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Hibiscus sabdariffaextract inhibits obesity and fat
accumulation, and improves liver steatosis in
humans
Hong-Chou Chang,
a
Chiung-Huei Peng,
b
Da-Ming Yeh,
cd
Erl-Shyh Kao*
e
and Chau-Jong Wang*
fg
Obesity is associated with a great diversity of diseases including non-alcoholic fatty liver disease. Our
previous report suggested that Hibiscus sabdariffaextracts (HSE) had a metabolic-regulating and liver-
protecting potential. In this study, we performed a clinical trial to further confirm the effect of HSE.
Subjects with a BMI S27 and aged 18–65, were randomly divided into control (n¼17) and HSE-treated
(n¼19) groups, respectively, for 12 weeks. Our data showed that consumption of HSE reduced body
weight, BMI, body fat and the waist-to-hip ratio. Serum free fatty acid (FFA) was lowered by HSE.
Anatomic changes revealed that HSE improved the illness of liver steatosis. Ingestion of HSE was well
tolerated and there was no adverse effect during the trial. No alteration was found for serum a-amylase
and lipase. The clinical effect should mainly be attributed to the polyphenols of HSE, since composition
analysis showed that branched chain-amino acids, which is associated with obesity, is not obviously
high. In conclusion, consumption of HSE reduced obesity, abdominal fat, serum FFA and improved liver
steatosis. HSE could act as an adjuvant for preventing obesity and non-alcoholic fatty liver.
1. Introduction
Obesity, which is generally characterized by overweight, high
body mass index (BMI), and fat deposition, is prevalent in most
industrialized countries and even in developing countries.
1,2
The same trend of obesity was noted in Taiwan, which is asso-
ciated with reduced life expectancy and the increased mortality
of cardiovascular disease, cancer, and other related diseases.
3–7
Accumulation of total body fat and/or abdominal fat, high
triacylglycerol (TG), high low-density lipoprotein cholesterol
(LDL-C), low high-density lipoprotein cholesterol (HDL-C) and
free fatty acid ux (FFA), are common symptoms in metabolic
syndrome patients.
8
Since low density lipoprotein (LDL) clear-
ance and high density lipoprotein (HDL) recruitment in the liver
regulate the plasma lipid level, liver steatosis must be consid-
ered as an important factor in the pathogenesis. The observa-
tion of liver disorder is oen measured by elevated serum
aspartate transaminase (AST), alanine transaminase (ALT), and
ultrasonic images.
9
Hibiscus sabdariffaL. (Malvaceae), whose calyx is used
worldwide as a cold or hot beverage, is benecial for the
prevention and treatment of many diseases such as hyperten-
sion, inammation and liver disease.
10–12
In our previous report,
H. sabdariffaextract (HSE) inhibited low-desity lipoprotein
(LDL) oxidation in vitro and decreased serum cholesterol levels
in cholesterol-fed rats and rabbits.
13
HSE capsule reduced
serum cholesterol in human subjects.
14
The present study performed a clinical trial to further
conrm the HSE effect on metabolic regulation. We aimed to
observe the effect of HSE on obesity, body fat, waist circum-
stance, serum lipid proles, thus prevent the occurrence of fatty
liver in obese subjects.
2. Methods and materials
2.1. HSE Capsules
The HSE capsules were prepared from H. sabdariffaL. The dried
owers were macerated in hot water (95 C, 6000 L) for 2 hours,
and the aqueous extract was evaporated under vacuum at
85 C. The extracted solution was ltered and then lyophilized
to obtain 75 g of HSE, and then stored at 4 C before use. The
total anthocyanins content in the HSE was determined using
the Fuleki and Francis method.
15
The total avonoids content
was determined using the method reported by Jia et al., using
rutin as a standard.
16
The nal extract was composed of 1.43%
a
Institute of Medicine, Chung-Shan Medical University, Taiwan
b
Division of Basic Medical Science, Hungkuang University, Taiwan
c
School of Medical Imaging and Radiological Sciences, Chung Shan Medical University,
Taiwan
d
Department of Medical Imaging, Chung Shan Medical University Hospital, Taiwan
e
Department of Beauty Science And Graduate Institute of Beauty Science Technology,
Chienkuo Technology University, No. 1, Chiehshou N. Road, Changhua City 500,
Taiwan. E-mail: kaoes@cc.ctu.edu.tw
f
Institute of Biochemistry and Biotechnology, Chung-Shan Medical University, No. 110,
Sec. 1, Jianguo N. Road, Taichung 402, Taiwan. E-mail: wcj@csmu.edu.tw
g
Department of Medical Research, Chung Shan Medical University Hospital, Taiwan
Cite this: Food Funct.,2014,5,734
Received 15th October 2013
Accepted 30th December 2013
DOI: 10.1039/c3fo60495k
www.rsc.org/foodfunction
734 |Food Funct.,2014,5,734–739 This journal is © The Royal Society of Chemistry 2014
Food &
Function
PAPER
avonoids, 2.5% anthocyanins and 1.7% phenolic acid, as
measured by quantitative analysis. Amino acids of HSE were
determined by automated ion-exchange chromatography.
17
One
dose of a HSE treatment capsule contains 450 mg HSE extract
and 50 mg starch. The placebo dose treatment contained
500 mg starch.
2.2. Subjects
This study was approved and executed with the permission of
the Institute Review Board of Chung Shan Medical University
Hospital (CSMUH no.: CS08028). All participants gave
informed consent in writing. In this project males or non-
pregnant females aged 18–65 with BMI S27 (the criteria of
obesity of the Department of Health in Taiwan), fatty liver and
not under a course of treatment were recruited. Those who had
one of the following were excluded: a drinking habit (S20 g
alcohol daily), ALT 3-fold higher or bilirulin above 2 mg dL
1
,
kidney dysfunction, cardiovascular disease, endocrine or
severe systemic disturbance, mental disorder or taking any
OTC or prescribed medication and nutraceutics. Forty subjects
fullled the above criteria and were recruited for the study
(Table 1).
2.3. Study design
The study was conducted from July 2007 to June 2009. Before
and aer the experiment, the basal serum parameters
(glucose, TG, cholesterol, LDL-C, HDL-C, FFA, AST and ALT),
BMI, waist-to-hip ratio, body fat and the fatty liver score (FS,
described below) were measured as curative indexes. The
subjects were double-blinded, randomized and divided into 2
groups (20 subjects in each): one taking a 2 HSE capsule-dose
aer meals, 3 times a day, and the other the placebo, respec-
tively. Body weight, body fat, and the waist-to-hip ratio were
measured at week 0 and 12. Serum parameters and safety
evaluations, including creatine kinase (CK), gamma-glutamyl
transpeptidase (g-GT), blood urea nitrogen (BUN), creatinine
(CRE), albumin (ALB), uric acid, blood and urine were also
measured. The recruited subjects were asked to take 3-day
records of daily meals and physical activity at each of the time
points before the trial, rst 6 weeks and last 6 weeks, respec-
tively. At the end of the study, 36 subjects had completed all
the experiments: 17 in the control (9 males and 8 females) and
19 (12 males and 7 females) in the HSE group. 4 subjects did
not adhere to the following appointments thus withdrew from
the trial.
2.4. Serum parameters and safety evaluations
Serum glucose, TG, total cholesterol, LDL-C, HDL-C, AST, ALT,
BUN, CK, g-GT, CRE, ALB, amylase, lipase and uric acid were
analyzed on a Beckman Synchron CX9 clinical system. FFA was
analyzed using a Free Fatty Acid Quantication Kit (ab65341,
abcam).
2.5. Body fat and waist-to-hip ratio
The body fat and waist-to-hip ratio in this work were measured
with a Tanita TBF-300GS analyzer. The waist-to-hip ratio was
calculated using the waist circumference (just above the upper
hip bone) divided by the hip circumference at its widest part.
2.6. Ultrasonic image and fatty liver scores (FS)
Liver ultrasonic imaging was applied using the Aloka system
(Prosound SSD-4000, with 5.0 MHz convex transducer). The
fatty liver characteristic evaluations included hepatic clearance,
far gain attenuation and opaqueness of the bladder wall, portal
area and hepatic vein. Each item was classied as 0 ¼normal,
1¼mild to moderate and 2 ¼severe. The FS in this research
was presented as the sum of these ve items. The estimation of
sample size: we designed the type I error (a) is 0.05, the type II
error (b) is 0.2, therefore the power of this study is 0.8. The main
target of the study is fatty liver score (FS), we could expect the FS
of the HSE treatment group to go from 6 down 4.5, and the FS of
the placebo group from 6 down to 5.5. Due to the standard
deviation (SD) being equal to 1, and the expected withdraw rate
of 20%, therefore, this study needs 40 participants to examine
the hypothesis.
2.7. Statistical analysis
Using an unpaired Student’st-test for the control and HSE-
treated groups, and a paired Student’st-test for the pre- and
post-trial, a pvalue of less than 0.05 was considered statis-
tically signicant. All the analyses were performed with
SigmaPlot 11.0.
Table 1 Baseline demographic data of the subjects
a
HSE group Control group
pvalue(N¼19) (N¼17)
Biometrics
Age (y/o) 37.32 8.61 38.59 10.51 0.692
Height (m) 1.67 0.08 1.66 0.09 0.591
Body weight (kg) 88.52 15.96 84.93 12.79 0.465
BMI (kg m
2
) 31.51 4.01 30.91 3.71 0.641
Body fat (%) 37.37 6.22 38.44 9.80 0.696
Waistline (cm) 98.00 11.75 95.32 10.43 0.477
Hip (cm) 107.66 7.49 106.32 8.00 0.609
W/H 0.91 0.07 0.90 0.06 0.554
Diabetes indicators
TCHO (mg dL
1
) 213.47 28.88 207.53 42.38 0.623
LDL-c (mg dL
1
) 132.63 24.68 126.29 37.11 0.546
HDL-c (mg dL
1
) 44.63 8.46 43.35 6.12 0.611
TG (mg dL
1
) 172.32 71.60 190.29 102.57 0.543
FFA (U min
1
mg
protein
1
) 0.81 0.27 0.83 0.35 0.823
Glucose (mg dL
1
) 106.58 22.53 106.71 13.13 0.984
Hepatic function
ALT (U L
1
) 57.21 35.45 35.47 24.04 0.033*
AST (U L
1
) 33.05 17.82 23.18 9.34 0.049*
F S 5.21 1.72 4.82 2.22 0.560
a
TCHO: total cholesterol, W/H: waist-to-hip ratio. Data are presented as
mean SD and analyzed by the Student t-test. p< 0.05 was considered
statistically signicant.
This journal is © The Royal Society of Chemistry 2014 Food Funct.,2014,5,734–739 | 735
Paper Food & Function
3. Results
3.1. HSE reduced body weight and BMI
Before the trial, the body weight and BMI showed no signicant
difference between the HSE and control groups (Table 1). Aer
12 weeks of treatment, the body weight and BMI signicantly
decreased in the HSE group (88.53 15.96 kg to 87.28
16.02 kg, p< 0.008; 31.51 4.01 kg m
2
to 31.09 4.23 kg m
2
,
p< 0.009) (Table 2). The reduction in body weight and the
percentage of change during the trial is shown in Fig. 1, indi-
cating that about 60% of the weight change occurred between
0–6 weeks. Almost 70% of the HSE-treated subjects had a
reduced body weight and BMI (data not shown).
3.2. HSE reduced body fat and waist-to-hip ratio
During the trial, signicant alterations in body fat existed
neither in the HSE nor control groups. However, by the end of
the treatment, HSE showed a signicant effect on the pre–post
difference compared with the control group. The waist-to-hip
ratio of the HSE group signicantly decreased from 0.91 0.07
to 0.90 0.06 (p< 0.01), which could be attributed to the
lowering of the waist circumference. No alteration was found in
the control group (Table 2).
3.3. HSE decreased serum FFA
About 63% of the HSE-treated subjects showed a reduced level
of FFA (data not shown). The serum FFA level of the HSE group
decreased from 0.81 0.27 to 0.64 0.24 (p¼0.025), whereas
no alteration was found in the control (Table 2). By the end of
Table 2 Treatment effects
a
HSE group (N¼19) Control group (N¼17)
0 week 12 week pvalue*0 week 12 week pvalue*pvalue †
Biometrics
Body weight (kg) 88.52 15.96 87.28 16.02 0.008*84.93 12.79 84.27 13.14 0.086 0.307
BMI (kg m
2
) 31.51 4.01 31.09 4.23 0.009*30.91 3.71 30.65 3.76 0.062 0.396
Waist (cm) 98.00 11.75 97.16 10.94 0.089 95.32 10.43 95.94 10.25 0.222 0.038 †
Hip (cm) 107.66 7.49 108.13 7.05 0.281 106.32 8.00 106.76 8.25 0.311 0.957
W/H ratio 0.91 0.07 0.90 0.06 0.010*0.90 0.06 0.90 0.06 0.571 0.026 †
Body fat (%) 37.37 6.22 36.67 6.61 0.16 38.44 9.80 39.08 9.82 0.144 0.044 †
Diabetes indicators
TCHO (mg dL
1
) 213.47 28.88 209.68 31.66 0.507 207.53 42.38 209.88 36.66 0.707 0.464
LDL-c (mg dL
1
) 132.63 24.68 133.16 26.31 0.922 126.29 37.11 128.88 21.79 0.682 0.802
HDL-c (mg dL
1
) 44.63 8.46 44.58 8.41 0.967 43.35 6.12 44.76 5.29 0.264 0.411
TG (mg dL
1
) 172.32 71.60 154.47 52.87 0.114 190.29 102.57 167.82 103.68 0.025*0.747
FFA (U min
1
mg
protein
1
) 0.81 0.27 0.64 0.24 0.025*0.83 0.35 0.89 0.49 0.421 0.026 †
Glucose (mg dL
1
) 106.58 22.53 111.84 26.42 0.365 106.71 13.13 108.12 9.62 0.425 0.540
Hepatic function
ALT (U L
1
) 57.21 35.45 55.63 35.62 0.741 35.47 20.04 28.94 11.69 0.075 0.410
AST (U L
1
) 33.05 17.82 31.11 17.25 0.427 23.18 9.34 19.53 3.97 0.062 0.583
FS 5.21 1.72 4.42 2.01 0.018*4.82 2.22 4.06 2.42 0.043*0.957
a
Data are presented as mean SD and analyzed by paired ttest. *p< 0.05 indicates the signicance of each difference at 12 week compared with
the baseline. †p< 0.05 indicates the signicance of each 12–0 week difference between the control and HSE-treated groups.
Fig. 1 The reduction in body weight (kg) and percentage of change at
0–6 weeks, 6–12 weeks, and 0–12 weeks.
736 |Food Funct.,2014,5,734–739 This journal is © The Royal Society of Chemistry 2014
Food & Function Paper
the treatment, no other signicant change of lipid prole
existed between the HSE and control groups.
3.4. HSE improved the FS
In the HSE-treated subjects, the FS was signicantly decreased
by about 15%, from 5.21 1.72 to 4.42 2.01 (p¼0.018)
(Table 2). No signicant alteration was found in the AST or ALT
levels in both the HSE and control groups. Also, the pre–post
differences between the two groups were not signicant.
3.5. HSE did not change the safety evaluation markers
The safety evaluation markers almost remained the same
during the trial, except for ALB and BUN. Serum ALB slightly
decreased in the HSE group. BUN decreased in both the HSE
and control groups, while the pre-post difference was signi-
cant only in the control group (Table 3). Noticeably, a-amylase
and lipase was not altered, implying the safety and lack of
metabolic side effects on the pancreas.
4. Discussion
In the present study, we demonstrated the anti-obesity and
liver-protection potential of HSE. HSE decreased body weight,
BMI and body fat, and reduced abdominal fat distribution. HSE
decreased serum FFA, exerting a benecial effect on metabolic
regulation, while improving the liver steatosis. Noticeably, the
safety evaluation revealed that HSE did not harm the human
body. This is the rst study to investigate HSE for the attenua-
tion of human obesity and fatty liver.
BMI is one of the most popular anthropometric indices. In
2000, WHO dened the BMI cut-offpoints as 23 kg m
2
(over-
weight), 25 kg m
2
(obesity class I), and 30 kg m
2
(obesity class
II) for people living in the Asia Pacic region. All the subjects in
the trial had a BMI > 25 kg m
2
(obesity class I) and had been
diagnosed with fatty liver for more than one year. However,
although the BMI is widely used and adopted in this study, it
may still have limitations. For some populations who have
shorter lower limbs, using standing height alone may over-
estimate the number of individuals that are overweight and
obese, and at risk for type 2 diabetes mellitus and cardiovas-
cular disease.
18
On the contrary, central obesity predicts a high prevalence of
hepatic steatosis and related disorders. A previous analysis
revealed that the waist circumference and waist/height ratio
had a signicant association with the development of fatty liver,
whereas the BMI did not. In this study, we measured the waist
circumference and used the waist-to-hip ratio as an index,
which should more adequately reect the regulatory effect of
HSE on abdominal fat distribution and central obesity.
19
Non-alcoholic fatty liver is generally considered to be the
liver component of metabolic syndrome, including an excessive
waist circumference, dyslipidaemia, hyperglycaemia, and
hypertension.
20
In a clinical situation, the ultrasonic examina-
tion of fatty liver is usually qualitative but not quantitative. To
overcome this limitation, we cited and mimicked the semi-
quantitative FS scores, and demonstrated the effect of HSE on
improving fatty liver.
21
H. sabdariffaimproved the lipid proles of patients with
metabolic syndrome.
22
Recently, HSE was reported to prevent
hepatic steatosis through down-regulation of PPAR-gand
SREBP-1c, which plays an important role in obesity-induced
inammation, especially in the liver, adipose tissue, and
vascular system.
23,24
According to the previous report, the calyx
of H. sabdariffaL. is rich in polyphenols, including anthocya-
nins, avonoids and phenolic acids.
25
H. sabdariffapolyphenols
prevented hyperglycemia and hyperlipidemia, inhibited hepatic
lipogenesis, while they promoted hepatic lipid clearance.
26,27
Many of them, such as gallic acid derivative, chlorogenic acid,
caffeic acid, quercetin, and tiliroside, were demonstrated to be
effective on reducing obesity and related disorders (Table 4).
Galloyl ester decreased the body weight, liver weight, and
Table 3 Safe evaluation markers
a
HSE group (N¼19) Control group (N¼17)
0 wk 12 week pvalue 0 week 12 week pvalue
WBC 7.56 1.47 7.28 0.97 0.328 7.70 1.34 7.77 1.66 0.811
RBC 5.11 0.44 5.09 0.44 0.68 5.13 0.55 5.04 0.62 0.211
HB 15.22 1.38 15.14 1.42 0.462 14.74 1.52 14.51 1.74 0.255
CK (U L
1
) 46.42 14.47 46.21 19.73 0.97 46.18 12.81 46.70 17.10 0.92
r-GT (U L
1
) 49.26 45.39 50.05 40.00 0.812 40.88 32.57 35.65 26.08 0.051
ALB (g dL
1
) 4.55 0.33 4.42 0.25 0.004*4.31 0.94 4.43 0.23 0.554
BUN (mg dL
1
) 13.21 2.44 12.26 2.90 0.098 12.41 1.77 10.88 2.17 0.035*
CRE (mg dL
1
) 1.00 0.20 1.01 0.19 0.63 0.97 0.19 0.94 0.20 0.311
UA (mg dL
1
) 6.99 1.56 7.04 1.56 0.837 6.57 0.37 6.27 0.34 0.202
TSH (mIU mL
1
) 1.69 1.00 1.67 1.05 0.916 1.75 1.07 1.80 0.79 0.837
Free T4 (ng dL
1
) 1.10 0.13 1.08 0.11 0.598 1.09 0.13 1.04 0.13 0.138
Urine PH 6.32 0.56 6.16 0.44 0.301 6.38 0.45 6.44 0.68 0.773
Amylase (U L
1
) 69.32 21.01 66.95 16.94 0.704 67.35 15.20 72.47 20.83 0.413
Lipase (U L
1
) 33.02 9.88 35.55 13.68 0.517 34.73 9.53 33.07 7.99 0.589
a
WBC: white blood cell, RBC: red blood cell, Hb: hemoglobulin, TSH: thyroid stimulating hormone, T4: thyroxine, UA: uric acid. Data are presented
as mean SD and analyzed by paired t-test. *p< 0.05 indicates the signicance.
This journal is © The Royal Society of Chemistry 2014 Food Funct.,2014,5,734–739 | 737
Paper Food & Function
hepatic lipid.
28
Chlorogenic acid lowered serum cholesterol and
attenuated fatty liver by up-regulating the expression of PPAR-
a.
29
Chlorogenic acid and caffeic acid improved body weight,
lipid metabolism and obesity-related hormone levels in high-fat
fed mice.
30
Recently, it was reported that caffeic acid inhibits
hepatic lipogenesis but promotes lipolysis via regulating AMPK
in HepG2 cells.
31
Non-alcoholic fatty liver disease rats (NAFLD)
have higher serum levels of IL-18 but lower levels of IL-10 than
their healthy counterparts. Quercetin treatment reversed the
cytokine expressions and helped to delay the progression of
NAFLD.
32
An in vitro experiment showed that quercetin exerts
anti-adipogenesis activity by activating the AMPK signal
pathway in 3T3-L1 preadipocytes, while it induces the apoptosis
of mature adipocytes by modulation of the ERK and JNK path-
ways.
33
Tiliroside, a glycosidic avonoid, ameliorates hyper-
insulinemia and hyperlipidemia in obese-diabetic mice by
activating adiponectin signaling and the hepatic lipid oxida-
tion.
34
In addition, anthocyanins contained in H. sabdariffaL.
could exert anti-obesity and liver-protective effects. It was
reported that puried anthocyanins reduced the body weight
and body fat of rats fed with a high-fat diet.
35
Recently, Wu et al.
reported that anthocyanins inhibit body weight gain, reduce
insulin resistance, increase serum adiponectin while decrease
leptin, lower the adipocytes and lipid accumulation, improve
serum and liver lipid proles, and ameliorate the impaired
hepatic function in diet-induced obese mice.
36,37
Under normal
circumstances, anthocyanins even have the capability to reduce
body weight and food intake through its modulation of NPY and
GABAB1R in the hypothalamus.
38
Some literature has reported
that branched chain-amino acids are associated with obesity
and insulin resistance.
39
We have analyzed the amino acid
composition of HSE (Table 5), whereas only aspartic is obviously
high. Hence the clinical effect of HSE should mainly be attrib-
uted to the polyphenols.
In this trial, aer HSE treatment, no signicant difference
was observed in the lipid prole except for FFA. These results
are in accordance with that of Kuriyan, Kumar and Kurpad
(2010),
40
which might attribute to the dose of HSE (1 g day
1
)
being too low. The optimum dose of HSE intake should be
determined in future clinical work. Further research on the
bioavailability and pharmacokinetics of HSE is needed. In
conclusion, HSE has the potential to act as an adjuvant for
preventing obesity and related fatty liver.
Acknowledgements
We thank Aiken Co.,Taiwan for preparing all experimental
capsules.
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hepatic disorder
Ingredient Effect Ref.
Galloyl ester Decrease body weight 28
Decrease hepatic lipid 28
Chlorogenic acid Decrease body weight 30
Regulate obesity-related hormone 30
Regulate lipid metabolism 30
Attenuate fatty liver 29
Caffeic acid Decrease body weight 30
Regulate obesity-related hormone 30
Regulate lipid metabolism 30
Inhibit hepatic lipogenesis 31
Promote hepatic lipolysis 31
Quercetin Attenuate fatty liver 32
Inhibit adipocyte differentiation 33
Induce adipocyte apoptosis 33
Tiliroside Regulate obesity-related hormone 34
Promote hepatic lipolysis 34
Anthocyanines Decrease body weight 35–37
Decrease body fat 35 and 36
Improve serum and liver lipid proles 37
Ameliorate impaired hepatic function 37
Table 5 Amino acid composition of HSE
Amino acid Content (mg/100 g)
Aspartic acid 1811.90
Threonine nd
a
Serine 106.41
Glutamic acid 227.31
Glycine 123.61
Alanine 109.74
Cysteine 48.30
Valine 49.21
Methionine 13.35
Isoleucine 42.19
Leucine 75.34
Tyrosine 27.94
Phenylalanine 73.68
Lysine 137.05
Histidine 58.41
Arginine 68.81
Proline 53.14
Total 3026.11
a
nd: not detected.
738 |Food Funct.,2014,5,734–739 This journal is © The Royal Society of Chemistry 2014
Food & Function Paper
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