RESEARCH REPORTS
Clinical ­­­­
S. Thitasomakul1*, S. Piwat1, A.
Thearmontree1, O. Chankanka1, W.
Pithpornchaiyakul1, and S. Madyusoh2
1
Department of Preventive Dentistry, Faculty of Dentistry,
Prince of Songkla University, Hatyai, Songkhla, 90112,
Thailand; and 2Dental Division, Thepa Hospital, Thepa,
Songkhla, Thailand; *corresponding author, songchai.t@psu
ac.th
J Dent Res 88(2):137-141, 2009
abstract
Because of the high incidence of early childhood car-
ies (ECC), a longitudinal study to identify risk factors
from the prenatal period to the child’s first birthday
among 9- to 18-month-old children was conducted
with negative binomial modeling. Overall, 495 chil-
dren had dental examinations at ages 9, 12, and 18
months. Mothers were interviewed during the 2nd
trimester of pregnancy and when the children had
dental examinations. The highest incidence of caries
was found among children who were born to mothers
with ≥ 10 decayed teeth and who never received
calcium supplements during pregnancy, and children
who were not fed supplementary foods at age 3
months, had sweet-tasting foods at 5 months, started
snacking at 5 months, had sugary snacks, had soft
drinks, and did not have their teeth brushed daily at
9 months. Thus, prenatal care and child-rearing-
practices during and after birth are important risk fac-
tors for the incidence and incremental rate of ECC.
KEY WORDS:   early childhood caries, longitudinal
study, negative binomial models, incidence density,
crude caries increment.
DOI: 10.1177/0022034508328629
Received July 12, 2007; Last revision August 11, 2008;
Accepted October 23, 2008
A supplemental appendix to this article is published elec-
tronically only at http://jdr.sagepub.com/supplemental.
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Risks for Early Childhood Caries
Analyzed by Negative Binomial
Models
INTRODUCTION
E
arly childhood caries (ECC) among children in Southeast Asia is reported
to be high (Carino et al., 2003; Vachirarojpisan et al., 2004; Thitasomakul
et al., 2006; van Palenstein Helderman et al., 2006). The risk factors for ECC
in this region have not been well-documented compared with those in
Western countries, where cultures, living styles, and child-rearing practices
are markedly different. Longitudinal design studies that follow the develop-
ment of ECC in children from birth until the age of one year are particularly
lacking. Advantages of the longitudinal study design include multiple obser-
vations of the children and the investigators’ ability to follow the progression
of ECC. The development of and change in child-rearing practices can also
be monitored. Since the causes associated with ECC are multi-factorial, sev-
eral risk factors have been indicated in relation to the prevalence of ECC.
These include oral hygiene procedures, use of fluoride, infant feeding habits,
dietary habits, consumption of sugary foods, and psycho-social factors
(Vanobbergen et al., 2001;Carino et al., 2003; Vachirarojpisan et al., 2004;
van Palenstein Helderman et al., 2006; Weintraub et al., 2006). A limitation
of these studies is their design; cross-sectional and retrospective studies are
prone to recall bias when participants’ mothers/caretakers are interviewed.
The aim of this study was to identify and relate the risk factors from the pre-
natal period until the child’s first birthday to the incidence density of ECC
and the crude caries increment among 9- to 18-month-old children.
MATERIALS & METHODS
Design and Sample
A longitudinal observational community-based study was conducted in the Thepa
district, Thailand, six of the seven subdistricts of which are categorized as rural. The
population numbers 66,990, with 90% living in the rural areas and usually consuming
rice with spicy cooked meat, fish, and vegetables. The fluoride concentration in the
drinking water ranges from 0.1 to 0.2 ppm (Ministry of Public Health, 2000). Dental
care is available only at a district hospital, and is provided by two general dental prac-
titioners and two dental nurses. All 795 women in the district who gave birth between
November, 2000, and October, 2001, constituted the study population. Only 599
infants were given dental examinations at ages 9, 12, and 18 mos; the remaining 196
dropped out because of inconvenience, moving out of the study area, or uncooperative-
ness. Overall, 406 (67.8%) infants completed the 3 follow-up examinations at ages 9,
12, and 18 mos, while 75 (12.5%) and 14 (2.3%) completed the 2 examinations at the
ages of 9 to 12 mos and 12 to 18 mos, respectively. The children who had only one
dental examination were excluded. Therefore, only 495 infants were included in the
present study. This study was approved by the National Ethics Committee, Ministry of
137
138  Thitasomakul et al.  J Dent Res 88(2) 2009
Public Health. All eligible infants’ guardians provided their consent to
join the study.
Clinical Examination
The children were examined in a knee-to-knee position by means of the
WHO probe (#621) under natural light. Using standardized methods,
five dentists categorized the dental status of each examined surface as:
(1) unerupted tooth, (2) normal enamel surface, (3) initial caries or caries
limited to enamel, (4) caries in dentin, and (5) caries involving pulp.
Kappa coefficients for intra- and inter-examiner reproducibility were
0.75-0.91 and 0.68-0.89, respectively (Thitasomakul et al., 2006). Caries
reversal in the follow-up examinations was eliminated by comparison of
current records with previous records after completion of each child’s
examination. Each reversed code was re-examined by two dentists and
given the correct code in both current and previous records. The inci-
dence of ECC was described in 3 terms: The first term was the crude
caries increment from 9 to 12 mos and from 12 to 18 mos. This was the
number of events in which a sound surface converts to a carious surface
(Beck et al., 1997; Broadbent and Thomson, 2005). The second term
was the incidence density of a tooth surface developing caries. This was
defined as the number of new caries-affected surfaces per surface-time
at risk (see Appendix). The third term was the incidence density ratio,
which is the ratio of incidence density among those exposed to the inci-
dence density to those unexposed to the particular independent variable
concerned (Incidence density-exposed /Incidence density-unexposed).
The Questionnaire Interview
A structured questionnaire, with both open- and closed-ended questions,
was used. The first interview was completed with mothers during the
second trimester of pregnancy and gathered data on income, education
level, supplementary calcium use, and milk intake during pregnancy (see
Appendix). Thereafter, the mothers were given a dental examination to
record the number of untreated decayed teeth. Further interviews were
conducted when the children were 3, 9, and 12 mos old. The children’s
birthweight was measured at delivery. An interview when the infant was
3 mos old collected data on type of milk-feeding, infant supplementary
food such as cooked rice and commercial cereal, the child’s age when the
mother started sweetening food, and the age when the child began eating
snacks, vegetables, and fish. These data were re-collected at 9 and 12 mos
of age. Toothbrushing habits were collected at the nine-month visit.
Statistical Analysis
The data were checked for accuracy and entered into a computer equipped
with Epidata® software, Version 3.1, and analyzed with R software ver-
sion 2.1.1. Analyses first resulted in descriptive statistics on characteris-
tics of the children and the mothers. The rates of ECC development were
presented as crude caries increment separated into 2 follow-up periods.
We performed a t test and one-way ANOVA to test the differences in
mean crude caries increment by characteristics of the mothers and the
children. The correlation and association among independent variables
were conducted by correlation coefficient or cross- tabulation, as appro-
priate. Multivariate analysis was begun with the Poisson regression
(McCullagh and Nelder, 1998), to demonstrate how independent varia-
bles could estimate the rate of incidence density. However, the Poisson
regression model did not ideally fit the data, due to over-dispersion of the
incidence density scores. Therefore, the negative binomial model was
applied and gave a better fit to the data (Lawless, 1987; McCullagh and
Nelder, 1998). Negative binomial regression assumes that incidence
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© 2009 International & American Associations for Dental Research
density score has no excessive zeros or missing values. Therefore, only
the children who had 2 consecutive examinations were included in the
analysis—that is, 481 and 420 children ages 9 to 12 mos and 12 to 18
mos, respectively. Seventeen associated independent variables were
entered into the multivariate analysis. For simplicity, the incidence den-
sity was reported in number(s) of surface(s) per 100 surface-months at
risk. We calculated the incidence density ratio to determine the effect size
of each individual variable on incidence density.
RESULTS
Characteristics of the Children
and the Mothers or Primary Caregivers
The final number of children included in the data analysis was
495; 254 (51.3%) were boys, and 241 (48.7%) were girls (see
Appendix).
Risk Factors for the Incidence of New Caries Lesions
The overall mean ± SD dmft for the ages of 9, 12, and 18 mos
were 0.1 ± 0.4, 0.8 ± 1.6, and 2.8 ± 2.7, respectively, whereas the
dmfs were 0.1 ± 0.6, 1.1 ± 2.7, and 5.2 ± 6.1, respectively. The
crude caries increment between 9 and 12 mos was 1.1 ± 2.6,
whereas it was 4.2 ± 5.1 between 12 and 18 mos; boys did not
differ from girls. No strong association or correlation was found
among the independent variables. The crude caries increment
between 9 and 12 mos was associated with low income and with
children whose mothers did not have a daily intake of milk and
did not receive supplementary calcium during pregnancy; addi-
tionally, the crude caries increment was also related to children
who were breast-fed, did not have commercial cereal at 3 mos,
and had soft drinks at 9 mos (p < 0.05, Table 1). The crude caries
increment between 12 and 18 mos was significantly higher
among children whose mothers had only primary school educa-
tion and had poor oral health status. There was also a signifi-
cantly higher crude caries increment among children who were
breast-fed, had sugary snacks, and had local traditional desserts
at 9 mos, and among those who started eating vegetables later
than 6 mos (p < 0.05).
Negative Binomial Analyses for Incidence Density
The baseline incidence of new caries developing during the
period of 9 to 12 mos was 0.4 surfaces/100 surface-months,
which is the exponential of the intercept value (Table 2). The
incidence density was significantly higher during the period of 12
to 18 mos (p < 0.001), with a baseline incidence density of 0.8
surfaces/100 surface-months. The incidence density between 12
and 18 mos was 1.8 times higher than the incidence density
between 9 and 12 mos. The incidence density was significantly
higher among children whose mothers had poor oral health status,
had 10 or more decayed teeth, and had never received supplemen-
tary calcium during pregnancy. The incidence density was also
significantly higher among children who were not fed cooked rice
or commercial cereal by the age of 3 mos, and among children
whose mothers sweetened their food and allowed them to have
sugary food by the age of 5 mos. Children who consumed sugary
J Dent Res 88(2) 2009 Risk for ECC by Negative Binomial   139

Table 1.    Bivariate Analyses Showing Mean ± SD of Crude Caries Increment by Characteristics of the Mother or
Caregiver, Child-rearing Practices, and Dietary Habits of the Child from 9 to 12 and from 12 to 18 mos

Crude Caries Increment Crude Caries Increment

9 to 12 mos 12 to 18 mos
(number of surfaces) (number of surfaces)

N Mean ± SD N Mean ± SD

Overall 481 1.1 ± 2.6 420 4.2 ± 5.1

  1. Educational level Primary school 306 1.1 ± 2.4 270 4.9 ± 5.2
Secondary school/higher 163 0.9 ± 2.8 146 3.0 ± 4.6*
  2. Annual Income ≤ 101,000 Baht 331 1.2 ± 2.7 289 4.4 ± 5.1
>101,000 Baht 138 0.6 ± 1.9 127 3.8 ± 5.1
  3. Mother’s decayed teeth ≤ 3 teeth 140 1.1 ± 2.5 132 3.8 ± 5.0*
4-9 teeth 228 1.1 ± 2.7 197   4.3 ± 4.7*
≥ 10 teeth 54 1.2 ± 2.6 40 6.9 ± 6.9*
  4. Calcium supplement during pregnancy No 344 1.2 ± 2.7 308 4.4 ± 5.1
Yes 96 0.5 ± 1.7* 78 4.2 ± 5.4
  5. Drinking milk during pregnancy No/Irregularly 269 1.4 ± 2.9 187 4.6 ± 5.4
Yes/Daily 94 0.7 ± 1.9* 86 3.7 ± 4.7
  6. Infant’s birthweight ≤ 2500 g 47 0.7 ± 1.9 42 3.5 ± 4.1
> 2500 g 414 1.1 ± 2.6 368 4.3 ± 5.2
  7. Type of milk feeding Breast-feeding 221 1.5 ± 3.1* 188 5.1 ± 5.1*
Bottle-feeding 20 0.6 ± 1.8 17 4.3 ± 7.3
Mixed breast- and bottle-feeding 227 0.7 ± 1.8* 198 3.5 ± 4.8*
  8. Having commercial cereal at 3 mos No 215 1.3 ± 2.9 187 4.6 ± 5.4
Yes 246 0.8 ± 2.1* 222 3.9 ± 4.9
  9. Having rice at 3 mos No 122 1.3 ± 3.0 105 3.8 ± 5.3
Yes 295 1.1 ± 2.4 250 4.8 ± 5.1
10. Mother started sweetening food at ≤ 5 mos 207 1.2 ± 2.8 181 4.6 ± 5.5
≥ 6 mos 256 0.9 ± 2.2 230 3.9 ± 4.7
11. Child start having snacks at ≤ 5 mos 231 1.1 ± 2.4 206 4.6 ± 5.5
≥ 6 mos 232 1.0 ± 2.7 205 3.9 ± 4.6
12. Child started having vegetables at ≥ 6 mos 257 1.1 ± 2.3 224 4.7 ± 5.6
≤ 5 mos 206 1.0 ± 2.8 187 3.6 ± 4.4*
13. Child started having fish at ≥ 8 mos 176 1.1 ± 2.4 151 4.6 ± 5.1
≤ 7 mos 288 1.0 ± 2.6 260 4.0 ± 5.1
14. Child started having sugary snacks at 9 mos No 161 0.8 ± 2.2 143 3.5 ± 4.5
Yes 305 1.2 ± 2.8 258 4.7 ± 5.4*
15. Child started having local traditional dessert at 9 mos No 103 1.0 ± 2.1 88 5.4 ± 4.7
Yes 363 1.1 ± 2.7 313 3.9 ± 5.2*
16. Child started having soft drinks at 9 mos No 323 0.9 ± 2.1 281 4.0 ± 5.1
Yes 143 1.5 ± 3.4* 120 4.7 ± 5.1
17. Mother brushed the child’s teeth at 9 mos No 175 1.0 ± 2.4 145 4.0 ± 5.3
Yes 290 1.1 ± 2.6 256 4.4 ± 5.0

*  p < 0.05.

snacks, drank soft drinks, and did not have their teeth brushed at
9 mos also had significantly higher new caries development dur-
ing the 2 follow-up periods.
The large incidence density ratio or large coefficients could
be observed among children whose mothers started them on
sweetened foods at ≤ = 5 mos (Table 2), with an incidence den-
sity of exp(-5.4 + 0.5) = 0.7 surfaces/100 surface-months, and
an incidence density ratio of 0.7/0.4 =1.6, and among children
whose teeth had not been brushed, whose incidence density was
exp(-5.4 + 0.5 + 0.4) = 1.1 surfaces/100 surface-months, and for
whom the incidence density ratio is 1.1/0.4 = 2.5. Apart from
these, a higher incidence density could be observed in children
whose mothers had poor oral health status and among children
who did not eat commercial cereal at 3 mos.
DISCUSSION
The incidence and increment of ECC among 9- to 18-month-old
children in the present study were substantially high. Few longitu-
dinal studies have been conducted in a population of such a young
age. This study clearly indicates that the risk of getting ECC starts
at the very young stage and is increased by poor pregnancy care as
well as the mother’s own poor oral hygiene; the child-rearing prac-
tices used in the first year of life also influence the risk of ECC.

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140  Thitasomakul et al.  J Dent Res 88(2) 2009

Table 2.   Coefficients from Negative Binomial Regression with 95% Confidence Intervals in Parentheses, Incidence Density of New
Caries-affected Surfaces per 100 Surface-months, and Incidence Density Ratio of Being Exposed vs. Unexposed, 9 to 18 mos

Negative Binomial Incidence Density/ Incidence

Coefficient (95%CI) 100 Surface-months Density Ratio Significance

Intercept -5.4 (-6.0, -4.8) 0.4

Follow-up period, 12 to 18 mos 0.6 (0.4, 0.8) 0.8 1.8 p ≤ 0.001
Primary school education 0.1 (-0.1, 0.3) 0.5 1.1
Income < 101,000 Baht 0.1 (-0.1, 0.3) 0.5 1.1
Mother’s decayed teeth = 4-9 teeth 0.1 (-0.1, 0.3) 0.5 1.1
Mother’s decayed teeth ≥ 10 0.4 (0.1, 0.7) 0.6 1.5 p ≤ 0.05
No calcium supplement during pregnancy 0.3 (0.0, 0.5) 0.6 1.3 p ≤ 0.05
No daily milk-drinking during pregnancy 0.1 (-0.2, 0.3) 0.5 1.1
Child’s birthweight ≤ 2500 grams -0.1 (-0.4, 0.3) 0.4 1.0
Exclusively bottle-feeding -0.1 (-0.7, 0.5) 0.4 0.9
Mixed breast- and bottle-feeding -0.6 (-0.8, -0.4) 0.2 0.5 p ≤ 0.001
No rice at 3 mos 0.3 (0.1, 0.5) 0.6 1.3 p ≤ 0.05
No commercial cereal at 3 mos 0.5 (0.3, 0.7) 0.7 1.7 p ≤ 0.001
Mother start sweetening food at ≤ 5 mos 0.5 (0.3, 0.7) 0.7 1.6 p ≤ 0.001
Child started snacking at ≤ 5 mos 0.3 (0.1, 0.5) 0.6 1.4 p ≤ 0.01
Child started having vegetables at ≤ 5 mos -0.2 (-0.4, 0.0) 0.4 0.8
Child started having fish at ≤ 7 mos 0.0 (-0.2, 0.2) 0.4 1.0
Child started having sugary snacks at 9 mos 0.2 (0.0, 0.4) 0.6 1.2 p ≤ 0.05
Child started having local traditional dessert at 9 mos 0.1 (-0.2, 0.3) 0.5 1.1
Child started having soft drinks at 9 mos 0.3 (0.1, 0.5) 0.6 1.3 p ≤ 0.01
No daily toothbrushing at 9 mos 0.4 (0.2, 0.6) 0.7 1.5 p ≤ 0.001

The poor oral health status among mothers reflects their oral
health care practices, which have a significant influence on the
oral health status of their children. Better oral health concern
among mothers leads them to promote better oral health for
their children. Further, the high prevalence of untreated caries
among mothers could also promote the harboring of cariogenic
bacteria, which can be later transmitted to the children (Li et al.,
2005). The crude caries increment from 9 to 12 mos of age is
reduced by more than half among children whose mothers ever
received calcium supplements. Deciduous incisors and canines
are developed and calcified at the age of 4 to 6 wks in utero.
Therefore, higher calcium intakes may have resulted in a more
acid-resistant tooth enamel (Pinkham et al., 2005).
Most Thai and Southeast Asian mothers practice breast-feeding
on demand. This results in a high frequency of breast-feeding in
this region, with an average feeding frequency of 5 in the daytime
and 4 during the night. The main reason for a high frequency of
breast-feeding is to delay fertility of the mother (Israngkura et al.,
1989; Kennedy, 1990; Amatayakul et al., 1991; van Palenstein
Helderman et al., 2006). A large number of breast-feedings, both
during the day and at night, leads to the accumulation of milk on
the child’s tooth surface, especially on the upper incisors, where the
salivary flow rate is usually low. This could explain why children
who were exclusively breast-fed had higher levels of caries.
Another reason is that children usually can drink higher volumes of
milk from the bottle than from the breast (Bowen and Pearson,
1993; Petti et al., 2000; Hallett and O’Rourke, 2002; Vachirarojpisan
et al., 2004; van Palenstein Helderman et al., 2006).
We did not expect to see such a heavy and early consumption
of sugary foods under the age of 1 yr, and it has not been previ-
ously reported. Urbanization, development of the food industry,
and and food advertisements induce mothers or caregivers to feed
children snacks early and more frequently. Easy access to con-
venience stores and an increase in small grocery shops in the
villages have also promoted sugary food consumption among
small children. Having commercial sugary snacks and soft drinks
at the age of 1 yr has significantly increased the incidence of car-
ies. Conversely, the eating of freshly prepared household desserts
does not increase caries increments, since most of the household
desserts contain less sugar, and the textures are usually more solid
and non-sticky compared with commercial snacks. Thus, the
cariogeni­city of household desserts is relatively low.
The negative binomial regression confirmed the results of
the bivariate analyses. The rate of caries increment (incidence
density) in the second follow-up period was significantly higher,
simply because children had a higher frequency of exposure
for each risk factor. The factors with the largest impact on the
increment of incidence density were: mother starting to give
sweetened foods to the child at the age of 5 mos, no cereal con-
sumption at 3 mos, and no daily toothbrushing at 9 mos. The
most common reason for the mothers sweetening their infant’s
food was to stimulate the children to eat more food. It was also
found that children who were fed rice and cereals in addition to
milk by the age of 3 mos had a lower caries incidence. This
could be because rice and cereals are more difficult to digest
when compared with milk, and thus it takes more time for the
child to become hungry again. Therefore, this could reduce the
frequency of food intake and acid exposure.
The recommendation of using toothpaste at this age does not
exist in the national oral health care program, but dental plaque
removal by daily brushing is important. This study supports the
results of previous studies indicating that starting to brush chil-
dren’s teeth early could reduce the prevalence of caries (Carino
et al., 2003; Jose and King, 2003; Peretz and Gluck, 2006).

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J Dent Res 88(2) 2009 Risk for ECC by Negative Binomial   141
In conclusion, the substantially high incidence and high incre-
ment of ECC from the ages of 9 to 18 mos are related to the quality
of prenatal care, from the fetal stage to the first year of age. The
negative binomial regression used in this longitudinal study pro-
duced a multidimensional risk indicator model for ECC. During
pregnancy, factors considered important are mother’s milk intake
and calcium supplementation. After birth, the major factors are
child-rearing practices, denoted as the type of infant milk feeding,
the type of infant supplementary food, the age of sweetening the
infant’s food, the frequency of snacks, and the control of oral
hygiene.
ACKNOWLEDGMENTS
This study was supported by Prince of Songkla University, the
Thailand Research Fund (MRG4780013), the Thai Health
Promotion Foundation (48-00-0286), and RDH-PSU. We
acknowledge Prof. G. Dahlén, Asst. Prof. N. Jansakul, and
Dr. A. Geater for their academic advice. The cooperation of the
children and parents is also appreciated.
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