Effect of Breakfast Composition On Cognitive Performance - Systematic Review (2014)
Effect of Breakfast Composition On Cognitive Performance - Systematic Review (2014)
626 Am J Clin Nutr 2014;100:626–56. Printed in USA. Ó 2014 American Society for Nutrition
BREAKFAST AND COGNITIVE PERFORMANCE 627
alterations of the gastrointestinal tract and potentially modify the varied but generally considered breakfast as the first food or meal
neurohormonal milieu and, therefore, cognitive and academic consumed through the day, although some interventions did not
performance (7, 10–12). In particular, the macronutrient com- provide explicit control for previous intakes. Studies providing
position of the meal per se may be important with respect to a comparison of different breakfast types were included. Studies
both performance efficiency and mood: specific foods and nu- that compared breakfast and “no breakfast” options were ex-
trient combinations (eg, carbohydrate and protein) may influence cluded, unless when several breakfast treatments with specified
blood glucose and insulin concentrations, acting on brain neu- energy or composition were simultaneously available and were
rotransmitter synthesis (13). Similarly, the energy load of the compared one with the other. Studies were included regardless
breakfast meal alone is also likely to play a moderating role in of the content of the meal (eg, drinks or cereal bars). However,
the disposal of energy and neurotransmitter bioavailability, es- we excluded those studies in which breakfast interventions dif-
pecially in short-term mental processes (7). fered by the presence or absence of coffee only. Studies that
The aim of the current systematic review was to collect existing assessed the effects of glucose-based or emulsion-based ma-
evidence on the role of nutrient composition or energy intake at nipulations (including foam-like vanilla creams, gelatins re-
breakfast, in absolute or relative terms, on the accomplishment of sembling milkshakes in consistency, and spoonable creams) were
school-related tasks and cognition. Although there is still debate on excluded. Studies that considered intakes at other mealtimes were
the role of breakfast as a determinant or as a short-term indicator of excluded, except when there was a clear indication of the separate
cognitive performance, these issues may have important fallouts in effect of different breakfast options during the morning.
the definition of public health guidelines, maximizing the potential
benefits of breakfast consumption for the overall population, and in Outcome measures
the assessment of the nutritional, educational, and economic value
Studies referring to any standardized outcome measure of
of school breakfast programs already carried out in many de-
cognitive, academic (school grades and standardized achieve-
veloping and developed countries (14).
ment tests), and school (enrollment, attendance, achievement, in-
class behavior and behavior at school, and school dropout)
MATERIALS AND METHODS performance in general were included. Studies based on teachers’
subjective ratings of performance or that relied only on qualitative
Literature search strategy measures of cognitive performance were excluded. Studies that
We carried out a systematic search through MEDLINE via examined fatigue or physical endurance only were excluded.
PubMed (http://www.ncbi.nlm.nih.gov/pubmed/) to identify all Acute (= performance assessed within 12 h of breakfast con-
the articles on the relation between cognitive, academic, and sumption) and habitual effects of breakfast manipulations (typ-
school performance and breakfast composition and energy intake ically, through school breakfast programs) were included. When
published in English up to 22 November 2013 based on the available, we included the name of the performed test, together
following string (breakfast OR “breakfast composition” OR with the corresponding psychological construct assessed. Oth-
“daily meal distribution”) & (“energy intake” OR “energy erwise, we just indicated the specific neurocognitive construct.
contribution” OR “energy expenditure” OR quality OR energy
OR skipping OR “glycemic index”) & (“intellectual perfor- Exposure measures
mance” OR “neuro-performance” OR “mental performance”
Energy intake at breakfast. Studies providing quantitative es-
OR “cognitive performance” OR “academic performance” OR
timates of total energy intake at breakfast for different breakfast
“school performance” OR performance),” following the
treatments, including absolute intakes of total energy or percent-
guidelines from the Preferred Reporting Items for Systematic
ages of daily energy intake provided by breakfast, were included.
Reviews and Meta-Analyses (PRISMA) group (15). Two authors
Studies based on standardized breakfast options with a fixed
(VR and VE) independently selected the articles and retrieved
quantitative estimate of energy intake, were excluded. Survey
and assessed the potentially relevant ones. The reference lists of
studies showing specific dietary patterns of subpopulations of
the identified articles and of other systematic reviews focusing
interest (eg, subjects of a defined ethnic origin), were not included.
on similar topics were also scanned. Discrepancies in article
Information on energy intake at breakfast was consistently ex-
selection were resolved by involving a third researcher (CA).
pressed in kilocalories throughout the article.
Breakfast composition. Studies that provided quantitative es-
Inclusion and exclusion criteria timates of the macronutrient composition of different breakfast
Articles were included or excluded according to the following options were included. This included those breakfast meals stan-
criteria. dardized for energy supply. When the authors declared in the ar-
ticles that the available breakfast options were isoenergetic or
Participants similar in energy content, we reported this information in the
tables. When the difference in energy content between treatments
Studies of children and adolescents or adults of either sex were was .10% and there was the possibility to distinguish the energy
included. We excluded studies based on subjects with acquired content associated with each effect in the statistical models, we
metabolic disorders (such as hyperlipidemia or type 2 diabetes). included the corresponding article in the analysis concerning en-
ergy intake at breakfast. We excluded from the review all surveys
Breakfast definition describing the macronutrient composition of breakfast for selected
Breakfast was defined according to the descriptions of the subpopulations of interest. We also excluded those studies that
meals or foods consumed provided in the articles reviewed. These assessed the relation between cognition and the interaction
628 EDEFONTI ET AL
between macronutrient composition of the breakfast and glucose and $2 different breakfast meals, but with no available com-
tolerance, because there was no possibility to assess the separate parisons between alternative breakfast meals; other meals pro-
effect of breakfast composition. vided together with breakfast (eg, midmorning snack, evening
meal, lunch, or a combination of meals), with no possibility to
Association between exposure and outcome measures assess the individual contribution of energy or composition of
Studies providing information on any form of relation between each meal; breakfast options based on a combination of re-
cognitive and academic performance and breakfast composition quirements on energy intake and number of “healthy” nutrients
or energy intake at breakfast were included. This included results or foods consumed. Six additional articles were identified from
derived from different statistical approaches, including simpler manual searches of reference lists of selected original and re-
tests and CIs, correlation analysis, multiple regression models, and view articles. Thus, 15 articles, providing information on 15
multivariate repeated-measures ANOVA. We excluded studies different studies were included in our systematic review. Of
providing only histogram-like representations, with means and these, 3 studies provided information on the relation between
SDs (or SEs) superimposed, to distinguish the differential effect cognitive and academic performance and energy intake at
of the available breakfast meals. Finally, we chose not to exclude breakfast, 11 provided the same information for the macronu-
studies on the basis of their quality, because of their limited trient composition of breakfast, and 1 provided both aspects of
number and the huge variation in the adequacy of descriptions the problem (Figure 1).
provided. Experimental and observational studies on the effects of
breakfast on various performance variables are presented in
Tables 1 (16–19) and 2 (19–30). The main characteristics of the
Data extraction 4 selected studies describing the relation between energy intake
Quantitative and qualitative data were extracted from each of at breakfast and cognitive and academic performance are shown in
the studies selected for in-depth review by 2 independent re- Table 1. The corresponding articles were published between 1990
searchers (VR and VE); any discrepancies were resolved after and 2007; the studies were carried out in the United States (16) and
consultation with a third author (CA) to maintain consistency. in Europe, including Sweden and Denmark (17), Spain (18), and the
Information extracted included the following: 1) general char- United Kingdom (19). All 4 studies recruited children and ad-
acteristics of the studies (first author and year of publication of olescents of either sex from local schools, including suburban
the article, country, sponsorship, number and age of the partic- (16, 17) and urban (18) schools. Two articles (16, 19) provided
ipants, percentage of males and females, inclusion and exclusion details on the mean SES of the families attending those schools;
criteria, and study location); 2) design and characteristics of the 1 article (16) chose to limit variability by using a ninth grade
intervention and presence of any school program in support of it class from a school with a middle-class background, and the
(type of design, randomization, counterbalancing and crossover other (19) chose to include in the study schools from a range of
details, and when available the number of days of observation socioeconomic areas. Moreover, 2 articles defined strict in-
and schedule, information on the dinner the night before and on clusion criteria on age range and on the presence of chronic
explicitly stated overnight fast, and schedule of the breakfast); 3)
definition of breakfast: list of the available breakfast options and
corresponding details on absolute and relative values of energy
intake and on the macronutrient composition of the different
treatment options; 4) definition of the outcome according to the
different standardized tests used in the article and information
on how and when performance was assessed with respect to
breakfast (in the standardized time unit of minutes); and 5) main
results on the association between breakfast characteristics and
cognitive and academic performance (corresponding to those
statistical models adjusted for all the available confounders, if
models were fitted).
RESULTS
From the literature search of PubMed database, we identified
102 articles, of which 83 remained when we limited our search to
humans and to the English language. Their full texts were re-
trieved for detailed evaluation. After the exclusion of 12 review
articles, 62 original research articles were also excluded because
they met the exclusion criteria indicated previously. In detail, the
most frequent reasons for exclusion were as follows: absence of
information about cognitive and academic performance and/or
breakfast; information on consumption or frequency of breakfast,
without extra details on energy intake or macronutrient com-
position of the available breakfast options; a fixed estimate of FIGURE 1. Flowchart of the study selection process for the systematic
energy intake; several breakfast options, including no breakfast review. PubMed, http://www.ncbi.nlm.nih.gov/pubmed/.
TABLE 1
Studies that evaluated the effect of energy intake at breakfast on cognitive/academic performance in different settings1
Reference Design and
(sponsorship: intervention (school Definition of the Measure of the
yes or no) Study subjects program: yes or no) Definition of breakfast outcome outcome Results Comments
Cromer et al, 1990 n = 34 Independent groups 424 kcal (government 1) Rey auditory- Tested at 60 and 240 No significant Preliminary Peabody
(16) school BF, n = 18) verbal learning test min after BF differences of BF picture vocabulary
(verbal learning options on the test revised to
and immediate measures exclude subjects
memory) considered (no with IQ ,85
Bonferroni
correction)
USA Mean: 14 6 0.4 y Overnight fast 12 kcal (low-calorie 2) Matching familiar Assessment of Tanner
BF, n = 16) figures test pubertal staging, of
(impulsivity) Hollingshead
measure of SES:
groups were fairly
similar according to
these aspects
No 41% M, 59% F BF at 0700 3) Continuous Quantification of
performance test usual BF in terms of
(sustained attention number of days per
and impulsivity) week and content
No chronic diseases, Yes Statistical analysis:
nonintellectual chi-square test of
compromised independence,
correlation analysis,
repeated-measures
ANOVA
Ninth-grade class,
suburban middle-
class background
school
Metabolic ward in
BREAKFAST AND COGNITIVE PERFORMANCE
research laboratory
Wyon et al, 1997 (17) n = 195 Independent groups: .20% daily EI or 1) Addition (math) Tested in two 40-min Reduced EI at BF was Statistical analysis:
2 standardized BF 5362/4342 kcal for lessons before significantly and chi-square test of
options with high- M and F, lunch negatively independence,
(A) or low- (B) respectively (A) associated with correlation analysis,
energy within each creativity thinking Mann-Whitney test,
sex group for 4 d C-score among M no statistical
from Tuesday to but not among F models, and no
Friday (ABAB or adjustment
AABA) variables
Sweden and 10 y Return of uneaten BF ,10% daily EI or 2) Multiplication Other tests were not No information on
Denmark food for each day 1702/1212 kcal for (math) significant habitual BF
M and F,
respectively (B)
(Continued)
629
630
TABLE 1 (Continued )
United Kingdom 6–11 y (3 age groups) Overnight fast Low-GI BF: All Bran Tests for the other No information on
(35 g) (98 kcal and domains were not habitual BF
42 GI; plus 125 mL significant
semiskimmed milk)
No Mean: 9 y BF at 0930
41% M, 59% F No
Schools from different
SES areas
School setting
1
Coco Pops and All Bran manufactured by Kellogg’s. BF, breakfast; EI, energy intake; GI, glycemic index; IQ, intelligence quotient; SES, socioeconomic status.
2
Mean intakes for each treatment option and sex.
631
632
TABLE 2
Studies evaluating the effect of breakfast composition on cognitive and academic performance in different settings1
Reference Design and
(sponsorship: intervention (school Measurements of the
yes or no) Study subjects program: yes or no) Definition of breakfast Definition of outcome outcome Results Comments
Lloyd et al, 1996 (20) n = 16 Crossover with Low-fat, high-CHO 4 computer-based tasks: Tested in 4 sessions at No significant Similar protein
counterbalancing, (600 kcal, 98.7 g 230 min before BF difference in content provided by
same day on CHO, 15.2 g P, and 30, 90, and 150 performance among any BF treatment
4 consecutive 18.4 g fat) min after BF BF conditions,
weeks, plus excluding no BF
a familiarization
session
United Kingdom Mean: 26 6 0.4 y Self-selected similar Medium-fat, medium- 1) Bakan task (visual No significant Statistical analysis:
dinner on each CHO (601 kcal, information interaction effect of repeated-measures
occasion 74.8 g CHO, 13.8 g processing) time and BF ANOVA
P, 29.3 g fat) conditions (assessment time 3
treatment 3
order of BF
consumption)
(No) 12% M, 88% F Overnight fast High-fat, low-CHO 2) 2-finger tapping (motor Low-fat, high-CHO
(608 kcal, 56.2 g speed) BF similar in
CHO, 14.5 g P, macronutrient
38.5 g fat) composition to the
isoenergetic BF habitual BF of the
subjects, but
definitely higher in
energy content
EDEFONTI ET AL
United Kingdom Mean: 21 y Overnight fast 50 g high-RAG (diet A high-SAG BF Statistical analysis:
2) (219.5 kcal, 31.3 significantly 3-factor ANOVA
g CHO, 3.65 g P, improved on the (treatment 3
8.85 g fat, 65.9 GI, number of abstract assessment time 3
0.05 SAG, 21.15 words recalled immediate/delayed
RAG) throughout the recall) with
morning repeated measures
on the last 2 factors
(No) 100% F BF at 0900 Because there was no
interaction with
immediate/delayed
recall factor,
immediate and
delayed scores were
summed to get
a global score
80% habitual BF (No) No quantification of
eaters habitual BF
Research laboratory
Benton and Nabb, n = 323 Independent groups 50 g high-SAG (230 1) Free word recall Tested at 30, 90, 150, A high-SAG BF Partly overlap with
2004 (22) kcal, 34.0 g CHO, (immediate and 210, 270, 330, and significantly Benton et al 2003
3.3 g P, 8.8 g fat, 42 delayed memory) 390 min after BF improved on the (21)
GI, 7.9 SAG, 18.8 number of words
RAG) recalled, as
compared with the
high-RAG BF, at
210 min after BF
(significant
BREAKFAST AND COGNITIVE PERFORMANCE
treatment 3
assessment time
interaction)
United Kingdom 3 studies combined Overnight fast 50 g high-RAG 2) Simple and choice No significant The 2 BF meals
(Choco Krispies: reaction times differences between offered an identical
219 kcal, 34.0 g SAG and RAG BF weight of CHO, but
CHO, 4.9 g P, 7.3 g for the other tasks different amounts
fat, 66 GI, 0.05 of RAG and SAG
SAG, 21.1 RAG; or
Coco Pops: 220
kcal, 34.0 g CHO,
3.9 g P, 8.3 g fat,
0.4 SAG, 21.6
RAG) BF
(Continued)
633
TABLE 2 (Continued ) 634
(Yes: in part by Mean: 20 y BF time not provided No BF 3) Sustained attention The high-RAG BF
Danone Vitapole) was obtained with
Coco Pops in study
2 and Choco
Krispies in study 3,
but the RAG and
SAG contents were
very similar
100% F 100% compliance in The primary aim of
consuming all food the article was to
on plates study the
interaction between
different BF
treatments and
alcohol consumed
with the previous
dinner and lunch;
here, we reported
results on the effect
of BF meals during
the morning for the
no-alcohol-intake
EDEFONTI ET AL
group
Healthy, no history of (No) Statistical analysis: 4-
gastrointestinal factor ANOVA
problems, BMI of (treatment 3
20 to 25 kg/m2 alcohol at dinner 3
assessment time 3
immediate/delayed
recall) with
repeated measures
on the last 2
factors; because
there was no
interaction with
immediate/delayed
recall factor,
immediate and
delayed scores
were summed to
get a global score
Recruitment with No information on
response to a poster habitual BF
Research laboratory
(Continued)
TABLE 2 (Continued )
Mahoney et al, 2005 n = 60 Counterbalanced High-GI: ready-to-eat 6 constructs: Tested 60 min after BF Experiment 1: The 2 BFs provided
(23)2 randomized cereal (36 g) and in weeks 1, 2, and 3 approximately
crossover, same day 125 mL skim milk and 215 min equal amounts of
on 4 consecutive (200 kcal, 36 g before BF in weeks fat, sugar, and EI
weeks CHO, 5 g P, 1.5 g 2, 3, and 4 for the but different
fat, 1 g fiber, long-term memory amounts of fiber
22 g sugars) assessment and protein
USA Experiment 1: n = 30 Overnight fast Low-GI: oatmeal (43 1) Spatial memory A low-GI BF Statistical analysis:
g) and 125 mL skim significantly repeated measures
milk (200 kcal, 38 g improved short- ANOVA including
CHO, 8 g P, 2 g fat, term memory, in F treatment as
3 g fiber, 19 g only, in the a repeated measure
sugars) isoenergetic backward digit span and sex
BF task (significant
treatment 3 sex
interaction), as
compared with the
high-GI BF
(No) 9–11 y BF at 0815–0830 No BF 2) Backward and forward No difference for Quantification of
digit span tasks (short- forward digit span usual BF by using
term memory) task short surveys on
how often children
consumed BF
before school,
quality of their
normal BF, and
their opinions on
the BF meals used
BREAKFAST AND COGNITIVE PERFORMANCE
in the study
Experiment 2: n = 30 (No) 3) Rey complex figure No significant
copy and recall test at differences between
20 and 50 min high- and low-GI
(immediate and BFs for the other
delayed visual tasks, regardless of
perception) the different
dependent
measures and
indexes included
4) Visual sustained Experiment 2:
attention
(Continued)
635
636
TABLE 2 (Continued )
Ingwersen et al, 2007 n = 64 Repeated measures (A) High-GI: Coco Cognitive drug research Tested in 2 sessions at The decrease over No control for GL,
(19) counterbalanced Pops (35 g) (133 computerized 230 min before BF morning time can different
kcal and 77 GI; assessment battery and 10, 70, and 130 be significantly macronutrient
plus 125 mL assessing 5 constructs: min after BF reduced after the composition of the
semiskimmed milk) intake of a low-GI BF treatments
BF, as compared
with a high-GI BF,
for accuracy of
attention and
secondary memory
United Kingdom 6–11 y (3 age groups) 3 assessments on (B) Low-GI: All Bran 1) Speed of attention Tests for the other Statistical analysis: 3-
consecutive days (35 g) (98 kcal and domains were not factor mixed
(familiarization 42 GI; plus 125 mL significant ANOVA
session + 2 testing semiskimmed milk) (assessment time 3
sessions) treatment 3 sex)
with repeated
measures on the
first 2 factors,
Bonferroni
adjustment for
pairwise
comparisons
(No) Mean: 9 y Overnight fast 2) Speed of memory No information on
habitual BF
41% M, 59% F BF at 0930 3) Accuracy of attention
Schools from different (No) 4) Secondary memory
SES areas
School setting 5) Working memory on 9
BREAKFAST AND COGNITIVE PERFORMANCE
tasks (immediate/
delayed word
recognition,
immediate/delayed
word recall, simple/
choice reaction time,
digit vigilance, spatial/
numeric working
memory) (sustained
attention and memory)
(Continued)
637
638
TABLE 2 (Continued )
Benton et al, 2007 n = 19 Unbalanced repeated High-GL (196 kcal, 1) Classroom behavior in Tested in 2 sessions at ANOVA: significant Assessment of SES
(24) measures: 3 BF 33.9 g CHO, 4.7 g P, 3 time blocks of 10 min 180 min after BF interaction effect of through Welsh
meals designed to 1.7 g fat, 17.9 GL) treatment 3 time index of multiple
be isoenergetic for head down deprivation: groups
working; in the first were fairly similar
10 min spent doing according to SES
their schoolwork,
eating the low-GL
meal significantly
increased time
spent on task as
compared with the
medium- or high-
GL meal
United Kingdom 5–7 y Each day in a 4-wk Medium-GL (168 2) Recall of objects test of No significant effects No control for GI,
program; 1 BF kcal, 21.7 g CHO, the British ability scale on immediate/ different
provided at random 8.9 g P, 5.2 g fat, for memory (verbal/ delayed memory or macronutrient
to all children 12.1 GL) spatial, immediate/ attention composition of the
delayed memory in BF treatments
their combinations,
EDEFONTI ET AL
Australia 14–17 y Overnight fast Low-GI: All Bran A high-GI BF Statistical analysis:
(30 g, 30 GI) significantly Student’s t test,
and 125 mL improved the ANOVA with
semiskimmed milk number of items assessment time/
(158 kcal, remembered, as delay, treatment
20.5 g CHO, 8.8 g P, compared with the and treatment 3
2.8 g fat) (almost) low-GI BF, at the assessment time/
iso-energetic BF5 long delay only, for delay interaction;
the remembering/ details were not
forgetting indexes provided, post hoc t
(significant tests
treatment 3
assessment time/
delay interaction
effect)
(No) Mean: w16 y BF at 0830 No significant Quantification of
difference between usual BF in terms of
high- and low-GI average number of
BFs in the raw days per week BF
memory retention skipped
scores for free or
cued recall phases
EDEFONTI ET AL
United Kingdom 11–14 y Overnight fast High-GL, high-GI 2) Immediate word recall A low-GI and a high- 2-step BF: anything
(378.7 kcal, 65.2 g task GL BF significantly eaten or drunk on
CHO, 12.6 g P, 9.3 g improved speed of the way to school or
fat) information since arriving at
processing school (“snack”)
(significant GI and was considered if it
GL effects) and contributed .10 g
Serial Sevens task CHO; however, the
(significant GI and covariate “having
GL main effect and a snack” was
interaction) unrelated to the
cognitive domains
(No) Mean: w13 y BF at 0815 Low-GL, low-GI (272 3) Stroop selective A high-GL BF The BF meals differed
kcal, 34.5 g CHO, attention task significantly in energy content,
10.2 g P, 11.3 g fat) improved the % energy from fat
matrixes task and CHO but not
(significant GL from protein
effect)
40% M, 60% F (No) Low-GL, high-GI 4) Matrixes (inductive Tests for the other However, the 2 low-
(240.3 kcal, 35.4 g reasoning) domains were not GL BFs had similar
CHO, 9.7 g P, 7.7 g significant energy contents,
fat) BF and the 32%
difference in energy
between the 2 high-
GL BFs was not
significant
Habitual BF eaters 5) Number search task Statistical analysis:
BREAKFAST AND COGNITIVE PERFORMANCE
performance in
lower-SES groups;
significant GL 3
sex and GI 3 sex
interactions in
matrixes and speed
of information
processing,
respectively
Micha et al, 2011 (27) n = 64 (32 matched Balanced, High-GL, low-GI 1) Word-generation task Tested in 2 sessions at No. of words of the Pilot study to assess
pairs) randomized, (470 kcal, 86.6 g (verbal fluency) 90 min after BF by word-generation the validity of the
crossover CHO, 13.9 g P, using 2 versions of task increased cognitive test on
7.1 g fat, 41 GL, the same test significantly after a comparable
48 GI) battery the intake of a low- population
GI BF (significant
GI effect)
(Continued)
TABLE 2 (Continued )
United Kingdom 11–14 y Each pair given by High-GL, high-GI 2) Immediate word recall Number search task Within the same GL
a high-GL and low- (469 kcal, 90.4 g task and Serial Sevens group, high- and
GL group child CHO, 14.0 g P, 5.3 g task showed low-GI BFs had
fat, 55 GL, 61 GI) a significantly similar energy and
better performance macronutrient
in the high-GI BF compositions,
group (significant separating any GI
GI effect) effects from
potential EI and
macronutrient
content differences
(Yes: in part by Mean: w13 y Within each GL Low-GL, low-GI (281 3) Stroop selective Time of completion in Statistical analysis:
School Food group, children kcal, 43.2 g CHO, attention task Stroop task was repeated-measures
Trust) were given a high- 12.5 g P, 6.4 g fat, significantly lower ANOVA including
GI and a low-GI BF 21 GL, 48 GI) in the high-GL, GI and GL as main
high-GI BF effects and
(significant GI and adjustment for age,
GL interaction sex, order of BF
effect) consumption,
height, weight,
BMI, mood, and
glucose and cortisol
concentrations at
baseline
% of M and F not 3 assessments Low-GL, high-GI 4) Matrixes (inductive Tests for the other No quantification of
provided (screening + 2 (276 kcal, 45.2 g reasoning) domains were not habitual BF
testing sessions CHO, 12.0 g P, 5.1 g significant
2 wk apart) fat, 28 GL, 61 GI)
BF
BREAKFAST AND COGNITIVE PERFORMANCE
TABLE 2 (Continued )
United Kingdom 12–14 y 4 separate morning Low-GI (for a 50-kg 2) Sternberg paradigm for A low-GI BF The high- and low-GI
assessments participant: 420 kcal, working memory (3 significantly BFs contained 1.5 g
7 d apart 75.0 g CHO, 15.5 g P, levels with different improved accuracy available CHO/kg
(familiarization 6.4 g fat, 36 GL, memory loads) in the Stroop body mass and
session + 3 testing 48 GI) isoenergetic selective attention were matched for
sessions) task, as compared EI, protein, and fat
with a high-GI BF, contents
overall (significant
treatment effect)
and across the
morning
(significant
treatment 3
assessment time
interaction effect)
645
(Continued)
646
TABLE 2 (Continued )
(No) Mean: w13 y Self-selected similar No BF 3) Flanker selective A low-GI BF The 2 BF meals
dinner on each attention task significantly provided a fixed
occasion (congruent and improved on available CHO
incongruent levels) response times in content
Sternberg paradigm
of working memory
across the morning,
as compared with
a high-GI BF
(significant
treatment 3
assessment time
interaction effect)
44% M, 56% F Overnight fast Response times on the Statistical analysis:
Stroop test were linear mixed-effects
quicker overall with models, with a
EDEFONTI ET AL
Nilsson et al, 2012 n = 40 Balanced randomized High-GI or WWB 2 constructs: Tested in 2 sessions at G-WWB significantly Statistical analysis: 2-
(30)2 crossover, 3 (124 g white-wheat 90, 135, 180, and improved selective factor repeated-
assessments flour-based bread, 225 min after BF attention (correct measures ANOVAs
(familiarization 100 GI) for working responses) at the different
session + 2 testing memory (2 separate compared with assessment times
sessions) sessions of 4 WWB BF at 120 (order of BF
subsets given in 2 min for the overall consumption 3
different orders) test (significant treatment),
and at 75, 120, 165, time 3 treatment correlation analysis
and 210 min after interaction) and,
BF for selective over the entire test
attention period (75–225
min), when only
the last half of the
test (most
demanding part)
was considered
(significant
treatment effect)
Sweden 49–71 y Standardized dinner Low-GI or G-WWB 1) Working memory with A significant No information on
on each occasion BF (179 g white- 8 different tests, of improvement in habitual BF
wheat flour-based which 4 performed on selective attention
bread plus guar each day (correct responses)
gum, 45 GI) was observed along
BREAKFAST AND COGNITIVE PERFORMANCE
TABLE 2 (Continued )
normal fasting
blood glucose
concentrations
Research laboratory
1
Coco Pops, All Bran, Choco Krispies, and Cornflakes manufactured by Kellogg’s. BF, breakfast; CHO, carbohydrate; EI, energy intake; G-WWB, guar gum–enriched white-wheat bread; GI, glycemic
index; GL, glycemic load; P, protein; RAG, rapidly available glucose; SAG, slowly available glucose; SES, socioeconomic status; WWB, white-wheat bread.
2
The tasks were expressed in terms of both response or reaction times and accuracy (proportion, number of correct responses, or response rates).
3
Actual mean intakes for each treatment option.
4
The tasks were expressed in terms of both raw memory retention scores and derived remembering/forgetting indexes, calculated to control for individual differences in the total items recalled in the
previous recall phase.
5
The GI values provided in the article refer to the cereal intake only, whereas the other information refers to the complete BF meal.
BREAKFAST AND COGNITIVE PERFORMANCE 649
diseases or intellectual difficulties and dietary issues for the Eight studies were conducted among children (19, 23, 24, 26–
included subjects (16, 17), whereas the other 2 (18, 19) did not. 28) and adolescents (25, 29) recruited in schools or through
Three studies were based on an experimental design; two of public advertisement, whereas the remaining 4 included adults
them (16, 17) showed an independent group design (subjects of different mean ages [w20 (21, 22), 26 (20), and 63 (30) y,
were assigned at random to one breakfast option only) and the respectively], which were examined in research laboratories.
other provided repeated measures (subjects received each The size of the study populations was limited, and studies were
breakfast option) (19). One study (17) was designed to alter the of short duration (,1 mo). Selected studies examined pre-
child’s breakfast regimen at home. dominantly healthy, mixed-sex populations from general edu-
Absolute values of breakfast energy intake varied from 12 cation. Four studies reported information on SES: some of them
(low-calorie breakfast) (16) to 536 kcal (mean value representing recruited children from low- (24) or middle- (23) SES families
.20% of the recommended daily energy intake, for boys only) and another one recruited children from schools of different SES
(17). The ratio of breakfast to the overall daily energy intake was (19). One study adjusted the statistical models for SES (26).
tested as ,10% compared with .20% (17), or as ,20% com- Most studies were based on repeated-measures designs, and 6
pared with $20% (18), with values of w20% a priori indicating studies explicitly stated that a crossover design was used (20, 23,
adequate breakfasts. 27–30), of which 4 specified randomization of subjects to the
As for performance measures, one article assessed the effect of different treatment options. Seven of the selected studies con-
breakfast on academic performance using the Spanish version of sidered isoenergetic breakfast options and provided a control
a standard achievement test, the Scholastic Aptitude Test, and over actual breakfast consumption, either checking that all food
provided details on the overall test score and on single domains of on the plates was consumed or recording percentages of uneaten
verbal, reasoning, and calculation abilities (18). The remaining food (20, 22–25, 27, 28). Two studies were designed to assess
articles considered different aspects of cognitive performance, the effects of isoenergetic breakfast options but did not explicitly
referring to different tests. Overall, 2 studies assessed the effect of provide information on actual breakfast consumption of the
breakfast on attention and memory (16, 19) and the other 2 subjects (21, 29). The remaining studies did not provide iso-
studies (17, 18) focused on math and reasoning abilities; a third energetic breakfast options of different composition (19, 26) or
pair of studies was on verbal learning (16, 18). Two articles did not specify the energy content of the different breakfast
focused also on creativity (17) and impulsivity (16). treatments (30). By design, available breakfast options included
A higher value of breakfast energy intake significantly im- meals with a different fat and carbohydrate content (20), with
proved creativity among boys only (mean: 536 kcal compared a different GI (19, 21, 25, 30) or glycemic load (GL) (24), with
with 170 kcal, within this subgroup) (17). A lower value of w100 a different GI and a fixed available carbohydrate content (22, 23,
kcal (compared with 133 kcal) allowed a limit of the natural 29), with different combinations of GI and GL (26, 27), or with
decline of cognitive performance over time for accuracy (but not different combinations of GL and dairy products (28). [Carbo-
speed) of attention and secondary (but not speed of) memory, hydrate foods that are consumed in isoglucidic amounts produce
although this effect may have been mainly driven by the dif- different glycemic and insulinemic responses depending on the
ferent values of glycemic index (GI) provided by the treatment nature of the food (ie, ratio of amylose to amylopectin) and
options under comparison (19). Moreover, in a different article type and extent of food processing. The GI is a component-
from the United States, no significant differences in verbal referenced index able to capture the qualitative difference in the
learning/immediate memory, impulsivity, and sustained atten- carbohydrate content of foods. The GL is derived from GI as
tion were found between 2 breakfast options of w10 and 400 GI 3 carbohydrate intake; therefore, it is a measure of both the
kcal, respectively (16). Concerning percentages of daily energy quality and quantity of the carbohydrates and represents a mea-
intake, a breakfast providing .20% of daily energy intake im- sure of the dietary insulin demand (31).]
proved creativity significantly, but not math and logical and As for cognitive and academic performance, domains under
associate thinking, in a subgroup of boys (17). Similarly, in the investigation included short-term (primary), long-term (sec-
Scholastic Aptitude Test, the overall test score (measuring ver- ondary), immediate/delayed, verbal/spatial, and working mem-
bal, reasoning and calculation abilities) and logical reasoning ory (19–30); visual/auditory selective and sustained attention
scores were significantly higher for subjects consuming $20% (19, 22–24, 26–30); related reaction time, speed of processing,
of daily energy intake, after adjustment for age, sex, and school visual information processing, perceptual speed, inspection
(18). Finally, 2 of the selected studies were sponsored in whole time, and motor speed (20, 22, 26–28); verbal fluency (26, 27);
(18) or in part (17) by industry. and inductive reasoning (26, 27). Corresponding tests varied
The main characteristics of the 12 selected studies describing greatly across studies, and number and schedule of test sessions
the relation between macronutrient composition of breakfast and varied also, with studies testing subjects either before and after
cognitive and academic performance are shown in Table 2. The breakfast (19, 20, 23, 28) or after breakfast only; the number of
articles were published between 1996 and 2012, and the studies sessions per day ranged from 1 to 7 and had a maximum time
were carried out in Europe (19–22, 24, 26, 27, 29, 30)—mainly interval between breakfast and the last test performed that
in the United Kingdom (19–22, 24, 26, 27, 29)—the United ranged from 60 to 390 min.
States (23) and Australia (25, 28). A few studies were carried Memory ability was significantly sensitive, to various degrees,
out by the same groups of researchers (21, 22, 24, 26, 27); one to different breakfast compositions in 9 studies (19, 21–27, 29).
study (21) is indicated as study 1 in a more recent publication In detail, in 2 articles from the United Kingdom, a high slowly
with an extended data collection and a different research ques- available glucose or low-GI breakfast enhanced the number of
tion (22) and another study (26) was a pilot cross-sectional study words recalled of a combined score of immediate and delayed
of a more recent randomized controlled trial (27). memory in young female adults later in the morning, as compared
650 EDEFONTI ET AL
with a high rapidly available glucose (or high-GI) meal (21, 22). In emerged for the number of false alarms or the reaction times for
another article from the same research group, no immediate/de- the same task or for visual sustained attention (23). Moreover,
layed or verbal/spatial combined memory effect emerged for a study from UK showed that children who had consumed a low-
breakfast treatments with a different GL from an ANOVA analy- GL breakfast (as compared with a medium- or high-GL break-
sis, but an extra correlation analysis showed a significant im- fast) had significantly increased time spent on task in the first 10
provement effect of a lower-GL breakfast in children for min of school work and were less likely to display lapses in
immediate (but not delayed) verbal memory (24). Moreover, as attention for the ability to sustain attention when a 12-s delay
compared with a high-GI breakfast, a low-GI breakfast signifi- was tested for a second time (24). In 2 studies from the same
cantly improved short-term memory, among girls only, in the research group (26, 27), the time of completion in the Stroop
backward digit span task, but no corresponding difference was selective attention task was significantly lower in the high-GL/
found in the forward digit span task, or for spatial memory and high-GI breakfast for the latter article (27), but was not different
immediate/delayed visual perception (23). for the former one (26); the number search task for speed of
In the pair of studies from the United Kingdom investigating information processing/selective attention was better with a low-
the effect of both GI and GL, a high-GI breakfast significantly GI or a high-GL breakfast in the former article (26), but im-
improved immediate (but not delayed) word recall (26), although proved for a high-GI breakfast only in the latter article (27).
results from the immediate and delayed word recall tasks were Finally, 2 articles investigated explicitly selective attention in
nonsignificant in the more recent study (27). In the Serial Sevens terms of both the number/proportion of correct responses and
task used in both articles, working memory was significantly reaction or response times (29, 30). The article from Sweden
better in the high-GL/low-GI breakfast option, with significant GI (30) showed that a low-GI breakfast significantly improved ac-
and GL main effects and interaction (26), or in the high-GI curacy, compared with a high-GI breakfast, over the 75–225-min
breakfast option only (27). In another article from the United test period, when only the most demanding part of the test was
Kingdom, both accuracy and response times to the Sternberg test considered, or during the second day of testing. However, no
assessing working memory were improved across morning after significant difference depending on breakfast was observed in
a low-GI breakfast, although for accuracy this was only evident reaction times for selective attention (30). Similarly, the article
on the more complex test level (29). from the United Kingdom showed that accuracy in the Stroop
Concerning memory under conditions of divided attention, and Flanker tests improved across the morning after a low-GI
although no significant differences emerged between the high- breakfast, as compared with a high-GI breakfast. For the Flanker
and low-GI breakfast meals in the raw memory retention scores test, this was only evident on the more complex test levels;
for free or cued recall phases at the short or long delay, a high-GI however, for the Stroop test, this was also evident overall (29).
breakfast significantly improved the number of items re- Response times were nonsignificant for the Flanker test, but
membered, at the long delay, for an extra analysis based on the improved overall with a high-GI breakfast in the Stroop test
remembering/forgetting indexes, which took into account in- (29).
dividual differences in the total items recalled in the previous Moreover, the number of words of the word-generation task for
recall phase (25). assessing verbal fluency increased significantly after the intake of
Concerning long-term memory, in an article from Sweden and a low-GI breakfast in 1 (27) of the 2 articles assessing this do-
Denmark, the natural decline in secondary memory (as measured main, but not in the other (26).
by a composite score) of children over time was significantly Overall, data were less supportive for the effects of breakfast
reduced after the intake of a low-GI breakfast, as compared with composition on other cognitive variables, such as inductive
a high-GI breakfast (19), although the same was not true in an reasoning, speed of processing, visual information processing,
article from the United States for the long-term recall of material perceptual speed, motor speed, and reaction time (here intended
previously learned during the spatial memory, visual perception, as a direct measure and not as a proxy for a more complex
and verbal memory tasks (23). cognitive function such as attention). Finally, 4 selected studies
On the opposite side, no significant effect was detected for free were sponsored in part (22, 24, 27, 28) by industry.
word recall and all breakfast options differing in fat and car- A summary of the findings on the relation between the amount
bohydrate contents (20), for speed of memory and working of energy intake at breakfast, breakfast composition, and cog-
memory and breakfast options with a different GI (19, 30), and nitive and academic performance—grouped by broad cognitive
for short-term or working memory and different breakfast modality (row) and research question (column)—is shown in
combinations of GL and dairy products (28). Table 3. Specific domains of interest are reported in separate
Attention was influenced by different breakfast compositions rows, including also for reference the original terms provided in
in 7 articles (19, 23, 24, 26, 27, 29, 30), whereas only 2 showed the corresponding articles. Significant and nonsignificant results
nonsignificant results concerning sustained attention and dif- are reported in separate columns. In the following, we comment
ferent slowly available glucose or rapidly available glucose only on the constructs that were investigated in terms of both
breakfast meals (22), and attention switching and different amount of energy intake and composition in the selected arti-
breakfast combinations of GL and dairy products (28). In detail, cles. For the remaining constructs, we refer the reader to the
a low-GI breakfast could reduce the natural decrease in accuracy comments to Tables 1 and 2. With the exception of the combined
of sustained attention of children over time, although the same score of immediate and delayed memory (21, 22), this construct
was not true for speed of attention (19). Similarly, a low-GI was only partially affected by different amounts of energy intake
breakfast significantly improved the number of hits or misses of at breakfast or breakfast composition. Nonsignificant results
an auditory sustained attention test in 6–8-y-old children (but not were equally distributed between long-term (secondary) (23)
in 9–11 y old children), although no significant differences and working memory (19, 28, 30), whereas they were the
TABLE 3
Summary of findings on the relation between amount of energy intake at breakfast/breakfast composition and cognitive and academic performance, grouped by cognitive domain (row) and research question
(column)1
Amount of energy intake at breakfast Breakfast composition
Cognitive and
academic modality Significant effect Nonsignificant effect Significant effect Nonsignificant effect
Memory
Short-term and working memory
Verbal short-term memory [short- 424- compared with 12-kcal Better with low-GL BF under Different fat/CHO BF and no
term (primary) memory, BF (16) certain conditions (24) BF (20)
immediate verbal memory,
immediate word recall,
(immediate) free word recall]2
Better with low-GI BF under certain Different GL/GI BF (27)
conditions (23)
Better with high-GI BF, but Different GL/dairy products
nonsignificant GI and GL BF (28)
interaction (26)
Different GI BF and no BF (23)
Verbal short-term memory with Different GI BF (25)
secondary motor task3
Visuospatial short-term memory Different GL BF (24)
(immediate spatial memory)
Different GI BF and no BF (23)4
Working memory 100- compared with 133-kcal Better with high-GI BF, but Different GI BF (19)
BF (19) nonsignificant GI and GL
interaction (27)
Better with low-GI BF under Different GI BF (30)5
certain conditions (29)5
Better with low-GI, with high-GL BF, Different GL/dairy products BF (28)
and with high-GL/low-GI BF (26)
BREAKFAST AND COGNITIVE PERFORMANCE
Delayed memory
Verbal delayed memory Different GL BF (24)
(delayed word recall)
Different GL/GI BF (27)
Better with high-GI BF with Different GI BF with raw memory
remembering/forgetting indexes retention scores (25)3
under certain conditions (25)3
Different GL/GI BF (26)
Visuospatial delayed memory Different GL BF (24)
(delayed spatial memory)
Different GI BF and no BF (23)4
(Continued)
651
652
TABLE 3 (Continued )
DISCUSSION
breakfast interventions that differ in a single nutrient component, 18. López-Sobaler AM, Ortega RM, Quintas ME, Navia B, Requejo AM.
when possible, to provide more effective and sound messages of Relationship between habitual breakfast and intellectual performance
(logical reasoning) in well-nourished schoolchildren of Madrid
public health. (Spain). Eur J Clin Nutr 2003;57(suppl 1):S49–53.
19. Ingwersen J, Defeyter MA, Kennedy DO, Wesnes KA, Scholey AB. A
The authors’ responsibilities were as follows—VE: wrote the entire man-
low glycaemic index breakfast cereal preferentially prevents children’s
uscript, refined Tables 1 and 2, and prepared Table 3; VE and VR: collected
cognitive performance from declining throughout the morning. Appe-
the existing literature and selected the included articles with the supervision tite 2007;49:240–4.
of CA; VR: prepared the first draft of Tables 1 and 2; MF and AD: provided 20. Lloyd HM, Rogers PJ, Hedderley DI, Walker AF. Acute effects on
useful suggestions to summarize details on design and statistical analysis of mood and cognitive performance of breakfasts differing in fat and
the included studies; MP and GN: provided useful suggestions to summarize carbohydrate content. Appetite 1996;27:151–64.
details on the available breakfast options and contributed to the Discussion 21. Benton D, Ruffin MP, Lassel T, Nabb S, Messaoudi M, Vinoy S, Desor
section; LF and EF: provided useful suggestions to summarize details on the D, Lang V. The delivery rate of dietary carbohydrates affects cognitive
study design; and CA: conceived the systematic review. All authors read and performance in both rats and humans. Psychopharmacology (Berl)
approved the final version of the manuscript. The authors declared that they had 2003;166:86–90.
no conflicts of interest. The Italian Association for Cancer Research had no role 22. Benton D, Nabb S. Breakfasts that release glucose at different speeds
interact with previous alcohol intake to influence cognition and mood
in the design, implementation, analysis, and interpretation of the data.
before and after lunch. Behav Neurosci 2004;118:936–43.
23. Mahoney CR, Taylor HA, Kanarek RB, Samuel P. Effect of breakfast
composition on cognitive processes in elementary school children.
Physiol Behav 2005;85:635–45.
REFERENCES 24. Benton D, Maconie A, Williams C. The influence of the glycaemic
1. Rampersaud GC, Pereira MA, Girard BL, Adams J, Metzl JD. load of breakfast on the behaviour of children in school. Physiol Behav
Breakfast habits, nutritional status, body weight, and academic per- 2007;92:717–24.
formance in children and adolescents. J Am Diet Assoc 2005;105:743– 25. Smith MA, Foster JK. The impact of a high versus a low glycaemic
60, quiz 761–2. index breakfast cereal meal on verbal episodic memory in healthy
2. Benton D. The influence of dietary status on the cognitive performance adolescents. Nutr Neurosci 2008;11:219–27.
of children. Mol Nutr Food Res 2010;54:457–70. 26. Micha R, Rogers PJ, Nelson M. The glycaemic potency of breakfast
3. Wachs TD. Necessary but not sufficient. The respective roles of single and cognitive function in school children. Eur J Clin Nutr 2010;64:
and multiple influences on individual development. Washington, DC: 948–57.
American Psychological Association, 2000. 27. Micha R, Rogers PJ, Nelson M. Glycaemic index and glycaemic load
4. Pollitt E. Malnutrition and infection in the classroom. Paris, France: of breakfast predict cognitive function and mood in school children:
UNESCO, 1990. a randomised controlled trial. Br J Nutr 2011;106:1552–61.
5. Grantham-McGregor S, Baker-Henningham H. Review of the evidence 28. Brindal E, Baird D, Danthiir V, Wilson C, Bowen J, Slater A, Noakes
linking protein and energy to mental development. Public Health Nutr M. Ingesting breakfast meals of different glycaemic load does not alter
2005;8:1191–201. cognition and satiety in children. Eur J Clin Nutr 2012;66:1166–71.
6. Kanarek R. Psychological effects of snacks and altered meal frequency. 29. Cooper SB, Bandelow S, Nute ML, Morris JG, Nevill ME. Breakfast
Br J Nutr 1997;77(suppl 1):S105–18; discussion S118–20. glycaemic index and cognitive function in adolescent school children.
7. Pollitt E, Mathews R. Breakfast and cognition: an integrative summary. Br J Nutr 2012;107:1823–32.
Am J Clin Nutr 1998;67:804S–13S. 30. Nilsson A, Radeborg K, Bjorck I. Effects on cognitive performance of
8. Hoyland A, Dye L, Lawton CL. A systematic review of the effect of modulating the postprandial blood glucose profile at breakfast. Eur J
breakfast on the cognitive performance of children and adolescents. Clin Nutr 2012;66:1039–43.
Nutr Res Rev 2009;22:220–43. 31. Monro JA, Shaw M. Glycemic impact, glycemic glucose equivalents,
9. Adolphus K, Lawton CL, Dye L. The effects of breakfast on behavior glycemic index, and glycemic load: definitions, distinctions, and im-
and academic performance in children and adolescents. Front Hum plications. Am J Clin Nutr 2008;87:237S–43S.
Neurosci 2013;7:425. 32. Kennedy C, Sokoloff L. An adaptation of the nitrous oxide method to
10. Gilsenan MB, de Bruin EA, Dye L. The influence of carbohydrate on the study of the cerebral circulation in children; normal values for
cognitive performance: a critical evaluation from the perspective of cerebral blood flow and cerebral metabolic rate in childhood. J Clin
glycaemic load. Br J Nutr 2009;101:941–9. Invest 1957;36:1130–7.
11. Maffeis C, Fornari E, Surano MG, Comencini E, Corradi M, Tommasi 33. Chiron C, Raynaud C, Maziere B, Zilbovicius M, Laflamme L, Masure
M, Fasan I, Cortese S. Breakfast skipping in prepubertal obese chil- MC, Dulac O, Bourguignon M, Syrota A. Changes in regional cerebral
dren: hormonal, metabolic and cognitive consequences. Eur J Clin Nutr blood flow during brain maturation in children and adolescents. J Nucl
2012;66:314–21. Med 1992;33:696–703.
12. Sedlackova D, Kopeckova J, Papezova H, Hainer V, Kvasnickova H, 34. Thorleifsdottir B, Bjornsson JK, Benediktsdottir B, Gislason T,
Hill M, Nedvidkova J. Comparison of a high-carbohydrate and high- Kristbjarnarson H. Sleep and sleep habits from childhood to young
protein breakfast effect on plasma ghrelin, obestatin, NPY and PYY adulthood over a 10-year period. J Psychosom Res 2002;53:529–37.
levels in women with anorexia and bulimia nervosa. Nutr Metab 35. Kleinman RE, Murphy JM, Little M, Pagano M, Wehler CA, Regal K,
(Lond) 2012;9:52. Jellinek MS. Hunger in children in the United States: potential be-
13. Messier C. Glucose improvement of memory: a review. Eur J Phar- havioral and emotional correlates. Pediatrics 1998;101:E3.
macol 2004;490:33–57. 36. Alaimo K, Olson CM, Frongillo EA Jr. Food insufficiency and
14. Ells LJ, Hillier FC, Shucksmith J, Crawley H, Harbige L, Shield J, American school-aged children’s cognitive, academic, and psychoso-
Wiggins A, Summerbell CD. A systematic review of the effect of di- cial development. Pediatrics 2001;108:44–53.
etary exposure that could be achieved through normal dietary intake on 37. Timlin MT, Pereira MA, Story M, Neumark-Sztainer D. Breakfast
learning and performance of school-aged children of relevance to UK eating and weight change in a 5-year prospective analysis of adolescents:
schools. Br J Nutr 2008;100:927–36. Project EAT (Eating Among Teens). Pediatrics 2008;121:e638–45.
15. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items 38. McCulloch A, Joshi HE. Neighbourhood and family influences on the
for systematic reviews and meta-analyses: the PRISMA statement. cognitive ability of children in the British National Child Development
BMJ 2009;339:b2535. Study. Soc Sci Med 2001;53:579–91.
16. Cromer BA, Tarnowski KJ, Stein AM, Harton P, Thornton DJ. The 39. Moore GF, Tapper K, Murphy S, Lynch R, Raisanen L, Pimm C,
school breakfast program and cognition in adolescents. J Dev Behav Moore L. Associations between deprivation, attitudes towards eating
Pediatr 1990;11:295–300. breakfast and breakfast eating behaviours in 9-11-year-olds. Public
17. Wyon DP, Abrahamsson L, Jartelius M, Fletcher RJ. An experimental study Health Nutr 2007;10:582–9.
of the effects of energy intake at breakfast on the test performance of 10- 40. le Coutre J, Schmitt JA. Food ingredients and cognitive performance.
year-old children in school. Int J Food Sci Nutr 1997;48:5–12. Curr Opin Clin Nutr Metab Care 2008;11:706–10.