DIETARY PATTERNS RELATED TO CARIES IN A LOW-INCOME ADULT POPULATION
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Abstract
The
aim of this study was to examine the relationship between dietary
patterns and caries experience in a representative group of low-income
African-American adults. Participants were residents of Detroit,
Michigan, with household incomes below 250% of the federally-established
poverty level (n = 1,021). Dietary histories were obtained by trained
interviewers in face-to-face interviews with the adult participants,
using the Block 98.2® food frequency questionnaire developed by Block
Dietary Systems, Berkeley, CA. Caries was measured by the ICDAS criteria
(International Caries Detection and Assessment System). There were 200
dietary records whose data were judged to be invalid; these participants
were omitted from the dietary analyses to leave n = 821. Analyses were
conducted using software from SAS and SUDAAN. Factor analysis identified
patterns of liquid and solid food consumption, and the resulting factor
scores were used as covariates in multivariable linear regression.
Caries was extensive, with 82.3% of the 1,021 participants (n=839)
having at least one cavitated lesion. Nearly three-quarters of the adult
participants were overweight or obese. This population has severe
caries, poor oral hygiene, and diets that are high in sugars and fats
and low in fruits and vegetables. Apart from tapwater, the most
frequently consumed food item by adults of all ages was soft drinks; 19%
of all energy from sugar came from soft drinks alone. In both the
bivariate analyses and in the regression model, frequency of soft drink
consumption and the presence of
gingival plaque deposits were
significantly associated with caries. Interventions to promote oral
health are unlikely to be successful without improvements in the social
and physical environment.
Keywords: diet,
dietary patterns, soft drinks, sugars, fat consumption, caries, plaque
deposits, oral hygiene, adults, disparities, low-income
Introduction
Sugars are an integral part of caries etiology [Gustafsson et al.,1954; Sheiham, 2001].
Even though the sugars/caries relationship in the modern era of
widespread fluoride exposure is not as clear and direct as was
previously assumed [Burt and Pai, 2001], sugars' role in caries development is still not seriously disputed.
There
is far less certainty, however, about the relationship between overall
dietary patterns and caries: i.e., does a poor-quality diet predispose
to caries? By the term “poor-quality diet,” we mean one that provides
adequate energy but has an imbalance in nutrient intake when measured
against recommended levels: too much fat and sugars and not enough
fruits and vegetables. Such diets in high-income countries have been
linked to a number of disease states [Dreeben, 2001; Kayrooz et al., 1998].
Poor-quality diets have perhaps been linked most clearly to obesity,
and the increase in obesity over recent years in the United States [Flegal et al., 2002]
is a serious public health problem. This is true for adults as well as
for children, and obesity-related problems are found at all
socioeconomic levels [Ogden et al., 2002].
From the dental viewpoint, we might intuitively expect that
poor-quality diets promote caries, but apart from sugars' role there is
little firm evidence to support such a relationship. Caries is certainly
higher in children who have been high sucrose consumers all their lives
when compared to children with lower lifetime sucrose intake [Ruottinen et al., 2004].
This
paper examines the relationship between dietary patterns and caries
experience in a representative group of low-income African-American
adults in Detroit, Michigan, USA. The study was conducted by the Detroit
Center for Research in Oral Health Disparities. The Center has the
overall goal of identifying reasons for the community-level and
individual-level disparities in oral health found among this population,
where families appear to live under much the same social and economic
circumstances.
Materials and Methods
The
study was conducted in accordance with the principles of the
Declaration of Helsinki. All participants gave written consent to taking
part. The study was approved by the Institutional Review Board (IRB)
for Health Sciences at the University of Michigan, Ann Arbor.
Study Population
The
participants were African-Americans in Detroit with household incomes
below 250% of the poverty level as defined by the federal government.
Participants were selected using a multistage area probability sample
design based on data from the US census of 2000. The 39 census tracts
within Wayne County (where Detroit is located) with the highest
proportion of low-income African-American households were selected, and a
random sample of 565 blocks divided into 118 neighborhood segments was
drawn from them. A household listing of these blocks was conducted from
June to August 2002. From that household list, a number of housing units
were chosen to yield the target sample of 1,000 persons for the first
wave of data collection. Between September 2002 and August 2003, a field
team visited the selected housing units and successfully screened and
recruited 1,021 families to take part in the study. A family, for the
purposes of this study, was defined as a primary caregiver and one
African-American child who had not yet attained his/her sixth birthday.
Data Collection
Data
were collected by interview and clinical dental examination at the same
facility in Detroit. Questionnaires, completed by trained interviewers
working with the adult participants, were designed to explore the
sociodemographic and lifestyle characteristics of each adult and child,
as well as their general and oral health history. Dietary histories were
obtained by trained interviewers from adult participants, using the the
Block 98.2® food frequency questionnaire (FFQ) developed by Block
Dietary Systems, Berkeley, CA. This FFQ asks the frequency of
consumption of a wide variety of food items over the last year, plus the
number of servings per ingestion and the portion size (judged by the
respondent from photographs and food models of various portion sizes).
Algorithms used by Block Dietary Systems, based on data from several
National Food Consumption Surveys conducted by the U.S. Department of
Agriculture, permit the calculation of energy and nutrient intake as
well as the frequency of consumption of food items.
Measurement of Body Mass Index
Participants
were weighed on a calibrated digital scale and had their height
measured from a wall-mounted tape measure, both from standard protocols.
Body Mass Index (BMI), a broad measure of adiposity, is computed as
weight in kilograms divided by the square of height in meters [National Institutes of Health, 2005].
Staff were trained over a period of one month, and the quality of the
interviews was regularly checked throughout the 11-month data collection
period by reviewing videotapes of the interviews. The investigators
also conducted periodic face-to-face reviews with the interviewers.
Measurement of Dental Caries and Plaque Deposits
Caries
was measured by the ICDAS criteria (International Caries Detection and
Assessment System) applied by four trained dentists. ICDAS is a system
of caries detection and assessment that was developed by an
international group of caries researchers over the period 2002-05 [Pitts, 2004].
It was intended that the criteria (a) reflect the current scientific
understanding of the process of dental caries; (b) be adopted for use in
dental surveillance, research, practice, and education; and (c) provide
a foundation for incorporating and validating new caries diagnostic
tools.
In the Detroit study, four dentists carried out
the scoring for dental caries, periodontal conditions, and plaque
deposits. Participants were examined in a standard dental operatory in
the reclining position with a standard light source. The teeth were
cleaned of loose debris with a scaler, where necessary, and plaque
deposits assessed. Teeth were then examined for caries using the ICDAS
criteria. Assessment of caries was primarily visual. Caries criteria
necessarily varied slightly from pit and fissures to proximal to smooth
surfaces. To illustrate the ICDAS criteria, the scoring system for pit
and fissure caries was as follows:
0- Sound tooth surface: no loss of integrity after air-drying for 5 s.
1- First visual change in enamel.
2- Distinct visual change in enamel.
3- Non-cavitated surface with underlying dark shadow from dentine.
4- Localized enamel breakdown, with no dentine visible.
5- Distinct cavity with dentine visible.
6- Extensive distinct cavity with dentine visible.
The caries outcome measure in data analysis was D1MFS, where “D” included both noncavitated and cavitated lesions, i.e., ICDAS categories 1-6 above. A second measure, D2MFS,
recorded just cavitated lesions (ICDAS categories 4-6). However, these
two measures were tightly correlated (Pearson's r = 0.95, p < 0.001),
so we used just D1MFS as the more complete outcome measure of caries.
Plaque deposits were scored by the Patient Hygiene Performance (PHP) index [Podshadley and Haley, 1968] applied to the “Ramfjord” index teeth [Ramfjord, 1959].
These teeth are the maxillary right first molar; maxillary left central
incisor; maxillary left second premolar; mandibular left first molar;
mandibular right central incisor; and mandibular right second premolar.
The PHP index scores the degree of visible plaque deposits, after a
disclosing rinse, as 0 (no plaque), 1 (recent plaque deposit), or 2
(long-term plaque deposit) in each of five zones of the tooth surface.
Statistical Analyses
Statistical analyses were conducted using software from SAS® [SAS Institute, 2005}, and SUDAAN® [Research Triangle Institute, 2005]
to estimate variances adjusted for the design effect. Significance was
set at the conventional level of p <0.05, and the Wald F test was
used to derive p-values.
Completed FFQs were mailed to
Block Dietary Systems for analysis. All other data were entered twice
using a custom-designed Access program. Data checking for error was
conducted using SAS. Discrepancies between the first and second data
entries were reviewed and resolved by a senior investigator (WS).
After data cleaning and filing, bivariate analyses were conducted to relate frequently-reported foods to caries experience (D1MFS scores). When the population was categorized into tertiles by D1MFS
scores, we selected the food items that were consumed at least once per
day by at least 5% of the adult participants in the high-caries
tertile, and again by at least 5% in the low-caries tertile. Some foods
were reported in both tertiles, others were found only in one tertile
and not the other. There were 29 such food items selected this way, and
subsequent analysis was focused on them.
Factor analysis
was conducted to identify the patterns of liquid and solid food
consumption, and the resulting factor scores were then used as
covariates in multivariable linear regression to relate dietary patterns
to caries levels. Separate factor analyses were carried out for eight
liquid food items (soft drinks were not included due to the high
frequency of their consumption and strong bivariate association with
caries) and 20 solid food items, using PROC FACTOR from the SAS package.
The number of factors was determined by scree plots and by what made
sense from the nutritional viewpoint. The resulting factor scores, along
with the weekly servings of soft drinks, were then used as continuous
independent variables in the multivariable linear regression model with D1MFS
values as the continuous dependent variable. Square root transformation
was performed to improve normality. The multivariable linear regression
was carried out by using PROC REGRESS available in SUDAAN,
incorporating sampling design and weights. The other independent
variables included were: (a) oral health variables: the number of times
teeth were brushed during the last week; and PHP plaque scores; (b)
demographic variables: age; education; income; employment status.
We
carried out backward elimination model selection to determine the most
parsimonious predictive model for caries. We began with the full model
that included all independent variables, proceeding at each step by
dropping from the model the variable with the highest p-value.
(Demographic variables were retained because of their fundamental
importance, regardless of their statistical significance). This process
was repeated until only food, drink, or oral hygiene variables with a
p-value< 0.10 remained in the model.
Results
The
demographic characteristics and Body Mass Index of all adult
participants who had at least one tooth (n=1,005), related to dental
caries experience as measured by the D1MFS index, are shown in Table 1.
Socioeconomic status (SES) is not included because the study
population, by design, was clustered at the lower end of the SES
spectrum.
Demographic characteristics and Body Mass Index (BMI)* related to caries experience (D1MFS)**
among participating adults with at least one tooth (n = 1,005) in Phase
1 of data collection by the Detroit Center for Research on Oral Health
Disparities.
Nutrient Intake and Body Mass Index
The
study began with 1,021 adults. There were 200 FFQ interviews classed as
invalid because they included far too many (≥17) or far too few (≤3)
food items per day relative to national norms. Block Dietary Systems
identified these records which were then eliminated from further dietary
analyses. All analyses on diet and dietary patterns are therefore based
on n = 821, the completed FFQs considered valid. There was still some
missing data in a few FFQs, which is why the totals in some analyses are
less than 821.
The Body Mass Index (BMI) is a broad measure of weight related to height. From the data in Table 1, it can be seen that nearly three-quarters of the participants were either overweight or obese.
Average
daily energy intake for adult females was 2,090 kilocalories, which
again is above average and consistent with the profile of overweight and
obesity. The proportions of participants who were overweight or obese
increased with increasing age: those aged under 26 were 68% overweight
or obese, for those aged 26 to <46 years it was 74%, and for those 46
or older it was 78%. Adults ingested 13.5% of total energy from
protein, 39.4% from fats, and 47.1% from carbohydrates (15.0% from
sugars).
Yet another indicator of poor overall dietary
quality comes with the reported consumption of fruits and vegetables.
Only 7.4% reported eating two or more servings of vegetables per day and
7.8% two or more servings of fruit.
The
most frequently reported food on a daily basis was tapwater. The second
most-reported food consumed daily was sugared soda (reported by 30.3%),
and the third was potato chips (22.1%). Fried chicken was ranked ahead
of green salad. Food sources for sugars for these adults were
predominantly liquid. Soft drinks dominated, with 19% of energy from
sugars coming from soft drinks alone.
Caries Status and Plaque Deposits
The
overall weighted kappa coefficient for inter-examiner reliability in
recording caries was 0.83 and the weighted kappa coefficient for
intra-examiner reliability was 0.74. Caries was commonplace and severe
in this population, with 839 of the 1,005 dentate participants having
one or more untreated cavitated lesions. In those aged 14-<35 years
only 0.2% had no carious lesions. In those aged 35-<47 (n = 140) it
was 1.9%, and in those aged 47 or more (n = 38) it was 3.6%.
The only plaque measure significantly related to D1MFS
scores was gingival plaque, i.e., visible plaque around the gingival
margin after a disclosing rinse (p < 0.02). Total PHP scores,
proximal surfaces and middle surface scores were not significantly
related to caries experience.
Diet and Caries
For
the independent variable in bivariate analyses we used tertiles of the
proportion of total energy (we called this energy%) from the food item.
By this measure D1MFS scores were not related to the intake of protein or fat, but they were significantly related to carbohydrate intake (Table 2), despite the absence of a trend. Because carbohydrates include both non-and low-cariogenic starches [Lingstrom et al., 2000]
as well as cariogenic simple sugars, when the same analysis was
restricted to sugars (all kinds) the sugars-caries relationship was even
more significant (Table 3). D1MFS scores were not related to total PHP scores, but they were related to gingival oral hygiene scores (Table 4).
Mean D1MFS scores for adults (n = 821) by tertiles of the proportion of energy (energy%) from carbohydrates.
Mean D1MFS scores for adults (n = 821) by tertiles of the proportion of energy (energy%) from sugars.
We also expressed the independent variable as daily servings of food items. No relation was found between D1MFS
scores and intakes of vegetables, fruit, grain, meat, dairy products,
tomato juice, orange juice, other real fruit juices, drinks with added
vitamin C, and milk. In bivariate analysis there was at first only a
weak relation between D1MFS and soft drink consumption, but
this relationship was age-confounded. The younger adults drank more soft
drinks and less coffee than the older adults, and when age-adjusted the
D1MFS scores were significantly related to soft drink consumption (p < 0.01; data not tabulated).
Factor
analysis resulted in four factors for 20 solid food items and four
factors for eight liquid food items (soft drinks were not included). The
four solid food factors represented fruits, chips/candy, breakfast
foods (e.g., eggs, sausage), and cheese snacks, and the four liquid food
factors represented real fruit juice, milk, fruit-flavored drinks
(e.g., HiC, Sunny Delight), and coffee/tapwater. These factor scores,
along with the weekly servings of soft drinks , were then used as
continuous independent variables in the multivariable linear regression
with D1MFS scores as the outcome. The full model is shown in Table 5.
Age, frequency of soft drink consumption and presence of gingival
plaque were significantly related to caries prevalence (p < 0.05).
The final model, after the backward model selection procedure was carried out, is shown in Table 6.
The independent variables retained in the final model (apart from the
demographic variables) were frequency of soft drink consumption and
presence of gingival plaque. Age was negatively associated with caries
severity, and soft drink consumption and presence of gingival plaque
were positively associated with caries severity. These results are
similar to those from the full model. Possible two-way interactions were
also explored based on the final model, but none of them were
statistically significant.
Discussion
Dietary patterns have been defined as multiple dietary attributes operationalized as a single exposure [Kant et al., 2004].
To measure dietary patterns in this study we first considered using an
existing index from the literature. However, while a number of indexes
to measure dietary quality have been devised, none has emerged as more
complete than the others [Kant, 1996].
We developed our own Recommended Food Index, based on US Department of
Agriculture recommendations, but it resulted in very low scores with
little variance between individual participants. This indicated a
population with a homogenous diet and low consumption of healthy foods,
so we did not use the Recommended Food Index in this analysis. The
approach adopted was to use factor analysis, which in this instance
detects dietary patterns that reduce the number of variables by finding
factors that comprise correlated dietary items [Kant, 2004].
Factor analysis has been shown to be a valid measure of dietary
patterns when the factor loadings are compared with the results of a
seven-day food diary [Togo et al., 2003].
The data in Table 1
are illustrative of the poor social conditions in this area. The vast
majority of families have no male head of household, which in itself
raises more social problems. The data also show that this is a severely
overweight population. Having nearly three-quarters of the
predominantly-female participants either overweight or obese is well
above the national average (Flegal et al., 2002).
Dietary quality is poor by several measures. The proportion of energy
from fats is above the level recommended by the US Department of
Agriculture, while the carbohydrates and protein levels are near the
bottom of the recommended range. Only 7.4% reported consuming two or
more servings of vegetables per day, and 7.8% two or more servings of
fruit. Current recommendations are to consume 2-2½ cups of fruit and
vegetables per day [US Department of Agriculture, 2005].
An alternative set of dietary guidelines has been published from
Harvard University. These differ from those put out by the US Department
of Agriculture mostly in recommending that a higher proportion of
energy come from fats, but only unsaturated fats, and less from
carbohydrates [Harvard University, 2005] The diet of the participants in our study is still poor under the Harvard guidelines.
Dietary
patterns of African-American adults is a subject that has not received
much research attention, but our results are similar to what little
information has been published. One study among African-Americans in
North Carolina, drawn from all socioeconomic levels, found that
participants' consumption of fruits and vegetables was below the levels
advised in national recommendations [Gary, et al., 2004].
This pattern is even more pronounced in our Detroit study, where the
study population, by definition, came from low socioeconomic levels and
we did not see the contrasting dietary patterns that would be expected
in a population drawn from all socioeconomic levels. It seemed to us
that at least part of the reason is the poor availability of
good-quality fruits and vegetables in sections of the city, with
cultural and economic issues compounding this complex relationship.
The
literature on the relationship between plaque deposits and caries is
mixed. There are studies which conclude that plaque deposits (or more
vaguely “poor oral hygiene”) are a risk factor for caries [Kleemola-Kujala and Rasanen, 1982; Mascarenhas, 1998], while others find no such association [Payette and Brodeur, 1992; Arrow, 1998; Etty et al., 1994]. Meticulous oral hygiene has been shown to reverse the caries process in accessible root lesions [Nyvad and Fejerskov, 1986].
The mixed literature is probably a result of studies' using
inappropriate plaque measures (e.g., scoring plaque from tooth surfaces
where caries is unlikely to be found), measuring caries only in the
cavitated stage, and fluoride effects. In our study, overall PHP index
scores were not related to caries levels, but the overall scores
included plaque measures from areas of the tooth surface where caries
was unlikely, e.g, the middle of the labial surface. When PHP scores
were confined to gingival areas only, we found a strong relationship
between plaque deposits and caries.
There was a time when
cariogenic foods were thought of as being mostly solid foods, e.g.,
candy, chocolate, baked goods. The influential Vipehölm study [Gustaffson et al., 1954]
in the 1950s emphasized the cariogenicity of “sticky” foods and
downplayed the importance of sugar in liquid form. More recently,
however, it has been documented that sugared beverages are a major risk
factor for caries development in children [Levy et al., 2003; Marshall et al., 2003].
Our data confirm these findings and demonstrate that in this population
the same picture applies to adults. It is noted that 55% of the adults'
energy from sugars comes from a few types of drinks, for children the
equivalent figure is 54% [Kolker et al., 2005]. This suggests similarities between the diets of the adults and the children.
It
was this clear evidence that sugar sources in this population were
predominantly liquid that led us to lift soft drinks out of the factor
analysis and leave it as a separate covariable. Soft drinks retained a
highly stable level of statistical significance throughout the backward
elimination model selection, this stability would seem to emphasize
their importance in the carious process. Other drinks in the
ever-growing menu of available beverages, real fruit juices included,
are sugary and hence are potentially cariogenic, but it is notable that
all combinations of both liquids and solids identified by the factor
analysis had dropped out of the final model while soft drinks remained.
The model also retained its R2 value of 0.24. The conclusion
would seem to be that the quality of the overall diet by itself does not
much influence caries in this population, but soft drink consumption in
the presence of plaque retention around the gingival margins certainly
does.
Our findings are that gingival
plaque deposits and soft drinks are the major individual-level
determinants of caries in this population. This leaves the door open for
several intervention areas, i.e., improving both oral hygiene and
dietary quality, specifically cutting back on soft drink consumption.
However, achieving permanent beneficial change in individual behavior
will remain a challenge in this population unless there are also
structural changes in the community and in key aspects of its social
functioning. We cannot expect people living in deep poverty, without
prospects for improvement, and for whom violence is a part of everyday
life, to successfully adopt the habits of healthy diets and careful oral
hygiene unless their physical and social environment is able to provide
a measure of hope and dignity.
Acknowledgements
This study was supported by grant number U-54 DE 14261 from the National Institute for Dental and Craniofacial Research (NIDCR).
Footnotes
Declaration of Interest: No author has any conflict of interest in the conduct of this study or in its findings.
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