jcim-2015-0030

Abstract

Evaluation of the effects of roselle (Hibiscus sabdariffa L.) on oxidative stress and serum levels of lipids, insulin, and hs-CRP in adult patients with metabolic syndrome: a double-blind placebo-controlled clinical trial Abstract Background: Roselle (Hibiscus sabdariffa L.) is a plant with antihyperlipidemic and antihypertensive effects. This study aimed to evaluate the effects of roselle calyces on the serum levels of lipids and insulin, inflammation, and oxidative stress in patients with metabolic syndrome (MetS). Methods: Forty adult patients with MetS were randomly assigned to receive either 500 mg of H. sabdariffa calyx powder or placebo once daily for 4 weeks. Systolic and diastolic blood pressures (SBP and DBP) and BMI (body mass index) as well as fasting serum levels of glucose (FPG; fasting plasma glucose), insulin, lipoproteins, triglycerides (TG), high-sensitivity C-reactive protein (hs-CRP), and malondialdehyde (MDA) were determined pre-and post-intervention and compared. Results: H. sabdariffa significantly reduced serum TG (p = 0.044) and SBP (p = 0.049) compared to placebo. All other variables were not significantly affected by the interventions. Conclusions: Daily consumption of 500 mg of H. sabdariffa L. calyx powder can decrease SBP and serum TG in MetS patients.

Full text

Sedigheh Asgary, Rasool Soltani*, Mohsen Zolghadr, Mahtab Keshvari
and Nizal Sarrafzadegan
Evaluation of the effects of roselle (Hibiscus
sabdariffa L.) on oxidative stress and serum levels
of lipids, insulin, and hs-CRP in adult patients
with metabolic syndrome: a double-blind
placebo-controlled clinical trial
DOI 10.1515/jcim-2015-0030
Received May 12, 2015; accepted January 20, 2016
Abstract
Background: Roselle (Hibiscus sabdariffa L.) is a plant
with antihyperlipidemic and antihypertensive effects.
This study aimed to evaluate the effects of roselle calyces
on the serum levels of lipids and insulin, inflammation,
and oxidative stress in patients with metabolic syndrome
(MetS).
Methods: Forty adult patients with MetS were randomly
assigned to receive either 500 mg of H. sabdariffa calyx
powder or placebo once daily for 4 weeks. Systolic and
diastolic blood pressures (SBP and DBP) and BMI (body
mass index) as well as fasting serum levels of glucose
(FPG; fasting plasma glucose), insulin, lipoproteins,
triglycerides (TG), high-sensitivity C-reactive protein (hs-
CRP), and malondialdehyde (MDA) were determined pre-
and post-intervention and compared.
Results: H. sabdariffa significantly reduced serum TG
(p = 0.044) and SBP (p = 0.049) compared to placebo. All
other variables were not significantly affected by the
interventions.
Conclusions: Daily consumption of 500 mg of H. sabdariffa
L. calyx powder can decrease SBP and serum TG in MetS
patients.
Keywords: clinical trial, Hibiscus sabdariffa L., hs-CRP,
lipid profile, metabolic syndrome, oxidative stress
Introduction
Metabolic syndrome (MetS) is a cluster of several cardio-
metabolic risk factors including hypertension and
increased waist circumference as well as elevated fasting
plasma glucose (FPG) and serum triglyceride (TG), and
decreased high-density lipoprotein cholesterol (HDL-C)
[1]. Since MetS has been established as a risk factor for
cardiovascular events [2], type 2 diabetes [3, 4], and pre-
mature death [5], it is a major public health concern. Both
cardiovascular disease (CVD) risk reduction efforts,
including treatment of dyslipidemia, and diabetes preven-
tion should be considered for all MetS patients [3]. Insulin
resistance is the major pathophysiologic characteristic of
MetS [2]. Therefore, many clinicians are now focusing on
treating insulin resistance in these patients [3].
It has been shown that high-sensitivity C-reactive
protein (hs-CRP), a systemic marker of inflammation, is
a strong and independent predictor of both diabetes [6]
and CVD [7]. Furthermore, elevated hs-CRP level in
patients with MetS has been confirmed in several studies
[8–11]. There is a positive association between CRP eleva-
tion and the number of MetS components [8, 10, 11]. This
suggests that low-grade inflammation could be impli-
cated in the pathogenesis of MetS [8].
A strong association between MetS and oxidative
stress has been found [12, 13]. Oxidative status is due to
hyperglycemia and inflammation, important components
of MetS, resulting in the production of reactive oxygen
species (ROS) [14]. ROS generation leads to oxidation,
and consequently dysfunction, of carbohydrates, lipids,
and proteins [12]. Furthermore, a significant reduction in
total antioxidant status (TAS) has been observed in MetS
*Corresponding author: Rasool Soltani, Department of Clinical
Pharmacy and Pharmacy Practice, Faculty of Pharmacy and
Pharmaceutical Sciences, Isfahan University of Medical Sciences,
Isfahan, Iran, E-mail: soltani@pharm.mui.ac.ir
Sedigheh Asgary, Isfahan Cardiovascular Research Center, Isfahan
Cardiovascular Research Institute, Isfahan University of Medical
Sciences, Isfahan, Iran
Mohsen Zolghadr, Department of Clinical Pharmacy and Pharmacy
Practice, Faculty of Pharmacy and Pharmaceutical Sciences, Isfahan
University of Medical Sciences, Isfahan, Iran
Mahtab Keshvari, Nizal Sarrafzadegan, Isfahan Cardiovascular
Research Center, Isfahan Cardiovascular Research Institute, Isfahan
University of Medical Sciences, Isfahan, Iran
J Complement Integr Med. 2016; aop
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[14, 15]. Therefore, phytochemicals with antioxidant
activity might have clinical value for the treatment of
MetS.
Roselle (Hibiscus sabdariffa L.), commonly known as
“sour tea”in Iran, is a tropical annual herbal shrub
belonging to the Malvaceae family and is characterized
by red calyces and flowers with a unique sour taste.
Roselle calyces are rich in polyphenols, anthocyanins
(including delphinidin-3-sambubioside, delphinidin-3-
monoglucoside, cyanidin-3-monoglucoside, and cyani-
din-3-sambubioside), flavonoids and proanthocyanidins
[16, 17]; these compounds are potentially bioactive with
cardiovascular effects through their antioxidant activities
[18, 19]. In traditional medicine, this plant is used for
antihyperlipidemic, antihypertensive, and anti-inflamma-
tory effects [20, 21].
The aim of this study was to evaluate the effects of
roselle calyces in the form of powder, on the serum levels
of lipids, hs-CRP, and insulin as well as the serum levels
of malondialdehyde (MDA; an end product of lipid per-
oxidation used as a biomarker of oxidative stress) in
adult patients with MetS.
Materials and methods
Preparation and standardization of the plant material
The calyces of H. sabdariffa L. were purchased from a local source
and were identified by the Pharmacognosy Department of the
Faculty of Pharmacy, Isfahan University of Medical Sciences,
Isfahan, Iran. The calices were dried and powdered by an electric
mixer (Moulinex, Germany). The powder was then pulverized and
sieved (30 mesh).
The prepared powder was standardized based on the total antho-
cyanin content using the pH differential method [22]. For this, two
1-g samples of powder were dissolved in 10 mL of buffer solution
with pH = 1 composed of 125 mL of KCl 0.2 M (Merck, Germany) and
375 mL of HCl 0.2 M (Merck, Germany), and 10 mL of buffer solution
with pH = 4.5 composed of 400 mL of sodium acetate 1 M (Merck,
Germany), 240 mL of HCl 1 M, and 360 mL of water, respectively.
Both solutions were diluted 10 times with the same buffer and their
absorbance was read at 510 nm using spectrophotometer
(PerkinElmer, USA). Total anthocyanin content was determined by
the following equation:
Anthocyanin concentration mg=LðÞ=
Abs pH1 −Abs pH4.5ðÞ× 484.82 × 1000 × DF=24825
In the equation, 484.82 is the molecular mass of cyanidin-3-gluco-
side chloride, 24,825 is the molar absorptivity at 510 nm in pH = 1,
and DF is the dilution factor.
Based on the above method, the anthocyanin content was 6 mg/g
of the prepared powder.
Preparation of drug and placebo capsules
Each drug capsule was filled with 500 mg of the prepared standar-
dized powder. The placebo capsules with shape, color, and size
similar to drug ones were filled only with dried granulated tribasic
calcium phosphate (Merck, Germany), an inert substance used as
diluent or filler in pharmaceutical industries.
Patient selection
Patients were selected from those who referred to the Isfahan
Cardiovascular Research Center. The inclusion criteria for participation
of patients in the study were (1) being diagnosed with MetS according to
the Adult Treatment Panel (ATP) III criteria [23], i.e. the presence of at
least three of the following five components: (a) abdominal obesity,
defined as waist circumference >102 cm for men or >88 cm for women;
(b) elevated serum TG ( ≥150 mg/dL); (c) low serum HDL-C (<40 mg/dL for
men and <50 mg/dL for women), (d) hypertension (blood pressure (BP)≥
130/85 mmHg) or current treatment for hypertension, and (e) impaired
fasting glucose (FPG ≥110 mg/dL); (2) age > 18 years; (3) free of diseases
affecting serum lipids (e.g. thyroid disorders and pancreatitis); (4) not
using drugs or supplements affecting serum lipids (e.g. statins, fibrate
derivatives, estrogens, progestins, β-blockers, thiazide diuretics, and fish
oil)withinthelast3monthsandatpresent;(5)notusinganyantidiabetic
drug including insulin within the last 3 months and at present; (6) free of
liver or kidney disease; (7) not being substance abuser (including alco-
hol) or smoker; and (8) not being pregnant or lactating (for women).
The exclusion criteria included (1) allergic reaction to roselle and
(2) irregular use of the capsules (consumption of less than 80% of
total capsules during the study).
Study design and interventions
This was a randomized double-blind placebo-controlled clinical trial
conducted in Isfahan Cardiovascular Research Center affiliated to
Isfahan University of Medical Sciences, Isfahan, Iran, from
September 2012 to March 2013. The study was registered in Iranian
Registry of Clinical Trials (IRCT) with the record number of
IRCT201310089662N8. Informed consent was obtained from all par-
ticipants and the study protocol was approved by the Ethical
Committee of Isfahan University of Medical Sciences and Research
Ethics Committee of Isfahan Cardiovascular Research Center.
Patients who met the inclusion criteria were randomly and equally
assigned to either the study drug (H. sabdariffa) or placebo groups.
Before intervention, the demographic characteristics as well as sys-
tolic and diastolic blood pressures (SBP and DBP, respectively) were
recorded for all patients. Also, after receiving 5 mL of fasting blood
sample from each participant and its centrifugation (10 min, 2,000
rpm), serum levels of glucose (FPG), insulin, total cholesterol, low-
density lipoprotein cholesterol (LDL-C), HDL-C, hs-CRP, and MDA
were determined. Also, the fasting serum levels of alanine amino-
transferase (ALT), aspartate aminotransferase (AST), blood urea
nitrogen (BUN), and creatinine were obtained for the detection of
any possible hepatic or renal side effect of the study drug. The
serum samples were frozen at –70 °C for assays as necessary. The
patients of drug and placebo groups were instructed to take one
medicinal and placebo capsules, respectively, once daily with food
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for 4 weeks. All patients were advised to maintain their usual diet
and physical activity and report any adverse effect during the study.
The patients’compliance was evaluated by counting their capsules
at the end of use and their results were applied for data analysis if
they used more than 80% of their capsules. At the end of 4 weeks,
all the above-mentioned variables were again determined and com-
pared with baseline values. For randomization and blindness, each
capsule container was given a code according to the type of its
content (drug or placebo). When giving a container to each patient,
its code was recorded on his/her own consent form. At the end of the
intervention and after determination of the patient’s own results, the
recorded code was identified regarding the type of intervention. All
participants, the physician, and the laboratory personnel were blind
to the intervention type.
Statistical analysis
SPSS 20.0 software (SPSS Inc., Chicago, IL, USA) was used for statis-
tical analysis of obtained data. Regarding normal distribution of all
continuous data, determined by Kolmogorov–Smirnov test, Student’s
t-test was used for comparisons. χ
2
-Test was done for comparison of
gender distribution in two groups. Paired-samples t-test was per-
formed for comparison of values at the beginning and end of inter-
vention within each group. One-way analysis of covariance (ANCOVA)
test was used for comparing the mean values between drug and
placebo groups. A p-Value<0.05 was considered as significant.
Results
Over the study period, a total of 113 MetS patients were
assessed for eligibility in the study, of whom, 63 patients
met the inclusion criteria. Forty patients who accepted to
participate in the trial and signed the consent form,
randomly and equally were divided into two intervention
groups. Finally, 18 patients in drug group and 17 patients
in placebo group fully completed the trial (Figure 1).
Table 1 shows the baseline demographic and clinical
characteristics of the study patients. As shown, all sub-
jects were matched regarding baseline values.
Table 2 comparatively shows the effects of interven-
tions on the evaluated parameters after 4 weeks in the
study subjects. As seen, H. sabdariffa significantly
reduced serum TG (P = 0.044) and SBP (P = 0.049) com-
pared with placebo. Furthermore, although H. sabdariffa
caused significant reduction of body mass index (BMI)
(P = 0.027) as well as increase of serum HDL (P = 0.048),
these effects were not statistically significant compared
with placebo. All other variables were not significantly
affected by the interventions.
Table3presentstheeffectsofH. sabdariffa and pla-
cebo on the liver and kidney function tests after 4 weeks.
As shown, no significant changes occurred in the tested
values during the study. Furthermore, no adverse effect was
reported by the study patients during the interventions.
Discussion
In the present study, we evaluated the effects of
H. sabdariffa L. calyx powder on several metabolic and
nonmetabolic parameters of MetS patients. Our results
showed that with the dose of 500 mg/day for 4 weeks,
the powder has no significant effect on the evaluated
variables including the markers of inflammation and oxi-
dative stress except for serum TG and SBP. At the best of
our knowledge, there is only one clinical study about the
effects of H. sabdariffa on MetS patients. This study,
conducted by Gurrola-Díaz et al., evaluated the effects
of H. sabdariffa extract powder (100 mg/day) on the lipid
profiles of MetS patients after 1 month of the intervention
113 patients were assessed for eligibility
63 patients met inclusion criteria
20 patients were assigned to
drug group
20 patients were assigned to
placebo group
18 patients completed the study 17 patients completed the study
2 patients were excluded
due to irregular use of
capsules
3 patients were excluded
due to irregular use of
capsules
40 patients accepted participation
Figure 1: Flowchart of patients’recruitment and enrollment in the study.
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[24]. According to the results, the MetS patients treated
with the extract had significantly reduced glucose and
total cholesterol levels and increased HDL level. The
reason for various results of these two studies may be
due to the fact that we used the roselle powder without
extraction, while the mentioned study applied the
extracted powder that contains higher concentrations of
polyphenols and other components. Several other animal
and clinical studies have shown hypolipidemic effects of
H. sabdariffa [25–28]; however, none of the clinical stu-
dies has been performed on MetS patients. Furthermore,
consistent to our results, several studies have failed to
show positive effects of this plant on one or all compo-
nents of serum lipid profile [28–31]. Considering the sig-
nificant increase of serum HDL (P = 0.048) and decrease
of BMI as well as insignificant desirable changes in other
variables compared with baseline values, it is possible
that the consumption of higher doses of the powder with
longer durations could affect them significantly com-
pared with placebo.
Regarding the effect of roselle on BMI, our results
showed significant reduction of this parameter only in
drug group (P= 0.027). The study of Chang et al. showed
significant reduction of body weight and BMI in subjects
with baseline BMI ≥27 kg/m
2
using H. sabdariffa extract for
12 weeks compared with control group [32]. The differences
in study population (MetS vs. non-MetS) and duration as
well as the type of consumed material (extract vs. non-
extracted powder) could be the cause of various results.
Table 1: Baseline demographic and clinical characteristics of the
study subjects.
Parameter, unit H. sabdariffa
(n =)
Placebo
(n =)
p-Value
Age, years . ±. . ±. .
Gender, % male . . .
BMI, kg/m

. ±. . ±. .
FPG, mg/dL . ±. . ±. .
Insulin, µU/mL . ±. . ±. .
Total cholesterol, mg/dL . ±. . ±. .
LDL-C, mg/dL . ±. . ±. .
HDL-C . ±. . ±. .
TG, mg/dL . ±. . ±. .
SBP, mmHg . ±. . ±. .
DBP, mmHg . ±. . ±. .
MDA, µmol/L . ±. . ±. .
hs-CRP, mg/dL . ±. . ±. .
BMI, body mass index; FPG, fasting plasma glucose; LDL-C, low-density
lipoprotein cholesterol; HDL-C, high-density lipoprotein cholesterol; TG,
triglyceride; SBP, systolic blood pressure; DBP, diastolic blood pressure;
MDA, malondialdehyde; hs-CRP, high-sensitivity C-reactive protein. The
values are presented as mean ±SD.
Table 2: The effects of interventions on tested parameters after 4
weeks in the study subjects.
Parameter, unit H. sabdariffa
(n =)
Placebo
(n =)
p-Value
(between
groups)
BMI, kg/m

.
Baseline . ±. . ±.
End . ±. . ±.
p-Value . .
FPG, mg/dL .
Baseline . ±. . ±.
End . ±. . ±.
p-Value . .
Insulin, µU/mL .
Baseline . ±. . ±.
End . ±. . ±.
p-Value . .
Total cholesterol,
mg/dL
.
Baseline . ±. . ±.
End . ±. . ±.
p-Value . .
LDL-C, mg/dL .
Baseline . ±. .±.
End . ±. . ±.
p-Value . .
HDL-C, mg/dL .
Baseline . ±. . ±.
End . ±. . ±.
p-Value . .
TG, mg/dL .
Baseline . ±. . ±.
End . ±. . ±.
p-Value . .
SBP, mmHg .
Baseline .±. . ±.
End . ±. . ±.
p-Value . .
DBP, mmHg .
Baseline . ±. .±.
End . ±. . ±.
p-Value . .
MDA, µmol/L .
Baseline . ±. . ±.
End . ±. . ±.
p-Value . .
hs-CRP, mg/dL .
Baseline . ±. . ±.
End . ±. . ±.
p-Value . .
BMI, body mass index; FPG, fasting plasma glucose; LDL-C, low-density
lipoprotein cholesterol; HDL-C, high-density lipoprotein cholesterol; TG,
triglyceride. SBP, systolic blood pressure; DBP, diastolic blood pressure;
MDA, malondialdehyde; hs-CRP, high-sensitivity C-reactive protein. The
values are presented as mean ±SD.
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Consistent to our results, several studies including the
above-mentioned research on MetS patients [24] have
demonstrated the blood pressure-lowering effect of
H. sabdariffa [33–35]. Interestingly, one study showed
similar effects of H. sabdariffa to captopril (an ACE
[angiotensin-converting enzyme]-inhibitor antihyperten-
sive drug) in lowering SBP and DBP [36].
Although we did not found the anti-inflammatory and
antioxidative effects of H. sabdariffa in our study subjects,
several studies have shown such effects. In the study of
Joven et al., polyphenols from H. sabdariffa calices were
administered to patients with MetS for 4 weeks. According
to the results, the extract displayed potent anti-inflamma-
tory (reduction of interleukin (IL)-6, IL-1βand IL-8) and
antioxidant (reduction of 8-isoprostane-F2αand rising of
serum paraoxonase activity) activities [37]; however, similar
to our results, hs-CRP was not significantly affected.
Therefore, it seems that at our evaluated dose, H. sabdariffa
cannot be considered as a nutritional supplement for pre-
vention of atherosclerosis in MetS patients. It is noteworthy
that the main limitations of this study were small sample
size, short duration of intervention, and the use of calyx
powder without extraction resulting in consumption of low
dose of the plant material.
In conclusion, daily consumption of 500 mg of
H. sabdariffa L. calyx powder can decrease SBP and
serum level of TG in MetS patients, but has not any sig-
nificant effect on other cardiometabolic characteristics of
these patients. Therefore, it can be considered as a potential
natural treatment for hypertension and hypertriglyceride-
mia in MetS patients. However, more studies with higher
doses, larger sample size, and longer periods of time are
recommended to detect unknown beneficial as well as
undesirable effects of the plant in this group of patients.
Author contributions: All the authors have accepted
responsibility for the entire content of this submitted
manuscript and approved submission.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played
no role in the study design; in the collection, analysis,
and interpretation of data; in the writing of the report; or
in the decision to submit the report for publication.
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Parameter, unit H. sabdariffa (n =) Placebo (n =)
Baseline Week p-Value Baseline Week p-Value
ALT, U/L . ±. . ±. . . ±. . ±. .
AST, U/L . ±. . ±. . . ±. .±. .
BUN, mg/dL . ±. . ±. . . ±. . ±. .
Creatinine, mg/dL .±. . ±. . . ±. . ±. .
ALT, alanine aminotransferase; AST, aspartate aminotransferase; BUN, blood urea nitrogen. The values are presented as mean ±SD.
S. Asgary et al.: Roselle calyx for treatment of metabolic syndrome 5
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