Asia Pac J Clin Nutr 2018;27(2):359-365 359

Original Article

Regular egg consumption at breakfast by Japanese

woman university students improves daily nutrient
intakes: open-labeled observations

Chie Taguchi PhD1, Yoshimi Kishimoto PhD1, Norie Suzuki-Sugihara PhD2, Emi Saita
1 3 3 3
PhD , Mika Usuda MSc , Wei Wang MSc , Yasunobu Masuda PhD , Kazuo Kondo MD,
1,4
PhD

1
Endowed Research Department “Food for Health”, Ochanomizu University, Tokyo, Japan
2
Department of Nutrition and Food Science, Graduate School of Humanities and Sciences, Ochanomizu
University, Tokyo, Japan
3
R&D Division, Kewpie Corporation, Tokyo, Japan
4
Institute of Life Innovation Studies, Toyo University, Gunma, Japan

Background and Objectives: Eggs, an important source of high-quality protein, contain a variety of key nutri-
ents and antioxidants. Here we conducted an intervention study to evaluate whether the additional consumption of
one egg per day would affect the daily nutritional intakes and blood antioxidant status in Japanese woman univer-
sity students. Methods and Study Design: For 4 weeks, the 14 subjects were provided a nutritious breakfast in-
cluding one boiled egg, and they were asked to keep a daily dietary record. Results: The subjects’ daily energy
intake during the intervention did not differ compared to the baseline, whereas the protein energy ratio and cho-
lesterol intake were significantly increased. The subjects’ consumption of confectionery during the intervention
was significantly decreased compared to the pre-trial period. The total score of adherence to the food-based Japa-
nese dietary guidelines for a healthy diet during the intervention was higher than that at baseline. The analysis of
fasting blood samples showed that the subjects’ serum lipids levels were not altered, whereas their malondialde-
hyde modified low-density lipoprotein (MDA-LDL) levels and the oxidative susceptibility of LDL were signifi-
cantly reduced after the intervention. More importantly, serum folic acid levels were significantly increased.
Conclusions: Our results suggest that regular egg consumption at breakfast can help improve the daily nutritional
status and dietary habits and also ameliorate certain indices of antioxidant status in young women.

Key Words: egg, breakfast, nutritional balance, dietary habit, antioxidant

INTRODUCTION adults — especially those living alone — tend to consume

According to the International Egg Commission survey convenience breakfasts such as white rice or bread with-
(2014), the reported per capita annual egg consumption in out side dishes, which comprise a nutritionally poor and
Japan was 329, the third highest in the world.1 Eggs are unbalanced diet. Tani et al recently reported that a higher
one of the most nutritious foods, with significant protein, proportion of total energy intake during the morning
vitamins and minerals, and eggs can make a great contri- might reduce the absolute intake of energy during the day
bution to a nutritious diet. It was reported that compared in Japanese women.7 It was also reported that increases in
to nonconsumers, the daily nutrient intake of American dietary protein at breakfast had greater effects on satiety
egg consumers was significantly greater for all nutrients compared to other mealtimes.8-10 These findings suggest
that the addition of a protein-rich breakfast might be an
except dietary fiber and vitamin B-6.2 Thus, eggs can be a
effective strategy to improve the nutritional balance and
nutritious inclusion in the diet for people of all ages and
appetite control in young people. Considering its relative-
at different stages of life, especially for those at risk of
ly low cost, ease of preparation and variety of dishes, the
low-nutrient intakes such as the elderly, pregnant women egg is an ideal source of high-quality protein, especially
and children.3-5
Although the importance of regular dietary habits and Corresponding Author: Dr Yoshimi Kishimoto, Endowed
not skipping breakfast is well appreciated, the percentage Research Department “Food for Health”, Ochanomizu Universi-
of breakfast skippers among college students in Japan is ty, 2-1-1 Otsuka, Bunkyo-ku, Tokyo 112-8610, Japan.
high. It was reported that managing the frequency of Tel: +81-3-5978-5810; Fax: +81-3-5978-2694
skipping breakfast and reducing it to <3 times per week Email: [email protected]
may be beneficial for the maintenance of bone health in Manuscript received 10 August 2016. Initial review completed
young women.6 Even among breakfast eaters, younger 08 November 2016. Revision accepted 16 December 2016.
doi: 10.6133/apjcn.042017.17
360 C Taguchi, Y Kishimoto, N Suzuki-Sugihara, E Saita, M Usuda, W Wang, Y Masuda and K Kondo

for breakfast. toast with margarine/jam, vegetable salad, low-sugar yo-

In addition to their macronutrients, eggs contain high gurt, fruit juice and black tea. Boiled eggs were obtained
amounts of antioxidants in both the egg white and yolk. from the Kewpie Corp. (Tokyo). This breakfast had 551
Several aromatic amino acids in egg (tryptophan and ty- kcal energy content with 20.3 g protein (14.8% of energy),
rosine), egg lipids such as phospholipids, and micronutri- 15.9 g fat (25.8% of energy), and 82.3 g carbohydrate
ents such as vitamin E, vitamin A, selenium, and carote- (59.4% of energy) on average. The subjects were asked to
noids are reported to have antioxidant properties.11,12 A complete two visual analog scales (VASs), one for sleep-
number of egg-derived peptides have been shown to have iness and one for appetite, before breakfast each weekday.
antioxidant activities in vitro.13-15 Carotenoids are lipo- These scales were 100-mm long with words anchored at
philic compounds responsible for the orange-yellow color each end expressing the most negative (score=0) and the
of the egg yolk. The xanthophyll carotenoids lutein and most positive rating (score=100). On holidays the sub-
zeaxanthin are known to be effective to protect the eyes jects were asked to consume breakfast containing a pro-
from age-related macular degeneration,16 and they also vided egg at home. The subjects were also asked to main-
play an important role in preventing atherosclerosis de- tain their normal lifestyle throughout the 4-week study
velopment through their antioxidant activities.17,18 An period.
intervention trial with elderly subjects revealed that con-
suming only one egg per day significantly increased the Dietary assessments
serum concentrations of both lutein and zeaxanthin.19 The At the beginning and again after the study period, the
health benefits of antioxidants are in large attributed to its subjects’ dietary habits during the previous month were
protective effect against reactive oxygen species damage assessed using a food frequency questionnaire, i.e., a
by quenching singlet oxygen and scavenging free radi- brief-type self-administered diet history questionnaire
cals.20 (BDHQ) which was validated by Kobayashi et al.21,22 The
Despite its essential nutritious aspects, eggs have some- subjects were also instructed to take pictures and record
times been considered an adverse food for human health, the contents of their daily meals, snacks, and beverages in
mainly due to their cholesterol content. Nowadays it is a diet diary for 5 weeks (1 week before the intervention
known that the response of cholesterol in human serum to started and for the 4 weeks of intervention). The diet dia-
dietary cholesterol consumption depends on several fac- ry was collected every weekday, and each subject’s meal
tors, such as an individual’s genetic makeup, hormonal intake and daily intakes of energy, fat, protein, carbohy-
factors and nutritional status. drate, and other nutrients were calculated from the diary
In the present study, we designed a nutritious breakfast record by an experienced dietitian on the basis of the
that included one egg to provide high-quality protein, and 2010 Standard Tables of Food Composition in Japan.23
we conducted an intervention study to evaluate the effects We also calculated a score for adherence to the food-
of consuming this breakfast for 4 weeks on the subjects’ based Japanese dietary guidelines, using a procedure de-
nutrient intake and blood parameters (including antioxi- veloped by Oba et al.24 Servings of (1) grain dishes, (2)
dant status) in women university students. vegetable dishes, (3) fish and meat dishes, (4) milk, and
(5) fruits, and (6) the energy intake from snacks and alco-
METHODS holic beverages were calculated from the food frequency
Subjects questionnaire, and the values were energy-adjusted by the
Subjects were recruited from the training course for regis- density method to obtain the values per 1800 kcal of en-
tered dietitians at Ochanomizu University through a re- ergy to enable a comparison with the recommended val-
cruitment poster with the exclusion criterion of allergy to ues.25 The six scores (ranging from 0 to 10 each) were
eggs. The study protocol was approved by the Ethics summed to provide the overall score on adherence to the
Committee of Ochanomizu University and conformed to food-based Japanese dietary guidelines (ranging from 0 to
the Declaration of Helsinki. This trial was registered with 60).
the UMIN-CTR (http://www.umin.ac.jp/ctr/index.htm) as
UMIN000011932. Fourteen woman students (ages 18–22 Blood sampling and measurements
years) were enrolled. Written informed consent was ob- Before and again at the end of the study period, each sub-
tained from the subjects, and parental consent was re- ject's body weight, abdominal circumference and blood
quired and obtained for minor subjects (<20 years). Ac- pressure were measured, and blood samples were ob-
cording to the results of a questionnaire distributed before tained between 7:00 am and 8:30 am after an overnight
the study, 10 of the 14 subjects were eating breakfast eve- fast from 8:00 pm of the previous day. Total protein was
ry day, and the others sometimes skipped breakfast. The measured by the Biuret method, and albumin was meas-
mean age of the subjects was 19.6±1.2 years, and the ured by the modified bromcresol purple (BCP) method.
BMI was 21.1±2.2 kg/m2. None of the subjects had any The blood glucose concentration was measured by the
degree of smoking habit. hexokinase UV method. The serum insulin and folic acid
concentrations were measured by a chemiluminescent
Study design and diets enzyme immunoassay (CLEIA). Total cholesterol, high-
A single-arm, open-design intervention lasting 4 weeks density lipoprotein (HDL) cholesterol, triglyceride, non-
was performed in October and November 2013. All sub- esterified fatty acids (NEFAs) and magnesium were
jects were provided a nutritious breakfast at 8:00–9:00 am measured by enzymatic procedures.
every weekday at their university. A breakfast menu was Each subject’s low-density lipoprotein (LDL) choles-
prepared consisting of one boiled egg, one piece of white terol was calculated using the Friedewald formula. The
 Breakfast with an egg for young women 361

serum iron concentration was measured by the Nitroso- Ann Arbor, MI) according to the manufacturer’s instruc-
PSAP method, and the serum ferritin concentration was tions.
measured using a latex agglutination immunoassay. The
serum calcium concentration was measured by the chlo- Statistical analyses
rophosphonazo-III method. The serum lutein+zeaxanthin All data are presented as mean±SD. Comparisons of the
and vitamin C concentrations were measured by high- data obtained before (baseline) and after the 4-week in-
performance liquid chromatography, and the vitamin E tervention were performed using a two-tailed Wilcoxon
concentration was measured by the fluorometric method. signed rank test. Differences were considered significant
The malondialdehyde modified LDL (MDA-LDL) con- when p<0.05. The statistical analyses were performed
centration was measured by an enzyme-linked immuno- using the GraphPad Prism 5 software package (GraphPad
sorbent assay (ELISA). The serum iron, ferritin, calcium Software, La Jolla, CA).
and magnesium levels were measured using an automated
clinical analyzer (BIOLIS 24i, Tokyo Boeki Machinery, RESULTS
Tokyo). The serum lutein+zeaxanthin level was measured Nutritional intakes
by Nikken Seil (Shizuoka, Japan), and the other basic All 14 subjects completed the intervention and did not
biochemistry tests were performed by the laboratory SRL miss the one egg per day requirement during the 4-week
(Tokyo). intervention. The subjects’ nutritional intakes from their
LDL was separated from plasma by single-spin density weekday breakfasts and their daily nutritional intakes
gradient ultracentrifugation at 100,000 rpm for 40 min at calculated from the dietary records are shown in Table 1.
4°C. The LDL oxidizability was determined by lag time All that the subjects ate or drank before 9:00 am was con-
assay as described.26 The prepared LDL samples (final sidered breakfast.
concentration of protein: 70 μg/mL) were oxidized by 200 The results of our analyses revealed that the subjects’
μM 2,2-azobis-4-methoxy-2,4-dimethylvaleronitrile energy intake at breakfast during the intervention was not
(Wako Pure Chemicals, Osaka, Japan). The kinetics of significantly different from that before the intervention,
LDL oxidation were determined by monitoring the ab- but that the intakes of protein (12.7±2.2% to 14.8±0.3%,
sorbance of conjugated dienes at 234 nm using a spectro- p<0.01) and some vitamins such as α-tocopherol, folate
photometer (DU800, Beckman Coulter, CA, USA) at 4- and ascorbic acid, dietary fiber, and cholesterol were sig-
min intervals at 37°C. nificantly higher during the intervention.
The total antioxidant capacity was determined by a As for daily intakes, the subjects’ energy intake during
2,2'-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid) the intervention was not significantly different from that
(ABTS) radical scavenging assay (Cayman Chemical, before the study. However, the energy percentage from

Table 1. The subjects’ nutritional intakes for breakfast and daily

Breakfast† Daily‡
Baseline Egg period Baseline Egg period
Energy (kcal) 478 ± 179 556 ± 29 1950 ± 388 1946 ± 247
*
Protein (g) 15.7 ± 7.5 20.5 ± 1.1 66.3 ± 13.6 70.3 ± 9.1
** *
Protein (% energy) 12.7 ± 2.2 14.8 ± 0.3 13.7 ± 1.1 14.5 ± 0.7
Fat (g) 15.2 ± 7.7 16.0 ± 1.3 64.9 ± 17.8 68.3 ± 11.1
#
Fat (% energy) 28.5 ± 7.1 25.7 ± 1.3 29.4 ± 3.0 31.0 ± 2.6
Saturated fatty acids (g) 5.3 ± 4.1 4.0 ± 0.6 20.5 ± 6.8 21.1 ± 4.5
Monounsaturated fatty acids (g) 4.9 ± 2.8 6.0 ± 0.4 23.5 ± 7.6 25.8 ± 4.3
*
Polyunsaturated fatty acids (g) 2.7 ± 1.2 3.7 ± 0.3 11.7 ± 3.0 12.3 ± 1.4
*** ***
Cholesterol (mg) 91 ± 77 216 ± 3.0 360 ± 103 495 ± 72
*
Carbohydrate (g) 68.8 ± 24.6 83.1 ± 4.7 266 ± 42.9 256 ± 32.4
*
Carbohydrate (% energy) 58.8 ± 7.3 59.5 ± 1.2 56.9 ± 2.8 54.5 ± 2.9
**
Soluble dietary fiber (g) 0.8 ± 0.3 1.0 ± 0.1 3.5 ± 0.5 3.4 ± 0.6
*
Insoluble dietary fiber (g) 2.3 ± 0.9 2.8 ± 0.2 10.2 ± 1.5 9.8 ± 1.9
#
Dietary fiber (g) 3.2 ± 1.3 3.8 ± 0.3 14.3 ± 2.3 13.6 ± 2.0
Calcium (mg) 187 ± 124 194 ± 26 552 ± 179 558 ± 103
Magnesium (mg) 63 ± 31 67 ± 6 257 ± 43 246 ± 30
Iron (mg) 1.7 ± 0.9 2.1 ± 0.1 8.1 ± 1.4 7.8 ± 0.8
Vitamin A (retinol equiv.) (μg)§ 123 ± 71 155 ± 16 560 ± 117 569 ± 111
* **
Vitamin D (μg) 0.7 ± 0.7 0.9 ± 0.1 3.6 ± 1.5 4.8 ± 1.2
**
α-Tocopherol (mg) 1.9 ± 0.8 2.6 ± 0.2 8.6 ± 2.3 8.7 ± 1.2
*
Vitamin B-12 (μg) 0.8 ± 0.7 0.7 ± 0.1 3.7 ± 1.4 4.7 ± 0.8
***
Folate (μg) 68 ± 30 103 ± 6 305 ± 70 306 ± 46
*** *
Vitamin C (mg) 19 ± 11 52 ± 9 102 ± 65 113 ± 28
Values are mean±SD (n=14). Comparisons of the values between baseline and during the intervention period were performed using a
two-tailed Wilcoxon signed rank test. ***p<0.001, **p<0.01, *p<0.05, #p<0.10.
†
Nutritional intakes from the subjects’ weekday breakfasts.
‡
Their daily nutritional intakes.
§
Sum of retinol, β-carotene/12, α-carotene/24, and cryptoxanthin/24.
362 C Taguchi, Y Kishimoto, N Suzuki-Sugihara, E Saita, M Usuda, W Wang, Y Masuda and K Kondo

Table 2. Adherence to the food-based Japanese dietary guidelines for a healthy diet

Baseline Egg period

Servings
Grain dishes (servings/1800 kcal) 3.4 ± 1.0 3.7 ± 1.0
#
Vegetable dishes (servings/1800 kcal) 5.7 ± 1.9 7.2 ± 1.8
Fish and meat dishes (servings/1800 kcal) 6.4 ± 2.6 6.2 ± 1.7
Milk (servings/1800 kcal) 2.0 ± 1.3 2.0 ± 1.1
**
Fruits (servings/1800 kcal) 0.6 ± 0.7 1.6 ± 0.7
**
Snacks and alcoholic beverages (kcal/1800 kcal) 226 ± 63 129 ± 51
Scores
Grain dishes 8.5 ± 2.3 8.7 ± 1.2
Vegetable dishes 8.3 ± 1.7 7.2 ± 1.7
Fish and meat dishes 5.3 ± 3.6 5.3 ± 3.0
Milk 5.1 ± 3.2 6.2 ± 3.4
*
Fruits 3.6 ± 3.2 7.5 ± 2.5
*
Snacks and alcoholic beverages 7.9 ± 2.0 9.9 ± 0.3
#
Total score 38.9 ± 7.9 44.9 ± 5.5
Values are mean±SD (n=14). Comparisons of the values between basal and during the investigation period were performed using a two-
tailed, Wilcoxon signed rank test. **p<0.01, *p<0.05, #p<0.10.
One serving of grain dishes contained 40 g carbohydrate; one serving of vegetable dishes was 70 g; one serving of fish and meat dishes
contained 6 g protein; one serving of milk contained 100 mg Ca; and one serving of fruits was 100 g.
Recommended values are as follows: grain dishes, 4–5 servings/1800 kcal; vegetable dishes, 5–6 servings/1800 kcal; fish and meat
dishes, 3–4 servings/1800 kcal; milk, 2 servings/1800 kcal; fruits, 2 servings/1800 kcal; and snacks and alcoholic beverages, ≤200
kcal/1800 kcal. Total score ranging from 0 to 60.

protein (13.7±1.1% to 14.5±0.7%, p<0.05), vitamin D Biochemical analysis

(3.6±1.5 μg/day to 4.8±1.2 μg/day, p<0.01), vitamin B-12 The subjects’ baseline characteristics were all within the
(3.7±1.4 μg/day to 4.7±0.8 μg/day, p<0.05), vitamin C normal ranges. As anthropometric measurements, the
(102±65 mg/day to 113±28 mg/day, p<0.05) and choles- abdominal circumference, systolic blood pressure and
terol intake (360±103 mg/day to 495±72 mg/day, p<0.001) diastolic blood pressure values did not change with the
were significantly higher during the intervention com- intervention, whereas the subjects’ body weight and BMI
pared to the baseline values. were slightly decreased at the end of the intervention. The
results of most of the biochemical tests such as total pro-
Food group intake tein and albumin levels showed no significant changes
The food group intakes were estimated using the results after 4 weeks compared to the baseline values (Table 3).
of the food frequency questionnaire. The frequencies of In addition, the serum lipids such as total cholesterol,
fruit and egg consumption were significantly increased HDL cholesterol, LDL cholesterol, and triglycerides were
due to the consumption of the fruit juice and eggs provid- not altered by the 4-week intervention, despite the signifi-
ed at breakfast. In contrast, the subjects’ consumption of cant increase in the intake of dietary cholesterol (360±103
confectionery (e.g., candy and sweets) during the inter- mg/day to 495±72 mg/day).
vention was significantly lower than that at the baseline
(44±18 g/day to 30±18 g/day, p<0.05). Serum concentrations of vitamins and carotenoids
Although the subjects’ serum vitamin C and vitamin E
Healthy diet score levels remained unchanged, the folic acid concentration
The total score of adherence to the food-based Japanese was significantly increased by the dietary intervention
dietary guidelines for a healthy diet during the interven- (15.4 ±5.9 nmol/L to 18.1±4.8 nmol/L, p<0.05). The se-
tion tended to increase compared with that at baseline rum lutein+zeaxanthin level was slightly increased after
(38.9±7.9 to 44.9±5.5, p<0.10) (Table 2). The number of the intervention, but the difference was not significant
servings of fruits was significantly increased (0.6±0.7 (0.98±0.43 μmol/L to 1.14±0.46 μmol/L) (Table 3).
servings/1800 kcal to 1.6±0.7 servings/1800 kcal, p<0.01),
and the numbers of snacks and alcoholic beverages were Serum antioxidant status
significantly decreased during the intervention (226±63 The parameters of the subjects’ serum antioxidant status,
kcal/1800 kcal to 129±51 kcal/1800 kcal, p<0.01). MDA-LDL concentration, lag time, and antioxidant activ-
ity are shown in Table 3. Compared to the baseline values,
Feeling of sleepiness and appetite a significant decrease in the MDA-LDL concentration,
The subjects’ feeling of sleepiness and their appetite be- which is an index of LDL oxidation (124±30 U/L to
fore breakfast were evaluated using the VAS scores. The 108±17 U/L, p<0.05), and a significant prolongation of
sleepiness score remained unchanged, but the appetite the lag time, which is an index of the resistance of free
score after the 4-week intervention period was slightly radical-induced LDL lipid peroxidation (33.7±3.5 min to
but not significantly higher than that at baseline, indicat- 37.2±4.5 min, p<0.01) were observed. The serum total
ing that the subjects tended to feel more hungry in the antioxidant capacity (TAC) value after the intervention
morning (63±19 to 74±15 points, p<0.10). was slightly higher than that at baseline, but the differ-
ence was not significant (1.8±0.4 mM Trolox equiv. to
 Breakfast with an egg for young women 363

Table 3. The blood biochemical parameters an egg has a greater effect on the subjective feelings of
appetite (increased hunger) compared to a normal-protein
Before After breakfast.30-33 A nutritious breakfast with an egg might
Total protein (g/L) 75 ± 3 76 ± 4 therefore increase satiety, which may have contributed to
Albumin (g/L) 48 ± 2 48 ± 2 the present subjects’ decrease in confectionery consump-
Glucose (mmol/L) 4.44 ± 0.22 4.33 ± 0.33 tion.
Insulin (pmol/L) 52.1 ± 25.7 49.3 ± 28.5 We also assessed the score of adherence to the food-
Total cholesterol (mmol/L) 4.74 ± 0.67 4.87 ± 0.57 based Japanese dietary guidelines for a healthy diet based
HDL-C (mmol/L) 1.86 ± 0.47 1.86 ± 0.44 on the Japanese Food Guide Spinning Top.34 Our sub-
LDL-C (mmol/L) 2.54 ± 0.57 2.69 ± 0.41 jects’ baseline scores were above the mean value of
Triglyceride (mmol/L) 0.73 ± 0.08 0.65 ± 0.05 Nishimura et al’s study,25 and their scores during the in-
Phospholipids (mmol/L) 2.67 ± 0.32 2.62 ± 0.21 tervention were slightly increased from baseline
NEFA (μEq/L) 414 ± 148 416 ± 179 (38.9±7.9 to 44.9±5.5 points). The improvement of the
Iron (μmol/L) 16.4 ± 6.43 17.6 ± 6.77 score might be attributed to the decrease of confectionery
Ferritin (pmol/L) 48.1 ± 38.0 51.2 ± 34.8 consumption and the increase in the consumption of fruit.
Calcium (mmol/L) 2.42 ± 0.05 2.38 ± 0.05 * There were no appreciable changes in our subjects’ an-
Magnesium (mmol/L) 0.82 ± 0.04 0.82 ± 0.04 thropometric measurements or basic biochemistry results
Vitamin C (μmol/L) 0.53 ± 0.12 0.53 ± 0.07 during the investigation. Despite a significant increase in
Vitamin E (μmol/L) 25.5 ± 4.6 23.2 ± 4.6 the dietary cholesterol (360±103 mg/day to 495±72
Folic acid (nmol/L) 15.4 ± 5.9 18.1 ± 4.8 * mg/day, p<0.001), the subjects’ blood cholesterol levels
Lutein+zeaxanthin (μmol/L) 0.98 ± 0.43 1.14 ± 0.46 remained unchanged. The lack of the increase of serum
MDA-LDL (U/L) 124 ± 8 108 ± 5 * cholesterol could be attributed to the relatively low
Lag time (min) 33.7 ± 0.9 37.2 ± 1.2 ** amount of loaded cholesterol and to the subjects’ charac-
TAC (mM Trolox equiv.) 1.8 ± 0.1 2.1 ± 0.1 teristics as young and normolipidemic women. In addi-
tion to dietary cholesterol, the balance of saturated fatty
NEFA: nonesterified fatty acids; MDA-LDL: malondialdehyde acids and unsaturated fatty acids is well known to influ-
modified LDL; TAC: total antioxidant capacity.
†
ence the serum cholesterol level.35-38 In the present study,
Values are mean±SD (n=12–14). Comparisons of the values the ratio of polyunsaturated to saturated fatty acid (the
between before and after the investigation period were per- P/S ratio) during the intervention period was not signifi-
formed using a two-tailed, Wilcoxon signed rank test. **p<0.01,
*
p<0.05.
cantly different from that in the pre-intervention period.
The intake of antioxidants through the daily diet is
known to be important in reducing oxidative stress and
2.1±0.3 mM Trolox equiv.). preventing many diseases. In our subjects, the serum vit-
amin C and vitamin E concentrations exhibited no signif-
DISCUSSION icant changes after the dietary intervention, whereas the
The additional intake of an egg at breakfast successfully serum lutein+zeaxanthin level was slightly but not signif-
increased the healthy young women’s dietary energy per- icantly increased (0.98±0.43 μmol/L to 1.14±0.46
centage from protein and some nutrients’ intake, both for μmol/L). It is known that vitamin E donates its phenolic
breakfast and daily. The 4-week consumption of such a hydrogen to scavenge free radicals,39 and carotenoids
nutritious breakfast led to (1) an increase in the score of neutralize singlet oxygen and free radicals and protect
adherence to the food-based Japanese dietary guidelines against oxidative damage.40 Lutein and zeaxanthin are
for a healthy diet, (2) a decrease in the consumption of antioxidants that are commonly found in egg yolk, which
confections, and (3) decreases in the serum MDA-LDL may be important to decrease the susceptibility of the
level and the oxidative susceptibility of LDL. LDL particles to oxidation.41
According to Japan’s National Health and Nutrition The oxidation of LDL is well known as a risk factor for
Examination Survey in 2013, 25.4% of Japanese women cardiovascular disease.42,43 Several studies have shown
in their twenties are skipping breakfast.27 There were that egg consumers had higher blood levels of lutein and
fewer breakfast skippers among the present study’s sub- zeaxanthin.19,44 In the present study, one of the oxidative
jects, as they were registered dietitians ‘in the making’ products of LDL, i.e., the MDA-LDL concentration, was
and might be more strongly aware of their meals than decreased significantly, and the LDL oxidizability was
others of their generation. The provided breakfast had significantly prolonged after the intervention. The slight
556±29 kcal energy, which was enough for a breakfast increase in the subjects’ serum TAC value might suggest
for a young woman, but this kcal energy value was not improved antioxidant defense capacity. Wang et al. re-
significantly different from that of the breakfasts con- ported that the antioxidant capacity in the blood was as-
sumed by the subjects before the intervention. On the sociated with the dietary intake of antioxidants.45
other hand, the dietary energy percentage from protein In addition, the serum folic acid concentration of the
both at breakfast and daily was increased, and the daily subjects was increased after the intervention. Folate is one
intakes of some nutrients such as vitamins D, B-12 and C of the antioxidant vitamins, and its concentration is high
were significantly higher during the intervention. in vegetables and fruits as well as eggs. An increased se-
During the intervention, a decrease of confectionery rum folic acid concentration could be beneficial; folate is
consumption was observed. Some studies suggested that an important nutrient especially for young women plan-
breakfast consumption is important for the regulation of ning a pregnancy, because low folic acid status is known
energy intake.7,28,29 Tani et al showed that a higher pro- to be associated with neural tube defects,46 and folate
portion of total energy intake during the morning might deficiency leads to increased plasma homocysteine con-
reduce the consumption of confections as well as the ab- centrations, which are linked to the risks of cardiovascu-
solute intake of energy within the day in Japanese wom- lar disease47 and osteoporosis.48 The present study’s
en.7 It is known that a high-protein breakfast that includes breakfast including an egg provided the benefits of in-
364 C Taguchi, Y Kishimoto, N Suzuki-Sugihara, E Saita, M Usuda, W Wang, Y Masuda and K Kondo

creasing the intakes of protein and essential nutrients (e.g., 8. Leidy HJ, Bossingham MJ, Mattes RD, Campbell WW.
vitamin D, vitamin B-12 and folate), and it is a good Increased dietary protein consumed at breakfast leads to an
breakfast for all women of childbearing age. initial and sustained feeling of fullness during energy
Our study has several limitations. First, the open design restriction compared to other meal times. Br J Nutr. 2009;
and small sample size could be limiting factors for the 101:798-803.
interpretation of the results. There were both breakfast 9. Leidy HJ, Racki EM. The addition of a protein-rich
skippers and breakfast eaters among the subjects. In addi- breakfast and its effects on acute appetite control and food
tion, our findings may not be limited to the effects of eggs intake in ‘breakfast-skipping’ adolescents. Int J Obes (Lond).
because the provided breakfast contained other dietary 2010;34:1125-33. doi: 10.1038/ijo.2010.3.
factors such as vegetables and fruit juice. On the other 10. Leidy HJ, Lepping RJ, Savage CR, Harris CT. Neural
hand, the study’s strengths were that we investigated the responses to visual food stimuli after a normal vs. higher
dietary records in detail, and that we identified the associ- protein breakfast in breakfast-skipping teens: a pilot fMRI
ation between the dietary intervention and blood antioxi- study. Obesity (Silver Spring). 2011;19:2019-25. doi: 10.
dant parameters. 1038/oby.2011.108.
In conclusion, eating one egg per day at breakfast could 11. Nimalaratne C, Lopes-Lutz D, Schieber A, Wu J. Free
be good for supplying protein and maintaining one’s nu- aromatic amino acids in egg yolk show antioxidant
tritional balance, and we observed that consuming a nutri- properties. Food Chem. 2011;129:155-61.
tious breakfast with an egg for 4 weeks positively affect- 12. Nimalaratne C, Wu J. Hen egg as an antioxidant food
ed the dietary habits and two serum oxidative stress commodity: a review. Nutrients. 2015;7:8274-93. doi: 10.
markers, i.e., the serum MDA-LDL level and the oxida- 3390/nu7105394.
tive susceptibility of LDL, in healthy young women. Our 13. Rao S, Sun J, Liu Y, Zeng H, Su Y, Yang Y. ACE inhibitory
findings indicate that eggs are a good source of protein peptides and antioxidant peptides derived from in vitro
and antioxidants that may be valuable in designing digestion hydrolysate of hen egg white lysozyme. Food
healthy and nutritious diets. Further studies with a larger Chem. 2012;135:1245-52. doi: 10.1016/j.foodchem.2012.05.
number of subjects in a randomized crossover design are 059.
needed to precisely evaluate the effect of egg consump- 14. You SJ, Wu J. Angiotensin-I converting enzyme inhibitory
tion on health in young women. and antioxidant activities of egg protein hydrolysates
produced with gastrointestinal and nongastrointestinal
ACKNOWLEDGEMENTS enzymes. J Food Sci. 2011;76:C801-7. doi: 10.1111/j.1750-
No competing interests are reported. We thank the Kondo labor- 3841.2011.02228.x.
atory members (Ochanomizu University) for their assistance 15. Xu M, Shangguan X, Wang W, Chen J. Antioxidative
with this clinical trial, and the volunteers for participating in the activity of hen egg ovalbumin hydrolysates. Asia Pac J Clin
study. Nutr. 2007;16:178-82.
16. Krinsky NI, Landrum JT, Bone RA. Biologic mechanisms
AUTHOR DISCLOSURES of the protective role of lutein and zeaxanthin in the eye.
CT, YK and ES are affiliated with an endowed research depart- Annu Rev Nutr. 2003;23:171-201. doi: 10.1146/annurev.
ment sponsored by Kewpie Corporation. nutr.23.011702.073307.
17. Iribarren C, Folsom AR, Jacobs DR, Jr., Gross MD, Belcher
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