Glycative Stress Research
Online edition : ISSN 2188-3610
Print edition : ISSN 2188-3602
Received : April 28, 2020
Accepted : May 20, 2020
Published online : June 30, 2020
doi:10.24659/gsr.7. 2_174

Original article

Effect of the postprandial blood glucose on lemon juice and rice intake.
Masayuki Yagi 1), Shiori Uenaka 1), Kaori Ishizaki 1), Chieko Sakiyama 1),
Rika Takeda 2), Yoshikazu Yonei 1)
1) Anti-Aging Medical Research Center and Glycative Stress Research Center, Faculty of Life and Medical Sciences,
Doshisha University, Kyoto, Japan
2) Pokka Sapporo Food & Beverage Ltd., Nagoya, Aichi, Japan

Abstract

Objective: Persistence of postprandial hyperglycemia causes elevation of glycative stress. The purpose of this study was
to examine the suppressing effect of lemon juice on postprandial hyperglycemia when ingesting cooked rice, thereby, thechanges in blood glucose (BG) levels were compared and verified, based on an intake of cooked rice alone as a standard, whenlemon juice was ingested before cooked rice.
Methods: Subjects were 12 healthy males and females aged 20 to 30 years old who participated in a briefing session heldin advance and provided written consent. The changes in BG level were verified between three test foods as follows: when
the cooked rice was ingested alone (A), 15 g of lemon juice was ingested before the rice (B), and 30 g of lemon juice wasingested before the rice (C). Lemon juice was ingested after diluting it with 150 mL of water. FreeStyle Libre Pro was used
for the test, and the measured glucose concentration in the interstitial fluid was taken as the BG level. The BG levels evaluatedwere collected before ingesting the test food (0 min), 15, 30, 45, 60, 90, and 120 min after the start of the test. The results
were evaluated by the BG level, the maximum BG change (ΔCmax) and the incremental area under the curve of BG (iAUC).
Bonferroni multiple test was performed for statistical analysis.
Results: here were no adverse events and no subject met the exclusion criteria for analysis, therefore, all 12 subjects were
included in the efficacy analysis. The blood glucose change (ΔBG) increased until 45 min after the start of the A to C intake
test, and decreased until 120 min thereafter. After 30 min, ΔBG of test food C tended to be lower than that of A and B (p < 0.1).
The highest value was shown 45 min after ingestion of the test foods A to C, when ΔBG was significantly lower in C than in
A (p < 0.05). ΔCmax was 20.3% lower in C than in A (p < 0.05). iAUC in C tended to be 24.8% lower than that of A (p < 0.1).
Conclusion: This study showed that a diet that ingest lemon juice prior to rice suppressed postprandial hyperglycemia thatwas observed when 30 g of lemon juice was taken. A dietary habit of ingesting a beverage containing lemon juice before
meals may reduce glycative stress by suppressing postprandial hyperglycemia, and may contribute to the prevention of aging
and disease progression.

KEY WORDS: glycative stress, postprandial hyperglycemia, lemon, citric acid

Introduction

Due to the acceleration of glycative stress, advanced
glycation end products (AGEs) are produced and accumulated
in our body. AGE-modification of tissue proteins involves
cross-linking, inflammation, and browning. Therefore,glycative stress causes physical, physiological, and visualdamage to tissues and cells in vivo 1). Glycative stress is one of
the risk factors for aging, and may be a cause of progressionof skin aging, diabetic complications, osteoporosis, anddementia. One of the factors that elevates glycative stress isthe persistent hyperglycemic state.
Even in healthy subjects, extreme postprandial
hyperglycemic conditions cause glycative stress. The methods

Contact Address: Professor Masayuki Yagi, PhD
Anti-Aging Medical Research Center, Graduate School of Life and Medical Sciences,
Doshisha University
1- 3 Tatara Miyakodani, Kyotanabe, Kyoto, 610 - 0321 Japan

TEL/FAX: + 81-774 -65-6394 e-mail: myagi@mail.doshisha.ac.jp
Co-authors: Uenaka S, ctud2025@mail4.doshisha.ac.jp;
Ishizaki K, ko-sei12@mail.doshisha.ac.jp; Sakiyama C, csakiyam@mail.doshisha.ac. jp;
Takeda R, rika.takeda@pokkasapporo-fb.co.jp; Yonei Y, yyonei@mail.doshisha.ac. jp_ 174 _

Glycative Stress Research 2020; 7 ( 2) : 174-180(c) Society for Glycative Stress ResearchGlycative Stress Research

to reduce glycative stress include suppression of postprandial
hyperglycemia, suppression of AGE production/accumulation,and reduced intake of diet- derived AGEs 2, 3). Postprandial
hyperglycemia can be suppressed by selecting low glycemic
index (GI ) foods and dietary modification. It has beenreported that postprandial hyperglycemia can be suppressedby ingesting carbohydrates (i.e. rice, bread), a vegetablesalad 4, 5), vinegar 6), vinegar beverage 7), grapefruit 8), or plain
yogurt 9) before meals. Furthermore, the suppression of
postprandial hyperglycemia is reported to be more effective
than eating udon or cooked rice alone by eating them withside dishes such as eggs, vegetable salad, Mabo eggplant 10),or beef bowl 11). The food information and ingestion methods
that suppress postprandial hyperglycemia may widen thevariety of diets that reduce glycative stress and provide
health information that can be reasonably and comfortably
continued. In this study, for the purpose of verifying theeffect of lemon juice on postprandial blood glucose (BG)
when ingesting cooked rice, the BG changes were compared
under two conditions, when the rice was ingested alone as astandard and when the lemon juice was ingested before rice.

Methods
Subject

Subject were 12 individuals who met the following
selection criteria ( Table 1): Men and women between the agesof 20 and 30 at the time of obtaining consent to participate
in the study; A healthy person without chronic illness; A

person who has a sufficient explanation about the purpose
and contents of this study, is capable of consenting, who
voluntarily participate after understanding well, and who canparticipate with a written consent; A person who can visit
and take the examinations on the designated day.

Survey items and examination contents
As a background survey, the subjects filled out aquestionnaire on their age, medical history and food allergy,
and underwent a blood examination ( Table 2). The test used
FreeStyle Libre Pro (Abbott Laboratories, Chicago, USA)and the glucose concentration in the tissue interstitial fluid
measured during the test period was used as the BG level 12).

Testing protocol
In this study, as in the previous report 4 -11), the test was
conducted according to a uniform protocol by the Japanese
Association for the Study of Glycemic Index (GI) 13).
Subjects were instructed to observe the following items
during the test period: Avoid irregular life such as lack ofsleep or overeating, and live a normal life; Diet, exercise, andsleep should be maintained in the same quantity and quality
as before participation in this study; It is prohibited to starttaking health foods and supplements; Other than that, it isprohibited to affect the test results.
Instructions were given on the day before and on the
day of the test so that the following items were observed:
Excessive exercise is prohibited the day before the preexamination and test; Sleep 6 hours or more the day before

Table 1. Subject’s profile.
Unit
Number of subjects
Age

years

Body heigt

cm

Body weight

kg

BMI

Total

Male

Female124823.1 ± 1.2

23.8 ± 0.5

22.8 ± 1.4

161 ± 9.8

172.1 ± 5.5

155.5 ± 5.6

21 ± 2.2

21.8 ± 3.4

20.6 ± 1.6

54.9 ± 10.7

65.1 ± 13.4

49.8 ± 3.8

Results are expressed as mean ± standard deviation. BMI, body mass index.

Table 2. Results of the blood chemistry test.
Test item

Unit

Measured value

Reference range

FBG

mg/dL

HbA1c

%

80.3 ± 6. 3

70 - 109

I RI

μU/mL

Total cholesterol

mg/dL

TG

mg/dL

HDL - C

mg/dL

LDL - Cmg/dL

5.3 ± 0. 2

4.6 - 6. 2

186.3 ± 19.7

12 0 - 219

67.4 ± 13. 5

4 0 - 85

5.8 ± 2. 2

74.3 ± 31.4

104.7 ± 17.9

1.7 - 10.4
3 0 - 149
65 - 139

Results are expressed as mean ± standard deviation. FBG, fasting blood glucose; IRI, immunoreactive insulin; TG,
triglyceride; HDL, high-density lipoprotein; LDL, low-density lipoprotein.

_ 175 _

Postprandial Blood Glucose on Lemon Juice and Rice Intake

the test; Intake of alcoholic beverages is prohibited from the
day before the test until the end of the test; For dinner on
the day before the pretest and the test, avoid high fat foods
and do not ingest anything other than water after 22:00;
On the day of the test, physical activity that may result in
exercise and sweating is prohibited until the end of the test;
For women, the test is not conducted during the menstrual
period.
During the test, participants were kept in a sitting andrest position; Prohibited phone calls, sleep, excessive brain
activity (i.e. e-mail, computer) and physical activity; Fasted
after eating the test food until the end of the test.
Subjects self-attached the Libre Pro sensor to theoutside of the upper arm two days or more before the test.
During the wearing period of the sensor, no restrictions wereplaced on bathing, swimming, or exercise. In the test, thetest food was ingested for 10 min at 10:00. Subjects thenwatched the DVD in a sitting position, allowing them toremain relaxed until 12:00, when the test ended.
The test food was swallowed 30 times or more afterchewing. The BG level was expressed as the measurement
value collected 15 min after starting the test food (first time),
15 min after starting the intake (second time), 30 min (thirdtime), 45 min (forth time), 60 min (fifth time), 90 min (sixthtime), and 120 min (seventh time).

Test foods
In this study, the nutritional components of the test
foods used were calculated using the values ​​displayed oneach food ( Table 3 ). Commercial packed rice and lemon juice
products were used as test foods. The test foods used wereas follows: a packaged cooked rice, " Sato no Gohan, 200 gof Koshihikari from Niigata" (Sato Foods Co., Ltd., Niigata,Japan), and a lemon juice product, " Pokka Lemon 100"
(Pokka Sapporo Food & Beverage Co., Ltd., Nagoya, Aichi,
Japan). The test foods were classified from A to C, and eachintake were as follows:
Test food A : Cooked rice 200 g(total carbohydrate: 6 7.8 g)
Test food B : Lemon juice 15 g + Cooked rice 200 g(total carbohydrate: 69.2 g)
Test food C : Lemon juice 30 g + Cooked rice 200 g(total carbohydrate: 70.6 g)juice was ingested for the first 5 min, followed by the ingestionof 200 g of rice. Lemon juice was ingested after diluting itwith 150 mL of water.

Selection of safety analysis objects
The objects for safety analysis selected the subjects who
took the test food only once.

Selection of efficacy analysis objects
The objects for efficacy analysis selected the subjects
who completed all the prescribed test schedules and test
contents, however, those who met the following exclusion
criteria were excluded: A person who was found to beprominent in acts that impair the reliability of test results; A
person who was found to have met the exclusion criteria or
was unable to comply with the restrictions after the start ofingestion.

Statistical analysis
Evaluation and analysis of the study were conductedby the safety analysis objects. The adverse events and side
effects were evaluated by tabulating the symptoms, degree,frequency, and relevance to the test food.
The efficacy analysis was conducted by the efficacy
analysis objects. The change in BG level (ΔBG) was obtainedby subtracting the value before ingesting the test food (firsttime; 0 min value) from the BG level after the test food
was ingested. The maximum change in BG level up to 120
min after the start of the test was defined as the maximum
BG change value (ΔCmax; maximum BG concentration).
Incremental area under curve (iAUC) was calculated
according to the uniform protocol of the Japan GI Study
Group 13). IMB SPSS Statics 26 (IMB Japan, Tokyo, Japan)
was used for the statistical analysis. The BG level was
expressed as the average value ± standard error (SE). For
comparison of test results between groups, Bonferroni
multiple test was performed, and it was judged as a significant
difference when the risk rate was less than 5% ( p < 0.05) ina two-sided test.

Ethical standards

As for the intake method of the test food, both A to C
were ingested within 10 min after the start of the test. In
particular, when the test foods B and C were ingested, lemonThis study was conducted in compliance with the
Declaration of Helsinki (revised at the 2013 WMA
Fortaleza General Assembly) and the ethical guidelines forhuman-based medical research (notification by Ministry of
Education, Culture, Sports, Science and Technology [MEXT]

Table 3. Nutrition facts of test foods.
Test foods

Serving unit(g)

Energy(kcal)

Protein
(g)

Fat
(g)

Carbohydrate
(g)

Fiber
(g)

Citric acid
(g)

A

200

294

4.2

0

67.8

0.6

0.0

B

215

299

4.2

0

69.2

0.6

0.95

C

230

304

4.2

0

70.6

0.6

1.9

Test foods A, cooked rice; B, lemon juice (15 g) before cooked rice; C, lemon juice (30 g) before cooked rice.

_ 176 _Glycative Stress Researchand Ministry of Health, Labour and Welfare [MHLW]). The
test content was fully explained to the subjects in advance.
The test was implemented after the applicant requested
participation in the test and received a voluntary consent
form. This study was conducted under the deliberation andapproval of the Ethics Review Committee of Doshisha
University (application No. 18039) and Sapporo HoldingsGroup Research Ethics Committee (reception No. 19- 005).
Concurrently, this test was registered in the public databaseestablished by the National University Hospital Meeting(UMIN Test ID: 000034009).

Efficacy evaluation
In this study, none of the subjects met the exclusion
criteria. Therefore, all 12 participants were included for theefficacy analysis.

Effect of ingestion of lemon juice and cooked riceon postprandial BG level
Table 4 shows the changes in BG levels after the startof the test. There was no significant difference in fasting
BG levels (0 min) before ingesting the test foods A to C.
The BG level of the subjects increased after ingestion ofeach test food, reached the maximum value after 4 5 min,and then reduced until after 120 min. The BG level at eachmeasurement time was slightly different between the test
foods, but it was not significant.
The transition of ΔBG is shown in Fig. 1. ΔBG increased
in all test foods A to C until 45 min after the start of the test.

Results

Safety evaluation
There were no reports of adverse events in this study(data not shown).

Table 4. Blood glucose level transition after a test food intake.
Time

A (mg/dL)
73.8 ± 4.0

0 min

95.8 ± 5. 2

15 min30 min(12.5)

133.4 ± 8. 2

(18.0)

133.0 ± 6. 2

(13.8)(6.5)

73.7 ± 4.7(10.2)

115.3 ± 4.9(10.8)

118.3 ± 6.2(13.6)

93.3 ± 4.2(9. 2)

89.8 ± 5.1(16.4)(13.7)(12.9)

126.8 ± 5.3

106.0 ± 5. 2

(11.3)

101.2 ± 5.1

91.8 ± 3.9(8.4)

C (mg/dL)

141.3 ± 5.9

127.8 ± 7.4(16.2)

99. 5 ± 3.8

120 min

101.5 ± 7.4(11.4)

110.3 ± 7.4

90 min77.3 ± 3.0(8.8)

129.8 ± 5.7

143.5 ± 6.3

45 min60 minB (mg/dL)(16.4)(8.6)(11.3)(11.7)(11.3)

Results are expressed as mean ± standard error and parentheses show 95% confidence interval, n = 12. Test foods A, cooked rice; B, lemon juice (15 g) before
cooked rice; C, lemon juice (30 g) before cooked rice.

80

A

Blood glucose (mg/dL)

70

B
＊

60
50

C

†

†

40
30
20
10
0
0

15

30

45

60

75

90

105

120

135

Time (min)Fig. 1. Fluctuation of the blood glucose level at the time of intaking lemon juice ahead of rice.

Results are expressed as mean ± standard error, n = 12, * p < 0.05, † p < 0.1 by Bonferroni test. Test foods A, cooked rice;
B, lemon juice (15 g) before cooked rice; C, lemon juice (30 g) before cooked rice.

_ 17 7 _Postprandial Blood Glucose on Lemon Juice and Rice Intake

After 30 minutes, ΔBG of test food C tended to be lower
than that of test foods A and B ( p < 0.1). ΔBG showed thehighest value 45 min after ingesting the test foods A to C,
and ΔBG of C was lower than that of A ( p < 0.05). ΔBG
of A to C decreased from 45 min to 120 min. The averagevalue of ΔBG at each time was lower in B and C than in A,
however, the difference was not significant.
ΔCmax was A: 71.3 ± 4.2 mg/dL, B: 67.4 ± 4.2 mg/dL,
C: 56.8 ± 3.6 mg/dL (Fig. 2). ΔCmax of C was 20.3 %(–14. 5 mg/dL) lower than in A (p < 0.05).
The iAUC was A: 5,032 ± 4 33 mg/dL . min, B: 4,368 ±354 mg/dL. min, C: 3,784 ± 323 mg/dL. min (Fig. 3 ). The
iAUC of C tended to be 24.8 % (–1,24 8 mg/dL. min) lower
than that of A (p < 0.1).

Discussion

Postprandial hyperglycemia suppression effect oflemon juice
For the purpose to examine the effect of lemon juice
on postprandial BG levels when ingesting cooked rice,
the effects on postprandial BG changes were comparedand verified under the following three test foods: A single
ingestion of cooked rice (A) as a standard, and 15 g (B) or
30 g (C) of lemon juice before ingested rice.
The intake of test food C was lower than that of A in
ΔBG (p < 0.1) after 30 min and in ΔBG (p < 0.05), ΔCmax(p < 0.05), and iAUC ( p < 0.1) after 45 min. The test food
B was lower than that of A in ΔBG (15. 4 %), ΔCmax(5. 5 %) and iAUC (13.2 %) after 60 min, but that was not
significant.
When the effects of test foods B and C were comparedwith those of A, reduction in ΔBG, ΔCmax and iAUC wasobserved depending on the intake of lemon juice. Therefore,
the inhibitory effect on postprandial hyperglycemia was100

considered to be the effect of the components contained inlemon juice.
The lemon juice used in the test contained 6.3% citricacid. The amount of citric acid in the test food calculated
from the intake was B: 0. 95 g and C: 1. 9 g ( Table 3 ). Thus,
it was estimated that the effective amount of citric acid forsuppressing postprandial hyperglycemia when ingesting 200 gof cooked rice was 1.9 g.
It has been already reported that the intake of
one grapefruit prior to bread can suppress postprandial
hyperglycemia 8). The amount of citric acid contained in one
grapefruit (about 200 g) is estimated to be about 2 g 14), thatwas comparable to 30 g of lemon juice (test food C ) in thisstudy. As well as citric acid, lemon contains various organic
acids such as ascorbic acid, malic acid, oxalic acid, and acetic
acid 15). Vinegar 6) and plain yogurt 9) have been reported tosuppress postprandial hyperglycemia when food containingacid is ingested before carbohydrate intake. It has been reported
that the postprandial hyperglycemia suppressing action ofacetic acid contained in vinegar involves delayed gastric
emptying 16), α-glucosidase inhibition 17), and improvement of
glucose metabolism 18). The inhibitory effect of plain yogurt
on postprandial hyperglycemia has been reported to relate to
the gelation of digests by lactate contained in whey 19), theenergy production by mitochondria in muscle tissue via
monocarboxylate transporter 21), the elongated gastric emptying
by suppressing the gastrin secretion due to stimulatedcholecystokinin (CCK) and secretin release 20), the elevatedincretin secretion by whey peptide 22). The organic acids otherthan citric acid may be involved in the suppressing action oflemon juice on postprandial hyperglycemia. Concurrently, it
has been reported that polyphenols contained in fruits havean α-glucosidase inhibitory effect 23), that has shown also inlemon peel extract 24). Taken together, these findings suggestthat the postprandial hyperglycemia-suppressing action oflemon juice may have been due to the organic acids, mainly
citric acid, and polyphenols contained in lemon.

5,000

iAUC (mg/dL・min)Cmax (mg/dL)

80
60
40
20
0

†

6,000

＊

4,000
3,000
2,000
1,000

A

B

0

C

Test foods

A

B

C

Test foods

Fig. 2. The amount of maximum blood glucose levelchange (ΔCmax) after intaking test food.

Results are expressed as mean ± standard error, n = 12, * p < 0.05 by
Bonferroni test. Test foods A, cooked rice; B, lemon juice (15 g) before
cooked rice; C, lemon juice (30 g) before cooked rice.

Fig. 3. The area under curve blood glucose level change(iAUC) after intaking test food.

Results are expressed as mean ± standard error, n = 12, † p < 0.1 byBonferroni test. Test foods A, cooked rice; B, lemon juice (15 g) before
cooked rice; C, lemon juice (30 g) before cooked rice.

_ 178 _Glycative Stress Research

Conclusion

Reduction of glycative stress by suppressing
postprandial hyperglycemia
Measures for reducing glycative stress include suppressing
postprandial hyperglycemia, inhibition of the production andaccumulation of AGEs, and reducing the intake of dietary
AGEs 2, 3). Since postprandial hyperglycemia leads to excessive
secretion of insulin, repeated extreme hyperglycemia is
involved in the induction of insulin resistance 25). It has also
been reported that blood levels of glycation intermediates, i.e.
3-deoxyglucosone, glyoxal, and methylglyoxal, increase in
response to an elevation in postprandial BG 26). Methylglyoxal
in blood damages vascular endothelial cells 27). Therefore,
suppression of postprandial hyperglycemia may prevent
tissue or organ damage secondary to microangiopathy. On
the other hand, the dietary guidance to eat vegetables firstprior to staple food may continue to suppress postprandial
hyperglycemia, thus is linked to HbA1c reduction andprevention of complications in diabetic patients 28). There isalso a meta-analysis that the habit of eating fruits reduces therisk of type 2 diabetes 29). Taken together with these findings,
the dietary habit of ingesting a beverage or food containing
lemon juice before meal may reduce glycative stress by
suppressing postprandial hyperglycemia, thus contributing to
the prevention of aging and age-related diseases.

This study showed that a diet that ingest lemon juice
prior to rice suppressed postprandial hyperglycemia that wasobserved when 30 g of lemon juice was taken. A dietary habitof ingesting a beverage containing lemon juice before meals
may reduce glycative stress by suppressing postprandial
hyperglycemia, and may contribute to the prevention of aging
and disease progression.

Conflict of Interest Statement

This research received support from Pokka Sapporo
Food & Beverage Ltd.

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