Influences of protein to energy ratios in breakfast on mood, alertness and attention in the healthy undergraduate students

doi:10.4236/health.2011.36065

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Vol.3, No.6, 383-393 (2011)

doi:10.4236/health.2011.36065

Health

Influences of protein to energy ratios in breakfast

on mood, alertness and attention in the healthy

undergraduate students

Yao-Chi Zeng1*, Shun-Min Li1, Guo-Liang Xiong1, Hui-Min Su2, Jian-Cheng Wan3

1Shenzhen Traditional Chinese Medicine Hospital, Shenzhen, China; *Corresponding Author: 0731zyc@163.com

2Shenzhen Bao’an Maternal and Child Health Hospital, Shenzhen, China;

3Guangzhou University of Traditional Chinese Medicine, Guangzhou, China.

Received 12 February 2011; revised 17 March 2011; accepted 6 May 2011.

ABSTRACT

Background: The high protein (HP) breakfast

reduced gastric emptying and the most satiat-

ing macronutrient appears to be dietary protein.

Few studies have investigated the effects of

protein to energy ratio in breakfast on mood,

alertness and attention. Objective: This study

was designed to investigate whether the HP

breakfast is more beneficial to mood, alertness

and attention of the healthy undergraduate

student than adequate-protein (AP) breakfast

through the rising body temperature and re-

maining stable blood glucose or through other

physiologic processes. Methods: Thirteen

healthy male undergraduate students (18 - 23 y)

were studied in a double-blind, randomized

crossover design. Blood samples, body tem-

perature, satiety, mood and Continuous Per-

formance Test (CPT) were assessed after the

consumption of two isocaloric breakfasts that

differed in their protein and carbohydrate con-

tent: an HP breakfast (50%, 30%, and 20% of

energy from protein, carbohydrate, and fat, re-

spectively) or an AP breakfast (10%, 70%, and

20% of energy from protein, carbohydrate, and

fat, respectively). Results: Consumption of an

HP breakfast resulted in more steady glucose

and insulin than AP breakfast consumption (p <

0.05). Satiety sc ores and body tem perat ure were

higher af ter HP breakfas t consumpt ion (p < 0.05).

And most import ant, the positiv e mood and CPT

scores w ere higher after HP breakfast than after

AP breakfast intake (p < 0.05). Conclusion: HP

breakfast can effectively stabilize postprandial

serum glucose concentration and elevate post-

prandial temperature of healthy male under-

graduate students. Our present findings dem-

onstrate the relationship between HP breakfast

and mood, alertness and attention. This study

indicated th at HP brea kfast may enhance hum an

performance probably by increasing the thermic

effect of a food and elevating body temperature.

Keywords: Protein; Body Temperature; Mood;

Alertness; Attention

1. INTRODUCTION

It is widely believed that there exists a strong rela-

tionship between eating and mood, and that diet and

particular dietary constituents can have important influ-

ences on behaviour, including alertness and mental per-

formance[1-3]. Wurtman RJ and Wurtman JJ [1] devel-

oped the hypothesis that carbohydrates can relieve de-

pression because that carbohydrate intake enhanced se-

rotonin synthesis. Their major theory was that a meal

high in carbohydrate increased the rate that tryptophan

entered the brain, leading to an increase in the level of

the neurotransmitter serotonin that modulates mood. As

for fat, it is thought that in many countries current popu-

lation intakes of the n-3 long-chain PUFA (LCPUFA;

also known as long chain omega-3 fatty acids) EPA and

DHA are lower than optimal for a variety of health out-

comes [2,4]. However, Peter J. Rogers’ [5] studies that

have shown substantially increasing EPA and DHA in-

take for 3 months was found not to have beneficial or

harmful effects on mood in mild to moderate depression.

With respect to energy expenditure, it is known that pro-

tein has the highest and most prolonged thermic effect of

the separate macronutrients (20 - 30%), followed by

carbohydrate (5 - 15%) and fat (0 - 3%)[3]. Protein has

been observed to increase satiety to a greater extent than

carbohydrate and fat and therefore can reduce energy

intake [6,7]. Now many positive outcomes associated

with increased dietary protein are thought to be due pri-

Y. C. Zeng et al. / Health 3 (2011) 383-393

384

marily to lower energy intake associated with increased

satiety [8-11], reduced energy efficiency and/or in-

creased thermogenesis [5,12,13], positive effects on

body composition, specifically lean muscle mass[14-16],

and enhanced glycemic control [16,17]. In addition, sev-

eral studies showed that eating breakfast can improve

cognitive performance and attention-concentration

compared with omitting breakfast [18-20], but the effect

of each macronutrient was not defined because of vari-

ous methodologic issues. In fact, the study [21] about the

relationship of macronutrients and memory performance

indicated all of the macronutrients improved paragraph

recall 15 min after ingestion, suggesting that energy in-

take can enhance specific aspects of cognition, in addi-

tion to the effects of energy ingestion on memory, each

macronutrient enhanced performance on various tasks,

possibly via unique mechanisms. Indeed, all three kinds

of macronutrients led to an initial, robust improvement

on delayed paragraph recall. Each macronutrient may

exert different effects on cognition by additional, unique

mechanisms [21]. Human beings should not ingest pure

protein, carbohydrate, or fat, but should pay attention to

the content of the various macronutrients reasonably

matched. However, there is little support for the influ-

ences of protein to energy ratio in breakfast on mood,

alertness and attention in healthy human volunteers. The

aim of the present study was to examine the effects of

HP breakfast on mood, alertness and attention of under-

graduate student. It was hypothesised that (1) some det-

rimental mood would be alleviated by HP breakfast; and

(2) postprandial alertness and attention be enhanced by

HP breakfast.

2. SUBJECTS AND METHODS

2.1. Subjects

Thirteen healthy male volunteer subjects, mean age

21.5 (S.D. 2.8), were recruited from a cohort of present

university students. The study was approved by the

ethical committee of the Guangzhou University of Tradi-

tional Chinese Medicine. All subjects gave their in-

formed consent, both verbally and in writing, after being

informed about the study. All subjects filled out a ques-

tionnaire on lifestyle, medical history, and dietary habits.

They were nonsmokers, no color blind, and had a mod-

erate body mass index (BMI) of 21.3 (S.D. 1.1) kg/m2.

Exclusion criteria for participation were chronic and

current illness; a history of psychiatric or medical illness;

medication use; metabolic, hormonal, or intestinal dis-

eases; irregular diets or deviant eating habits; excessive

use of alcohol, cigarettes, coffee, or drugs; allergy to

milk products; All subjects who participated in the ex-

periment had a BMI in the normal range of Asian adults

(BMI: 18.5 kg/m2 - 22.9 kg/m2), were nonsmokers, and

were not allowed to drink alcohol or take any drug for 2

d before and during the experiment.

2.2. Stud y Design

A repeated-measures, counterbalanced cross-over de-

sign was used. Each subject was tested in two sessions

separated by exactly 1 week. Subjects were told that

various physiological and psychological effects of food

intake were examined, but they were not aware of in-

gesting different ratios of macronutrients. To avoid in-

terferences of learning with treatment effects, the sub-

jects had to practice all questionnaires and tests on two

separate days in the week before the experimental period.

In this way, the subjects were familiar with the experi-

mental procedure.

To ensure similar baseline conditions, subjects were

not allowed to ingest alcohol or caffeine-containing

drinks and foods, and were requested to refrain from

violent physical activity the day before each testing. In

addition, all subjects consumed an identical supper meal

between 1800 and 1900 h on the evening before each

testing. The meal consisted of steamed rice (raw rice 150

g), steamed fish (100 g), almond beancurd (80 g), vege-

tables and fruits (250 g). It provided approximately 3400

kJ, with 65%, 15% and 25% of the energy derived from

carbohydrates, protein and fat, respectively, and the

composition of the meal suggested a medium glycemic

index (GI). In order to avoid a depletion of liver glyco-

gen stores over night the supper was rich in carbohy-

drates and scheduled late. Subjects were asked to ingest

all supper and to have no further food or drinks except

water before testing. Subjects were also asked to sleep

for at least 8 h. Subjects arrived at the institute by public

transport. All subjects were tested simultaneously, be-

ginning at 0700. Just after arrival, subjects had to fill out

a questionnaire checking their compliance with the re-

strictions on the day before as well as their sleep quality

and their actual mental and subjective physical per-

formance. Before the test meal, baseline assessments

were taken in the order (1) questionnaire, (2) alertness

and attention, (3) mood, (4) satiety, (5) body temperature,

(6) blood samplings. Twenty minutes were scheduled for

each of these assessments. Subsequently, the cream-like

test meal was served in a dessert bowl. Subjects spent 10

min to eat whole meal with a spoon and afterwards 5

min to fill in a questionnaire concerning the meal’s ac-

ceptance and sensory properties. For repeated postpran-

dial measurements within the next 4 h, subjects rotated

each hour through the same stations as at baseline. Sub-

jects had free access to pure water during the whole

study, but no additional food or beverages intake was

permitted. Preparation and intake of test breakfast were

Y. C. Zeng et al. / Health 3 (2011) 383-393

385385

controlled by a dietitian. Subjects were sedentary, and

only reading was allowed in a study room. (Figure 1)

Openly accessible at

2.3. Test Breakfast

The two breakfasts consisted of isoenergetic (3400 kJ),

differed in content of the carbohydrates and protein.

Suspensions mixed at three different ratios: the HP meal

with a PRO/CHO/FAT ratio of 5:3:2; the AP breakfast

with a PRO/CHO/FAT ratio of 1:7:2. All test meals was

controlled by a dietitian and had similar volume and

sensory properties (taste, consistency and color). They

were freshly prepared by mixing appropriate quantities

of basic ingredients and water to obtain 500 ml. Differ-

ent kinds of protein (milk protein and egg white powder)

and carbohydrates (glucose, maltodextrin, rice starch)

were combined to cover a broad range of the representa-

tive compounds that might affect cognitive behavior

differentially. The carbohydrate proportion of the test

meals suggested a medium GI. A differentiation was

only made in the content of carbohydrates and protein,

respectively (Ta b l e 1 ). The meals were served in a ran-

dom order one week apart. Each meal was ingested

within 10 minutes. The energy content of the test meals

was in the range of the subjects’ habitual energy intake

in the morning. Acceptance and sensory homogeneity of

the two meals were tested by staff members of clinical

nutrition department.

2.4. Study Protocol

The study was a 2-day, randomised, crossover trial. At

day 01, subjects were randomly assigned to receive a

breakfast with a high or low ratio of simple-to-complex

carbohydrates. At day 08, after at least 1-week wash-out

period, subjects received the alternate breakfast. The

subjects were instructed to eat and drink the same foods

the evening before a test day. After they subjects arrived

at the institute, they filled out a wellbeing questionnaire,

and were weighed. Their subjects blood glucose and

insulin concentrations were examined after an 8 hour

fast. When the subjects rested 10 min, their body tem-

perature were measured. Then, the subjects started eating

the test breakfast immediately. After breakfast, which

was consumed in 10 min, the subjects were not allowed

to eat or drink anything during 4 h. Blood was collected

at 0, 60, 120, 180, 240 min after breakfast. Immediately

after each blood sample was taken, the subjects filled out

Visual Analogue Scales (VAS) to measure their subjec-

tive feelings of hunger, fullness. Simultaneously, body

temperature was recorded .The subjects received tests

about mood, alertness and attention at fasting, 120, 240

min after breakfast.

A M S

T B

S T B

S T B ST B

9:35

A MS

T BA M S

T B

arrival and

uestionnaire

alertness and attentionmoo

satiet

lood sam

lin

tem

erature

test breakfast and questionnaire

Figure 1. Schedule of experimental procedures for the subjects on each test morning. The first and second pe-

riod followed the same order of procedures.

Y. C. Zeng et al. / Health 3 (20 11) 383-393

386

Table 1. Composition of the cream-like test meals (3400 kJ; 50 ml).

Basic ingredients

(g)a

Highprotein

PRO/CHO/FAT [5:3:2]

adequate-protein

PRO/CHO/FAT [1:7:2]

Glucoseb 6.1 14.9

Maltodextrinc 52 119.7

Rice starchd 6.1 14.9

Milk proteine 95.4 18.9

Dried chicken 10.6 2.1

Egg white

powderf

Soybean oilg 15 15

Water 350 300

aFor sensory acceptance, 0.5 g/L of a nonenergetic powdered mixture of sweeteners (aspartame:acesulfame-K = 1:1) as well as 3

ml/L of vanilla flavor (Beijing first delicious Food Co., LtdSwitzerland) were also added before mixing. The creams were later col-

ored, using an egg-yellow food color (1 ml/L, Shanghai Dyestuffs Research Institute Co., Ltd. China), to get an identical appetizing

yellow color. bGlucose, commercially available from Tanye (Tianjin) Food Co., Ltd. China. cMaltodextrin (Tanye). dRice strarch

(Tanye). eMilk protein, commercially available from Shanghai Insight Protein Nutrition Institute, China. fegg white powder, com-

mercially available from Shanghai Insight Protein Nutrition Institute, China. gSoybean oil, commercially available from COFCO,

China.

2.5. Blood Glucose and Insulin

Blood was collected by finger prick with a DR- II

Automatic Blood Sampler lancet device (Eicom, Japan).

Plasma glucose was measured by using a blood glucose

meter (OneTouch Ultra, LifeScan Inc.). Serum was

pooled for each subject, and plasma insulin was meas-

ured by radioimmunoassay using commercial kits (Bei-

jing North Institute of Biological Technology, China).

2.6. Body Temperature Measurement

Subjects were instructed to remain awake and not to

move, fidget or talk once test breakfast was finished

eating. Body temperature was measured by means of a

rectal thermistor (Zhangzhou Shuangjia Medical Equip-

ment Co., Ltd, China), except during showers and bowel

movements, and room temperature was maintained at 24

- 25℃ as measured with an air conditioner.

2.7. Satiety

A validated satiety score numerical scale was used

according to the method of Haber et al [23] on the basis

of a scoring system with grades from −10 cm (extreme

hunger) to 10 cm (extreme satiety) VAS. VAS are often

used to measure subjective appetite sensations and the

validity and reproducibility have been shown in several

studies [23,24]. Subjects were instructed to rate them-

selves by marking the scale at the point that was most

appropriate to their feeling at that time. The distance

from this point to the left end of the scale was measured

in mm; changes from baseline were calculated by sub-

tracting the baseline score (−5 min) from the score at a

certain time point.

2.8. Mood and Alertness State

The VGZ [25] is a self-administered questionnaire

assessing how participants “feel at the moment.” Sub-

jects were asked to rate 15 items in relation to their

mood. The items were clustered into the 5 dimensions of

negative affect (depressed, unhappy, and queasy), posi-

tive affect (happy, well, and cheerful), information up-

take (fascinated, interested, and uninterested), arousal

(calm, nervous and agitated), and alertness (tired, sleepy

and awake). All answers were given on a 5-point rating

scale ranging from not at all to very much.

2.9. Continuous Performance Test

The continuous performance test (or continuous atten-

tion test) presents stimuli-target and non-target in a mix-

ture at regular intervals. The CPT is a tool to test task

vigilance and distractibility by allowing the subject to

react in the presence of a prescribed specific target. Vis-

ual stimuli consisted of individual letters and were pre-

sented sequentially on a computer screen for 250 ms

each. Subjects were instructed to press a button when-

ever the letter A (correct cue) was followed by the letter

X (correct target). All other sequences were to be ig-

nored, including sequences in which an incorrect cue

(designated ‘B’, but comprising all letters other than A or

X) was followed by the target letter (X) or sequences in

which a correct cue (A) was followed by an incorrect

target (designated ‘Y’, but comprising all letters other

than A or X). Stimuli were presented in four blocks of

280 stimuli (140 pairs) each. Within each block, 50% of

Y. C. Zeng et al. / Health 3 (20 11) 383-393

387387

the cue-target sequences were presented with short (0.8 s)

interstimulus interval (ISI) and 50% with long ISI (4 s).

Short and long ISIs were pseudorandomly intermixed.

The time between stimulus pairs was constant at 0.8 s.

Of the stimulus pairs, 70% were AX sequences; all other

sequences (BX, AY, BY) occurred with a probability of

0.1 each. The results were converted into values of as-

sessments on the basis of standard computation from the

normal group of the same age [26]. The measured values

were used for statistical analyses.

2.10. Statistics

All statistical analyses were performed with SPSS

version 15.0 for Windows (SPSS Inc., Chicago, IL,

USA). Results were expressed as mean ± standard de-

viation (s.d.), unless stated otherwise. The obtained data

(blood parameters and questionnaires) were analysed by

means of t-tests to investigate the differences between

the two sorts of breakfast. A repeated-measures analysis

of variance was carried out to determine possible differ-

ences between conditions. Linear correlation analyses

were performed to determine the relations between body

temperature and selected variables. Effects of HP were

evaluated using repeated-measures ANOVAs with ses-

sions (HP vs AP) and time (baseline vs HP/AP admini-

stration) as repeated measures. For the analyses of per-

formance of CPT, dependent measures consisted of hit

rate (correct detection of AX sequences) and false alarm

rates to BX, AY, or BY sequences. Effects of HP break-

fast on hit rate were evaluated with 2 × 3 × 2 factorial

repeated-measures ANOVAs with session (HP vs AP),

time (baseline vs HP/AP administration), and ISI (short

vs long) as repeated measures. For analyses of false

alarm rates, an additional within-subject factor with

three levels denoting false alarm type (BX vs AY vs BY)

was included. Differences between rates of BX errors

and AY and BY errors, respectively, during the two

phases of both sessions were evaluated with simple

within-subject contrasts involving session (contrast: HP

vs AP), time (contrast: Baseline vs HP/AP administra-

tion), and false alarm type (contrast: BX vs AY; BX vs

BY). Post hoc paired t-tests were used to assess specific

differences if indicated. Significance was defined as P <

0.05.

3. RESULTS

3.1. Glucose and Insulin

Postprandial plasma glucose and insulin concentra-

tions after the HP were increased less than after the AP

within 60 minutes. However, plasma glucose and insulin

concentrations after the HP meal were decreased less

than after the AP 60 minutes, with significant differences

between the HP and AP, with significant differences be-

tween the HP and AP meals. There were also significant

Meal × Time interactions (F = 1745.32, P = 0.000 for

glucose; F = 886.80, P = 0.000 for insulin) (Figure 2).

3.2. Body Temperature

Body temperature rose steadily all experiment session

on both diets. The change in body temperature from the

fasting baseline value was +0.1℃, +0.1℃, +0.2℃, +0.4

℃ at 0 min, 60 mim, 120 min, 180 min and 240 min

after the AP breakfast meal respectively; after the HP

breakfast meal, the change in body temperature from the

240180120

Before

Time (min)

（mmol/L）

Glucose

AP 400

300

200

100

(pmmol/L)

Insulin

< 0.01

240 180 120

Before

Time (min)

Figure 2. Profile plots for glucose and insulin responses to HP breakfast and AP breakfast. Mean

(S.E.M.); n = 13.

Y. C. Zeng et al. / Health 3 (20 11) 383-393

388

fasting baseline value was +0.1℃, +0.2℃, +0.6℃, +0.8

℃, +0.7℃ respectively. Body temperature after HP in-

creased more than AP (t120 min = 2.41, p = 0.024; t180 min =

3.77, p = 0.001; t240 min = 3.88, p = 0.001) There were

also significant Meal × Time interactions (F = 74.56, P =

0.000) (Figure 3).

3.3. Satiety

Ingestion of HP breakfast resulted in a significantly

higher satiety than the AP breakfast, with significant

differences between the HP and AP meals. There were

also significant Meal × Time interactions (F = 106.03, P

= 0.000) (Figure 4).

3.4. Mood and Alertness State

Consumption of breakfast showed positive effects on

the mood of the study population. Intake of HP breakfast

caused improvements in positive affect (time240:t = 5.22,

P = 0.000), information uptake (time120:t = 2.89, P =

0.008; time240:t = 2.67, P = 0.013) and alertness

(time120:t = 2.77, P = 0.011; time240 :t = 3.07, P = 0.005)

and a decrease in negative affect (time120:t = −2.36, P =

0.027; time240:t = −2.91, P = 0.008) and arousal

(time120:t = −2.37, P = 0.026; time240:t = −2.44, P =

0.023). There were also significant Breakfast × Time

interactions (Table 2).

240180 120

Before

Time(min)

37.2

37.0

36.8

36.6

36.4

℃

Body temper ature

< 0.01

Figure 3. Profile plots for body temperature responses to HP

breakfast and AP breakfast. Mean (S.E.M.); n = 13.

240

180

120

< 0.01

Time

Satiet

(

)

Satiety score

Before

Figure 4. Profile plots for satiety score responses to HP break-

fast and AP breakfast. Mean (S.E.M.); n = 13.

Table 2. Effect of breakfast on mood (VGZ) and results of multifactorial analysis of variance with repeated measures.

Score, Mean ± SD Breakfast Time Breakfast* Time

HP AP F P F P F P

Negative affect, t Before

Negative affect, t120

Negative affect, t240

Positive affect, t Before

Positive affect, t120

Positive affect, t240

Informationuptake, tBefore

Information uptake,t120

Information uptake, t240

Arousal, t Before

Arousal, t120

Arousal, t240

Alertness, t Before

Alertness, t120

Alertness, t240

3.60 ± 0.54

3.31 ± 0.51*

3.25 ± 0.52*

5.20 ± 0.67

6.27 ± 0.59

6.97 ± 0.72*

4.57 ± 0.39

5.29 ± 0.37*

5.40 ± 0.48*

2.84 ± 0.15

2.39 ± 0.29*

2.41 ± 0.36*

4.14 ± 0.52

4.91 ± 0.47*

5.03 ± 0.57*

3.91 ± 0.37

3.73 ± 0.37

3.77 ± 0.39

5.00 ± 0.63

6.18 ± 0.62

5.66 ± 0.54

4.56 ± 0.35

4.91 ± 0.31

4.92 ± 0.44

2.96 ± 0.29

2.64 ± 0.26

2.71 ± 0.27

4.08 ± 0.53

4.41 ± 0.45

4.36 ± 0.54

20.002

37.922

40.904

36.762

42.196

0.001

0.000

339.033

678.440

382.220

100.652

104.656

0.000

23.767

184.933

133.940

5.751

31.928

0.000

0.009

0.000

*Significantly different from AP, P < 0.05 (mixed-model ANOVA).

Y. C. Zeng et al. / Health 3 (20 11) 383-393

389389

3.5. Continuous Performance Task

HP breakfast was associated with a significant raise

the hit rate at both ISIs. Post hoc t-tests confirmed sig-

nificantly higher hit rates during HP breakfast than dur-

ing the baseline and AP session. HP breakfast was asso-

ciated with a decline of false alarms, which was most

pronounced for false alarms to AY and BX sequences at

long ISIs. HP breakfast also declined for false alarms to

AY and BX sequences at short ISIs. In addition, there

were not false alarms to BY at any moments in two ses-

sions (Figure 5).

4. CORRELATIONS

4.1. Blood Glucose and Target Variables

Three kinds of positive emotion were correlated with

concentrations of blood glucose at 240 min (r240min =

0.65, p = 0.000). Two kinds of negative emotion were

negative correlation with concentrations of blood glu-

cose (r240min = −0.53, p = 0.006). Total continuous per-

formance task scores at 240 min were correlated with

concentrations of blood glucose (r240 min = 0.87, p =

0.000). No significant associations were observed be-

tween total CPT scores and concentrations of blood glu-

cose at 0 min, 120 min.

4.2. Body Temperature and Target Variables

Three kinds of positive emotion at three moments

were correlated with body temperature significantly (rbe-

fore = 0.86, p = 0.000; r120min = 0.95, p = 0.000; r240min =

0.95, p = 0.000). Two kinds of negative emotion at three

moments were negative correlation with body tempera-

ture (rbefore = −0.78, p = 0.000; r120 min = −0.95, p = 0.000;

r240 min = −0.91, p = 0.000). Furthermore, total continu-

ous performance task scores before breakfast, at 120 min

and 240 min after breakfast all were correlated with

body temperature (rbefore = 0.59, p = 0.002; r120 min = 0.73,

p = 0.000; r240 min = 0.85, p = 0.000).

5. DISCUSSION

The present study showed that differences within pro-

tein to energy ratios in an isoenergetic breakfast can re-

sult in a different effect on perception of satiety, mood

state and CPT scores in healthy male subjects. Our data

reveal significant HP breakfast meal effects as well as

Meal × Time interactions for CPT scores after the inges-

tion of meals with different protein to energy ratios in

the morning. Overall CPT performance was better after

HP breakfast meal than after AP breakfast. In addition,

changes in CPT performance and mood were related to

postprandial changes in glucose concentrations and body

temperature. Two test meals were moderately liked by

the subjects. As energy content, volume, acceptance, and

sensory properties of our test meals were matched, the

observed effects on metabolic, mood, and CPT scores

can be attributed to the ratio of protein to energy in-

gested. Interpreting cognitive effects after macronutrient

ingestion, the energy content, sex, age and the constitu-

tion of the subjects as well as the time have to be con-

sidered [27]. Our subjects were healthy young male stu-

dents, and the test meals matched their habitual breakfast

size. The subjects’ glycogen stores were approximately

not completely depleted because of the carbohy-

drate-rich

240 min 120 min

Before

1.0

0.8

0.6

0.4

0.2

0.0

1.0

0.8

0.6

0.4

0.2

0.0

Short ISI Hit Rate

a a

Long ISI Hit Rate

Hit

HP 0.08

0.07

0.06

0.05

0.04

0.03

0.02

0.01

0.0

Short ISI FA Rate

0.1

0.08

0.06

0.04

0.02

0.0

Short ISI FA Rate

a e

0.08

0.07

0.06

0.05

0.04

0.03

0.02

0.01

0.0

Long ISI FA Rate

0.1

0.08

0.06

0.04

0.02

0.0

Long ISI FA Rate

240 min120 min

Before 240 min120 min

Before

Figure 5. Effects of HP breakfast and AP breakfast on CPT performance. Mean (S.E.M.); n = 13. Bars without a

common superscript differ significantly (P < 0.01).

Y. C. Zeng et al. / Health 3 (20 11) 383-393

390

meal on the evening before the test day. Because the GI

of the evening meal was approximately medium, it may

not have influenced the glucose tolerance of the subjects

at the following morning significantly. Young healthy

males are less sensitive to nutritional variables than

young females and older people [28] or stress-prone in-

dividuals [29]. So our observed effects might be even

more pronounced in vulnerable or malnourished popula-

tion [30].

The Recommended Daily Allowance for protein is 0.8

g/kg and the typical Chinese consumes 1.16 g/kg or

about 15% of dietary energy as protein [31]. Advocates

of high protein diets often recommend that protein in-

takes meet or exceed 25% of dietary energy. High pro-

tein diets can reduce postprandial glucose rise and

maintain stabilization of postprandial insulin are known

[32,33]. Consistent with the protein content of our test

meals, plasma glucose and insulin concentration changed

less after the HP meals than after the AP meal. These

differences were most pronounced at 0 min, 60 min and

240 min after test meal ingestion. Because the brain is

very sensitive to changes in nutrient supply, small meta-

bolic changes may influence behavior performance [34].

An ‘inverted U’-shaped dose-response curve was re-

ported for the effects of plasma glucose [35], and insulin

concentration [36] on cognitive functions. It is likely that

the ascending or descending part of an ‘inverted U’ rela-

tion represents the acute positive and negative effects of

a rise or fall [37,38] in blood glucose concentration on

specific cognitive functions. However, constant meta-

bolic conditions [39] might optimize overall cognitive

performance [34,27] for a longer time period. The

plasma glucose concentration remained nearly constant

after the HP meal in present study.

In general, the typical thermic effect of protein is 20%

- 35% of energy consumed, this number usually falls

between 5% and 15% for carbohydrate [40]. A main

reason for the difference in the thermic effects of food

may be due to the fact that the body has no storage ca-

pacity for protein and thus it needs to be metabolically

processed immediately. The synthesis of protein and the

high ATP cost of peptide bond as well as the high cost of

urea production and gluconeogenesis are often cited

reasons for the higher thermic effect of protein [41,42].

Furthermore, concomitant with the thermic response to

the test diets was a slight rise in body temperatures. HP

feeding was associated with a greater degree of body

temperature change versus high carbohydrate (HC)

feeding [42] the changes in body temperature were sig-

nificantly different by diet, HP breakfast was associated

with a greater degree of body temperature change versus

AP breakfast, and at 120 min, 180 min, and 240 min this

change was significant, supporting the contention of

Brundin and Wahren [43] that protein ingestion elicits a

pyrogen-like effect.

There is convincing evidence that a higher protein in-

take increases satiety compared to diets of lower protein

content [33,44,45] at least in the short term. We con-

firmed also that the HP breakfast would increase subjec-

tive satiety, but longer experiments would be useful to

test whether these beneficial effects on the regulation of

appetite can be maintained and have a clinical relevance.

However, the mechanisms by which protein may affect

satiety remain elusive. Satiety is a complicated interac-

tion of psychological, behavioral and physiological

mechanisms. One theory was developed by Mellinkoff

[46]. Since amino acid concentrations are correlated with

a reduction in appetite, Mellinkoff believed there to be a

satiety center in the brain. The satiety center is sensitive

to serum amino acid levels and when levels reach a cer-

tain point, hunger would cease. Another possible mecha-

nism is a relationship between satiety and dietary in-

duced thermogenesis. In the investigation by Wester-

terp-Plantenga [10], differences in satiety over a period

of 24 hour were significantly correlated with differences

in 24 hour dietary induced thermogenesis.

In addition, Blom WA et al [33] believed the HP

breakfast reduced the gastric emptying rate and in-

creased satiety, probably through increased secretion of

cholecystokinin and glucagon-like peptide 1. This study

indicated the effects of HP breakfast on the mood of

healthy males. In assessments performed 0 min, 120 min

and 120 min after breakfast, participants of HP session

reported increased positive affect, information uptake

and alertness. At the same time, participants of HP ses-

sion decreased negative affection and arousal. In contrast,

participants of AP session reported contrary results.

Evidence indicates that macronutrient composition may

influence mood by affecting the synthesis of monoamine

neurotransmitters [47]. It has been suggested that car-

bohydrate-rich meals lead to increased fatigue and de-

creased alertness, whereas meals rich in protein increase

alertness and decrease drowsiness [48,28].

The present study indicated HP breakfast can raise the

hit rate at long ISI and decline of false alarms of both

ISIs than AP breakfast and fasting. Considerable effort

has been devoted to studying the relationship between

body temperature and human performance [49-51]. It

has been reported that cognitive function is improved by

increasing body temperature slightly above the normal

temperature of 37℃ and that cognitive function is re-

duced by decreasing body temperature below normal

[52,53]. Kleitman [54] originally proposed that the speed

of thinking depends on the level of metabolic activity of

the cells of the cerebral cortex, and by the raising of the

latter through an increase in body temperature we indi-

Y. C. Zeng et al. / Health 3 (20 11) 383-393

391391

rectly speed up the thought process. Kleitman’s hy-

pothesis is supported by results from studies [55,56] that

higher brain temperatures resulted in faster transmission,

whereas lower brain temperature resulted in slower

transmission. Moreover, when body temperature was

high, alertness was rated higher.

We also hypothesized that protein exerts its mood ef-

fects partly through the elevation of postprandial body

temperature and glucose concentrations. By bivariate

correlation analyses, we found the positive association

between body temperature and subjective positive mood,

CPT scores at all moments(0 min, 120 min and 240 min);

whereas negative association between body temperature

and subjective negative mood. However, the above-

mentioned association between glucose concentrations

and subjective mood, CPT scores only at 240 min after

test breakfast.

6. CONCLUSIONS

To conclude, HP breakfast can effectively stabilize

postprandial serum glucose concentrations and elevate

postprandial temperature of healthy male undergraduate

students. Our present findings demonstrate the relation-

ship between HP breakfast and mood, alertness and at-

tention. This study indicated that HP breakfast may en-

hance human performance probably by increasing the

thermic effect of a food and elevating body temperature.

This randomized trial demonstrated positive short-term

effects of HP breakfast on mood and CPT performance

in undergraduate students. The observed differences ac-

cording to gender and potential mediating effects be-

tween mood and performance deserve further investiga-

tion.

7. ACKNOWLEDGEMENTS

We thank Li-Bo Zhou for providing us with the statistical expertise.

We thank Yan-Lin Zhou, Wen-Feng Zhao and Yun-Zhang for their

technical assistance. We are also grateful to the research volunteers and

a number of assistants of our hospital for their experimental assistance

during the study.

Competing interests: The authors declare that they have no com-

peting interests.

Authors’ contributions: YZ designed and carried out the experi-

ment of this manuscript and drafted the manuscript and approved the

final manuscript; SL and GX participated in the design of the study and

revised the manuscript. HS and JW participated the experiment. All

authors read and approved the final manuscript. All authors lacked any

conflict of interest.

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ABBREVIATIONS

HP: high protein;

AP: adequate protein;

CPT: continuous performance test;

MI: body mass index;

HC: high carbohydrate;

GI: glycemic index;

VAS: visual analogue scales