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Sleep Disordered Breathing and
Academic Performance:
A Meta-analysis
Barbara Galland, PhDa, Karen Spruyt, PhDb,c, Patrick Dawes, MBChB, FRCSd, Philippa S. McDowall, PhDe,
Dawn Elder, MBChB, FRACP, PhDe, Elizabeth Schaughency, PhDf
abstract BACKGROUND AND OBJECTIVE: Sleep-disordered breathing (SDB) in children is associated with daytime
functioning decrements in cognitive performance and behavioral regulation. Studies
addressing academic achievement are underrepresented. This study aimed to evaluate the
strength of the relationships between SDB and achievement in core domains and general
school performance.
METHODS: Data sources included PubMed, Web of Science, CINAHL, and PsycINFO. Studies of
school-aged children investigating the relationships between SDB and academic achievement
were selected for inclusion in a systematic literature review using Preferred Reporting Items
for Systematic Reviews and Meta-Analyses guidelines. Data extracted were converted into
standardized mean differences; effect sizes (ES) and statistics were calculated by using
random-effects models. Heterogeneity tests (I
2
) were conducted.
RESULTS: Of 488 studies, 16 met eligibility criteria. SDB was significantly associated with poorer
academic performance for core academic domains related to language arts (ES –0.31; P,.001;
I
2
= 74%), math (ES –0.33; P,.001; I
2
= 55%), and science (ES –0.29; P= .001; I
2
= 0%), and
with unsatisfactory progress/learning problems (ES –0.23; P,.001; I
2
= 0%) but not general
school performance.
CONCLUSIONS: Variable definitions of both academic performance and SDB likely contributed to
the heterogeneity among published investigations. Clear links between SDB and poorer
academic performance in school-age children are demonstrated. ES statistics were in the small
to medium range, but nevertheless the findings serve to highlight to parents, teachers, and
clinicians that SDB in children may contribute to academic difficulties some children face.
Departments of aWomen’s & Children’s Health, and dSurgical Sciences, Dunedin School of Medicine, Universit y of Otago, Dunedin, New Zealand; bDepartment of Developmental and Behavioral
Pediatrics, Jiao Tong University School of Medicine, Shanghai, China; cFaculty of Psychology, Vrije Universiteit Brussel and School for Mental Health and Neurosciences, Maastricht University,
Maastricht, Netherlands; eDepartment of Paediatrics and Child Health, Wellington School of Medicine, Universit y of Otago, Wellington, New Zealand; and fDepartment of Psychology, University
of Otago, Dunedin, New Zealand
Dr Barbara Galland conceptualized and designed the project and drafted the initial manuscript; Dr Spruyt contributed to the data collection methods, carried out the data
analyses, and reviewed and revised the manuscript; Drs Dawes and McDowall carried out the quality review of the papers included in the meta-analysis and reviewed and
revised the manuscript; Dr Elder contributed to the quality review of the papers included in the meta-analysis and reviewed and revised the manuscript, Dr Schaughency
contributed to the design of the project and data collection methods and reviewed and revised the manuscript; and all authors approved the final manuscript as submitted.
www.pediatrics.org/cgi/doi/10.1542/peds.2015-1677
DOI: 10.1542/peds.2015-1677
Accepted for publication Jul 21, 2015
Address correspondence to Barbara Galland, PhD, Department of Women’s & Children’s Health, University of Otago, PO Box 56, Dunedin 9054, New Zealand. E-mail:
barbara.galland@otago.ac.nz
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2015 by the American Academy of Pediatrics
REVIEW ARTICLE PEDIATRICS Volume 136, number 4, October 2015
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Sleep-disordered breathing (SDB) in
children covers a spectrum of
breathing abnormalities ranging from
habitual snoring, to upper airway
resistance syndrome, to frank
obstructive sleep apnea (OSA).
1
The
prevalence of habitual snoring
reported in the pediatric literature,
based mainly on parental report,
ranges from 1.5% to 27.6%
2–4
but is
most commonly estimated at 6% to
12%,
5
whereas OSA is estimated to
affect up to 1% to 4% of children.
6,7
Adenotonsillar hypertrophy is
a major contributor to SDB in
children, and removing these
(adenotonsillectomy) leads to
significant improvement in SDB
symptoms for most children,
8
but
obesity, craniofacial genetics, and
neural control mechanisms of upper
airway patency are other
contributory factors.
9
Since the late 1990s, a large body of
literature has focused on the
neurocognitive correlates of SDB.
Research indicates the most common
behavioral and neurocognitive effects
to be evident in measures of constructs
such as intelligence, memory,
executive function, attention, and
hyperactivity.
10–12
Poorer performance
in these domains has been suggested
to affect daytime functioning, leading
to suboptimal academic achievement
compared with healthy peers. For
example, links between attention-
executive functioning, an umbrella
term incorporating attentional control,
behavioral inhibition, working
memory, and academic achievement,
are well documented,
13,14
as are links
between the symptoms of attention-
deficit/hyperactivity disorder and
academic underachievement.
15,16
Limited developmental growth in
executive functioning predicts
behavioral and emotional adjustment
difficulties and negative academic self-
concept
17
with potential deleterious
effects on later academic
achievement.
18
The neurocognitive sequelae of SDB
resolve to some extent when treated
by adenotonsillectomy.
19–21
Outcomes beyond 1 year are largely
unknown aside from 1 study of
school-age children that reported
improvements within some
neurocognitive domains 4 years after
adenotonsillectomy.
22
Although
the positive outcomes of
adenotonsillectomy are well
documented, studies addressing
academic performance as an outcome
are underrepresented compared with
other functional outcomes, and little
is known about the potentially
remedial effects of SDB treatment on
school performance. The majority of
studies report parent or teacher
ratings or global measures of school
performance, with fewer reporting
results of more labor- and time-
intensive standardized achievement
test results. Methodological factors
potentially contribute to obtained
results; observed links between
potential neurocognitive sequelae of
SDB and achievement may vary
depending on how each is
measured,
14
and measures used may
not be sensitive to treatment
effects.
23
Differences in cultural and
educational contexts add to the
complexity; nevertheless, research
consistently links potential
neurocognitive sequelae of SDB to
achievement across cultural
contexts.
24
However, many studies
fail to consider general underlying
traits in the relationship between SDB
and academic achievement, such as
the associations between sleep
problems and general intellectual
ability.
25
The purpose of this report is to
systematically review the literature in
respect of the association between
SDB and academic performance and,
through meta-analyses, quantify the
reported associations. Because there
are currently no universally accepted
disease cutoffs for diagnosing SDB in
children, and because of the wide
range of definitions used, we included
studies where either subjective
reports or objective measures defined
SDB. For academic performance, we
chose to only include studies that
either directly reported on school
performance (eg, grades) or assessed
performance in academic skill areas
(eg, reading, math). These data should
better inform medical and
nonmedical professionals who
address children’s educational needs
regarding the potential role of SDB in
children’s performance at school.
METHODS
The protocol and data extraction was
conducted according to the 2009
Preferred Reporting Items for
Systematic Reviews and Meta-
Analyses (PRISMA) guidelines.
26
Search Strategy
A search strategy was developed to
identify studies related to SDB and
academic performance in school-age
children/adolescents. An extensive
literature search of 4 electronic
databases up to March 1, 2015, was
conducted: PubMed, Web of Science,
CINAHL, and PsycINFO. The search
strategy used for PubMed is
presented in Supplemental Appendix
1. Titles and abstracts were examined
to extract potentially relevant articles,
subsequently examined in more
depth for inclusion/exclusion criteria
by the main author (B.G.) and the
research assistant (C.L.). Reference
lists of original research and review
articles were also examined to search
for relevant studies. Articles for
which no abstract was available
online were reviewed on the full text.
Full text was retrieved if a decision
could not be made on the basis of the
article abstract. All possible effort
was made to obtain full-text articles,
including contacting the authors by
e-mail.
Inclusion Criteria
For inclusion, studies had to fulfill the
following criteria: (1) an original
article; (2) a study that was
observational, experimental,
longitudinal, cross-sectional, or
a cohort study that investigated the
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relationship between SDB and
academic performance; (3)
participants were school-age children
or adolescents; (4) participants were
drawn from a general community
population or patients referred to
a clinic for SDB concerns; (4) both SDB
and non-SDB (control) children were
included in the participant sample; (5)
article included $1 of the following
academic variables of interest: global
school grade; test performance or
grade on math, language arts (reading,
writing, spelling), or science; parent or
teacher report or subjective rating of
academic performance; (6) SDB was
reported as children being
symptomatically at risk for SDB or
clinically diagnosed as having SDB;
(7) sample was well described
(eg, number of subjects, gender,
recruitment criteria, etc); (8) data for
variables of interest presented
numerically or graphically with
a measure of central tendency and
variance, correlational, odds ratios, or
proportions; (9) data were published
in a peer-reviewed journal; and (9)
article available in English (either
written in English or a translation
available). Where data were presented
graphically, the authors were
contacted to attempt to obtain
numerical data. No time limits were
applied.
Exclusion Criteria: Potentially
Relevant Articles
Studies were excluded if they were
(1) case reports; (2) clinic population
studies that were not related to SDB;
(3) retrospective studies; and (4) if
$1 published report from the same
study was available, we included only
1 with either the most detailed
information or better standard of
reporting.
Quality Assessment
Two independent reviewers assessed
risk of bias and precision for each
study using questions extracted from
the RTI Item Bank
27
; a 29-item
validated tool (organized into 11
domains) with specific instructions
for focusing evaluations of
observational studies of interventions
or exposures included in systematic
evidence reviews and can be adapted
for cross-sectional studies. This tool
allows customization from the
investigator to adapt it to the design
and requirements of the research
question of interest. Eight domains
were suitable for this study
comprising 15 items detailed in
Supplemental Appendix 2. Possible
responses to each item were
combinations of yes, no, partially,
cannot determine, and not applicable.
We grouped “cannot determine”and
“partially”into “unclear risk of bias.”
Two investigators (P.D. and P.M.)
scored the articles independently, and
discrepancies were resolved through
consultation with the other authors
(D.E. and B.G.).
SDB Category
Agreement was reached by 2 authors
(K.S. and B.G.) as to criteria for
inclusion in the study. Ideally, the
severity of SDB would be considered;
however, this was not possible given
the heterogeneity of SDB definitions
including different polysomnography
(PSG) indices used as cutoffs to
denote SDB or not, and no single
index is precise.
28
SDB included
objective and subjectively reported
snoring and OSA, including symptoms
of OSA used in reporting
classifications. Thus, the range
reported included primary snoring,
habitual snoring, symptomatic and
clinically diagnosed OSA, and
generalized SDB. In studies in which
data were presented with $2 levels
of severity of SDB (eg, mild, moderate,
and severe OSA or occasional and
habitual snoring), scores were
aggregated from all SDB groups.
Academic Performance Categories
Academic performance was measured
in several ways in the literature and
categorized broadly as follows: (1)
general performance (global
measures of self- parent- or school-
reported academic performance or
grade point average); (2) language
arts (reading, reading comprehension,
spelling, English [or other first
language in non-English speaking
countries], dictation); (3) math
(mathematics in general or number
operations); (4) science; and (5)
unsatisfactory progress (learning
problem, grade failure, poor school
performance). These categories were
agreed on by 2 authors (E.S. and B.G.).
Where there was $1 language art or
math measure available, data were
aggregated for each domain.
Data Analyses
Meta-analyses were performed by
using Comprehensive Meta-Analysis
software (version 2.2.064; Biostat,
Englewood, NJ). The statistical results
extracted from all studies were
converted into standardized mean
difference (d). Meta-analytic data
analyses require independence of
effect sizes (ES); therefore, when
studies reported multiple ES, these
were combined to independent ES by
intrastudy meta-analyses. Results
reflect relative weight under the
random effects model. Cohen’sd
classification of ES was used, such
that between group ES (within study)
of d#0.20 are small, d= 0.50 are
medium, and d$0.80 are large. The
average ES estimates for each
outcome variable of interest are
illustrated in Forest plots. Cohen’sU
3
index, which determines the percent
change in SDB group scores/grades
from the pooled mean estimates of
non-SDB groups, was used to
estimate the practical value of the
effect.
29
The percentage of observed
total variation across studies due to
real heterogeneity rather than chance
was evaluated by using the I
2
statistic
test. The value of I
2
ranges from 0%
to 100% with 0 indicating no
heterogeneity, 25% low
heterogeneity, 50% moderate
heterogeneity, and 75% high
heterogeneity. Heterogeneity and
statistical significance are reported on
plots to describe the variation
between studies.
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RESULTS
The search criteria from all databases
(with duplicates eliminated) yielded
488 articles (Fig 1). Of those, 218
were deemed to be of potential
interest by title and abstracts
examined to extract 79 articles of
interest. All articles were downloaded
to examine and apply the more
stringent inclusion/exclusion criteria.
Fifty-nine articles were excluded,
1 added (identified from a reference
list), leaving 21 articles for review
containing data suitable to extract for
meta-analysis. Authors of studies
were contacted to obtain a correction
to numerical data,
30
clarification of
the source providing academic
ratings,
31
and confirmation of
participant overlap within 2 studies
from 1 group,
32,33
2 studies from
a second group,
22,34
and 3 studies
from a third group.
35–37
Numerical
data were extracted from the graphs
provided by 1 study after
unsuccessful attempts to contact the
authors.
38
The final meta-analysis
included 16 articles.
Articles Reviewed
Table 1 presents the 16 articles
included in this review chronologically
and summarizes the important
aspects of each. All studies recruited
males and females, and all supplied
a breakdown. The review included
studies from 12 countries. The age of
the participants varied from 5 to 17
years. The number of participants in
each study ranged from 66 to 6349
with a median of 549.
Quality Assessment
Customization of the RTI Item Bank
questions for this study resulted in 8
domains suitable for use in this study
comprising 15 items given in
Supplemental Appendix 2. Results of
individual studies are given in
Supplementary Table 2 and
a graphical summary of the combined
results illustrated in Fig 2. All 16
studies were prospective, and the
majority of studies described the
study populations in detail with only
a few studies at unclear risk of bias by
providing partial information. We
chose to include PSG and individually
administered standardized
achievement tests as the highest
standards of measurement for SDB
and academic performance
respectively in consideration of the
studies using valid and reliable
measures. Eleven studies (69%) did
not use this standard of measurement
for SDB, and 14 (88%) did not use this
standard for academic performance
creating information bias. Two studies
(13%) were at high risk of selection
bias by not considering covariates, and
a further 7 (44%) only considered
some covariates in analyses, creating
an unclear risk of bias. Statistical
methods were evaluated as
appropriate in 75% of studies. In 10 of
the evaluated studies (63%), the
results were considered credible in
line with the individual study’s
limitations and 38% partially credible.
SDB Measures
Seven of the 16 studies used
habitual snoring as the core SDB
symptom based on parental
questionnaires
30,31,38–42
with only 2
studies providing evidence
supporting validity of questionnaires
used.
31,42
Witnessed apnea was used
as a core symptom of SDB,
43
and in
conjunction with habitual snoring, as
an addition/alternative symptom.
41
Validated questionnaire subscales
FIGURE 1
Systematic review search flow diagram based on Preferred Reporting Items for Systematic Reviews
and Meta-Analyses.
26
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TABLE 1 Summary of Studies Included in the Meta-analysis
Author (y) Country Subject Source, Age
Range or Grade,
nfor Study
SDB Defined/Diagnosed
Measure(s)
Academic Measure(s) Adjustment for
Covariates
Reported Findings
Ferreira
39
(2000)
Portugal Schools, 6–11 y,
n= 976
Parent reported:
frequency of loud
snoring
Parent reported: general
school performance
Unadjusted, however
stated that age,
gender, parental SES,
sleep duration all
nonsignificant
between SDB groups
Loud snoring not
associated with school
achievement
Arman
40
(2005)
Turkey Schools, 9.3–9.4 y
(mean), n= 286
Parent reported:
frequency of snoring
Parent reported: learning
disability, academic
performance failure
rating
Unadjusted; however,
stated that parent
education, parental
smoking, SES similar
across groups
No correlation between
HS and learning
disability or academic
performance failure
rating
Goodwin
37
(2005)
USA Schools, 11y,
n= 480
PSG: RDI $1 Parent reported:
frequent learning
problem
Adjusted for previous
factors with P,.1
predictive of SDB
Positive likelihood ratios
for learning problems
when SDB present
Ng
43
(2005) Hong
Kong
Schools, 6–12 y,
n= 3047
Parent reported:
witnessed apnea
Parent reported: general
performance in exam
results from previous
term; grade E for poor
grade
Adjusted for age, allergic
rhinitis, asthma,
mouth dryness when
rising
Witnessed apnea
marginal significance
for poor academic
results
Perez-Chada
41
(2007)
Argentina Schools, 10–15 y,
n= 1900
Parent reported:
frequency of snoring
Math and language
school grade
Adjusted for: age, gender,
BMI zscore, sleep
hours and specific
school
Occasional and frequent
snorers significantly
lower scores for math
and language
compared with
nonsnorers
Giordani
47
(2008)
USA Cases: otolaryngology
clinic; controls:
pediatric general
surgery clinic, 5–13 y,
n=66
PSG: scheduled for AT
with OAI $1 (AT/OSA+)
or OAI ,1 (AT/OSA–)
Child assessment: WIAT
for math, number
operations, spelling,
reading and reading
comprehension
Adjusted for age AT/OSA–had significantly
lower scores for math,
spelling, reading,
and reading
comprehension than
controls; AT/OSA+
groups significantly
lower scores for math
than controls
Sahin
31
(2009)
Turkey Schools, 7–13 y,
n= 1164
Parent reported:
frequency of snoring
Teacher reported:
examination results
from previous class
Adjusted for significant
demographic and
behavioral variables in
unadjusted model
No significant association
between HS and poor
school performance
Arslan
38
(2010)
Turkey Schools, 6–16 y,
n= 1952
Parent reported:
frequency of snoring
Parent reported: general
school performance
Unadjusted Significantly higher
occurrence of poorer
general school
performance in HS vs
never snorers
Li
42
(2010) China Schools, 5–14 y,
n= 6349
Parent reported:
frequency of snoring
Parent reported: poor
school performance
Adjusted for age, gender,
BMI zscore, atopic
symptoms, and
environmental and
SES factors
HS demonstrated to be
an independent
predictor of poor
school performance,
whereas occasional
snoring was not
Kim
44
(2011) Korea Schools, third grade,
n= 299
Parent reported: Sleep-
Related Breathing
Disorder Scale
School obtained
examination scores
for math, science and
language
Unadjusted Mean examination scores
for each subject
higher in controls
than SDB group, but
not significant
Ting
45
(2011) Taiwan Schools, 6–11 y,
n= 138
PSG: SDB severity based
on AHI .1 and #5,
or .5 and #15, and
AHI .15
Teacher-rated academic
performance on math
and language
Adjusted for age, gender,
BMI, parental
education, and
prematurity
Different severities of
SDB groups did not
show significant
associations with
math or language
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were used in 3 studies to identify
SDB.
44–46
Five studies used the
diagnosis of SDB based on PSG using
varying but related indices of
respiratory events; apnea hypopnea
index, respiratory disturbance index,
and obstructive apnea hypopnea
index with thresholds of .1or
$1.
32,34,37,47,48
Academic Performance Measures
Studies used different indicators of
school achievement; for general
school performance, mainly parent or
school reported general school
performance was used. Only 2 studies
directly assessed the children’s core
skills using standardized achievement
tests for math, spelling, or reading or
reading comprehension.
34,47
The
remainder used subject grade or
ratings as reported by the school,
teacher, or parent.
Meta-analyses
Forest plots for each outcome can be
found in Figs 3 and 4 illustrating the ES
estimates for SDB compared with
controls (non-SDB) on the academic
performance categories. A negative ES
estimate indicates those with SDB
performed worse on measures of
academic performance compared with
controls.
The pooled adjusted ES for general
school performance based on data
from 4 studies
30,38,39,45
were –0.15
(95% confidence interval [CI]: –0.38
to 0.01; Fig 3A). This ES did not
reach statistical significance
(P= .21). There was significant and
“moderate”evidence of
heterogeneity (I
2
= 67%; P= .03). All
studies were based on parent- or
teacher-reported school grades,
stated as the previous term or year
grade, or not stated.
Eight studies reported on language
arts measures that included spelling,
reading, reading comprehension, and
TABLE 1 Continued
Author (y) Country Subject Source, Age
Range or Grade,
nfor Study
SDB Defined/Diagnosed
Measure(s)
Academic Measure(s) Adjustment for
Covariates
Reported Findings
Bourke
34
(2011)
Australia Cases: pediatric sleep
clinic; controls:
community, 7–12 y,
n= 137
PSG: Primary snorers
(OAHI #1 with snoring
history or OAHI .1),
mild OSAS (1,OAHI
#5) and moderate/
severe OSAS
(OAHI .5)
Child assessment: WRAT-3
for math, spelling,
reading
Adjusted for SES Trends for all SDB groups
for elevated
impairment of
academic function
compared with
controls; statistically
significant for reading
and math for primary
snoring group and
math for moderate/
severe OSA
Kim
45
(2012) Korea Schools, 11–12 y,
n= 618
Parent reported: 4
questions on SDB
questionnaire;
preschool and present
School performance
score: sum of the
latest midterm and
final examination
scores
Adjusted for SDB stages
at preschool age and
gender
Examination scores not
significantly different
from controls for past,
present, or continuous
SDB
Brockmann
30
(2012a)
Chile Schools, 7–17 y,
n= 274
Parent reported:
frequency of snoring
School report grade for
math, language, and
average school grade
Adjusted for age, gender,
BMI, and hyperactivity
scale score
HS group compared with
never snorers had
significantly lower
grades for math and
average school grade,
but not language
Brockmann
32
(2012b)
Germany Schools, 9.5 y (mean),
n=92
PSG:OSA (AHI $1), UARS
(AHI ,1 and RDI = 1),
primary snoring (AHI
and RDI ,1 and
oxygen desaturation
index ,4)
School report form:
previous terms grade
for math, science, and
spelling
Adjusted for age, gender,
maternal and paternal
education, and class
membership
Compared with children
who never snored,
primary snorers and
UARS/OSA had
significantly lower
percentile grades for
math, science and
spelling
de Carvalho
46
(2013)
Brazil Schools, 7–10 y,
n= 2384
Parent reported: SBD
subscale of Sleep
Disturbance Scale for
Children
Teacher-reported grades
for math, and
language
Adjusted for age and
gender
Children with elevated
SBD had significantly
lower grades for math
and language
compared with those
with no symptoms of
sleep disorders
AHI, apnea hypopnea index; AT, adenotonsillectomy; HS, habitual snoring; NSD, no significant difference; OAHI, obstructive apnea hypopnea index; OAI, obstructive apnea index;
RDI, respiratory disturbance index; SBD, Sleep-breathing disorder; SES, socioeconomic status; UARS, upper airway resistance syndrome; WIAT, Wechsler Individualized Achievement Test ;
WRAT-3, Wide Range Achievement Test-3.
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English/other first language grades/
scores.
30,32,34,41,44,46–48
Tests from
validated performance measures
were used in just 2 studies. When
studies were combined for meta-
analyses, a significant (P,.001)
negative association between
SDB and language arts skills was
found (ES –0.31; 95% CI –0.46 to
–0.16) (Fig 3B) with a near “high”
level of heterogeneity (I
2
= 77%;
P,.001).
Thesame8studies
30,32,34,41,44,46–48
reporting on language arts also reported
math grades/scores showing a combined
significant negative association w ith
SDB (ES –0.33; 95% CI –0.45 to –0.22;
Fig 3C) with “moderate”heterogeneity
(I
2
=61%;P=.01).
Science grades were reported by just
2 studies
32,44
yielding a combined
significant negative association
with SDB (ES –0.29; 95% CI –0.49
to –0.10; Fig 3D). No obvious
heterogeneity was found (I
2
=0%;
P= .94).
Combining academic skill data from
general school performance, language
arts, math, and science data yields
a negative association with SDB with
a significant ES difference of –0.30
(CI –0.38 to –0.22) and no evidence of
heterogeneity (I
2
= 0%; P= .57). This
combined measure reflects
a generalized estimate of effect given
the heterogeneity of the data from
which the “overall”ES is calculated.
Five studies presented
unsatisfactory academic progress
data
31,37,40,42,43
(Fig 4). When these
studies were combined, SDB was
found to be significantly associated
with unsatisfactory school progress
(ES –0.23; 95% CI –0.35 to –0.10).
There was no evidence of
heterogeneity (I
2
=0%;P=.44).
Practical interpretation
To facilitate interpretation of the
practical significance of the outcomes,
Cohen’sU
3
index was used to
estimate the magnitude of change
from the pooled mean estimates for
significant outcomes. Thus SDB
scores/grades/ratings for language
arts, math and science, were 12.3%,
13.1% and 11.6% respectively below
non-SDB mean estimates. Combined
academic scores yielded
a deterioration of 11.8%.
DISCUSSION
This review combined evidence in the
literature to show that SDB in
children is significantly associated
with poorer academic performance in
domains related to core academic
language arts and numeracy skills,
and science ratings/grades. In
addition, SDB was significantly
associated with unsatisfactory
progress but not general school
performance. Integration of these
data through meta-analysis confirms
the frequently cited notion that SDB
in children is related to academic
underperformance. ES statistics are in
the small to medium range. Practical
application using the Cohen’sU
3
index
29
suggests 11.8% deterioration
in SDB groups for core academic
skills. Few studies assessing core
academic skills stated participants’
performance were outside of the
average range. However, our results do
have implications for children not
being able to reach their full academic
potential. All studies represent
achild’s academic performance at one
point in time. Additive negative effects
over time cannot be ruled out.
49
FIGURE 2
Risk of bias by 8 domains (in bold) summarized for all studies (n= 16) using 15 items from the RTI Item Bank.
27
Results in the right-hand panel show the
level of risk of bias (%) as high, unclear, or low risk.
e940 GALLAND et al
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FIGURE 3
Effects sizes and 95% CIs from the included studies of academic performance measures of general performance (A), language arts (B), math (C), science
(D), and combined academic skills (E) comparing SDB to non‐SDB. Square represents the area proportional to the weight assigned to the study within
each meta‐analysis; diamond represents the overall summary estimate for the analysis (width of the diamond represents the 95% CI).
PEDIATRICS Volume 136, number 4, October 2015 e941
by guest on November 14, 2016Downloaded from
Compared with the large number of
studies using standardized tests for
other functional outcomes (eg,
behavior and cognition), only a few
studies used standardized tests to
assess academic achievement. The
majority documented subject grade or
ratings as reported by the school,
teacher or parent. Teachers’ratings
could potentially reflect hyperactive
and disruptive classroom behavior
influenced by SDB.
50
Improvements in
cross-study comparisons could be
made if more studies evaluating
academic achievement used
standardized and validated
achievement measures. For large-
scale studies, costs and time to
administer tests were likely important
reasons individually administered
standardized achievement tests were
not used, pointing to the need for
considerations of both efficiency and
effectiveness in educational
assessment.
Variable definitions of both academic
performance and SDB measures may
have contributed to the heterogeneity
among published investigations. Only
5 studies reported SDB based on gold
standard PSG diagnoses. Just under
half the studies used habitual snoring
as the core SDB symptom from parent
report. Although parental reports
may be susceptible to reporting bias,
there is some objective evidence
that supports the reliability and
accuracy of the subjective reporting
of habitual snoring, at least in young
children.
51,52
Older children are not
as frequently observed during sleep
as younger children, and therefore
parent history to define SDB may be
less reliable in studies of older
children.
It was not possible to relate the
severity of SDB to outcomes of
academic achievement due to the
array of SDB definitions used;
however, some previous studies
have failed to demonstrate a dose-
response relationship between
PSG-derived severity of SDB with
learning
53
and other functional
outcomes.
54–56
Habitual snoring has
been related to as many, or more,
behavior and executive function
problems as moderate to severe
OSA, and sometimes across multiple
domains.
11,57
In contrast, others
have shown a dose-response
relationship with behavior and
cognition.
58,59
Where PSG has been
used, these differences may reflect
the fact that signs of obstruction,
such as airflow limitation and effort
of breathing, may be seen without
overtevidenceofscorableapnea.
The apnea index alone may not
be optimal to assess these
relationships.
Multivariate statistical analyses
incorporating adjustments for
important covariates were used in the
majority of studies. However, 2 did not
state that they adjusted for covariates,
and 3 adjusted for only 1 or 2
variables, but the fact that academic
achievement was not the primary
outcome of all studies may provide
some explanation. Maternal education
is an important covariate to consider
because of the strong link with child
academic achievement.
60–62
Only 4
studies stated specifically that they
took maternal or parental education
into account. Four studies considered
BMI. Previous studies have found an
association between the combined
obesity/OSA condition and poorer
academic functioning.
63–66
Other
common covariates included age,
gender, socioeconomic status, and
behavioral factors. Failure to consider
important covariates, particularly
maternal education, could mean the
ES were overestimated in some
studies.
The neurobehavioral pathway(s)
linking SDB to deficits in academic
performance are unclear, but data
from our laboratory indicate that
the relationships are most likely
mediated through domains of
executive function and/or language
skills. Thus, in children 1 year into
schooling (age 6), the relationship
between SDB and poorer academic
performance was not direct, but
linked to reduced performance in
domains important for learning
outcomes.
67
Domains such as
verbal and nonverbal intelligence,
memory, and executive functioning
contribute to children’s learning-
related skills and behavior.
68
Adverse effects on these domains
could potentially underlie
associations between SDB and
academic performance.
The meta-analytic data from studies
in which children were identified as
having unsatisfactory academic
progress (Fig 4) yielded a significant
ES of –0.23, adding further
support to the evidence that SDB
is associated with deficits in
educational performance with
children performing below grade-
level expectations. There is also
evidence that substantial gains in
school grades can be made after
adenotonsillectomy in children
who have SDB and are struggling
FIGURE 4
Effects sizes and 95% CIs from the included studies of academic performance measures of un-
satisfactory progress comparing SDB to non‐SDB. Square represents the area proportional to the
weight assigned to the study; diamond represents the overall summary estimate for the analysis
(width of the diamond represents the 95% CI).
e942 GALLAND et al
by guest on November 14, 2016Downloaded from
academically.
69,70
In 1 longitudinal
study, a history of SDB or behavioral
sleep disorders in the first 5 years of
life significantly increased the
likelihood of children needing special
education at age 8, even after
controlling for many confounders.
71
These data highlight the need to
identify children with SDB who
perform poorly at school.
72
It is not
uncommon for SDB to go untreated
because SDB symptoms are
underreported by parents at general
practice visits,
73
and although the
condition may resolve with
increasing age as airway size
increases relative to the size of the
adenoids and tonsils,
74
it can also
persist into adolescence and
adulthood.
At present, studies demonstrating
results of intervention effectiveness
for treatment of SDB to improve
educational outcomes are limited to
a few studies. One before-after
treatment study of children (7–11
years) reported significant
improvements in writing, reading,
and math at follow-up (1 and 6
months postadenotonsillectomy),
with ES ranging from 0.25 to 0.34.
75
Another before-after treatment
studyof44childrenreports
a 76% resolution of low
school performance 9 months
posttreatment.
60
The only study
comparing cases with controls
reports significantly greater
improvements in case children on
academic achievement tests 1 year
posttreatment.
76
The first
randomized controlled trial of
adenotonsillectomy treatment of
OSA was recently published but
has not reported on academic
performance specifically.
56
Results
to date report mean neurocognitive
performance in the average
range at baseline but no statistically
significant improvements at
7-month follow-up, although
statistically significant improvements
in functioning in the school setting
were found on teacher ratings.
Possible explanations for this pattern
include sensitivity of measures to
detect functional impairment
56
or
reflect treatment outcome.
23,77
Longer-term follow-up trials are
needed to determine whether
improvements in school achievement
and cognitive function are detected
and sustained over time and thus
promote future success.
Although it could be argued that the
strength of the study is seen within
the replication of findings from many
studies and across several age
ranges and cultures, interpretation
of the reported ES is limited by
a lack of detail in the study designs
employed regarding SDB and
academic performance measures and
the failure of some studies to
control for important covariates.
Contributory factors to the
measurement issues identified
within the quality evaluation may be
a lack of consensus on what
measures should be used to define
school achievement and the milieu of
definitions for SDB. Not only is this
problematic in data synthesis, it
also affects educational and clinical
settings, limiting an understanding
of the nature of treatment effects
because cross-study comparisons
are made difficult. Further
limitations were evident within the
evaluation of the quality of the
reviewed studies, reflecting some
degree of measurement error, also
demonstrated within the moderate
to high heterogeneity of included
studies within most specific
domains. In addition, only a small
number of studies could be included
in some of the meta-analyses,
for example, only 2 studies for
science. With this small number
of studies, adequate power to
detect heterogeneity would be
compromised. It has been reported
that a median of 4 studies are
required before a meta-analysis for
an outcome in a systematic review
settles down around a final value to
get within 10% of the final point
estimate.
78
Finally, although our best
attempts to search the literature
rendered few studies with no
association between SDB and
academic performance, potential
publication bias also needs to be
considered given the possibility that
research with null findings may not
be reported in the literature.
CONCLUSIONS
According to the results of the
present meta-analysis, there is clear
evidence for poorer academic
performance in school-age children
with SDB. The ES is within the small
to medium range, but nevertheless
the findings serve to highlight to
parents, teachers, and clinicians
thatSDBinchildrenmaycontribute
to academic difficulties some
children face. In light of these
findings, screening for SDB should
be included in pediatric and
multidisciplinary assessments of
children’slearningdifficulties, with
appropriate medical follow-up as
indicated. Future research should
consider the neurobehavioral
pathways through which SDB may
exert its effects on academic
performance. However, more
appropriate and standardized tools
for assessing academic performance
across studies are required, and far
more research is needed on the
comparative effectiveness of
interventions targeting children
with SDB.
ACKNOWLEDGMENTS
We thank the valuable input of
research assistant Carmen Lobb
(C.L.) for database entry and
crosschecking final articles for the
study.
ABBREVIATIONS
CI: confidence interval
ES: effect size
OSA: obstructive sleep apnea
PSG: polysomnography
SDB: sleep-disordered breathing
PEDIATRICS Volume 136, number 4, October 2015 e943
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FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
FUNDING: No external funding.
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.
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