Breakfast and cognition: an integrative summary1,2

Ernesto Pollitt and Rebecca Mathews

ABSTRACT In this supplement, the papers presented at the International Symposium on Breakfast and Performance in Napa, CA in 1995 are summarized and integrated with data published since that time. In particular, the focus is on issues of research design, measurements, mechanisms, potential effect modifiers (eg, age), and relevance for public policy. No definitive conclusions can be drawn from the existing data on either the long- and short-term benefits of breakfast on cognition and school learning or the mechanisms that mediate this relation. The pooled data suggest that omitting breakfast interferes with cognition and learning, an effect that is more pronounced in nutritionally at-risk children than in well-nourished children. At the very least, breakfast consumption improves school attendance and enhances the quality of the students diets. Am J Clin Nutr 1998;67(suppl):804S13S. INTRODUCTION The papers presented at the International Symposium on Breakfast and Performance in Napa, CA were summarized by Mathews (1) in 1996, 1 y after the publication of a review by Pollitt (2) on breakfast research as it relates to children and school performance. The data suggest that children perform certain tasks of cognition (eg, working memory) more successfully after eating breakfast than after fasting overnight. However, there are inconsistencies in the data, partly attributable to differences in study design, the cognitive measures used, and the inherent characteristics of the study population (ie, nutritional status). In this integrative summary we present the key findings reported at the Napa symposium as well as data published since the meeting and a review of related topics. In particular, we discuss research design, measurements, mechanisms, potential effect modifiers (eg, age), and issues of public policy, so that future studies may address them. RESEARCH DESIGN Short-term evaluations of breakfast and cognitive performance have used experimental and quasi-experimental research designs (Table 1). Experimental schemes control for the potential effect of confounders such as the timing and composition of the evening and breakfast meals, duration of fasting, compliance to fasting, and motor activity of the subjects (eg, table games) (36). Randomized, controlled crossover designs within this scheme further minimize intersubject variability by exposing the same subjects to both breakfast and fasting periods. 804S A quasi-experimental design has some of the features of an experimental design, but does not control for all potentially confounding factors (713). For example, in a study of Israeli schoolchildren, variability in breakfast timing and composition may have been partly responsible for the lack of effects on performance of breakfast eaten at home compared with breakfast provided at school (9). Similarly, the lack of a breakfast effect in a study of Chilean children could have partly resulted from inadequate control of food intake on the morning of the evaluation (8). Although parents were instructed to send their children to school without breakfast, 23% of the children in this study reported they had eaten something the morning of the experiment. Short-term studies, usually with a maximum duration of 24 h, are designed to answer basic research questions related to whether an extended overnight fast affects particular brain functions. Evaluations of school feeding programs, on the other hand, have broader objectives related to whether the intervention changes scholastic achievement independent of and in relation to school attendance, habitual diet, and nutritional status of the subjects under study. COGNITIVE FUNCTIONS Theoretically, there are two plausible biological mechanisms by which breakfast may affect brain function and cognitive test performance. One involves metabolic changes associated with an extended overnight fast to maintain the availability of fuel and other nutrients to the central nervous system. The other involves the long-term salutary changes that breakfast may have on nutrient intake and nutritional status, which in turn could affect cognition. For example, it is known that repletion of iron stores and rehabilitation from anemia result in improved school performance in tests of memory and visual attention (13). The most widely studied tasks used in determining the effects of breakfast omission are those relating to short-term memory. Diminished speed and accuracy on tests of visual and auditory short-term memory, immediate recall, delayed recall, recognition memory, and spatial memory were observed in children and young adults (3, 5, 912). Skipping breakfast also influenced cognitive functions unrelated to memory. Three studies of children reported lower performance in visual discrimination of com-

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1 From the Department of Pediatrics, School of Medicine, University of California Davis, and R Mathews & Associates, Hudson, OH. 2 Address reprint requests to E Pollitt, Department of Pediatrics, TB-139, University of California, Davis, CA 95616.

Am J Clin Nutr 1998;67(suppl):804S13S. Printed in USA. 1998 American Society for Clinical Nutrition

TABLE 1 Studies evaluating the acute effects of breakfast omission on cognitive performance1 Study design Randomized, blinded, crossover study of BR2 and NBR in a metabolic ward. BR served at 08000830. Cognitive tests (IQ, MFFT, HCIT) given at 1115. Crossover occurred after 1 wk. Randomized, blinded, crossover study of BR2 compared with NBR. BR served at 08000830. Cognitive tests (IQ, MFFT, HCIT) given at at 1115. Crossover occurred after 1 wk. Intervention of BR3 or NBR on four occasions 1 wk apart on all subjects. Tests (CPT, arithmetic) assessed at 0950, 1100, and 1210. Randomized, blinded, crossover study of BR4 or NBR groups. BR served at 0800. Cognitive tests [coding, uency, arithmetic, digit span (backwards and forward), MFFT] given at 1100. Crossover occurred after 1 wk. Randomized study of BR5 or NBR. BR served at 0700. Cognitive tests (IQ, AVLT, MFFT, CPT, STAIC) given at 0800 and 1100. Subjects classied into four groups, depending on habitual intake: BR only, BR plus a midmorning snack. NBR with midmorning snack, and NBR and no snack. Cancellation test assessed at 1200 and 1400 (before and after lunch). Subjects performed better on a CPT of visual stimuli and an arithmetic test after BR than after NBR More errors were observed on the MFFT test with NBR than with BR. HCIT recall scores were higher after NBR than after BR. Recall of the last item in the test was no different between BR and NBR. Subjects made more errors in a task of picture identication (MFFT) with NBR than with BR. A test used to measure attention processes (HCIT) indicated higher recall scores after NBR than after BR. Recall of the last item in the test was signicantlybetter after NBR. Signicant interaction between treatment and IQ. Subjects with IQs below the group median made more MFFT errors with NBR than with BR. Results Comments

Study, location, setting, and year

Sample characteristics

Pollitt et al, United States, metabolic ward, 1981 (reviewed in reference 3)

32 911-y-old middle-class, well-nourished, boys and girls.

Pollitt et al, United States, metabolic ward, 1983 (reviewed in reference 3)

39 911-y-old middle-class, well-nourished boys and girls.

IQ was independent of MFFT results.

Conners and Blouin, United States, metabolic ward, 1983 (4)

10 911-y-old well-nourished children

Randomization of study and sex of participants not reported. Small sample size.

Simeon and Grantham-McGregor, Jamaica, metabolic ward, 1989 (reviewed in reference 5)

90 911-y-old boys and girls. Group 1: severely malnourished in rst 2 y of life (n = 30). Group 2: stunted in growth (n = 30). Group 3: average growth (n = 30).

With NBR, groups 1 and 2 had lower scores on verbal uency and coding tests than with BR. Similarly, wasted children had lower scores on MFFT test and digit span test with NBR. BR omission did not signicantly impact performance in adequately nourished children (group 3), with the exception that on one task (arithmetic) higher scores were observed.

Low height-for-age is an indicator of undernutrition. Average growth is an indicator of adequate nutrition. Wasting (low weight-for-height) is an indicator of recent nutritional deprivation.

BREAKFAST AND COGNITION SUMMARY

Cromer et al, United States, metabolic ward, 1990 (6)

34 middle-class, well-nourished boys and girls, average age 14 y; 18 experimental subjects, 16 control subjects.

No signicant differences in performance on CPT, MFFT, AVLT, or STAIC between BR and NBR groups.

Dickie and Bender, United Kingdom, school, 1982 (7)

227 boys and girls from three London schools, average age 12.5 y, and 260 boys and girls, average age 15.3 y. Nutritional status was not reported.

A task of visual acuity, attentiveness and vigilance (cancellation Study had several potentially test) indicated no differences between the groups. confounding factors not controlled for, ie, timing and composition of BR, effects of midmorning snack, effects of lunch, and the disproportionate sample size of each group. continued

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TABLE 1 (continued) Study design Randomized crossover study of BR and NBR groups. BR served at 0745. Tests (addition, sentence verication, MAST) given on 3 consecutive days at 1100. Crossover occurred after 1 wk; 55 subjects took memory and addition tests, 53 took sentence verication test. Randomized intervention of BR6 and NBR. Cognitive tests (short-term visual memory, problem solving, and attention) given at 09001100, 1 h after BR. Randomized crossover study of BR7 and NBR8. Tests of verbal uency, digit span, visual search, and speed of information processing were given. Crossover occurred after 2 wk. No differences in short-term visual memory, problem solving,or attention tasks were observed among the three groups of differing nutritional status with NBR. Results Comments

Study, location, setting, and year

Sample characteristics

Dickie and Bender, United Kingdom, school, 1982 (7)

108 boys and girls from four boarding schools, average age 1617 y.

No differences in performance on addition, sentence verication, Nutritional status and composition or MAST between periods with BR and NBR. of BR not reported (BR provided 2 MJ energy).

Lopez et al, Chile, school, 1993 (8)

279 811-y-old boys and girls with low SES categorized into normal, wasted, and stunted.

No control on timing or composition of dinner the previous day. Twenty-three percent of subjects ate BR before school on the test day.

Chandler et al, Jamaica, school, 1995 (reviewed in reference 5)

197 811-y-old boys and girls with low SES from rural schools. Ninety-seven were undernourished (low weight-for-age) and 100 were adequately nourished (normal weight-for-age). Randomized crossover study of BR9 and NBR conditions. BR served at 0800. Cognitive tests (stimulus discrimination, SMST) given at 1100. Crossover occurred after 1 wk. Subjects reported on the types and amount of BR foods they had eaten on the day of the experiment. Tests (AVLT and for memory for narrative prose and visual memory) given at 08550935 at school. Experimental subjects participated in a 2-wk study. Subjects were told not to eat anything at home. Subjects ate BR10 at 08000820. Tests (AVLT and for memory for narrative prose and visual memory) were given at 08550935 at the end of 2 wk. Control subjects received no instructions on BR.

Undernourished children had lower performance scores on a test Timing of BR and administration of verbal uency with NBR; no difference was observed in of cognitive tests were not adequately nourished children. No effects of BR were observed reported. for the visual search test, digit span test, or speed of information processing tests between groups.

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Pollitt et al, Peru, home, 1997 (reviewed in reference 3)

Fifty-two 911-y-old, lower-middle-class; 23 undernourished, 29 well-nourished.

Performance on SMST and SDT were adversely affected during the NBR period among the undernourished children. NBR had no adverse cognitive effects on the well-nourished children and improved scores on a few of the tasks

Vaisman et al, Israel, school, 1996 (9)

Four hundred ninety-one 1113-y-old boys and girls with varying SES backgrounds

On a task of immediate recall, children with BR scored signicantly higher than those with NBR. No differences were observed in the other cognitive tasks measured (77% ate BR on the morning of the test).

No standardization or control of BR eaten at home in relation to composition and timing.

Vaisman et al, Israel, school, 1996 (9)

Of 503 1113-y-old boys and girls with varying SES backgrounds, 322 were experimental subjects and 181 were control subjects.

No differences were observed between BR and NBR on most of the tests related to recall, recognition, and learning. However, all test scores were signicantly higher for those who ate BR at school compared with those who ate BR at home or with those who ate NBR. Researchers suggest timing of BR is important because the subjects who ate 30 min before testing performed better than those who ate at home 2 h before testing.

Sixty-six percent of the control subjects ate BR at home. There was no standardization of composition or timing of BR consumed at home.

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TABLE 1 (continued) Study design Subjects fasted from the time of their evening meal the previous day and had NBR or a milk-based nutritional beverage in the research laboratory. Tests (spatial memory, immediate recall) were given 2 h after BR. Subjects assigned to NBR, cooked BR11, or cereal-and-toast BR12 with coffee or decaffeinated coffee. Subjects fasted from 0000 and were tested at 08000830. Additional tests (reaction time task, serial response task, and RDVT) were given at 0930 and 1030. BR had no effect on performance of sustained attention tasks, although it increased pulse rate and inuenced mood. Caffeine improved performance of sustained attention tasks and increased mental alertness. Improvement in mood was also observed with cooked BR. Similar design to Smith (11), using different tests (free recall, delayed recognition, memory task, semantic processing task, RDVT). Only the NBR and the cooked BR conditions were used. BR improved the subjects performance on free recall and recognition memory tasks, had no effect on a semantic memory task, and decreased performance on a task of logical reasoning. BR had no effect on the RDVT performance (which is a measure of sustained attention). BR had an effect on free recall in mid-morning but had no effect in late morning. NBR had no adverse effects on cognitive tasks related to visual information processing, free recall, reaction time, or speed of nger tapping. A signicant improvement in mood was observed in the low fat, high-CHO BR group. The BR group took less time to nish memory tasks than the NBR group. The number of errors was not inuenced by BR consumption. Results Comments

Study, location, setting, and year

Sample characteristics

Benton and Parker, United Kingdom, research laboratory, 1992 (10)

Thirty-three university students, average age 21 y (16 women, 17 men).

Smith, United Kingdom, research laboratory, 1994 (reviewed in reference 11)

Forty-eight university men and women.

Small sample size assigned to each of the six treatment conditions.

Smith, United Kingdom, research laboratory, 1992 (reviewed in reference 12)

Forty-eight university men and women.

BREAKFAST AND COGNITION SUMMARY

Lloyd et al, research laboratory, 1996 (12)

16 habitual breakfast eaters; 14 female and 2 male, average age 26 y.

On the same day on 4 consecutive weeks, subjects ate NBR; low-fat, high-CHO BR13; medium-fat, medium-CHO BR; or high-fat, low-CHO BR. BR served at 0830. BVIP (memory), two-nger tapping task (motorspeed), free recall, simple, and reaction time tests were given at 30, 90, and 150 min after BR.

1 AVLT, Rey Auditory-Verbal Scale; BR, breakfast, or subjects who ate breakfast; BVIP, Bakan Visual Information Processing Test; CHO, carbohydrate; CPT, Continuous Performance Task; HCIT, Hagen Central Incidental Test; IQ, intelligence quotient; MAST, Memory and Search Test; MFFT, Matching Familiar Figures Test; NBR, no breakfast, or subjects who ate no breakfast; RDVT, Repeated Digits Vigilance Task; SDT, Stimulus Discrimination Test; SES, socioeconomic status; SMST, Sternberg Memory Search Test; STAIC, State-Trait Anxiety Scale. 2 Wafes, syrup, margarine, orange juice, and milk. 3 Cereal with sugar, milk, eggs, juice, and toast. 4 Cheese, nutribun (Jamaican School Feeding Program), and milk. 5 Doughnut, orange juice, and chocolate milk. 6 Grain cakes and avored milk. 7 Cheese sandwich and chocolate milk. 8 Orange slice. 9 Grain cake, Amilac milk substitute (Institutuo de Investigacion Nutricional, La Molina, Lima, Peru). 10 Sugared corn akes and whole milk. 11 Scrambled eggs with semi-skim milk, bacon, whole-meal bread, and margarine. 12 Cornakes, semiskim milk, sugar, whole-meal bread, margarine, and marmalade. 13 Each breakfast consisted of bread rolls, margarine, jam, and a milk shake. Fat content was manipulated by varying the margarines and adding cream to milk shakes. Carbohydrate content was increased by adding maltodextrin.

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POLLITT AND MATHEWS ble to these stresses and would therefore be most likely to benefit from breakfast consumption. These hypotheses have not yet been tested because age as a modifier of the breakfast response has not been evaluated. The primary focus of breakfast and cognition studies is on children because of the potential educational and public health implications. Most of the studies have focused on children in the 912-y age group, with many showing a beneficial effect, as noted previously (35, 15, 2224). Only three studies focused on a teenage population: one study of 1113-yolds reported a positive effect of breakfast consumption (9), but two other studies of teenagers found no such effects (6, 7). The effect of breakfast omission on cognition in adults is not a major topic in this supplement. Data from the previously mentioned studies suggest that cognition in adults is vulnerable to the effects of skipping breakfast, and additional studies observed that glucose consumption before testing improves memory test performance among aged adults (1013, 26, and see the biochemical relations section of this article). The findings suggest the possibility of a U-shaped curve in describing the relation between age (x axis) and cognitive enhancement from breakfast consumption (y axis). Future studies are called for to assess the existence, if any, of such a relation. NUTRITIONAL STATUS The association between poor nutritional status and poor mental development is well documented in children (26). Given this association, the issue in question is whether the effects of breakfast on cognition are moderated by nutritional status. It is plausible that undernourished children may be particularly vulnerable to the metabolic effects of breakfast omission. For example, because of a history of poor dietary intake (in both quantity and quality), stunted children may be less likely to perform as well as their well-nourished counterparts on tests of cognitive efficiency. Likewise, it is possible that a decline in cerebral iron from a diet deficient in iron may intensify the stresses associated with an extended overnight fast. Three studies that evaluated nutritional status as a potential modifier of cognitive performance after breakfast consumption and omission observed, as expected, that undernourished children performed better after breakfast than after an extended fast, but that this was not the case for their adequately nourished peers (3, 5, 15). In these three studies conducted in Jamaica and Peru, only the undernourished children significantly differed in performance between the fed and the fasted states. However, in contrast with observations in the United States, breakfast had no effect on adequately nourished children in Jamaica and Peru. This discrepancy may be better understood as we learn more about the metabolic factors that modify the relation between breakfast and cognitive function, including possible nutritional and physiologic adaptations. BIOCHEMICAL RELATION Extension of an overnight fast leads to a gradual decline in blood glucose and insulin concentrations, along with other metabolic (eg, neurotransmitter) changes that may interfere with certain aspects of cognitive function (Table 3). In comparisons of the fed and fasted states, it is biologically plausible that several biochemical changes associated with the duration of the fast, as well as the timing, size, and composition of the breakfast meal,

peting stimuli, eg, the Matching Familiar Figures Test (MFFT) (3, 5). The no-breakfast condition was also associated with a decline in performance on a verbal fluency test (5, 15) and tasks of arithmetic, continuous visual stimulus (4), and stimulus discrimination (3). Although the reported data do not lend themselves to a direct comparative analysis, the pooled findings suggest that attentional processes are also vulnerable to a prolonged fast. On the other hand, tasks requiring sustained attention, eg, a repeated digits vigilance task, were not affected by breakfast omission (11, 12), nor was speed of general knowledge retrieval (5, 12). In some studies, none of the cognitive function measures related to memory, computational skills, or attentiveness were significant between the breakfast and the no-breakfast groups (68, 13). However, the lack of statistically significant effects was primarily observed in those studies that did not control for potential confounders. The specific tests chosen to assess cognitive function must be an effective measure of the group being studied. For example, one of the studies that did not find a beneficial breakfast effect indicated that the test used (MFFT) may not have been appropriate for the adolescents in the study, because a very low error rate was observed in both treatment and control groups (6). The apparent lack of a breakfast effect in a series of computerized cognitive tests administered to a group of Chilean children from low socioeconomic backgrounds could have been related to their unusually high motivation while using a computer for the first time (8). Apart from school feeding (breakfast) studies, long-term assessments of breakfast omission and cognitive function have not been conducted. It is plausible that repeated breakfast omission contributes to nutrient inadequacies (1621), but the impact of repeated breakfast omission on nutritional status and subsequent cognitive performance is not clear. SCHOLASTIC ACHIEVEMENT AND SCHOOL ATTENDANCE Do the effects of breakfast on cognition, observed in shortterm studies, translate into long-term scholastic benefits? It seems so, but no definitive conclusions are warranted. Three studies that attempted to answer this question had design limitations (Table 2), but all three reported improved scores on some of the scholastic tests given in schools participating in a breakfast program (2224). Improvements were observed in these studies as follows: in overall combined scores of language, reading, and math in a study of US low-income students (23), in arithmetic in a study of rural Jamaican schoolchildren (22), and in vocabulary scores in a study of undernourished Peruvian children (24). In all three evaluations, participation in the school breakfast program significantly increased school attendance. This factor alone could contribute to enhanced long-term scholastic achievement, simply because improved attendance exposes children to a learning environment for a longer period. AGE It is postulated that brain function is vulnerable to the metabolic stresses of fasting in both children and adults. Individuals at both ends of the spectrumyoung children whose cognitive processes are still maturing and older adults whose cognitive processes are on the declineare likely to be the most suscepti-

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TABLE 2 Summary of studies evaluating the effects of school breakfast programs on cognitive and behavioral performance1
Study, location, and year Powell et al, Jamaica, 1983 (22) Sample characteristics Undernourished children with low attendance records from a rural school, average age 12.5 y, with the lowest standard achievement scores. Forty-four subjects were given BR, 38 subjects had NBR, and 33 control subjects were given syrup. Low-income public schoolchildren in grades 36 were classied as a SBP participant (n = 335) or nonparticipant (n = 688). Study design Longitudinal study with 2 control groups. School progress was monitored for 23 mo before and after SBP2 intervention. Growth, school attendance, and achievement were assessed. with the WRAT. Results School breakfast had a signicant effect on arithmetic scores and attendance. The improvement in arithmetic scores remained even after attendance, sex, and age were controlled for. BR had no effect on spelling, growth, or weight. Comments Random allocation of subjects into treatment and control groups not reported. More boys than girls were in all groups.

Meyers et al, United States, 1989 (23)

Longitudinal study with SBP3 participants and nonparticipants. School achievement scores were assessed by the CTBS before the SBP was in place and 3 mo after. Change in attendance was monitored over 5 mo.

Participation in the SBP increased the CTBS total scale score and decreased tardiness and absenteeism. CTBS included tests in language, reading, and math.

Subjects were not randomly assigned to groups. Subjects were classied as a participant if they attended the SBP 60% of the time, and a non-SBP participant if they did not attend SBP on any of the days monitored. Predominantly boys in both treatment and control groups.

BREAKFAST AND COGNITION SUMMARY

Jacoby et al, Peru, 1996 (reviewed in reference 24)

Children in grades 45, average age 11 y, with lower SES from 10 rural schools. Undernourished children were included. Two groups consisted of 201 SBP subjects and 151 non-SBP subjects.

Short-term study evaluating the scholastic performance of SBP4 participants and nonparticipants. Cognitive tests specic for this age group were administered before the program was implemented and 1530 d after implementation.

School attendance signicantly increased among SBP participants compared with nonparticipants. Mean total cognitive scores did not differ between SBP subjects and non-SBP subjects. However, children who were nutritionally at-risk improved in their vocabulary test scores after SBP participation

BR, breakfast, or subjects who ate breakfast; CTBS, Comprehensive Test of Basic Skills; NBR, no breakfast, or subjects who ate no breakfast; SBP, school breakfast program; SES, socioeconomic status; WRAT, Wide Range Achievement Test. 2 Banana cake or meat and vegetable pastry with milk. 3 Type of breakfast served was not specied. 4 Cake and a nutritionally fortied milk-like beverage that provided 30% of daily energy requirements, 100% iron needs, and 60% of recommended dietary allowances for most vitamins and minerals (25).

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TABLE 3 Breakfast studies evaluating the effects of glucose administration on cognitive performance1
Study and year Benton and Parker, 1998 (10) Sample characteristics 80 university women. Study description Subjects followed their normal routine of eating or skipping BR. Subjects were randomly assigned to the following groups: 1)BR with drink containing 50 g glucose, 2)BR with placebo drink, 3) NBR with drink containing 50 g glucose, and 4) NBR with placebo drink. Testing began 20 min after drinks were served. Subjects followed their normal routine of eating or skipping BR. Subjects were randomly assigned to the following groups: 1) BR with drink containing 50 g glucose, 2) BR with a placebo drink, 3) NBR with drink containing 50 g glucose,and 4) NBR with a placebo drink. Testing began 20 min after the drinks were served. On two occasions 1 wk apart, all subjects were tested in early morning after an overnight fast. Subjects consumed 16 oz (473 mL) lemonade sweetened with 50 g glucose or a placebo drink with saccharin. Testing began 15 min after drinks were served. Design similar to Hall et al (reviewed in reference 25). Tasks of complex memory and nonmemory were administered. Design similar to Hall et al (reviewed in reference 25) except that the cognitive tests were appropriate in difculty for this age group. Memory and nonmemory tests were given. Results Groups 1, 2, and 3 had similar performance scores on the BrownPeterson task (recall of trigrams while counting backwards), group 4 did not perform as well as the other 3 groups. Comments BR consisted of cereal and milk, cereal and toast, or all.

Benton and Parker, 1998 (10)

137 women, 47 men, average age 22 y.

Among the subjects with NBR, group 3 recalled more words on a word recall task than group 4. For those who had eaten breakfast, the type of drink did not inuence recall. However, in a task requiring recall of a story, performance was improved only by BR and not by the glucose drink.

Intelligence test results and the outcome of a rapid information processing task were not inuenced by BR or the glucose drink.

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Hall et al, 1989 (reviewed in reference 26)

College-age and elderly subjects

Improved performance on a test of contextual verbal memory of a prose passage after glucose administration was observed only in the elderly subjects. Other cognitive tests were not affected.

Tests of intelligence, short-term memory, attention, and motor function were not inuenced by the glucose drinks.

Craft et al, 1994 (28)

27 young adult and 32 elderly subjects.

Glucose improved performance on declarative memory paragraph in male subjects. Men, regardless of age, were more likely to show memory facilitation with glucose administration than women. Glucose improved performance on a test of immediate and delayed recall of narrative prose, a test of attention, and in the speed of completion of a vigilance test.

Other cognitive tests were not affected.

Korol and Gold, 1998 (26)

18 college students (13 male, 5 female)

Other cognitive tests were not affected.

BR, breakfast; NBR, no breakfast.

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BREAKFAST AND COGNITION SUMMARY may be concurrently at work to determine the extent to which cognitive performance is affected. Benton and Parker (10) and Korol and Gold (26) proposed elsewhere in this supplement that blood glucose plays a role in cognitive function, particularly in those tasks involving recall from memory (Table 3). In one case, 50 g glucose administered in a drink 1520 min before testing improved the subjects performance on specific cognitive tasks, ie, immediate recall, contextual verbal memory, and delayed recall of narrative prose. The glucose-related effect was initially observed only in the elderly, but similar effects were more recently seen in young adults (26). These studies also suggest that the rate at which blood glucose returns to baseline concentrations may be important in enhancing cognitive efficiency (26, 29). Because glucose is a primary substrate used by the brain for cognitive activity, conditions that affect glucose regulation and utilization may also affect cognition (28, 29). Not all studies that obtained glucose determinants and tested the relation between glucose and cognitive test performance found such an association (Table 4). In a short-term experimental study of children in Peru, improved performance on a memory and stimulus discrimination test was not associated with blood glucose changes (3). Similarly, in one of the studies of university students (10), performance of a word recall task was enhanced with breakfast or a glucose drink, whereas only breakfast improved a task of written recall of a story after it was read aloud. One of the studies that measured metabolic changes observed alterations in neurotransmitter concentrations after an extended overnight fast, indicating the possibility of other mechanisms at work (3). BREAKFAST COMPOSITION, SIZE, AND TIMING Attributes of the breakfast meal, such as its composition, size, and time of consumption, can induce several metabolic alterations, including changes in blood glucose, insulin, and neurotransmitter concentrations, and therefore it is plausible that characteristics of the meal itself may influence cognitive function. Although these factors were recognized as potential modifiers of performance, they were not the primary focus of this supplement because most breakfast studies thus far have not attempted to differentiate the effects of different breakfast meals from those of breakfast timing on cognition. No change in cognitive performance was observed in a comparison of a cooked compared with a cereal-and-toast breakfast (11), nor in a study of differing fat and carbohydrate breakfast meals (13). However, both of these studies reported a change in mood; one study observed an improvement in mood with the cooked breakfast and the other noted a positive mood change after a low-fat, high-carbohydrate breakfast. Furthermore, findings not presented in this supplement suggest that specific foods and nutrient combinations influence blood glucose concentrations and brain neurotransmitter synthesis. Certain foods produce a flattened or metered glucose response, whereas others produce a sharp elevation and dip in blood glucose concentration before returning to baseline concentrations (30, 31). Similarly, it is known that different nutrient combinations (ie, carbohydrate and protein) alter brain neurotransmitter (ie, serotonin) synthesis (32, 33). The energy load of the breakfast meal is also likely to play a moderating role. One study reported in this supplement indicates that a breakfast providing 25% of the average daily requirements

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improved performance on a creativity test in a group of 276 children age 10 y old compared with a breakfast providing less than 10% of daily energy requirements (34). Another study that made a similar evaluation of adolescents reported a beneficial effect on immediate recall in short-term memory with higher-than-normal energy intakes, but a negative effect on concentration (35). A few studies have addressed the issue of breakfast timing on cognitive performance. A recent study conducted in Israel observed that children who ate a school breakfast 30 min before cognitive testing had signicantly higher overall cognitive scores than those who ate breakfast at home or who did not eat breakfast (9). It is necessary, however, to point out that several studies noted a breakfast effect even with a 3-h interval between breakfast consumption and testing (35). In a study of university students (12), breakfast had an effect on free recall in midmorning but had no effect in late morning, suggesting that there is an optimum time after breakfast consumption for the enhancement of certain cognitive tasks. RESEARCH DATA, PROGRAMS, AND POLICIES
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Where do we go from here? Research suggests that breakfast omission does affect the performance of specific cognitive tasks, particularly those involving memory. However, significant gaps remain as to how age, sex, nutritional status (past and current), and the timing, size, and composition of the morning meal modify these effects. The underlying physiologic mechanisms also remain unknown. Apart from these potential cognitive enhancements, US studies indicate that eating breakfast has nutritional benefits (1621). Subjects who ate breakfast, either at home or at school, improved their overall intake of fiber, vitamins, and minerals. Breakfast may also play a role in improving overall nutritional status and health. Increased intakes of iron, for example, may aid certain populations, such as adolescent females, who are at risk for iron deficiency anemia, and who subsequently may also be at risk for reduced cognitive efficiency. Nonetheless, breakfast consumption in the United States has declined steadily over the past 26 y for all age groups, and particularly among adolescent girls (36, 37). Therefore, it is important to encourage the general public to eat breakfast. School feeding programs are one avenue for achieving this goal. The US Department of Agriculture School Breakfast Program is the largest of its kind in the world, yet a schools enrollment in the program does not guarantee individual participation. Age, sex, family income, race, geographic location, and perceived social stigma of the program are some of the factors inuencing a childs decision to participate (17). Overcoming these obstacles is essential for increasing participation in US school breakfast programs, as is increasing public awareness of the benets of breakfast consumption. Several developing countries in the Caribbean, Latin America, Africa, and Asia have school breakfast programs, but few have provided insight into their educational or nutritional effectiveness (38). In many of these countries, and particularly in rural areas, not all children are enrolled in school, and those who attend have a high dropout rate, especially those in first and second grades. School feeding will likely increase attendance partly because the program is as an incentive for parents to send children to school. The greater the time spent in the classroom, the greater the potential improvements in scholastic performance. The nutritional, educational, and economic value of school feeding is increasingly evident in developing countries. The

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TABLE 4 Breakfast studies evaluating the effects of glucose administration on cognitive performance1
Study and year Pollitt et al, 1981 (reviewed in reference 3) Sample characteristics Thirty-two 911-y-old, well-nourished children. Study description Crossover study in which cognitive tests were given after an overnight fast or 3 h after eating a BR of wafes, syrup, margarine, orange juice, and milk. Results Subjects with largest BG changes from NBR to BR condition were more likely to have more errors on MFFTs. Comments Compared with BR period, fasting was associated with a decrease in glucose and insulin and an increase in BOHB, lactate, FA, ACR, and catecholamine. Insulin concentrations were signicantly lower in the fasting period than in the BR period.

Pollitt et al, 1982 (reviewed in reference 3)

Thirty-nine 911-y-old, well-nourished children.

Crossover study in which cognitive tests were given after an overnight fast or 3 h after eating a BR of wafes, syrup, margarine, orange juice and milk. Cognitive tests were given after an overnight fast or 1 h after eating a BR of a doughnut, orange juice and chocolate milk. Subjects were randomly assigned into experimental and control groups. Crossover study in which cognitive tests were given after an overnight fast or 3 h after eating a BR of a grain cake and milk-like beverage Cognitive tests were given after an overnight fast or 2 h after drinking a milk-based nutritional beverage for BR. Subjects were equally distributed between. the two groups.

Errors on MFFTs were negatively associated with BG concentrations. During the BR period, HCIT scores did not improve and were not correlated with BG.

POLLITT AND MATHEWS

Cromer et al, 1990 (6)

Thirty-four 14-y-old well-nourished adolescents.

None of the cognitive measures were different between the NBR and the BR groups. BG was not correlated with performance.

BOHB was not correlated with performance.

Pollitt et al, 1997 (reviewed in reference 3)

Fifty-two 911-y-old well- and undernourished boys.

BG was not associated with performance on any of the cognitive measures even though improved performance was observed in the undernourished group Enhanced performance on two memory tests observed after BR was correlated with BG. A higher BG concentration was correlated with better performance on a spatial memory test in relation to time taken and number of errors

Benton and Sargent, 1992 (reviewed in reference 10)

Thirty-three university students (16 women, 17 men).

ACR, adrenal adrenocorticoid; BR, breakfast; BG, blood glucose; BOHB, b-hydroxybutrate; FA, fatty acids; HCIT, Hagen Central Incidental Test; MFFT, Matching Familiar Figures Test; NBR, no break-

fast.

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BREAKFAST AND COGNITION SUMMARY challenge is to overcome the numerous obstacles that prevent the successful operation of these programs, including limited monetary resources, irregularity of food supply and distribution, ration dilution (ie, stretching inadequate supplies), reduced instructional time for teachers who must help distribute the food, students departure from school immediately after the meal, and children receiving less food at home because of the school meal (15). However, the overall benefits of school feeding far outweigh the hurdles to implementation. CONCLUSION No denitive conclusions can be drawn from the existing data on either the long- and short-term benets of breakfast on cognition or the mechanisms that mediate this relation. The data strongly suggest that omitting breakfast interferes with cognition and learning, an effect that is more pronounced in nutritionally atrisk children. At the very least, breakfast consumption improves school attendance and enhances the quality of the students diets. REFERENCES
1. Mathews R. Importance of breakfast to cognitive performance and health. Perspect Appl Nutr 1996;3:20412. 2. Pollitt E. Does breakfast make a difference in school? J Am Diet Assoc 1995;95:11349. 3. Pollitt E, Cueto S, Jacoby ER. Fasting and cognition in well- and undernourished schoolchildren: a review of three experimental studies. Am J Clin Nutr 1998:67(suppl):779S84S. 4. Conners CK, Blouin AG. Nutritional effects of behavior of children. J Psychiatr Res 1983;17:193201. 5. Simeon DT. School feeding in Jamaica: a review of its evaluation. Am J Clin Nutr 1998:67(suppl):790S4S. 6. Cromer BA, Tarnowski KJ, Stein AM, Harton P, Thornton DJ. The school breakfast program and cognition in adolescents. Dev Behav Pediatr 1990;11:295300. 7. Dickie NH, Bender AE. Breakfast and performance in schoolchildren. Br J Nutr 1982;48:48396. 8. Lopez I, de Andraca I, Perales CG, Heresi E, Castillo M, Colombo M. Breakfast omission and cognitive performance of normal, wasted and stunted school children. Eur J Clin Nutr 1993; 47:53342. 9. Vaisman N, Voet H, Akivis A, Vakil E. Effect of breakfast timing on the cognitive functions of elementary school students. Arch Pediatr Adolesc Med 1996;150:108992. 10. Benton D, Parker PY. Breakfast, blood glucose, and cognition. Am J Clin Nutr 1998:67(suppl):772S8S. 11. Smith A, Kendrick A, Maben A. Effects of breakfast and caffeine on cognitive performance, mood, and cardiovascular functioning. Appetite 1994;22:3945. 12. Smith A, Kendrick A, Maben A. Effects of breakfast and caffeine on performance and mood in the late morning and after lunch. Neuropsychobiology 1992;26:198204. 13. Lloyd HM, Rogers PJ, Hedderley DI. Acute effects on mood and cognitive performance of breakfasts differing in fat and carbohydrate content. Appetite 1996;27:15164. 14. Pollitt E. Iron deficiency and cognitive function. Annu Rev Nutr 1993;13:52137. 15. Grantham-McGregor SM, Chang S, Walker SP. Evaluation of school feeding programs: some Jamaican examples. Am J Clin Nutr 1998:67(suppl):785S9S. 16. Nicklas TA, ONeil CE, Berenson GS. Nutrient contribution, secular trends, and the role of ready-to-eat cereals: a review of the data 22.

813S

17. 18. 19. 20.

21.

23.

24.

25. 26. 27.

28.

29. 30.

31.

32. 33.

34.

35.

36.

37.

38.

from Bogalusa Heart Study. Am J Clin Nutr 1998: 67(suppl):757S63S. Kennedy E, Davis C. US Department of Agriculture School Breakfast Program. Am J Clin Nutr 1998:67(suppl):798S803S. Tietyen JL, Fleming K. Nutrient intake of breakfast vs. non-breakfast eaters. J Am Diet Assoc 1995;95(suppl):A55. Morgan KJ, Zabik ME, Stampley GL. Breakfast consumption patterns of US children and adolescents. Nutr Res 1986;6:63546. Morgan KJ, Zabik ME, Stampley GL. The role of breakfast in diet adequacy of the US adult population. J Am Coll Nutr 1986;5:55163. Morgan KJ, Zabik ME, Stampley GL. Breakfast consumption patterns of older Americans. J Nutr Elder 1986;5:1944. Powell C, Grantham-McGregor SM, Elston M. An evaluation of giving the Jamaican government school meal to a class of children. Hum Nutr Clin Nutr 1983;37C:3818. Meyers AF, Sampson AE, Weitzman M, Rogers BL, Kayne H. School breakfast programs and school performance. Am J Dis Child 1989;143:12349. Jacoby E, Cueto S, Pollitt E. Benefits of a school breakfast programme among Andean children in Huaraz, Peru. Food Nutr Bull 1996;17:5464. National Research Council. Recommended dietary allowances. 10th ed. Washington, DC: National Academy Press, 1989. Korol DL, Gold PE. Glucose, memory, and aging. Am J Clin Nutr 1998:67(suppl):76471S. Pollitt E, Golub M, Gorman K, et al. A reconceptualization of the effects of undernutrition on childrens biological, psychosocial, and behavioral development: social policy report, Society for Research in Child Development. Ann Arbor, MI: University of Michigan, 1996. Craft S, Murphy G, Wemstrom J. Glucose effects on complex memory and nonmemory tasks: the influence of age, sex, and glucoregulatory response. Psychobiology 1994;22:95105. Gold PE. Role of glucose in regulating the brain and cognition. Am J Clin Nutr 1995;61(suppl):987S95S. Jenkins DJA, Jenkins AL, Wolever TMS, et al. Lente carbohydrate or slowly absorbed starch: physiolgical and therapeutic implications in dietary fiber. In: Kritchevsky D, Bonfield C, Anderson JW, eds. Chemistry, physiology and health effects. New York: Plenum Press, 1988:24759. Jenkins DJA, Wolever TMS, Leeds AR, et al. Dietary fibres, fibre analogues, and glucose tolerance: importance of viscosity. Br Med J 1978;2:13924. Fernstrom JD, Wurtman RJ. Brain serotonin content: increase following ingestion of carbohydrate diet. Science 1971;174:10235. Spring B, Maller O, Wurtman J, Digman L, Cozolino L. Effects of protein and carbohydrate meals on mood and performance: interactions with sex and age. J Psychiatr Res 1983;17:15567. Wyon DP, Abrahamsson L, Jartelius M, Fletcher RJ. An experimental study of the effects of energy intake at breakfast on the test performance of 10-year-old children in school. Int J Food Sci Nutr 1997;48:512. Michaud C, Musse N, Nicolas JP, Mejean L. Effects of breakfast size on short-term memory, concentration, mood and blood glucose. J Adolesc Health 1991;12:537. Siega-Riz AM, Popkin BM, Carson T. Trends in breakfast consumption for children in the United States from 1965 to 1991. Am J Clin Nutr 1998:67(suppl):748S56S. Haines PS, Guilkey DK, Popkin BM. Trends in breakfast consumption of US adults between 1965 and 1991. J Am Diet Assoc 1996;96:46470. Jacoby ER, Cueto S, Pollitt E. When science and politics listen to each other: good prospects from a new school breakfast program in Peru. Am J Clin Nutr 1998:67(suppl):795S7S.

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