contribution of tobacco smoke exposure to learning disabilities
TRANSCRIPT
Contribution of Tobacco SmokeExposure to Learning DisabilitiesLaura Anderko, Joe Braun, and Peggy Auinger
CorrespondenceLaura Anderko, RN, PhD,School of Nursing andHealth Studies, GeorgetownUniversity, 3700 ReservoirRoad NW, Washington, [email protected]
Keywordstobacco smoke exposurelearning disabilities
ABSTRACT
Objective: To investigate the contribution of exposure to prenatal tobacco smoke (PTS) and environmental tobacco
smoke (ETS) to parent-reported learning disabilities.
Design: A nationally representative, cross-sectional survey conducted in the United States, the National Health and
Nutrition Examination Survey (NHANES) 1999 to 2002, was used to explore the association between reported
learning disability and exposure to PTS and ETS.
Participants: Data were analyzed from 5,420 children ages 4 to 15 years old.
Methods: Secondary data analysis was conducted using logistic regression controlling for a number of potential
confounders and covariates.
Results: Overall, 10.6% of children had a parent-reported learning disability (LD), exceeding previous estimates.
Exposure to PTS (odds ratio [OR] 5 1.6) and ETS (OR 5 1.6) were significantly associated with increased odds for
LD in children, with a greater odds noted (OR 5 2.6) when exposed to PTS and ETS.
Conclusion: Exposure to tobacco smoke significantly increases the odds for children to have a learning disability.
Overall, results indicate that if tobacco exposure is causally associated to LD, eliminating exposures could prevent an
estimated 750,000 of parent-reported learning disabilities in the United States. Results underscore the need for
diligence in the promotion of smoking prevention and cessation efforts.
JOGNN, 39, 111-117; 2010. DOI: 10.1111/j.1552-6909.2009.01093.x
Accepted July 2009
Learning disabilities (LD), de¢ned as disorders
that a¡ect the brain’s ability to receive, pro-
cess, store, and respond to information among
individuals who have average intelligence, are esti-
mated to a¡ect more than 6 million children (ages 6
through 21), almost 9.2% of this population. As
many as one in every ¢ve people in the United
States has a learning disability. More than half of
students receiving special education services
through the public schools are identi¢ed as having
learning disabilities, with many having di⁄culties in
the area of reading (U.S. Department of Education,
2009). The number of children diagnosed with LD
continues to increase, along with the need for spe-
cial education services (Stein, Schettler,Wallinga, &
Valenti, 2002). Despite these trends, little is known
about what underlies these high rates: improved
recognition and reporting, altered diagnostic crite-
ria, or true increases (Hermann, King, & Weitzman,
2008; U.S. Department of Education).
Learning disabilities create enormous emotional
and ¢nancial burdens for individuals, families, and
society (Harpin, 2005; Stein et al., 2002). These dis-
orders have widespread societal impacts including
health and educational costs. Estimated costs of
neurobehavioral disorders in the United States are
staggering, with billions of dollars spent annually
(Landrigan, Schechter, Lipton, Fahs, & Schwartz,
2002). When intellectual and classroom perfor-
mance are impaired due to LD, a child faces
di⁄culty in achieving academic success; more than
31% of children with LD drop out of high school
compared to 11% of the general student population
(U.S. Department of Education, 2009). This adds to
societal costs when children are not able to develop
skills necessary to be gainfully employed.
The causes and risk factors for LD are largely un-
known. There is some evidence that problems
during labor and delivery, low-socioeconomic sta-
tus, and low level of maternal formal education are
associated with LD (U.S. Department of Education,
2009). Still, these factors provide few clues for spe-
ci¢c causal risk factors of LD. Risk factors for LD
need to be evaluated within a more comprehensive
Laura Anderko, RN, PhD,is Robert and KathleenScanlon Endowed Chair forValues Based Health Carein the School of Nursingand Health Studies,Georgetown University,Washington, DC.
Joe Braun, RN, MSPH, isa research assistant inthe Department ofEpidemiology at theUniversity of NorthCarolina, Chapel Hill, NC.
Peggy Auinger, MS, is anassistant in the Departmentof Neurology, University ofRochester School ofMedicine and the AmericanAcademy of PediatricsCenter for Child HealthResearch, Rochester, NY.
JOGNN I N F O C U S
http://jognn.awhonn.org & 2010 AWHONN, the Association of Women’s Health, Obstetric and Neonatal Nurses 111
framework that explores other important maternal,
prenatal, and postnatal characteristics, including
exposure to toxins.
Despite the widespread, increasing prevalence of
LD, the association between them and a variety of
toxic exposures remains an important but largely
unstudied association (Braun, Kahn, Froehlich,
Auinger, & Lanphear, 2006; Linnet et al., 2003). Al-
though exposures to maternal smoking during
pregnancy, prenatal tobacco smoke (PTS) expo-
sure, or having a smoker in the home, environ-
mental tobacco smoke exposure (ETS), have been
linked in varying degrees to children’s ability to rea-
son and learn, this study is the ¢rst to use a
nationally representative sample to explore the as-
sociation between smoking exposures and LD
controlling for lead, a known neurotoxin.
Tobacco smoke, which is composed of more than
3,800 di¡erent chemical compounds, has been as-
sociated with a variety of health problems in
children including neurodevelopmental and/or be-
havioral problems such as reduced intellectual
ability, hyperactivity, decreased attention span, lan-
guage skills, and grade retention (Braun et al., 2006;
Huizink & Mulder, 2005; Kukla, Hruba, & Tyrlik,
2008; U.S. Department of Health and Human Ser-
vices (USDHHS), 2006; Yolton, Auinger, Dietrich,
Lanphear, & Hornung, 2005). Prenatal tobacco
smoke exposure may be a preventable cause of in-
tellectual disability with evidence of a dose-
response relationship (Braun et al.; Linnet et al.,
2003; Rauh et al., 2004). Altered brain development
may occur with tobacco smoke exposure through
fetal hypoxia from the nicotine that reduces blood
£ow or from carbonmonoxide that produces higher
levels of carboxyhemoglobin. Nicotine may also tar-
get neurotransmitter receptors in the fetal brain,
causing abnormalities in cell proliferation and
di¡erentiation (Fried,Watkinson, & Siegel,1997). In-
fant exposure to tobacco smoke can occur through
inhalation or through breast milk (Tyler,White-Scott,
Ekvall, & Abula¢a, 2008).
The purpose of this study was to investigate the im-
pact of PTS and ETS exposure on reported LD in
children using the NHANES 1999 to 2002 data set
and controlling for a variety of potentially important
confounders such as gender and socioeconomic
status.
MethodsA nationally representative, cross-sectional survey
conducted in the United States, the National Health
and Nutrition Examination Survey (NHANES) 1999
to 2002, was the most recent source of data for this
study (National Center for Health Statistics [NCHS],
2004a-2004c). This household survey of the nonin-
stitutionalized, civilian population uses complex,
multistage probability-sampling design (NCHS,
2004a). For this study, data for all children ages 4
to 15 years of age (N 5 5,420) who participated in
NHANES were used to explore the association be-
tween ETS and PTS exposure and LD. Methods for
data collection conducted through NHANES in-
cluded personal interviews, health assessment,
and the collection of biologic samples, such as
blood.
The survey questionnaire included, among other
items, questions on LD, smoking history, and care
received in a neonatal intensive care unit (NICU).
The dependent variable, learning disability, was de-
¢ned as a parent answering yes to the question,
‘‘Has a representative from a school or health pro-
fessional told you that your child had a learning
disability’’?
Independent variables collected via the survey in-
cluded the following: smoker at home (or the
measure of ETS exposure) was de¢ned as answer-
ing yes to the question, ‘‘Does anyone who lives
here smoke cigarettes, cigars or pipes, anywhere
inside this home?’’ and mother smoked while preg-
nant (or the measure of PTS exposure) was de¢ned
as answering yes to the question, ‘‘Did (subject par-
ticipant’s) biological mother smoke at any time
while she was pregnant with (him/her)?’’ Covariates
included in the analysis were age, race, gender,
care in a NICU, attendance at a preschool or day-
care, and socioeconomic status (as measured by
Poverty Income Ratio [PIR]). This variable is de-
¢ned as the total household income divided by the
poverty threshold determined by the government
and based on family size for a particular year
(http://www.census.gov/hhes/www/poverty/de¢ni
tions.html).
Recent declining smoking rates in the United States
and increasing LD prevalence underscore the need
to explore the impact of other environmental toxins.
Because of lead’s impact on intellectual capacity
and the potential role that iron de¢ciency can play
in lead’s ability to damage the neurological system,
several biomarkers were explored in this study, in-
cluding levels of blood lead, serum cotinine, and
ferritin (measure of iron status).
Risk factors for learning disabilities, estimated to affect5% to 10% of U.S. children, are poorly understood.
112 JOGNN, 39, 111-117; 2010. DOI: 10.1111/j.1552-6909.2009.01093.x http://jognn.awhonn.org
I N F O C U S Tobacco Smoke and Learning Disabilities
Due to the high degree of correlation between se-
rum cotinine (a metabolite of nicotine) and self-
reported measures of ETS exposure (Spearman
correlation 5 0.56), these variables were analyzed
separately in logistic regression models to deter-
mine the individual e¡ects on LD based on a
chi-square statistical analysis that was adjusted for
the following variables: age, gender, mother
smoked while pregnant, NICU admission, birth
weight, and ferritin. Once added to the full model,
cotinine, although signi¢cant in the bivariable
analysis (o 0.0001), was no longer signi¢cantly as-
sociated with LD (a large number of serum cotinine
values were missing). Therefore, the primary analy-
sis was performed using self-reported ETS
exposure.
Statistical AnalysisSample weights were applied according to the
National Center for Health Statistics (NCHS) guide-
lines to produce accurate national estimates
adjusting for the oversampling of minority and
young children. Regression diagnostics were con-
ducted to determine outliers, which were excluded
from analyses. Correlation analyses assessed mul-
ticollinearity, in which none was noted. Due to the
high prevalence of parent-reported LD in the sam-
ple population, odds ratios (OR) were adjusted to
better represent the relative risk.
Bivariable analyses were initially conducted to de-
termine associations with parent-reported learning
disability and included potential risk factors based
on previous studies: low birth weight, admission
into an NICU (Avchen, Scott, & Mason, 2001; En-
gland, Kendrick, Gargiullo, Zahniser, & Hannon,
2001); race and income (Coutinho, Oswald, & Best,
2002; U.S. Department of Education, 2009); age
and gender (U.S. Department of Education); and
lead (Lanphear et al., 2005). Variables found to be
associated with a reported learning disability based
on chi-square (p o .2) were included in the logistic
regression analyses and ¢ndings reported as an
OR, which, in this study, is the ratio of the probability
of a learning disability being reported for a child to
the probability of no learning disability being re-
ported for a child. Poverty Income Ratio levels were
presented as quartiles to make the results easier to
interpret and also to illustrate any dose-response
relationships for LD.
Population-attributable risk was calculated for risk
factors independently associated with LD and to-
bacco smoke exposure, including PTS and ETS
exposure separately and combined.
ResultsOverall, 581 (10.6%) of the 5,420 children aged 4 to
15 years who participated in NHANES 1999 to 2002
were reported by a parent to have been diagnosed
with a LD, which translates to an astounding 5.1
million children nationwide. The prevalence of
LD increased signi¢cantly with child’s age, male
gender, decreasing PIR (increasing poverty),
mother smoking during pregnancy, whether any-
one smoked in the home, increasing serum
cotinine levels, low birth weight, and admission into
a NICU (Table 1).
A signi¢cant association of parent-reported LD was
found with the following variables: age (o 0.0001),
gender (0.014), NICU admission (0.036), and birth
weight (0.003). Although PIR was signi¢cant in the
bivariable analysis, it became nonsigni¢cant when
other risk factors were introduced into the model
(Table 2).
Most importantly, ORs were signi¢cantly greater for
LDs in children exposed to PTS (OR 5 1.6, p 5
.044) and ETS (OR 5 1.6, p 5 .024).These ¢ndings
indicate that children exposed to PTS are more than
1 1/2 more likely to experience LD when compared
with non-PTS exposed children, and that children
exposed to ETS are more than11/2 times more likely
to experience LD when compared with non-ETS
exposed childrenThe adjusted OR for LD increased
to 2.6 for children who were exposed to PTS and
ETS (p o .0001), meaning children exposed to both
are almost 3 times more likely to report a learning
disability than children who are not exposed.
Table 3 reports on the attributable risk of LD as a re-
sult of exposure PTS and ETS. Excess cases of LD
were attributable to tobacco exposure in each cat-
egory analyzed and resulted in 750,000 excess
cases for children exposed to one or more tobacco
exposure measure. This number represents the
number of cases that could have been prevented
through interventions such as smoking prevention
or cessation.
DiscussionThis study speci¢cally examines the association
between LD and tobacco smoke exposure using a
Children exposed to prenatal and environmental tobaccosmoke are almost 3 times more likely to have a learning
disability than children who are not exposed.
JOGNN 2010; Vol. 39, Issue 1 113
Anderko, L., Braun, J., and Auinger, P. I N F O C U S
nationally representative sample; tobacco smoke
exposure was signi¢cantly associated with parent-
reported LD in U.S. children after controlling for
potential confounders. Findings support previous
studies that found signi¢cant associations with
tobacco exposure and cognitive de¢cits or be-
havioral problems (Braun et al., 2006; Yolton et al.,
2005).
In this study,10.6% of children had a parent-reported
learning disability. This exceeds previous estimates
from the U.S. Department of Education (2009) that
reported that 9.2% of children in the U.S. population
had a learning disability. However, it should be noted
that estimates of the prevalence for LD may vary by
study for several reasons. For example, criteria for
what it means to have LD vary by state, and the use
of parental self-report may re£ect a range in the un-
derstanding of the actual LD ‘‘diagnosis.’’
Table 1: Prevalence of Self-Reported
Learning Disabilities Among Persons Age
4 to 15 in NHANES 1999 to 2002
According to Demographic and Medical
Factors (N 5 5,420)
Variable
Sample
Size
Weighted
Percent (95%) p Value
Age (in years) .001
4-6 1,097 6.3 (4.4, 8.8)
7-9 1,152 7.4 (5.6, 9.8)
10-12 1,372 12.6 (10.4,15.1)
13-15 1,799 15.9 (12.4, 20.3)
Gender o .0001
Male 2,654 12.8 (11.0,15.0)
Female 2,766 8.2 (7.2, 9.4)
Poverty Income Ratio (PIR) .001
1st quartile (0-1.03) 1,741 15.4 (12.4,18.9)
2nd quartile (1.04-2.08) 1,328 11.8 (9.4,14.6)
3rd quartile (2.09-3.74) 990 8.7 (6.1,12.2)
4th quartile (3.75-5.0) 836 7.3 (5.5, 9.5)
Does anyone smoke in the
home?
o .0001
No 4,198 8.4 (7.2, 9.8)
Yes 1,156 17.8 (15.4, 20.4)
Mother smoked while
pregnant
o .0001
No 4,599 8.5 (7.3, 9.9)
Yes 747 19.4 (15.4, 24.2)
NICU .001
No 4,775 9.4 (8.2,10.8)
Yes 605 17.9 (14.0, 22.5)
Low birth weight .003
� 2,500 g 4,883 9.9 (8.8,11.1)
o2,500 g 476 18.2 (13.8, 23.6)
Note. NHANES 5 National Health and Nutrition Examination Survey.
Table 2: Adjusted ORs for Self-Reported
Learning Disabilities Among Persons 4 to
15 Years of Age, NHANES 1999 to 2002
(Smoker in the Home as Index of Postnatal
Smoke Exposure)
Variable OR (95% CI) p Value
Age (in years) 1.16 (1.08,1.24) o .001
Gender
Female Referent
Male 1.5 (1.1, 2.0) .014
Race
White Referent
Other Hispanic 0.9 (0.4,1.9) .758
Mexican 0.7 (0.4,1.2) .197
Black 0.9 (0.6,1.3) .490
Other-multiracial 0.6 (0.3,1.3) .206
Poverty to income ratio 0.9 (0.7,1.0) .114
Mother smoked while pregnant
No Referent
Yes 1.6 (1.0, 2.6) .044
Smoker at home
No Referent
Yes 1.6 (1.1, 2.3) .024
Birth weight (g) 0.9 (0.9,1.0) .003
NICU
No Referent
Yes 1.6 (1.0, 2.6) .038
Blood lead (log transformed) 1.2 (0.9,1.6) .129
Note. OR 5 odds ratios; CI 5 con¢dence intervals ; NICU 5 neo-
natal intensive care unit.
114 JOGNN, 39, 111-117; 2010. DOI: 10.1111/j.1552-6909.2009.01093.x http://jognn.awhonn.org
I N F O C U S Tobacco Smoke and Learning Disabilities
LimitationsThere were limitations of this analysis. First, the de-
pendent variable, LD, was not medically con¢rmed
for this study speci¢cally but rather de¢ned as a
parent answering yes to the question, ‘‘Has a repre-
sentative from a school or health professional told
you that your child had a learning disability?’’ Al-
though parents can be expected to know their
children better than others, there is the possibility
that they may misunderstand a child’s diagnosed
learning problem.
Second, measures of important variables including
mother’s alcohol habits during pregnancy and ed-
ucational level of the parents were not possible due
to the lack of data in this NHANES data set (Batty,
Der, & Deary, 2006; Gilman, Gardener, & Buka,
2008). Finally, the cross-sectional nature of this
study and the natural history of LD limit the ability
to examine the temporal relationship of exposures
to tobacco smoke on learning abilities.
Comparisons With Previous StudiesLow birth weight and admission into NICU were sig-
ni¢cantly associated with LD, supporting previous
studies that explored developmental disabilities
(Jaddoe et al., 2007). It is clear from previous stud-
ies that maternal smoking during pregnancy can
signi¢cantly a¡ect birth weight; babies born to
mothers who smoke tend to be lower in birth weight
and therefore, more likely to be admitted to an NICU.
Although these associations need further explora-
tion regarding their impact on LD, the logical
health intervention is to eliminate or reduce smok-
ing by the mother during pregnancy.
In contrast with several previous studies, a relation-
ship of race or income with LD was not found
(Coutinho et al., 2002; U.S. Department of Educa-
tion, 2009). Race was not identi¢ed as a risk factor
when PTS and ETS were removed from the model
(p 5 .058). It may be that tobacco exposure, which
has been suggested to be higher in low-income
homes and tend to be more predominate in non-
White families, play a more important role than sim-
ply the socioeconomic status of the children’s
household or race of the child (Coutinho et al.; U.S.
Department of Education).
Males were found to have a signi¢cantly higher
odds of LD in this study, which is consistent with
previous ¢ndings (U.S. Department of Education,
2009). Although a variety of explanations for this
phenomena have been proposed including biases
in the LD identi¢cation process, it is important to
continue to explore the factors that may contribute
to this risk (Coutinho et al., 2002; Rutter et al.,
2004; U.S. Department of Education).
The likelihood for the diagnosis of LD increases
with age; our ¢ndings indicate that older age has a
higher prevalence of LD, which is consistent with
the majority of prior studies. The literature suggests
that the older the child and longer he or she attends
school, the more likely that he or she will be identi-
¢ed as learning disabled by school personnel (U.S.
Department of Education, 2009).
The value of using biomarkers such as serum coti-
nine to validate questionnaire responses related to
exposure to tobacco smoke has been described in
earlier documents; it can o¡set socially desirable
but inaccurate questionnaire responses and add
more precision to the model (Yolton et al., 2005). Still,
in this analysis we found that reported exposure to to-
bacco smoke was signi¢cantly associated with the
outcome of LD. It is likely that biomarkers of tobacco
smoke exposure are better predictors of certain out-
comes but may not accurately re£ect the long-term
e¡ects of lifetime exposures; self-reported exposure
may be as good or better for other outcomes (Cara-
ballo, Giovino, Pechacek, & Mowery, 2001).
Table 3: Population Attributable Risk for Self-Reported Learning Disabilities Among
Persons 4 to 15 years of age, NHANES 1999 to 2002
Exposed (%) Adjusted RR Attributable Fraction (95% CI) Excess Cases
Mother smoked while pregnant 18.2 1.6 6.8 (0.2,11.2) 350,000
Smoker in the home 23.6 1.6 8.9 (2.1,13.3) 450,000
PTS and ETS exposure 11.0 2.6 6.8 (4.7, 8.1) 350,000
� 1 exposure 30.1 1.9 14.8 (7.2,19.7) 750,000
Note. NHANES 5 National Health and Nutrition Examination Survey; RR 5 risk ratio; CI 5 con¢dence interval ; PTS 5 prenatal tobacco
smoke; ETS 5 environmental tobacco smoke.
The risk factors are not mutually exclusive and the estimates of attributable risk are not additive. All odds ratios and attributable risks are
adjusted for variables shown inTable 2.
JOGNN 2010; Vol. 39, Issue 1 115
Anderko, L., Braun, J., and Auinger, P. I N F O C U S
Although recent studies have shown that cogni-
tive de¢cits in children occur below Centers for
Disease Control’s current recommended blood
level, this study found no signi¢cant relationship
between reported LD and lead levels (Lanphear
et al., 2005). Although blood lead levels are rela-
tively stable, they may not accurately measure
lifetime exposure in older children and adolescents
measured in this study. Thus, though lead exposure
may contribute to LD, it was not apparent in this
analysis.
Overall, the results of these analyses indicate that if
tobacco exposure is causally linked to LD, eliminat-
ing exposures to tobacco smoke could prevent an
estimated 750,000 (14.7%) of the 5.1 million cases
of parent-reported LDs. The impact of reducing or
eliminating these exposures would profoundly re-
duce costs spent in remediation, not to mention the
emotional toll of living with a learning disability dur-
ing one’s lifetime.
Implications for PracticePreventing exposure of pregnant women, infants,
and children to tobacco smoke requires a multilevel
approach, including individual, institutional, and
community strategies. At the individual level, ad-
visement by a health care provider can be a simple
yet e¡ective means for supporting smoking cessa-
tion. However, studies indicate that health care
provider advisement is limited, despite evidence
that many mothers and expectant fathers indicate
a readiness to quit smoking (Everett et al., 2005;
USDHHS, 2008).
It is important that nurses not only conduct assess-
ment of smoking behaviors, but also incorporate
stop smoking messages and strategies that sup-
port cessation, such as Quit Lines (1-800-
QUITNOW) and computer- or Web-based smoking
cessation programs that have been very e¡ective.
Studies have also found a strong in£uence of male
partner’s smoking habits on women during and af-
ter pregnancy. Addressing a multiple range of
strategies, including the often-overlooked smoking
habits of the partner, will lead to a more successful
outcome (Albrecht et al., 2003; Fiore, 2008; Myung,
McDonnell, Kazinets, Seo, & Moskowitz, 2009;
USDHHS, 2001).
In the event that cessation proves too di⁄cult, and
because toxic particulate matter from smoke can
remain in upholstery, drapes, and carpeting, nurses
can provide information on measures to reduce in-
door air contamination through simple measures
such as smoking outdoors, not smoking in vehicles,
and never smoking in the presence of children.
At the institutional level, systems interventions such
as educating all personnel in e¡ective smoking
cessation strategies, mandating assessment for
smoking at each visit, and/or o¡ering smoking ces-
sation programs for pregnant women and partners
can increase success (Lumley, Oliver, Chamberlain,
& Oakley, 2004).
At the community level, the importance of smoke-free
ordinances or legislation cannot be underestimated
for improving the overall health of communities, in
particular our children. Almost 9 out of every 10
nonsmoking Americans are exposed to ETS, as
measured by the levels of cotinine in their blood
(USDHHS, 2006). As trusted and respected health
professionals, nurses have the power to act as
change agents, advocating for smoke-free commu-
nities. Examples exist of successful community-
wide approaches, such as smoke-free ordinances
developed, negotiated, and sustained by nurses
(Anderko, 2009).
ConclusionsThe causes and risk factors for LD are poorly un-
derstood. Findings from this study are notable as
they add to the scarce knowledge base on LD and
smoking, using a valid and reliable, population-
based sample. Developmental disabilities can arise
from awide range of exposures and interactions; to-
bacco exposures deserve special attention
because they are widespread and preventable.
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I N F O C U S Tobacco Smoke and Learning Disabilities
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Anderko, L., Braun, J., and Auinger, P. I N F O C U S