ref 1.58 (1.49 to 1.67) <0.01 2.39 (2.18 to 2.61) <0.01
Sensitivity analysis‡ Ref 1.71 (1.56 to 1.87) <0.01 2.95 (2.50 to 3.48) <0.01
Sensitivity analysis§ Ref 1.46 (1.40 to 1.53) <0.01 2.17 (2.02 to 2.33) <0.01
Sensitivity analysis¶ Ref 1.32 (1.24 to 1.41) < 0.01 1.79 (1.59 to 2.01) <0.01
Sensitivity analysis** Ref 1.54 (1.46 to 1.63) <0.01 2.24 (2.06 to 2.43) <0.01
*Estimated by Kaplan-Meier method.
†Adjusted for birth year of child, maternal age, alcohol consumption during pregnancy, smoking status during pregnancy, sex, rst birth, multiple birth, pre-eclampsia, anaemia, threatened
abortion, gestational weeks, caesarean section, vacuum extraction, nuchal cord, asphyxia, jaundice and transfusion, convulsion, incubator, oxygen inhalation, weight, height, head and chest
circumference at birth, weight at 4 months, bottle feeding at 4 months, people involved in child care at 4 months, support by family, friends, or neighbours at 4 months, and mother’s mental
status at 4 months.
‡Restricted to rst born singletons.
§Children with a propensity score below rst centile or above 99th centile were excluded.
¶Further adjusted for number of teeth at 9 months, treatment with fluoride varnish at 18 months and 3 years, tooth brushing alone at 18 months and 3 years, tooth brushing by parents at 18
months and 3 years (%), bottle feeding at 4 months and 9 months, baby food at 9 months, age at start of baby food, frequency of sweets at 18 months and 3 years, eating sweets irregularly at
18 months and 3 years, and drinking juice every day at 18 months and 3 years.
**Exponential regression analysis handling time to event data as interval censored.

doi: 10.1136/bmj.h5397 
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2015;351:h5397  thebmj
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6
that these associations were robust against the influ-
ence of behaviour patterns from the age of 4 months to
3 years. Supplementary table 4 provides propensity
score adjusted risk ratios for caries at 18 months and 3
years (that is, analysis as binary outcomes). Children
with family members who smoked had significantly
more decayed, missing, or filled teeth than those with
no smokers in the family. The mean DMF index at 18
months was 0.03 (2.5 centile: 0, median: 0, 97.5 centile:
0) with no family members who smoked, 0.07 (2.5 cen
-
tile: 0, median: 0, 97.5 centile: 0, P<0.01) with family
members who smoked away from infants, and 0.11 (2.5
centile: 0, median: 0, 97.5 centile: 2, P<0.01) with infants
exposed to tobacco smoke at age 4 months. The mean
DMF index at 3 years in the three groups was 0.44 (2.5
centile: 0, median: 0, 97.5 centile: 5), 0.72 (2.5 centile: 0,
median: 0, 97.5 centile: 7, P<0.01), and 1.07 (2.5 centile:
0, median: 0, 97.5 centile: 9, P<0.01), respectively.
Table 4 shows associations between maternal smok
-
ing during pregnancy and incidence of caries. The
crude risk of caries among children exposed to mater
-
nal smoking during pregnancy was higher than that of
those who were not exposed (crude hazard ratio 1.14,
95% confidence interval 1.00 to 1.30, P=0.05), but this
association was weakened in the propensity score
adjusted analysis (adjusted hazard ratio 1.10, 95% con
-
fidence interval 0.97 to 1.25, P=0.14). The mean DMF
index at 18 months was 0.04 (2.5 centile: 0, median: 0,
97.5 centile: 0) for infants exposed to secondhand
smoke, 0.04 (2.5 centile: 0, median: 0, 97.5 centile: 0,
P=0.59) for infants exposed to only maternal smoking
during pregnancy, 0.07 (2.5 centile: 0, median: 0, 97.5
centile: 0, P<0.01) for infants exposed to only house
-
hold smoking at 4 months, and 0.7 (2.5 centile: 0,
median: 0, 97.5 centile: 0, P<0.01) for infants exposed to
secondhand smoke during pregnancy and at 4 months.
The mean DMF index at 3 years was 0.42 (2.5 centile: 0,
median: 0, 97.5 centile: 5), 0.46 (2.5 centile: 0, median:
0, 97.5 centile: 8, P=0.74), 0.72 (2.5 centile: 0, median: 0,
97.5 centile: 7, P<0.01), and 0.84 (2.5 centile: 0, median:
0, 97.5 centile: 6, P<0.01), respectively.
Discussion
In this population based retrospective cohort study of
76 920 Japanese children, exposure to tobacco smoke
was associated with an approximately twofold
increased risk of caries in deciduous teeth. The risk of
caries was also increased, by 1.5-fold, among infants
exposed to smoking in the household, whereas the
eect of maternal smoking during pregnancy was only
1.1-fold. Dierences in behaviour patterns were appar
-
ent between those exposed to and not exposed to smok-
ing, such as lack of tooth brushing and irregular
consumption of sweets. We confirmed our findings
through sensitivity analysis using information about
behaviour patterns during the ages of 4 months to 3
years, but we cannot completely exclude the possibility
of bias due to residual confounding.
Secondhand smoke was operationally defined in pre
-
vious studies as exposure to smoking by one or both
parents or family members, maternal smoking during
pregnancy, or high serum cotinine levels. We used three
definitions for secondhand smoke—maternal smoking
during pregnancy, smoking in the household when the
infant was aged 4 months, and exposure to tobacco
smoke at age 4 months. Kobe City published guidelines
for prevention of secondhand smoke in 2004 and rec
-
ommended separation of smoking areas at home as
well as in the workplaces. In this study, fewer infants at
age 4 months were exposed to tobacco smoke than
those exposed to smoking in the household, possibly
reflecting the wide spread separation of smoking areas
at home, but the eects on the risk of caries were signif
-
icant even for smoking in the household. These findings
are consistent with past cross sectional studies in which
10 out of 11 studies found significant positive associa
-
tions between secondhand smoke and caries of
deciduous teeth.
10
On the other hand, only a few stud-
ies
22-24
have examined the eects of maternal smoking
during pregnancy. Two studies from the National
Health and Nutrition Examination Survey reported that
the incidence density ratios of maternal smoking
during pregnancy were 1.54 (P=0.02)
22
and 3.85
(P=0.054)
23
among children aged 2 to 5 or 6 years,
whereas the prevalence ratio of caries between 3 year
old Japanese children with and without exposure to
maternal smoking was 1.78 (P<0.05).
24
These results are
opposite to our findings. However, it is notable that in
the National Health and Nutrition Examination Survey
(NHNES) the eects of maternal smoking and house
-
hold smoking may be confounded
22
23
because exposure
to maternal smoking during pregnancy would be cor
-
related with household smoking after childbirth, which
was not handled separately in the NHNES analysis.
Other dierences in design include availability of data
on oral care and dietary habits, which could be import
-
ant confounders,
20
and cross sectional or cohort design.
Taken together, further research is needed for a defini
-
tive conclusion, although our findings suggest that the
eects of maternal smoking during pregnancy are
weaker than those of exposure to secondhand smoke
after childbirth.
The estimated hazard ratios of exposure to tobacco,
around 1.5-fold to twofold higher, are small but may be
important from a public health viewpoint. The three
year risk of caries in this cohort was 18.0%. This esti
-
mate is slightly lower than the averages in the United
States
2
and Japan,
3
and the high utilisation of fluoride
varnish, tooth brushing, and dental examinations may
have contributed to the reduction in risk of caries.
However, more than half of the children in this cohort
had family members who smoked, and most smokers
were their fathers. These results can be considered
representative of children in large cities in Japan,
given the high participation rate in this study. Indeed,
exposure to secondhand smoke is widespread among
children worldwide, at a rate of 40%, which is higher
than any other age categories.
15
The associations
between secondhand smoke and risk of caries would
support extending public health and clinical interven
-
tions to reduce secondhand smoke. For example,
education on the harm of secondhand smoke might

thebmj 
BMJ
2015;351:h5397  doi: 10.1136/bmj.h5397
RESEARCH
7
increase if dentists became aware of the risk of caries
due to secondhand smoke as well as tobacco con
-
sumption of their clients. However, further investiga-
tion is necessary to conclude whether a smoking
prevention programme would reduce the risks of car
-
ies, since the size of eects of secondhand smoke was
not large. Propensity score analysis allowed adjust
-
ment for confounders in this study, but residual bias
due to unmeasured confounders, although potentially
small, cannot be ruled out.
Limitations of this study
These findings must be interpreted in the context of
study limitations. Firstly, information on smoking status
was obtained by questionnaires completed by mothers,
and biomarkers such as serum cotinine levels were not
available in this study. In particular, the prevalence of
maternal smoking during pregnancy may be underre
-
ported. It is also dicult in an epidemiological study to
separate the eects of secondhand smoke from those of
third hand smoke—the residual contamination from
Table  | Propensity score analysis of maternal smoking during pregnancy and incidence of caries
Variables
Not exposed
tosecondhand
smokeduring
pregnancy and at
months (n= )
Exposed to only maternal
smoking during
pregnancy(n=)
Exposed to only
householdsmoking at
months(n= )
Exposed to secondhand
smoke during pregnancy
andat  months (n=)
Hazard ratio
(%CI) P value
Hazard ratio
(%CI) P value
Hazard ratio
(%CI) P value
Incidence of any caries (unadjusted) (%): 2848 (13.5*) 290 (15.1*) 4164 (20.2*) 1516 (23.1*)
Crude Ref 1.14 (1.00 to 1.30) 0.05 1.60 (1.52 to 1.69) < 0.01 1.89 (1.77 to 2.02) < 0.01
Propensity score adjusted† Ref 1.10 (0.97 to 1.25) 0.14 1.52 (1.44 to 1.60) < 0.01 1.71 (1.59 to 1.83) < 0.01
Sensitivity analysis‡ Ref 1.16 (0.93 to 1.43) 0.18 1.75 (1.58 to 1.93) < 0.01 2.05 (1.82 to 2.30) < 0.01
Sensitivity analysis§ Ref 1.10 (0.97 to 1.26) 0.14 1.51 (1.43 to 1.59) <0.01 1.74 (1.62 to 1.87) <0.01
Sensitivity analysis¶ Ref 1.04 (0.87 to 1.25) 0.65 1.30 (1.21 to 1.40) <0.01 1.46 (1.32 to 1.62) < 0.01
Sensitivity analysis** Ref 1.09 (0.97 to 1.23) 0.16 1.46 (1.39 to 1.53) <0.01 1.61 (1.51 to 1.72) < 0.01
Incidence of caries in maxillary anterior
teeth (unadjusted) (%):
1897 (9.1*) 178 (9.3*) 2802 (13.6*) 976 (14.8*)
Crude Ref 1.03 (0.88 to 1.21) 0.67 1.58 (1.49 to 1.68) <0.01 1.75 (1.61 to 1.90) <0.01
Propensity score adjusted† Ref 1.01 (0.86 to 1.18) 0.93 1.51 (1.42 to 1.61) <0.01 1.61 (1.48 to 1.75) <0.01
Sensitivity analysis‡ Ref 1.15 (0.93 to 1.43) 0.19 1.75 (1.59 to 1.93) <0.01 2.05 (1.82 to 2.31) < 0.01
Sensitivity analysis§ Ref 1.10 (0.97 to 1.26) 0.15 1.52 (1.44 to 1.60) <0.01 1.75 (1.62 to 1.88) < 0.01
Sensitivity analysis¶ Ref 1.04 (0.86 to 1.24) 0.70 1.31 (1.21 to 1.41) <0.01 1.46 (1.32 to 1.62) <0.01
Sensitivity analysis** Ref 1.01 (0.86 to 1.17) 0.94 1.48 (1.39 to 1.57) <0.01 1.57 (1.45 to 1.70) <0.01
Incidence of caries in maxillary molars
(unadjusted) (%):
856 (4.1*) 84 (4.4*) 1335 (6.5*) 543 (8.3*)
Crude Ref 1.08 (0.86 to 1.36) 0.51 1.63 (1.49 to 1.78) < 0.01 2.11 (1.89 to 2.36) <0.01
Propensity score adjusted† Ref 1.04 (0.83 to 1.31) 0.71 1.54 (1.41 to 1.69) <0.01 1.91 (1.70 to 2.14) < 0.01
Sensitivity analysis‡ Ref 1.16 (0.93 to 1.43) 0.19 1.75 (1.58 to 1.93) <0.01 2.06 (1.82 to 2.32) <0.01
Sensitivity analysis§ Ref 1.10 (0.96 to 1.25) 0.18 1.52 (1.44 to 1.60) <0.01 1.75(1.63 to 1.88) < 0.01
Sensitivity analysis¶ Ref 1.04 (0.87 to 1.25) 0.68 1.30 (1.21 to 1.40) <0.01 1.46 (1.32 to 1.63) <0.01
Sensitivity analysis** Ref 1.04 (0.83 to 1.31) 0.71 1.53 (1.40 to 1.67) <0.01 1.87 (1.67 to 2.09) <0.01
Incidence of caries in mandibular anterior
teeth (unadjusted) (%):
182 (0.9*) 18 (0.9*) 307 (1.5*) 102 (1.6*)
Crude Ref 1.09 (0.67 to 1.77) 0.74 1.73 (1.44 to 2.08) <0.01 1.81 (1.42 to 2.31) <0.01
Propensity score adjusted† Ref 1.04 (0.64 to 1.68) 0.89 1.60 (1.33 to 1.93) <0.01 1.57 (1.22 to 2.02) <0.01
Sensitivity analysis‡ Ref 1.15 (0.93 to 1.43) 0.20 1.75 (1.59 to 1.93) <0.01 2.07 (1.83 to 2.33) <0.01
Sensitivity analysis§ Ref 1.10 (0.96 to 1.26) 0.16 1.52 (1.44 to 1.60) <0.01 1.76 (1.63 to 1.89) <0.01
Sensitivity analysis¶ Ref 1.04 (0.87 to 1.25) 0.68 1.30 (1.21 to 1.41) <0.01 1.47 (1.33 to 1.64) <0.01
Sensitivity analysis** Ref 1.04 (0.64 to 1.68) 0.89 1.61 (1.33 to 1.94) <0.01 1.58 (1.23 to 2.03) < 0.01
Incidence of caries in mandibular molars
(unadjusted) (%):
1289 (6.2*) 14 4 ( 7. 6*) 2132 (10.5*) 848 (13.1*)
Crude Ref 1.24 (1.04 to 1.49) 0.02 1.77 (1.64 to 1.90) <0.01 2.27 (2.07 to 2.49) < 0.01
Propensity score adjusted† Ref 1.18 (0.99 to 1.41) 0.07 1.62 (1.50 to 1.74) <0.01 1.94 (1.76 to 2.13) <0.01
Sensitivity analysis‡ Ref 1.15 (0.93 to 1.43) 0.19 1.75 (1.58 to 1.93) <0.01 2.06 (1.83 to 2.32) <0.01
Sensitivity analysis§ Ref 1.10 (0.96 to 1.26) 0.16 1.52 (1.44 to 1.60) <0.01 1.75 (1.63 to 1.89) <0.01
Sensitivity analysis¶ Ref 1.04 (0.86 to 1.25) 0.70 1.30 (1.21 to 1.40) <0.01 1.47 (1.32 to 1.63) <0.01
Sensitivity analysis** Ref 1.17 (0.98 to 1.39) 0.08 1.58 (1.48 to 1.70) <0.01 1.86 (1.70 to 2.04) <0.01
*Estimated by Kaplan-Meier method.
†Adjusted for birth year of child, maternal age, alcohol consumption during pregnancy, smoking status during pregnancy, sex, rst birth, multiple birth, pre-eclampsia, anaemia, threatened
abortion, gestational weeks, caesarean section, vacuum extraction, nuchal cord, asphyxia, jaundice and transfusion, convulsion, incubator, oxygen inhalation, weight, height, head and chest
circumference at birth, weight at 4 months, bottle feeding at 4 months, people involved in child care at 4 months, support by family, friends, or neighbours at 4 months, and mother’s mental
status at 4 months.
‡Restricted to rst born singletons.
§Children with a propensity score below rst centile or above 99th centile were excluded.
¶Further adjusted for number of teeth at 9 months, treatment with fluoride varnish at 18 months and 3 years, tooth brushing alone at 18 months and 3 years, tooth brushing by parents at 18
months and 3 years (%), bottle feeding at 4 months and 9 months, baby food at 9 months, age at start of baby food, frequency of sweets at 18 months and 3 years, eating sweets irregularly at 18
months and 3 years, and drinking juice every day at 18 months and 3 years.
**Exponential regression analysis handling time to event data as interval censored.

RESEARCH
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tobacco smoke that remains on a variety of indoor sur-
faces. Secondly, oral conditions were not necessarily
assessed by paediatric dentistry. Thirdly, as we carried
out an observational study rather than a randomised
trial, it is impossible to establish causality. In addition to
the possibility of unmeasured confounders, we cannot
entirely exclude the potential of bias owing to missing
covariates. We calculated the propensity score with the
use of single imputation, but multiple imputation out
-
performs single imputation theoretically. However, we
expect that it would not make much dierence in this
situation. Fourthly, the portion of children exposed to
smoke only during pregnancy was relatively small and
therefore the non-significant results for maternal smok
-
ing may be due to low statistical power to detect a small
eect. Finally, given the substantial variability in the
prevalence of caries, exposure to secondhand smoke,
and lifestyle across countries, our results may not be
generally applicable to populations with dierent envi
-
ronmental and lifestyle factors. For example, fluorida-
tion of water in the community has not been carried out
in Japan since 1972, although fluoride varnish (table 2)
and fluoride toothpaste is common. Furthermore, sugar
intake for each person also varies across countries (for
example, 48 g/day in Japan, 84 g/day in the US, and 107
g/day in Britain in 2011).
25
Conclusion
Exposure to secondhand smoke at 4 months of age, which
is experienced by half of all children of that age in Kobe
City, Japan, is associated with an increased risk of caries
in deciduous teeth. Although these findings cannot estab
-
lish causality, they support extending public health and
clinical interventions to reduce secondhand smoke.
We thank the Child and Family Bureau and Public Health and Welfare
Bureau of Kobe City for providing the health check-up data and advice;
C Wilunda and C Hongyan (Kyoto University) for their advice; and
KFujii (Kyoto University) for secretarial assistance.
Contributors: ShT performed statistical analysis and had full access to
all the data in the study and takes responsibility for the integrity of the
data and the accuracy of the data analysis. MS, HT, and KK contributed
to the design and conduct of the study. SK and SaT contributed to the
writing of the manuscript. KK is the principal investigator and the
guarantor of the study. The sponsor of the study had no role in the
study design, data collection, data analysis, data interpretation, or
writing of the report.
Funding: This study was supported by a grant in aid for scientic
research 26860415.
Competing interests: All authors have completed the ICMJE uniform
disclosure form at www.icmje.org/coi_disclosure.pdf and declare: no
support from any organisation for the submitted work; no nancial
relationships with any organisations that might have an interest in the
submitted work in the previous three years; no other relationships or
activities that could appear to have influenced the submitted work.
Ethical approval: This study was exempt from obtaining individual
informed consent based on the Ethical Guidelines for Epidemiological
Research by Ministry of Health, Labour, and Welfare. The study
protocol was approved by the Ethics Committee, Kyoto University
Graduate School and Faulty of Medicine (E2045). We managed the
data based on the Act of Personal Information Protection in Kobe City
and take responsibility for their integrity.
Data sharing: No additional data available.
Transparency: The lead author (KK) arms that the manuscript is an
honest, accurate, and transparent account of the study being reported;
that no important aspects of the study have been omitted; and that
any discrepancies from the study as planned (and, if relevant,
registered) have been explained.
This is an Open Access article distributed in accordance with the
Creative Commons Attribution Non Commercial (CC BY-NC 4.0)
license, which permits others to distribute, remix, adapt, build upon
this work non-commercially, and license their derivative works on
dierent terms, provided the original work is properly cited and the
use is non-commercial. See: http://creativecommons.org/licenses/
by-nc/4.0/.
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