Article

Social inequalities in childhood dental caries: The convergent roles of stress, bacteria and disadvantage

University of British Columbia, Vancouver, BC, Canada.
Social Science [?] Medicine (Impact Factor: 2.89). 11/2010; 71(9):1644-52. DOI: 10.1016/j.socscimed.2010.07.045
Source: PubMed
ABSTRACT
The studies reported here examines stress-related psychobiological processes that might account for the high, disproportionate rates of dental caries, the most common chronic disease of childhood, among children growing up in low socioeconomic status (SES) families. In two 2004-2006 studies of kindergarten children from varying socioeconomic backgrounds in the San Francisco Bay Area of California (Ns = 94 and 38), we performed detailed dental examinations to count decayed, missing or filled dental surfaces and microtomography to assess the thickness and density of microanatomic dental compartments in exfoliated, deciduous teeth (i.e., the shed, primary dentition). Cross-sectional, multivariate associations were examined between these measures and SES-related risk factors, including household education, financial stressors, basal and reactive salivary cortisol secretion, and the number of oral cariogenic bacteria. We hypothesized that family stressors and stress-related changes in oral biology might explain, fully or in part, the known socioeconomic disparities in dental health. We found that nearly half of the five-year-old children studied had dental caries. Low SES, higher basal salivary cortisol secretion, and larger numbers of cariogenic bacteria were each significantly and independently associated with caries, and higher salivary cortisol reactivity was associated with thinner, softer enamel surfaces in exfoliated teeth. The highest rates of dental pathology were found among children with the combination of elevated salivary cortisol expression and high counts of cariogenic bacteria. The socioeconomic partitioning of childhood dental caries may thus involve social and psychobiological pathways through which lower SES is associated with higher numbers of cariogenic bacteria and higher levels of stress-associated salivary cortisol. This convergence of psychosocial, infectious and stress-related biological processes appears to be implicated in the production of greater cariogenic bacterial growth and in the conferral of an increased physical vulnerability of the developing dentition.

Full-text

Available from: Ling Zhan, Jun 19, 2014
Social inequalities in childhood dental caries: The convergent roles of stress,
bacteria and disadvantage
W. Thomas Boyce
a
,
*
, Pamela K. Den Besten
b
, Juliet Stamperdahl
c
, Ling Zhan
b
, Yebin Jiang
d
,
Nancy E. Adler
b
, John D. Featherstone
b
a
University of British Columbia, Vancouver, BC, Canada
b
University of California, San Francisco, USA
c
University of California, Berkeley, USA
d
University of Michigan, USA
article info
Article history:
Available online 15 September 2010
Keywords:
Dental caries
Socioeconomic status
Stress
Vulnerability
USA
Children
Psychobiological
abstract
The studies reported here examines stress-related psychobiological processes that might account for the
high, disproportionate rates of dental caries, the most common chronic disease of childhood, among
children growing up in low socioeconomic status (SES) families. In two 2004e2006 studies of kinder-
garten children from varying socioeconomic backgrounds in the San Francisco Bay Area of California
(Ns ¼ 94 and 38), we performed detailed dental examinations to count decayed, missing or lled dental
surfaces and microtomography to assess the thickness and density of microanatomic dental compart-
ments in exfoliated, deciduous teeth (i.e., the shed, primary dentition). Cross-sectional, multivariate
associations were examined between these measures and SES-related risk factors, including household
education, nancial stressors, basal and reactive salivary cortisol secretion, and the number of oral
cariogenic bacteria. We hypothesized that family stressors and stress-related changes in oral biology
might explain, fully or in part, the known soci oeconomic disparities in dental health. We found that
nearly half of the ve-year-old children studied had dental caries. Low SES, higher basal salivary cortisol
secretion, and larger numbers of cariogenic bacteria were each signicantly and independently associ-
ated with caries, and higher salivary corti sol reactivity was associated with thinner, softer enamel
surfaces in exfoliated teeth. The highest rates of dental pathology were found among children with the
combination of elevated salivary cortisol expression and high counts of cariogenic bacteria. The socio-
economic partitioning of childhood dental caries may thus involve social and psychobiological pathways
through which lower SES is associated with higher numbers of cariogenic bacteria and higher levels of
stress-associated salivary cortisol. This convergence of psychosocial, infectious and stress-related bio-
logical processes appears to be implicated in the production of greater cariogenic bacterial growth and in
the conferral of an increased physical vulnerability of the developing dentition.
Ó 2010 Elsevier Ltd. All rights reserved.
Introduction
Dental caries is a preventable infectious disease in which
bacterial fermentation of dietary carbohydrates in plaque produces
organic acids that erode the mineralized tissue of teeth (Selwitz,
Ismail, & Pitts, 20 07). Caries constitutes the single most common
chronic disease of childhood, affecting as many as 40e50% of
U.S. and British children (Pitts, Boyles, Nugent, Thomas, & Pine,
20 04, 2007) and 60e90% of children worldwide between the ages
of 2 and 11 years (Centers for Disease Control and Prevention, 2006;
Donahue, Waddell, Plough, Del Aguila, & Garland, 20 05; Edelstein,
2006). The disease accrues an annual U.S. treatment cost of at least
$4.5 billion (Aligne, Moss, Auinger, & Weitzman, 2003) and, if fully
treated within the developing world, would cost between US
$1600e3500 per 10 00 children, a gure easily exceeding the total
available public health budgets in resource-poor countries (Yee &
Sheiham, 2002). Childhood caries has been linked to slowed
somatic growth (Nicolau, Marcenes, Allison, & Sheiham, 2005) and
a diminished quality of life (World Health Organization, 2003), to
a variety of acute and chronic medical conditions (Loesche, 2007),
and, through inammatory mediators, to the development of
cardiovascular disease, the leading cause of adult mortality (Ford,
Yamazaki, & Seymour, 2007; Joshipura et al., 2006). Such
evidence for longer term developmental, psychological and
medical sequelae of childhood caries is also consistent with
*
Corresponding author.
E-mail address: tom.boyce@ubc.ca (W.T. Boyce).
Contents lists available at ScienceDirect
Social Science & Medicine
journal homepage: www.elsevier.com/locate/socscimed
0277-9536/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.socscimed.2010.07.045
Social Science & Medicine 71 (2010) 1644e1652
Page 1
emerging ndings that chronic adult diseases are often traceable to
the conditions and exposures of early life (Barker, 1990; Kuh & Ben-
Shlomo, 2004; Shonkoff, Boyce, & McEwen, 2009 ).
Socioeconomic and racial disparities occur in the incidence and
severity of childhood dental caries in virtually every country of the
world (Centers for Disease Control and Prevention, 2006; Edelstein,
2006; Hobdell et al., 2003). The disproportionate rates of caries
found among poor and minority children affect both concurrent and
future oral health, with trajectories of early caries tracking into adult
life (Broadbent, Thomson, & Poulton, 2008). Nearly twice the
proportion of U.S. children with family incomes less than the federal
poverty level (FPL) show decay of the primary or permanent denti-
tion (55%), compared to those whose family incomes are greater than
200% of the FPL (31%). Approximately one quarter of U.S. children
sustain 80% of the tooth decay found within the childhood population
at large (Kaste et al.,1996). Identifying factors that contribute to social
and racial disparities in childhood dental caries could thus affect
global health care costs, aid in addressing more general societal
inequalities in health and disease, and shed new light on the etiolo-
gies of chronic psychological and biomedical disorders in adult life.
A recently issued report by the WHO Commission on the Social
Determinants of Health marshals evidence for worldwide socio-
economic and racial disparities in physical and mental disease and
calls for the closure of societal gaps in health, especially child health,
within a generations time (Commission on Social Determinants of
Health, 2008; Irwin, Siddiqi, & Hertzman, 2007). With recognition
of the global pandemic of childhood dental caries (e.g., Edelstein,
20 06; Petersen, 2005), causal mechanisms by which socioeco-
nomic status (SES) is linked to dental health have been the focus of
new interest and study. Earlier acquisition of oral cariogenic bacteria
(Angulo, Pivel, Zinemanas, Jorysz, & Krasse, 1994), greater intake of
dietary carbohydrates (Touger-Decker & van Loveren, 2003), expo-
sures to environmental toxins, such as lead (Moss, Lanphear, &
Auinger, 1999) and tobacco smoke (Aligne et al., 20 03), differences
in enamel calcication (Seow, 1998), lack of uoridated water
(Centers for Disease Control and Prevention, 2002), and inaccessi-
bility of dental health care (Seale & Casamassimo, 2003) have all
been explored as possible sources of the excessive caries incidence
found among low income children.
Despite such evidence for multiple causal pathways in the social
partitioning of childhood caries, a widespread assumption is that
low SES and minority group parents, preoccupied with the
exigencies of disadvantaged lives, are less attentive to the dental
hygiene of their children (see, for example, Skeie, Riordan, Klock, &
Espelid, 2006) and that disparities in dental health are principally
attributable to parental neglect of hygienic practices. There is
limited evidence, however, that parental inattention to dental
hygiene plays a causal role in oral health inequalities (Milgrom
et al., 2000). Further, stressors and adversitiesdfactors that could
also contribute to dental health through activation of stress-
responsive, immune-regulatory neuroendocrine systemsdare also
disproportionately present in the lives of low income families
(Evans, Gonnella, Marcynyszyn, Gentile, & Salpekar, 20 05; Lupien,
King, Meaney, & McEwen, 2000). While there is agreement that
social, economic and environmental factors are key determinants of
dental disease, there has been little study of the psychosocial and
biological pathways through which socially partitioned adversities
might undermine oral health during the childhood years (
Newton
&B
ower,2005). The studies reported here, in two samples of
ve-year-old, kindergarten children, examined the possible
convergence of psychosocial, infectious and stress-associated bio-
logical processesdi.e., family nancial stressors, the number of oral
cariogenic bacteria, hypothalamic-pituitary-adrenocortical (HPA)
axis activation, and the physical vulnerability of deciduous
teethdthat could act as mechanisms linking SES and dental caries.
The Committee for the Protection of Human Subjects at the Uni-
versity of California, Berkeley and the Committee on Human
Research at the University of California, San Francisco reviewed and
approved the recruitment plan and measurement procedures for
both studies reported here.
Study 1: cariogenic bacteria, salivary cortisol and dental caries
in kindergarten children
Sample and methods
Kindergarten children participating in a longitudinal study of
social status, biological responses to adversity, and child health and
development (the Peers and Wellness Study (PAWS); N ¼ 338, in
three successive cohorts (2003e2005), approximately equal in size)
were enrolled in a dental health sub-study. The sub-sample,
recruited during the 2004e20 05 school year from the 98 children
in the second cohort, comprised 94 children (96%) who ranged in
age from 5.2 to 6.5 years (37 girls, 57 boys; 40 white, 48 non-white,
6 mixed), attended seven classrooms in three East San Francisco
Bay Area, California public schools, and were not absent from
school on the day that Study 1 procedures took place (see sub-study
ow chart, Fig. 1). The sub-sample did not differ from the larger,
longitudinal study sample on socioeconomic status (F ¼ 0.37,
p ¼ NS). Fifty-three children (56%) attended a morning class from
8:30 AMe12:00 noon, and 41 (44%) attended an afternoon class
from 12:00 noon e 3:30 PM. Because measurement of salivary
cortisol was a component of the study protocol, children taking
medications such as human growth hormone and exogenous
glucocorticoids were excluded from the sample.
Socioeconomic status (SES)
SES was indexed using parent-reported highest household
education level (1 ¼ some grade school; 2 ¼ completed grade
school; 3 ¼ some high school; 4 ¼ completed high school; 5 ¼ some
college or 2-year degree; 6 ¼ 4-year college graduate; 7 ¼ some
graduate or professional school; 8 ¼ graduate or professional
degree).
Family nancial stressors
Financial stress was assessed with four parent-report items
derived from Essex, Klein, Cho, and Kalin (2002) that measured, on
a1e5 scale, parents concerns about money problems, difculty
paying bills, lack of discretionary income, and limited opportunities
due to
nancial
constraints (
a
¼ .81).
Basal salivary cortisol secretion
For both morning and af ternoon students, saliva for cortisol
assays was collected in school two times p er day, in the rst and
Fig. 1. Flow diagram of study participationdStudies 1 and 2 (Ns ¼ 94 and 38).
W.T. Boyce et al. / Social Science & Medicine 71 (2010) 1644e1652 1645
Page 2
last 20 min of class, at the same time on each of three consecutive
school days. Children had not ingeste d solids or liquids in the
30 min prior to saliva collections. Salivary cortisol levels closely
correspond to plasma free cortisol and are reliable across
sampling days (Kirschbaum & Hellhammer, 1994). Samples
were collected using cotton rolls that children chewed for 20e30 s
and then deposited into salivette tubes (Sarsted t, Nümbrecht,
Germany) that were frozen a t 7
C until shi pped to the Univer-
sity of Dresden. After thawing, sample s were mixed and centri-
fuged 10 min at 2000e300 0 g to remove pa rticulate material.
Cortisol was assayed us ing a commerc ial immunoassay with
chemiluminescence detection (Cortisol Luminescence Immuno-
ass ay; IBL-Hambur g, Hamburg, Germany) for which the dete ction
limit was 0.41 nmol/L. The mean interassay and intra-assay vari-
ati ons were 8.5% and 6.1%, respectively. To normalize cortisol
distributions, raw values were log
10
-transformed. The mean
cortiso l values and collection times were computed across the six
collections, and the area under the curve with respect to ground
was cal cula ted using the method described by Pruessner,
Kirschbaum, Meinlschmid, and Hellhammer (2003).Finally,the
area under the curve was adjusted for class time to control for the
circadian patterning of cortisol secretion. The resulting variable
indexed childrens mean basal level of HPA activation dur ing c lass
time, averaged over three school days.
Salivary cortisol reactivity
During a week different from that in which basal cortisol
samples were collected, childrens HPA reactivity to standardized
challenges was assessed in a quiet, secluded room in the childs
school, using a previously described stress reactivity protocol for
middle childhood (Alkon et al., 2003). Children completed four
standardized social, cognitive, sensory and emotional challenges,
and at the beginning and end of the reactivity protocol, saliva was
collected for cortisol assays, using the same methods described
above for basal cortisol secretion. Standardized residual reactivity
scores were computed by regressing post-protocol cortisol values
on pre-protocol, baseline values.
Cariogenic bacteria
Oral cariogenic bacteria were sampled using a cotton-tipped
applicator swabbed over the buccal mucosa, gingival margin,
tongue and tooth surfaces. The tip was then placed in a sterile tube
containing 2 mL of phosphate buffered saline (PBS). Samples were
stored on ice, transferred to the laboratory, and within 24 h of
collection were processed for microbiological assays. Bacteria were
suspended in the PBS by vortexing for 1 min, followed by serial
dilutions of 1:10, 1:100 and 1:10 00 with PBS. The diluted samples
were plated (0.1 mL per plate) on Mitis Salivarius Sucrose Bacitracin
agar for mutans streptococci (MS) and on Tomato Juice-Rogosa agar
for lactobacillus species (LB). Plates were incubated anaerobically in
85% N
2
, 10% H
2
, & 5% CO
2
at 37
C for 72 h. The lower limit of
detection for MS and LB is 10 CFU/mL (logMS ¼ 1.0). Bacteria were
counted on plates appropriately diluted to show dened colonies.
The sum of log
10
-transformed counts of MS and LB was computed
as the number of oral cariogenic bacteria.
Dental Caries
A pediatric dentist, blind to other study data, completed
detailed, school-based dental examinations, in well-lighted condi-
tions, with the child in a supine position. Visual and tactile exam-
ination using a dental mirror and explorer produced counts of
decayed, missing and lled dental surfaces of the primary (dmfs)
and secondary teeth (DMFS), identied according to WHO criteria
(Petersen, Bourgeois, Bratthall, & Ogawa, 2005). Although assessing
the reliability of caries detection was not feasible within the context
of the current study, other work indicates that the presence of
caries is detected and rated with a between-observers reliability of
0.60e0.80 (see e.g., Ismail et al., 2007). For the purposes of this
report,
P
DMFS is used to refer to the sum of dmfs and DMFS
counts.
Statistics
Four of the ve independent variables (SES, Family Financial
Stressors, Basal Salivary Cortisol, Salivary Cortisol Reactivity, and
Cariogenic Bacteria) had missing values, ranging in proportion from
1 to 12%, which were imputed using linear regression within the
Stata/MP 11 single imputation procedure (StataCorp). Distributions
of independent and dependent (Dental Caries) measures were
examined, and Pearson correlation coefcients were computed to
assess univariate associations. Predictor and outcome distributions
violated the normality assumptions of ordinary least-squares (OLS)
regression, and, though the outcome was a count variable with
non-negative, integer values, its distribution also violated
assumptions of regular Poisson regression, due to the over-
dispersion of its values and the failure of its mean to approximate
the variance. Due to such overdispersion and the large number of
zeroes contained in the outcome distribution, zero-inated Poisson
(ZIP) regression (StataCorp) was used to estimate the direct and
interactive associations of predictor variables with
P
DMFS
(Gardner, Mulvey, & Shaw, 1995), with each predictor centered at its
mean. The Vuong statistic was used to conrm that the t of the ZIP
regression model signicantly exceeded that of the Poisson model.
ZIP regression accurately models the multivariate predictors of
a dependent measure with a high rate of zero values by appor-
tioning outcome variance to two component distributions: a Pois-
son model that computes its count dimension; and a logistic model
that computes the zero, not zero aspect of the outcome (Atkins &
Gallop, 2007). Where a signicant interaction was found, the
moderator effect was probed using scatter plots of
P
DMFS by one
interaction component variable (e.g., Cariogenic Bacteria), with
data points divided at the 75th percentile into low and high sub-
samples on the second component variable (e.g., the bottom 75%
and top 25% on Basal Salivary Cortisol Secretion).
Results
In this relatively well-educated East Bay Area sample, the mean
of the highest household education level approached some grad-
uate or professional school, with a range of some grade school to
graduate or professional degree (mean
¼ 6.7
, SD ¼ 1.4, range 1e8).
Four percent of parents had only a high school education or less,
17% had some college or a two-year degree, 22% were college
graduates, and 57% had at least some professional or graduate
education beyond college. Despite relatively high education levels
on average, nearly 16% of study households had incomes less the
federal poverty level for a family of four. Family Financial Stressors
were rated an average of 2.4 on the 1e5 point scale (5 corre-
sponding to the highest level of stress), with mean scores ranging
from 1 to 5. The mean raw, pre- and post-school salivary cortisol
levels were 7.9 nmol/L (SD ¼ 4.4; range ¼ 2.4e25) and 4.7 nmol/L
(SD ¼ 4.8; range ¼ 1.0e40.1), respectively. The mean pre- and post-
stress reactivity protocol cortisol levels were 5.0 nmol/L (SD ¼ 4.6;
range ¼ 1.2e36.0) and 4.3 nmol/L (SD ¼ 3.3; range ¼ 1.1e26.8).
Approximately one third of children (34%) showed an increase in
salivary cortisol over the course of the reactivity protocol. Oral MS
counts averaged 50,964 CFU/mL and ranged from none to
2,50 0,000 CFU/mL. Oral LB averaged 7372 CFU/mL, with a range of
none to 70,000 CFU/mL. No oral Cariogenic Bacteria of either
species were found in a subset of 42 children (45%). As shown in
Fig. 1, the 94 study children had a positively skewed distribution of
W.T. Boyce et al. / Social Science & Medicine 71 (2010) 1644e16521646
Page 3
P
DMFS, with a mean of 4.3 surfaces with lesions (SD ¼ 7.7;
range ¼ 0e38). Forty-four children (47%) had at least one caries
lesion, while 50 (53%) had none. All reported analyses were also run
using a count of decayed, missing and lled teeth (i.e., SDMFT),
rather than dental surfaces. Resulting associations were compa-
rable in direction and magnitude, but the stronger predictions were
derived from the SDMFS analyses. Only the latter results are thus
presented here.
Table 1 displays Pearson correlation coefcients among inde-
pendent and dependent variables. SES was signicantly and
inversely associated with Family Financial Stressors, Basal Salivary
Cortisol Secretion, Cariogenic Bacteria, and Dental Caries. Basal
Salivary Cortisol Secretion was positively associated with Family
Financial Stressors and Dental Caries, and Cariogenic Bacteria was
strongly linked to Dental Caries. Because Salivary Cortisol Reactivity
was unrelated to Dental Caries in the Study 1 sub-sample, this
variable was omitted from further analysis.
SES, Family Financial Stressors, Basal Salivary Cortisol Secretion,
and Cariogenic Bacteria were sequentially entered as predictors of
P
DMFS counts in the Poisson component of the computed ZIP
regression models (Table 2). Basal Salivary Cortisol and Cariogenic
Bacteria were the strongest bivariate predictors of Dental Caries,
and from a theoretical perspective, salivary cortisol could plausibly
suppress mucosal immunity against cariogenic bacteria. In light of
these considerations, an interaction term for these two predictor
variables was entered as a nal step in the computed Poisson
model. In addition, because those children with no oral pathogens
accounted substantially for the large numbers of zeroes among
P
DMFS scores, Cariogenic Bacteria counts were used to predict the
presence or absence of
P
DMFS in the models logistic component.
In the step at which each variable entered the model, SES, Basal
Salivary Cortisol Secretion and Cariogenic Bacteria bore strong,
independent associations with counts of Dental Caries. The coef-
cient for SES was 0.16, corresponding to an exponentiated odds
ratio of 0.85 or a 15% decrease in the number of caries for every one
unit increase in SES. Similarly, the coefcients for Basal Salivary
Cortisol Secretion and Cariogenic Bacteria were 0.19 and 0.12, cor-
responding to odds ratios of 1.21 and 1.13 or 21% and 13% increases
in caries for each one log
10
unit increase in cortisol secretion and
counts of oral bacteria. Further, the coefcient for SES diminished
by half when Cariogenic Bacteria was added to Model 4, indicating
that the SES - Dental Caries association was partially mediated by
the number of Cariogenic Bacteria.
The interaction of Basal Salivary Cortisol Cariogenic Bacteria
was also a signicant predictor of
P
DMFS scores. This interaction
was inspected using a scatterplot of the two component variables
predicting
P
DMFS (Fig. 2). The highest number of Dental Caries
was identied among children with the combination of high Basal
Salivary Cortisol Secretion and high Cariogenic Bacteria counts,
and the coefcient for the interaction was 0.23, corresponding to
an odds ratio of 1.26. The ZIP logistic regression component
revealed, at each model level, signicant effects of Cariogenic
Bacteria on the presence or absence of Dental Caries. To examine
the possibility that the prior exfoliation of primary teeth could
have biased
P
DMFS scores and confounded the identied asso-
ciations, regression analyses were repeated using counts of only
decayed or lled (but not missing) dental surfaces (DFS) as the
dependent variable; coefcients for both the Poisson and logistic
portions of these models were virtually unchanged from those
derived for
P
DMFS scores. In addition, the Vuong statistic for the
nal model was signicant, indicating that the zero-inated model
t the observed data better than an ordinary Poisson regression
(z ¼ 3.74e5.41, p < .001).
Multivariate regression models thus indicated that: a) lower
SES, higher Basal Salivary Cortisol Secretion, and higher counts of
Cariogenic Bacteria predicted the number of caries lesions; b)
children with the highest number of Dental Caries were those with
the combination of high Salivary Cortisol Secretion, high Cariogenic
Bacteria, low SES and high Family Financial Stressors; and c) counts
of Cariogenic Bacteria were a signicant predictor of the binary
presence or absence of Caries.
Study 2: salivary cortisol and the dental microanatomy of
exfoliated teeth
Sample and methods
To examine associations among salivary cortisol and the thick-
ness and density of dental tissue compartments, a second sub-
sample of children was recruited during their rst grade year, from
20 04 to 2006. This sub-sample comprised 38 children ranging in
age from 5.9 to 6.8 years (17 girls and 21 boys), recruited from all
three PAWS cohorts, and consisting of children who lost a tooth
during the 9 months of the rst grade academic year and from
whom we were able to collect the tooth for analysis (see sub-study
ow chart, Fig. 1). Again the sub-sample did not differ from the
larger, longitudinal study sample on socioeconomic status (F ¼ 0.91,
p
¼ NS).
During their kindergarten year, when basal and reactive
cortisol levels were assessed, 18 children (47%) had attended
Table 1
Bivariate Associations Among Independent Variables (1e5) and Dental Caries (6)d
Study 1 (Pearson Correlation Coefcients, N ¼ 94 children).
1. 2. 3. 4. 5. 6.
1. SES .34*** .23* .17 .41*** .32**
2. Family nancial stressors .22* .10 .11 .09
3. Basal salivary cortisol secretion .03 .13 .23*
4. Salivary cortisol reactivity .08 .03
5. Cariogenic bacteria (Study 1) .56***
6. Dental caries (Study 1)
yp < .10 *p < .05 **p < .01 ***p < .001.
Table 2
Zero-inated Poisson regression models predicting
P
DMFSdStudy 1 (N ¼ 94 children).
Independent variables Model 1 Model 2 Model 3 Model 4 Model 5
Coefcients B (SE)/Z B (SE)/Z B (SE)/Z B (SE)/Z B (SE)/Z
Poisson models
SES 0.16 (0.03) 5.56 *** 0.16 (0.03) 4.94*** 0.16 (0.03) 4.69*** 0.08 (0.04) 2.28* 0.08 (0.04) 2.08*
Family nancial stressors 0.00 (0.05) 0.05 0.06 (0.06) 1.13 0.04 (0.05)0.81 0.05 (0.05) 0.92
Basal salivary cortisol secretion 0.19 (0/05) 4.09*** 0.22 (0.05) 4.51*** 0.08 (0.06)1.30
Cariogenic bacteria 0.12 (0.02)5.67*** 0.11 (0.02) 5.30***
Basal salivary cortisol cariogenic bacteria 0.23 (0.05) 4.35***
Overall LR Chi
2
28.7*** 28.7*** 44.9*** 76.8*** 95.8***
Logistic models
Cariogenic bacteria 0.69 (0.14) 4.92*** 0.69 (0.14) 4.92*** 0.70 (0.14) 4.88*** 0.69 (0.14) 4.88*** 0.70 (0.14) 4.84***
yp .10; *p .05; **p .01; ***p .001.
W.T. Boyce et al. / Social Science & Medicine 71 (2010) 1644e1652 1647
Page 4
a morning class and 20 (53%) an afternoon class. Children taking
medications that could result in erroneous measures of salivary
cortisol were excluded from the sample.
Independent variables
SES, Family Financial Stressors, Basal Salivary Cortisol Secretion,
and Salivary Cortisol Reactivity were measured using the methods
described for Study 1.
Dental compartment thickness and density
Exfoliated primary mandibular incisors were collected from the
children. Parents/guardians were instructed to call the project
coordinator for tooth collection immediately after the tooth fell out.
The teeth were then transferred to sterile water with 0.1% thymol,
sterilized by overnight gamma radiation, and stored at 4
C.
A single investigator (YJ), blind to other study data, measured
the thickness and density of the enamel and dentin compartments
by scanning with a microtomography (
m
CT) scanner (Scanco
Medical AG, Bassersdorf, Switzerland). A small x-ray tube with
a micro focal spot was used as a source, and the detector consisted
of a linear CCD-array. A scout view scan was obtained rst, followed
by automatic positioning, measurement, and ofine reconstruction
(see Jiang et al., 2003). Images with isotropic resolution of 21
m
m
were obtained with 70 kVp and 85
m
A. For subsequent image
analyses, a subset of the original
m
CT section, containing entirely
enamel and readily distinguished from dentin by obvious differ-
ences in mineral density, was selected. Enamel data were thresh-
olded into binary data sets, and enamel tissue was segmented from
non-enamel in gray-scale images with a xed thresholding proce-
dure. Boundaries between enamel and dentin and between dentin
and pulp cavity were manually traced to measure the thickness and
density of the two layers.
Statistics
Preliminary analyses duplicated those of Study 1. OLS regression
was used to estimate the direct and interactive associations of
independent variables with dental compartment measures. Each
predictor variable was centered at its mean, and where a signicant
interaction was found, the moderator effect was probed using
scatter plots as in Study 1.
Results
In the Study 2 sub-sample, the mean of the highest household
education level and the standardized Family Financial Stressors
score were closely comparable to those of Study 1. The mean raw,
pre- and post-school salivary cortisol levels were 9.3 nmol/L
(SD ¼ 4.9; range ¼ 3.2e25) and 4.9 nmol/L (SD ¼ 3.3;
range ¼ 2.4e 22.6), respectively. The mean pre- and post-stress
reactivity protocol cortisol levels were 5.3 nmol/L (SD ¼ 2.6; range
1.7e15.7) and 4.2 nmol/L (SD ¼ 2.1; range ¼ 1.5e11.3). Again,
approximately one third of children (37%) showed an increase in
salivary cortisol during the reactivity protocol. The thickness and
density of the enamel and dentin layers were normally distributed,
with a mean Enamel Thickness of 0.25 mm (SD ¼ 0.04; range
0.15e0.33) and a mean Enamel Density of 1894 mg hydroxyapatite/
cm
3
(SD ¼ 39.5; range ¼ 1796e1961). Dentin Thickness and Density
had means of 1.05 mm (SD ¼ 0.14; range ¼ 0.80e1.44) and 1090 mg
hydroxyapatite/cm
3
(SD ¼ 25.7; range ¼ 1032e1137), respectively.
Compartment thicknesses were comparable to but slightly lower
than those previously observed using standard radiography (Hall,
Lindauer, Tufekci, & Shroff, 2007), differences possibly attribut-
able to variation in measurement technique and tooth selection.
Eighteen of the 38 children provided a second exfoliated primary
tooth, allowing an examination of the between-teeth reliability of
the microtomographic measures in this subset. The intraclass
correlation coefcients between tooth 1 and tooth 2, for measures
of compartment thickness and density, ranged from 0.63 to 0.97 (all
p .001), indicating a high level of measurement reliability.
Table 3 displays correlation coefcients among independent and
dependent variables. SES was signicantly and inversely associated
with Basal Salivary Cortisol Secretion, indicating that children from
more highly educated families had lower levels of tonic HPA acti-
vation. Basal Salivary Cortisol Secretion was unrelated, however, to
any Dental Compartment measure. Unexpectedly, SES was also
inversely and signicantly associated with Enamel Thickness and
Enamel Density, suggesting that children from lower SES families
had thicker and less vulnerable dental enamel. Because prior
observations have suggested that individuals of African ancestry
have phenotypically thicker dental enamel (Hall et al., 2007; Harris,
Hicks, & Barcroft, 2001), this unanticipated nding was explored by
Fig. 2. Interaction of Basal Salivary Cortisol Secretion and Cariogenic Bacteria Predicting
P
DMFSd Study 1 (N ¼ 94 children).
W.T. Boyce et al. / Social Science & Medicine 71 (2010) 1644e16521648
Page 5
jointly examining the childs ethnicity (AfricaneAmerican v other)
and SES in relation to Enamel Thickness. Analysis of variance
showed that African-American children had signicantly greater
Enamel Thickness (0.27 mm v 0.24 mm, F ¼ 3.97, p < .05) and that,
after adjustment for ethnicity, the signicant association with SES
disappeared. Finally and as shown in Fig. 3 for Enamel Thickness
and Density, Salivary Cortisol Reactivity was inversely and signi-
cantly or borderline signicantly associated with three of the four
Dental Compartment measures. Because Basal Salivary Cortisol
Secretion was unrelated to outcomes and its associations with
Dentin measures were generally smaller in magnitude, these vari-
ables were omitted from further analysis.
OLS linear regression models were next sequentially computed
to assess SES, Family Financial Stressors, and Salivary Cortisol
Reactivity as predictors of Enamel Thickness and Density (Table 4).
Because SES and Salivary Cortisol Reactivity had the strongest
bivariate associations with Enamel Thickness and Density,
a SES Salivary Cortisol Reactivity interaction term was entered in
the nal regression model. Within the series of regression models,
SES and Salivary Cortisol Reactivity again bore strong, independent
associations with Enamel Thickness and Density. In Model 4, with
the entry of the interaction term, the relation of SES to Enamel
Thickness and Density substantially diminished, suggesting that
SES effects were partially mediated by the signicant interaction
between SES and Salivary Cortisol Reactivity. As shown in Fig. 4,
higher SES children showed little difference in Enamel Thickness by
Salivary Cortisol Reactivity, while among low SES children, lower
Salivary Cortisol Reactivity was associated with higher Enamel
Thickness.
Study 2 multivariate analyses thus indicated that: a) lower SES
was associated with higher Enamel Thickness and Density, an
unexpected association possibly related to differences in enamel
structure among low SES, African-American children; b) higher
Salivary Cortisol Reactivity was associated with lower Enamel
Thickness and Density; and c) the children with the highest Enamel
Thickness were those with the combination of low SES and low
Cortisol Reactivity.
General discussion
The studies reported here yielded ve principal ndings: a)
approximately half of the children had developed dental caries by
ve years of age; b) low family SES was associated with nancial
stress, basal activation of the childs hypothalamic-pituitary-adre-
nocortical (HPA) axis, and higher counts of oral cariogenic bacteria;
c) cariogenic bacteria and salivary cortisol secretion were both
independently associated with the presence of caries; d) the
highest risk of dental caries was among children with high levels of
both salivary cortisol and cariogenic bacteria; and e) cortisol reac-
tivity to stress was associated with thinner, softer, and thus more
vulnerable enamel surfaces. Low SES was also associated with
thicker and more dense dental enamel, especially among those
with low cortisol reactivity, a nding perhaps accounted for, fully or
in part, by structural differences in enamel among African-Amer-
ican children.
Taken together, these ndings advance a conceptual model of
social and psychobiological inuences on caries incidence with two
biologically plausible and distinct but interactive pathways (see
Fig. 5).
First, children from lower SES families acquired cariogenic
oral bacteria at levels signicantly higher than their higher SES
peers. Counts of oral mutans streptococci (MS) and Lactobacillus
species (LB) were strongly linked to SES and substantially mediated
the SES-caries association. Second, higher levels of basal salivary
cortisol secretion and cortisol reactivity to stress may compromise
dental health by undermining protective, local defenses and
microanatomical structures. Exaggerated basal HPA activation was
associated with risk to the dentition through interactions with the
presence of cariogenic bacteria, and cortisol reactivity was linked to
risk through changes in the physical properties of dental enamel.
Importantly, the strongest risk factor for development of dental
caries was the joint presence of heightened expression of salivary
cortisol and high levels of cariogenic bacteria. To our knowledge,
these are the rst studies to implicate conjoint, interactive roles of
oral bacteria and salivary cortisol in the pathogenesis of childhood
dental caries.
Both cariogenic pathways are consistent with a number of prior
observations. First, low SES has been identied as a risk factor for
early colonization with cariogenic bacteria (e.g., Li, Caueld,
Dasanayake, Wiener, & Vermund, 2005), and transmission within
the rst year of life is associated with the development of caries in
early childhood (Alaluusua & Renkonen, 1983). Such transmission
may be either vertical, between mother and child (Lapirattanakul
et al., 2008), or horizontal, among peers and playmates
(Doméjean-Orliaguet et al., 2010). Further, mediation of the SES-
caries association by cariogenic bacteria counts is concordant with
reports that MS and LB are necessary pathogenic elements in the
production of caries and that mucosal vaccines against oral path-
ogens are capable of caries prevention (Smith, 2003). An innate
salivary defense against colonization utilizes mechanical rinsing,
buffering, antimicrobial peptides, and bacterial aggregation and
clearance (Tao et al., 2005). The rst line of defense, however, is
immunologic (Walker, 2004). Production of secretory immuno-
globulin A (sIgA) in saliva begins by one month of age (Smith,
20 03), and the capacity of sIgA antibody to recognize specic
bacterial antigens plays a critical role in the modulation and control
of infection with cariogenic organisms (Nogueira, Alves, Napimoga,
Smith, & Mattos-Graner, 2005).
The second possible pathway, by which SES was associated with
family nancial stressors, cortisol secretion, and physical properties
of the dental enamel, is similarly consistent with other reports. Low
family SES has been linked to a higher burden of acute and chronic
adversities of all types, not least nancial stressors (Duncan &
Brooks-Gunn, 2000; Evans & Schamberg, 2009), and children
from low SES families show evidence of heightened HPA activation
Table 3
Bivariate associations among independent variables (1e4) and dental compartment thickness and density (5e8)dStudy 2 (Pearson correlation coefcients, N ¼ 38 children).
1. 2. 3. 4. 5. 6. 7. 8.
1. SES .19 .47** .15 .42** .31* .22 .14
2. Family nancial stressors .25 .08 .07 .06 .23 .04
3. Basal salivary cortisol secretion .13 .15 .24 .31y .16
4. Salivary cortisol reactivity .29y.41** .29y.21
5. Enamel thickness .68*** .18 .28y
6. Enamel density .41** .70***
7. Dentin thickness .19
8. Dentin density
yp < .10 *p < .05 **p < .01 ***p < .001.
W.T. Boyce et al. / Social Science & Medicine 71 (2010) 1644e1652 1649
Page 6
and reactivity (Cohen, Doyle, & Baum, 2006; Kristenson, Eriksen,
Sluiter, Starke, & Ursin, 2004; Lupien et al., 2000). Greater expo-
sure to stressors has also been associated with acceleration in
dental disease in rats (Gaspersic, Stiblar-Martincic, & Skaleric,
20 02) and with lowered host resistance to periodontitis-related
bacteria in humans (Klages, Weber, & Wehrbein, 2005). Although
no prior work has examined salivary cortisol secretion and the
physical properties of teeth, enamel hypoplasia is known to
augment dental caries susceptibility (Hong, Levy, Warren, &
Broftt, 2009), and exposures to therapeutic corticosteroids can
induce hypoplasia (Bublitz, Machat, Scharer, Komposch, & Mehls,
1981) and narrow the dental pulp chamber by effecting new
dentin formation (Nasstrom, Odselius, & Petersson, 1996).
Finally, the previously unrecognized interaction of cortisol and
bacteria in the prediction of caries risk is consistent with prior
ndings that acute and chronic stressors can impair sIgA production
(Deinzer, Kleineidam, Stiller-Winkler, Idel, & Bachg, 2000; Phillips
et al., 2006), that cortisol is capable of affecting local, mucosal
immunity and oral microbial ora (Genco et al., 1998), and that
mucosal immune competence affects bacterial colonization and
growth (Kamma, Lygidakis, & Nakou, 1998; Nogueira et al., 2005).
Secretory IgA plays an important role in regulation of oral microbial
ecology (Teeuw, Bosch, Veerman, & Amerongen, 2004), and gluco-
corticoids can exert immunosuppressive effects through mecha-
nisms such as reductions in circulating lymphocytes, inhibition of
immune cell aggregation, down-regulation of chemotaxis and
degranulation, and diminution in cytokine production, including IL-
1, IL-2, tumor necrosis factor, and interferon gamma (Genco et al.,
1998). Collectively, these previous reports undergird our conclu-
sion that the socioeconomic partitioning of childhood dental caries
involves the convergent, stress-related processes of increased
cortisol secretion and the proliferation of cariogenic bacteria.
Several methodological and design limitations of these studies
should be taken into account in weighing the presented ndings.
First, the study samples, though socioeconomically representative
of the larger study from which they were drawn and, more
generally, of the East San Francisco Bay Area population, were on
average highly educated by national standards; such over-
representation of high SES families would arguably have operated
as a conservative bias, obscuring or diminishing associations
Fig. 3. Enamel Thickness and Density by Salivary Cortisol Reactivityd Study 2 (N ¼ 38 children).
Table 4
Linear regression models predicting dental compartment thickness and densitydStudy 2 (N ¼ 38 children).
Linear Regression Models
Independent variables Model 1 Model 2 Model 3 Model 4
Coefcients B (SE)/t B (SE)/t B (SE)/t B (SE)/t
Enamel thickness (N ¼ 38)
SES 0.02 (0.01) 2.75** 0.02 (0.01) 2.68** 0.02 (0.01) 2.43* 0.01 (0.01) 1.66y
Family nancial stressors 0.00 (0.01) 0.05 0.00 (0.01) 0.11 0.00 (0.01) 0.27
Salivary cortisol reactivity .02 (0.01) 1.50 0.01 (0.01) 2.39*
SES salivary cortisol reactivity 0.02 (0.01) 2.67 **
Overall F 7.59** 3.69* 3.30* 4.70**
Enamel density (N ¼ 38)
SES 12.18 (6.27) 1.94y13.08 (6.43) 2.03* 10.60 (6.14) 1.73y8.42 (6.45) 1.31
Family nancial stressors 4.08 (5.62) 0.73 2.71 (5.32) 0.51 3.56
(5.37) 0.66
Salivary cortisol reactivity 14.21 (6.05) 2.35* 16.36 (6.35) 2.58*
SES salivary cortisol reactivity 9.07 (8.43) 1.08
Overall F 3.78y 2.13 3.45* 2.89*
yp .10; *p .05; **p .01; ***p .001.
W.T. Boyce et al. / Social Science & Medicine 71 (2010) 1644e16521650
Page 7
between SES and measures of oral health. Second, cross-sectional in
design, the studies were incapable, in principle, of establishing
causally informative associations. The two-pathway model
advanced here, linking SES and caries, should be therefore regarded
as a conceptual synthesis of reported ndings, rather than as
a causal model of caries pathogenesis. Third, several known or
suspected oral health risk factors, such as the developmental
timing of cariogenic bacteria acquisition, the level of dietary
carbohydrates, lead and tobacco smoke exposure, and parental
attentiveness to childrens dental hygiene were unmeasured in this
study. Although the uoridation of drinking water was also not
evaluated, optimal uoride levels for the East Bay Area are moni-
tored and maintained by the California Department of Public
Health. Fourth, although conjectures have been made regarding the
possible immunological mediation of the cortisol bacteria inter-
action, no immune parameters were measured, and thus no direct
test of immune mediation was possible. Finally, the studies
employed unselected sub-samples of children from a larger,
longitudinal research project, and while the sub-samples did not
differ in SES from the larger study sample, they could be unrepre-
sentative in terms of other, unmeasured parameters.
These limitations not withstanding, our analyses yielded
substantive, coherent relations between social and psychobiolog-
ical factors and dental outcomes. They suggest that socioeconomic
disparities in stressful experience and HPA activation may
contribute to the social partitioning of dental caries through two
distinctive pathways: a) a low SES-linked predisposition to larger
acquisitions of oral cariogenic bacteria, augmented by higher basal
cortisol secretion that could accelerate local bacterial growth and
virulence, and b) glucocorticoid effects on mineralized dental
tissues, creating physical vulnerabilities to cariogenic bacteria. Such
pathways offer a new, heuristic, and biologically plausible account
for how early social conditions may interact with systemic and local
biological processes to determine short- and long-term disparities
in childhood dental health, disparities that may ultimately and
critically affect the chronic, more general morbidities of adult life.
Acknowledgements
This research was supported by grant awards R01 MH62320 and
R01 MH62320-S1 from the National Institute of Mental Health.
Dr. Boyce holds the Sunny Hill Health Centre-BC Leadership Chair in
Child Development. His work is also supported by the MacArthur
Foundation Research Network on Psychopathology and Develop-
ment and by the Canadian Institute for Advanced Research. The
authors are grateful to Drs. Barry Forer, Bruno Zumbo, and Jelena
Obradovi
c for their assistance with this manuscript.
References
Alaluusua, S., & Renkonen, O. V. (1983). Streptococcus mutans establishment and
dental caries experience in children from 2 to 4 years old. Scandinavian Journal
of Dental Research, 91(6), 453e457.
Aligne, C. A., Moss, M. E., Auinger, P., & Weitzman, M. (2003). Association of pedi-
atric dental caries with passive smoking. Journal of the American Medical
Association, 289(10), 1258e1264.
Alkon, A., Goldstein, L. H., Smider, N., Essex, M., Kupfer, D., & Boyce, W. T. (2003).
Developmental and contextual inuences on autonomic reactivity in young
children. Developmental Psychobiology, 42(1), 64e78.
Angulo, M., Pivel, L., Zinemanas, E., Jorysz, E., & Krasse, B. (1994). Dental caries and
microbial and salivary conditions in Uruguayan children from two different
socioeconomic areas. Acta Odontologica Scandinavica, 52(6), 377e383.
Atkins, D. C., & Gallop, R. J. (2007). Rethinking how family researchers model
infrequent outcomes: a tutorial on count regression and zero-inated models.
Journal of Family Psychology, 21(4), 726e735.
Barker, D. J. (1990). The fetal and infant origins of adult disease. British Medical
Journal, 301(6761), 1111.
Broadbent, J. M., Thomson, W. M., & Poulton, R. (2008). Trajectory patterns of dental
caries experience in the permanent dentition to the fourth decade of life.
Journal of Dental Research, 87(1), 69e72.
Bublitz, A., Machat, E., Scharer, K., Komposch, G., & Mehls, O. (1981). Changes in
dental development in paediatric patients with chronic kidney disease. In:
Proceedings of the European dialysis and transplant association, 18, 517e523.
Fig. 4. Interaction of SES and Salivary Cortisol Reactivity Predicting Enamel Thicknessd Study 2 (N ¼ 38 children).
Fig. 5. Conceptual Model of the Social Partitioning of Childhood Dental Caries
W.T. Boyce et al. / Social Science & Medicine 71 (2010) 1644e1652 1651
Page 8
Centers for Disease Control and Prevention. (2002). Populations receiving optimally
uoridated public drinking watereUnited States, 2000. MMWR Morbidity and
Mortality Weekly Reports, 51(7), 144e147.
Centers for Disease Control and Prevention (2006). Fact sheet: surveillance for
dental caries, dental sealants, tooth retention, edentulism and enamel uo-
rosiseUnited States, 1988e1994 and 1999e2002.
Cohen, S., Doyle, W. J., & Baum, A. (2006). Socioeconomic status is associated with
stress hormones. Psychosomatic Medicine, 68(3), 414e420.
Commission on Social Determinants of Health. (2008). Closing the gap in a genera-
tion: Health equity through action on the social determinants of health. Geneva:
World Health Organization.
Deinzer, R., Kleineidam, C., Stiller-Winkler, R., Idel, H., & Bachg, D. (2000). Prolonged
reduction of salivary immunoglobulin A (sIgA) after a major academic exam.
International Journal of Psychophysiology, 37(3), 219e232.
Doméjean-Orliaguet, S., Zhan, L., Denbesten, P. K., Stamper, J., Boyce, W. T., &
Featherstone, J. D. (2010). Horizontal transmission of mutans streptococci in
children. Journal of Dental Research, 89(1), 51e55.
Donahue, G. J., Waddell, N., Plough, A. L., Del Aguila, M. A., & Garland, T. E. (2005).
The ABCDs of treating the most prevalent childhood disease. American Journal
of Public Health, 95(8), 1322e1324.
Duncan, G. J., & Brooks-Gunn, J. (2000). Family poverty, welfare reform, and child
development. Child Development, 71(1), 188e196.
Edelstein, B. L. (2006). The dental caries pandemic and disparities problem. BMC
Oral Health, 6(Suppl 1), S2.
Essex, M. J., Klein, M. H., Cho, E., & Kalin, N. H. (2002). Maternal stress beginning in
infancy may sensitize children to later stress exposure: effects on cortisol and
behavior. Biological Psychiatry, 52,776e784.
Evans, G. W., Gonnella, C., Marcynyszyn, L. A., Gentile, L., & Salpekar, N. (2005). The
role of chaos in poverty and childrens socioemotional adjustment. Psychological
Science, 16(7), 560e565.
Evans, G.W., & Schamberg, M.A. (2009). Childhood poverty, chronic stress, and adult
working memory. In: Proceedings of the National Academy of Sciences U S A.
Ford, P. J., Yamazaki, K., & Seymour, G. J. (2007). Cardiovascular and oral disease
interactions: what is the evidence? Primary Dental Care, 14(2), 59e66.
Gardner, W., Mulvey, E. P., & Shaw, E. C. (1995). Regression analyses of counts and
rates: Poisson, overdispersed Poisson, and negative binomial models. Psycho-
logical Bulletin, 118(3), 392e404.
Gaspersic, R., Stiblar-Martincic, D., & Skaleric, U. (2002). Inuence of restraint stress
on ligature-induced periodontitis in rats. European Journal of Oral Sciences, 110
(2), 125e129.
Genco, R. J., Ho, A. W., Kopman, J., Grossi, S. G., Dunford, R. G., & Tedesco, L. A. (1998).
Models to evaluate the role of stress in periodontal disease. Annals
of Peri-
odontology, 3(1), 288e302.
Hall, N. E., Lindauer, S. J., Tufekci, E., & Shroff, B. (2007). Predictors of variation in
mandibular incisor enamel thickness. Journal of the American Dental Association,
138(6), 809e815.
Harris, E. F., Hicks, J. D., & Barcroft, B. D. (2001). Tissue contributions to sex and race:
difference in tooth crown size of deciduous molars. American Journal of Physical
Anthropology, 115(3), 223e237.
Hobdell, M. H., Oliveira, E. R., Bautista, R., Myburgh, N. G., Lalloo, R., Narendran, S.,
et al. (2003). Oral diseases and socio-economic status (SES). Britsh Dental
Journal, 194(2), 91e96, (discussion 88).
Hong, L., Levy, S. M., Warren, J. J., & Broftt, B. (2009). Association between enamel
hypoplasia and dental caries in primary second molars: a cohort study. Caries
Research, 43(5), 345e353.
Irwin, L. G., Siddiqi, A., & Hertzman, C. (2007). Early child development: A powerful
equalizer. Vancouver, BC: World Health Organization. (Commission on Social
Determinants of Health).
Ismail, A. I., Sohn, W., Tellez, M., Amaya, A., Sen, A., Hasson, H., et al. (2007). The
International Caries Detection and Assessment System (ICDAS): an integrated
system for measuring dental caries. Community Dentistry and Oral Epidemiology,
35(3), 170e178.
Jiang, Y., Zhao, J. J., Mitlak, B. H., Wang, O., Genant, H. K., & Eriksen, E. F. (2003).
Recombinant human parathyroid hormone (1e34) [teriparatide] improves both
cortical and cancellous bone structure. Journal of Bone and Mineral Research, 18
(11), 1932e1941.
Joshipura, K. J., Pitiphat, W., Hung, H. C., Willett, W. C., Colditz, G. A., &
Douglass, C. W. (2006). Pulpal inammation and incidence of coronary heart
disease. J Endod, 32(2), 99e103.
Kamma, J. J., Lygidakis, N. A., & Nakou, M. (1998). Subgingival microora and
treatment in prepubertal periodontitis associated with chronic idiopathic
neutropenia. Journal of Clinical Periodontology, 25(9), 759e765.
Kaste, L. M., Selwitz, R. H., Oldakowski, R. J., Brunelle, J. A., Winn, D. M., & Brown, L. J.
(1996). Coronal caries in the primary and permanent dentition of children and
adolescents 1e17 years of age: United States, 1988e1991. Journal of Dental
Research, 75 Spec No,631e641.
Kirschbaum, C., & Hellhammer, D. H. (1994). Salivary cortisol in psychoneur-
oendocrine research: recent developments and applications. Psychoneur-
oendocrinology, 19(4), 313e333.
Klages, U., Weber, A. G., & Wehrbein, H. (2005). Approximal plaque and gingival
sulcus bleeding in routine dental care patients: relations to life stress, soma-
tization and depression. Journal of Clinical Periodontology, 32(6), 575e582.
Kristenson, M., Eriksen, H. R., Sluiter, J. K., Starke, D., & Ursin, H. (2004). Psychobi-
ological
mechanisms of socioeconomic differences in health. Social Science and
Medicine, 58(8), 1511e1522.
Kuh, D., & Ben-Shlomo, Y. (2004). A life course approach to chronic disease epide-
miology. Oxford: Oxford University Press.
Lapirattanakul, J., Nakano, K., Nomura, R., Hamada, S., Nakagawa, I., & Ooshima, T.
(2008). Demonstration of mother-to-child transmission of Streptococcus
mutans using multilocus sequence typing. Caries Research, 42(6), 466e474.
Li, Y., Caueld,P.W.,Dasanayake,A.P.,Wiener,H.W.,&Vermund,S.H.
(2005). Mode of delivery and other maternal factors inuence the acqui-
sition of Streptococcus mutans in infants. Journal of Dental Research, 84(9),
806e811.
Loesche, W. (2007). Dental caries and periodontitis: contrasting two infections that
have medical implications. Infectious Disease Clinics of North America, 21(2),
471e502, vii.
Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2000). Childs stress hormone
levels correlate with mothers socioeconomic status and depressive state.
Biological Psychiatry, 48(10), 976e980.
Milgrom, P., Riedy, C. A., Weinstein, P., Tanner, A. C., Manibusan, L., & Bruss, J. (2000).
Dental caries and its relationship to bacterial infection, hypoplasia, diet, and
oral hygiene in 6- to 36-month-old children. Community Dentistry and Oral
Epidemiology, 28(4), 295e306.
Moss, M. E., Lanphear, B. P., & Auinger, P. (1999). Association of dental caries and blood
lead levels. Journal of the American Medical Association, 281(24), 2294e2298.
Nasstrom, K., Odselius, R., & Petersson, A. (1996). Energy dispersive X-ray micro-
analysis of the dentin in rat molars after corticosteroid treatment. Scanning
Microscopy, 10(2), 339e346, (discussion 346e 337).
Newton, J. T., & Bower, E. J. (2005). The social determinants of oral health: new
approaches to conceptualizing and researching complex causal networks.
Community Dentistry and Oral Epidemiology, 33(1), 25e34.
Nicolau, B., Marcenes, W., Allison, P., & Sheiham, A. (2005). The life course approach:
explaining the association between height and dental caries in Brazilian
adolescents. Community Dentistry and Oral Epidemiology, 33(2), 93e98.
Nogueira,R. D., Alves, A. C., Napimoga, M. H., Smith, D. J., & Mattos-Graner, R. O. (2005).
Characterization of salivary immunoglobulin A responses in children heavily
exposed to the oral bacterium Streptococcus mutans: inuence of specic antigen
recognition in infection. Infection & Immunity, 73(9), 5675e5684.
Petersen, P. E. (2005). Sociobehavioural risk factors in dental caries e international
perspectives. Community Dentistry and Oral Epidemiology, 33(4), 274
e2
79.
Petersen, P. E., Bourgeois, D., Bratthall, D., & Ogawa, H. (2005). Oral health infor-
mation systemsetowards measuring progress in oral health promotion and
disease prevention. Bulletin of the World Health Organization, 83(9), 686e 693.
Phillips, A. C., Carroll, D., Evans, P., Bosch, J. A., Clow, A., Hucklebridge, F., et al.
(2006). Stressful life events are associated with low secretion rates of immu-
noglobulin A in saliva in the middle aged and elderly. Brain Behavior and
Immunity, 20(2), 191e197.
Pitts, N., Boyles, J., Nugent, Z., Thomas, N., & Pine, C. (2004). The dental caries
experience of 14-year-old children in England and Wales. Surveys co-ordinated
by the British Association for the Study of Community Dentistry in 2002/2003.
Community Dental Health, 21(1), 45e57.
Pitts, N., Boyles, J., Nugent, Z., Thomas, N., & Pine, C. (2007). The dental caries
experience of 5-year-old children in Great Britain (2005/6). Surveys co-ordi-
nated by the British Association for the study of community dentistry.
Community Dental Health, 24(1), 59e63.
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003). Two
formulas for computation of the area under the curve represent measures of
total hormone concentration versus time-dependent change. Psychoneur-
oendocrinology, 28(7), 916e931.
Seale, N. S., & Casamassimo, P. S. (2003). Access to dental care for children in the
United States: a survey of general practitioners. Journal of the American Dental
Association, 134(12), 1630e1640.
Selwitz, R. H., Ismail, A. I., & Pitts, N. B. (2007). Dental caries. Lancet, 369(9555),
51e59.
Seow, W. K. (1998). Biological mechanisms of early childhood caries. Community
Dentistry and Oral Epidemiology, 26(1 Suppl), 8e27.
Shonkoff, J. P., Boyce, W. T., & McEwen, B. S. (2009). Neuroscience, molecular
biology, and the childhood roots of health disparities: building a new frame-
work for health promotion and disease prevention. Journal of the American
Medical Association, 301(21), 2252e2259.
Skeie, M. S., Riordan, P. J., Klock, K. S., & Espelid, I. (2006). Parental risk attitudes and
caries-related behaviours among immigrant and western native children in
Oslo. Community Dentistry and Oral Epidemiology, 34(2), 103e113.
Smith, D. J. (2003). Caries vaccines for the twenty-rst century. Journal of Dental
Education, 67(10), 1130e1139.
Tao, R., Jurevic, R. J., Coulton, K. K., Tsutsui, M. T., Roberts, M. C., Kimball, J. R., et al.
(2005). Salivary antimicrobial peptide expression and dental caries experience
in children. Antimicrobial Agents & Chemotherapy, 49(9), 3883e3888.
Teeuw, W., Bosch, J. A., Veerman, E. C. I., & Amerongen, A. V. N. (2004). Neuroen-
docrine regulation of salivary IgA synthesis and secretion: implications for oral
health. Biological Chemistry, 385,1137e1146.
Touger-Decker, R., & van Loveren, C. (2003). Sugars and dental caries. American
Journal of Clinical Nutrition, 78(4), 881Se
892S.
W
alker, D. M. (2004). Oral mucosal immunology: an overview. Annals of the
Academy of Medicine Singapore, 33(4 Suppl), 27e30.
World Health Organization. (20 03). The World Oral Health report 2003. Geneva,
Switzerland: World Health Organization.
Yee, R., & Sheiham, A. (2002). The burden of restorative dental treatment for chil-
dren in Third World countries. International Dental Journal, 52(1), 1e9.
W.T. Boyce et al. / Social Science & Medicine 71 (2010) 1644e16521652
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    • "But, all the studies mentioned here were cross-sectional and may have suffered from recall bias. The biological mechanisms through which psychosocial adversity is translated into ill health have been investigated in a series of studies that examined the relationships between family financial stressors, oral cariogenic bacteria, salivary cortisol and dental caries among preschool children in the USA (Boyce et al. 2010). The researchers showed that dental caries was related to the number of cariogenic bacteria in the mouth, but there was a significant interaction: the association between caries levels and the number of cariogenic bacteria was stronger in children with high basal salivary cortisol secretion, which in turn was related to low family socioeconomic position (Fig. 3.7). "
    [Show abstract] [Hide abstract] ABSTRACT: Oral diseases refer to conditions of the teeth, gums and mouth, and include dental caries, periodontal disease, and oral cancers. The impact of these conditions on quality of life is high, they are very common and their treatment is costly, therefore they are considered a major public health problem. Oral diseases are socially patterned, disproportionately affecting socially disadvantaged and marginalised populations. Because oral health and general health are inextricably linked and share common risk factors, caries and periodontal disease are useful markers of general health, and overall patterns of health inequalities. The literature on lifecourse epidemiology applied to oral health is still limited, although there is a strong argument for studying oral diseases within a dynamic life course framework: they are chronic in nature and cumulative over time. Critical periods, as well as accumulation of risk models are applicable to oral diseases. Given that childhood diet and oral hygiene are related to socio-economic and psychosocial factors, and that tooth loss is irreversible, adult oral health is rooted in early life conditions, while upward and downward social mobility influences oral health trajectories. In this chapter we review the theoretical and empirical developments in life course research on oral health, and suggest ways forward.
    Full-text · Chapter · Aug 2015
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    • "The slope was steepest for pain conditions and mental health problems, in accord with previous studies on the health impact of childhood adversity [45,48,80–82] and compatible with a recent study on the relationship between self-rated health and allostatic load in the HUNT population [83]. The trend was also present regarding a number of conditions where physiological dysregulation and life-style are known to interact and even enhance each other, such as obesity, diabetes, dental problems, asthma, COPD, and GERD [42,54,76,84,85] . We did not find any doseresponse relationship for hypertension in our study. "
    [Show abstract] [Hide abstract] ABSTRACT: Multimorbidity receives increasing scientific attention. So does the detrimental health impact of adverse childhood experiences (ACE). Aetiological pathways from ACE to complex disease burdens are under investigation. In this context, the concept of allostatic overload is relevant, denoting the link between chronic detrimental stress, widespread biological perturbations and disease development. This study aimed to explore associations between self-reported childhood quality, biological perturbations and multimorbidity in adulthood.
    Full-text · Article · Jun 2015 · PLoS ONE
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    • "Caries is related to sugary diet and negligent tooth brushing (Chankanka et al. 2011; Reisine and Psoter 2001; Steyn and Temple 2012), this is also the case among children (Harris et al. 2004) . However, the relationship is yet again altered and affected by social factors such as the diet of the mother (Tanaka et al., 2012), childhood factors (Pieper et al. 2012) and social status (Boyce et al., 2010; Dye et al. 2011; Chankanka et al., 2011; Ferro et al., 2012). As such, people's oral health is affected by other factors than their own choices (and their choices are also affected by these factors). "
    [Show abstract] [Hide abstract] ABSTRACT: Luck egalitarianism is often taken to task for its alleged harsh implications. For example, it may seem to imply a policy of nonassistance toward uninsured reckless drivers who suffer injuries. Luck egalitarians respond to such objections partly by pointing to a number of factors pertaining to the cases being debated, which suggests that their stance is less inattentive to the plight of the victims than it might seem at first. However, the strategy leaves some cases in which the attribution of individual responsibility is appropriate (and so, it seems, is asking people to pick up the tab for their choices). One such case is oral health or significant aspects of this. It is appropriate, the paper argues, to hold people responsible for a number of factors that affect their oral health. A luck egalitarian approach inspired by John Roemer can assess whether people have acted responsibly by comparing their choices to those of their peers. A luck egalitarian approach to oral health would recommend prioritizing scarce resources in a responsibility-weighted queuing system and include copayment and general taxation among its measures of financing. © The Author 2015. Published by Oxford University Press, on behalf of the Journal of Medicine and Philosophy Inc. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
    Full-text · Article · Apr 2015 · Journal of Medicine and Philosophy
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