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Mozaffari Khosravi2014
Mozaffari Khosravi2014
ScienceDirect
a
Department of Nutrition, Faculty of Health, Yazd Diabetes Research Center, Shahid Sadoughi University of
Medical Sciences, Yazd, Iran
b
Department of Biochemistry, Faculty of Medical Sciences, Shahid Sadoughi University of Medical Sciences,
Yazd, Iran
c
Department of English Language, Faculty of Medicine, Shahid Sadoughi University of Medical Sciences,
Yazd, Iran
KEYWORDS Summary
Objective: To identify the effect of some herbal products on insulin resistance. Regarding the
Ginger;
scientific evidences existing about ginger, this research was therefore carried out to identify
Diabetes mellitus;
the effect of ginger supplementation on insulin resistance and glycemic indices in diabetes
Insulin resistance
mellitus.
Methods: This is a randomized, double-blind, placebo-controlled trial in which 88 participants
affected by diabetes were randomly assigned into ginger (GG) and placebo (PG) groups. The
GG received 3 one-gram capsules containing ginger powder whereas the PG received 3 one-
gram microcrystalline-containing capsules daily for 8 weeks. HbA1c, fructosamine, fasting blood
sugar (FBS), fasting insulin, homeostasis model assessment insulin resistance index (HOMA-IR),
-cell function (ˇ%), insulin sensitivity (S%) and the quantitative insulin sensitivity check index
(QUICKI) were assessed before and after the intervention.
Results: FBS mean showed a decrease of 10.5% (p = 0.003) in the GG whereas the mean had
an increase of 21% in the PG (p = 0.01). Variation in HbA1c mean was in line with that of FBS.
Statistical difference was found in the two groups before and after the intervention in terms of
median of fasting insulin level, S% and HOMA-IR (P < 0.005). Moreover QUICKI mean increased
significantly in the two groups, the mean difference, however, was significantly higher in the
GG.
∗ Corresponding author. Tel.: +98 351 7249333; fax: +98 351 7258413.
E-mail address: mozaffari.kh@gmail.com (H. Mozaffari-Khosravi).
0965-2299/$ — see front matter © 2014 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ctim.2013.12.017
Please cite this article in press as: Mozaffari-Khosravi H, et al. The effect of ginger powder supplementation on insulin
resistance and glycemic indices in patients with type 2 diabetes: A randomized, double-blind, placebo-controlled trial.
Complement Ther Med (2014), http://dx.doi.org/10.1016/j.ctim.2013.12.017
+Model
YCTIM-1300; No. of Pages 8 ARTICLE IN PRESS
2 H. Mozaffari-Khosravi et al.
Conclusions: The study demonstrated that daily consumption of 3 one-gram capsules of ginger
powder for 8 weeks is useful for patients with type 2 diabetes due to FBS and HbA1c reduction
and improvement of insulin resistance indices such as QUICKI index.
© 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Mozaffari-Khosravi H, et al. The effect of ginger powder supplementation on insulin
resistance and glycemic indices in patients with type 2 diabetes: A randomized, double-blind, placebo-controlled trial.
Complement Ther Med (2014), http://dx.doi.org/10.1016/j.ctim.2013.12.017
+Model
YCTIM-1300; No. of Pages 8 ARTICLE IN PRESS
Ginger supplementation and insulin resistance in diabetes mellitus 3
Dose, type of supplement, and intervention index (HOMA-IR), beta-cell function (ˇ%) and insulin sen-
duration sitivity (S%) were calculated using a software calculation,
HOMA (HOMA calculator, version 2.2.2; Diabetes Trial Unit,
The patients were categorized into 2 groups of ginger (GG) University of Oxford, www.dtu.ox.ac.uk) and the quantita-
and placebo (PG) through table of random numbers, the GG tive insulin sensitivity check index (QUICKI) was calculated
consumed daily 3 one-gram capsules containing ginger pow- using the logarithmic transformation: 1/[log fasting insulin
der whereas the other group received capsules of the same (U/ml) + log fasting glucose (mg/dl)] 20
color and number as GG but containing cellulose microcrys-
talline, both after taking meals and for 8 weeks. Ethical considerations
The researchers gained access to these supplements by
Bou-Ali Sina herbal drug Researchers Corporation in Ghom, The study aims and methods were explained to the patients
Iran. Follow-up of the patients so as to control them for con- and the informed written consent was received from them
sumption of capsules, response to the relevant questions, provided they appeared to be interested in the participa-
and prevention of sample loss, was performed weekly by tion. On the other hand, the research was approved by
phone and every other week via monitoring the patients Ethics Commission of Deputy for Research in Shahid Sadoughi
referring to Yazd Diabetes Research Center to receive cap- University of Medical Sciences. This study has also been reg-
sules for the couple of weeks to come. istered at the Iranian registry of clinical trials (www.irct.ir)
Note that not all the supplements were totally delivered with IRCT 201104246278N1 code.
to the participants. To be assured of the consumption of sup-
plement and placebo by the participants and calculation of
rate of capsules consumption compliance, the participants Data analysis
were asked to first deliver the empty boxes of capsules and
then receive the new ones needed for the next two weeks. The data were analyzed by SPSS version 11 (SPSS Inc.,
The participants were also advised not to change their usual Chicago, IL, USA). Kolmogorov—Smirnov test was used to
diet, to stop self-reliant changes of their supplements doses, determine quantitative data distribution, paired t-test to
to stop physical activities during the intervention, and to compare mean of normal distribution variables in the two
stop consuming other ginger products. groups before and after the intervention, and student t-
test to compare the mean of variables between the two
groups. The quantitative data not following normal distri-
Measurements bution were analyzed through Wilcoxon and Mann—Whitney
tests. The results of the quantitative data with normal dis-
General information including age, weight, height, gender, tribution were reported as mean ± SD, but quantitative data
marital status, occupation, education, duration of being not normally distributed was reported using percentiles 25,
affected by the disease, type and dose of the drugs required 50 (median) and 75. The significance level was set at P-value
for diabetes control, were all accessed and recorded through equal or less than 0.05.
interview with the patients. Weight of the patients with light
clothing but without shoes, was measured through a balance
with 100 g accuracy; height, in standing position and without Results
shoes, was measured through a height-measurer with 0.5 cm
accuracy both at the beginning and the 8th week of the inter- Out of 88 patients who participated in the study, the follow-
vention. Body mass index (BMI) was calculated by weight ing cases were excluded from the intervention: 4 patients
(kg) divided by height squared (m). To study the patients who had no tendency to continue, 1 for her husband’s death,
diet in terms of daily intake of energy, carbohydrate, pro- and 2 for travel; the remaining 81 who continued to the end
tein, fiber, and total fat, a 24 h-dietary-recall questionnaire were all investigated (Fig. 1).
was used both at the beginning and the end of the interven- The compliance in consuming capsules in the two groups
tion. Nutritionist IV software (Nutritionist IV Diet Analysis, turned out to be higher than 98% thus demonstrating a well
First Data Bank Division, Hearst Corp., San Bruno, CA) was observation of the study protocol by the patients. All the
used to analyze 24 h dietary recall data. patients received oral hypoglycemic agents, 50 (61.7%) were
After 12 h of fasting, a 10 ml sample of venous blood was female and 31 (38.3%) male. The mean age of the patients in
taken from each patient by the laboratory technician at the GG and PG showed to be 49.83 ± 7.23 and 51.05 ± 7.70
the beginning and the end of intervention. The centrifuge respectively. The basic characteristics of the patients before
of the samples was performed at the room temperature the study have been reported in Table 1 showing no statisti-
and at 3000 rpm for 10 min so as to separate serum. FBS cal difference between the variables of the two groups.
was assessed using an enzymatic (glucose oxidize-peroxides) Daily dietary intake of energy and some nutrients has
in vitro test (Autoanalyser; Echo Plus Corporation, Roma, been reported in Table 2. According to the results, no statis-
Italy). HbA1c was measured using ion exchange chromatog- tical difference was found between the groups in terms of
raphy. Measuring fructosamine was also accomplished using daily dietary intake of energy and nutrients at the beginning
colorimetric method through alpha-classic autoanalyzer and the end of the intervention.
(made in Iranazma Corporation, Mashhad, Iran). Fasting The glycemic indices, QUICKI index, and BMI are shown
serum insulin concentration was also assessed using ELISA in Table 3. There was a significant decrease of FBS mean
kits (Diametra Corporation, Milan, Italy) with a sensitivity (10.5%) in the GG after the intervention (p = 0.003); how-
of 2 IU/ml. Homeostasis model assessment insulin resistance ever a significant increase of it (21%) was identified in the
Please cite this article in press as: Mozaffari-Khosravi H, et al. The effect of ginger powder supplementation on insulin
resistance and glycemic indices in patients with type 2 diabetes: A randomized, double-blind, placebo-controlled trial.
Complement Ther Med (2014), http://dx.doi.org/10.1016/j.ctim.2013.12.017
+Model
YCTIM-1300; No. of Pages 8 ARTICLE IN PRESS
4 H. Mozaffari-Khosravi et al.
Excluded (n= 62 )
♦ Not meeting inclusion criteria (n= 40 )
♦ Declined to participate (n=10 )
♦ Other reasons (n=12 )
Randomized (n=88)
Allocation
Allocated to ginger group (n= 44) Allocated to placebo group (n= 44)
Follow-Up
Lost to follow-up (give reasons) (n=2) Lost to follow-up (give reasons) (n= 2)
Discontinued intervention (give reasons) (n=2) Discontinued intervention (give reasons) (n= 1)
Analysis
Analysed (n=40 ) Analysed (n= 41 )
♦ Excluded from analysis (give reasons) (n= 0) ♦ Excluded from analysis (give reasons) (n=0 )
Please cite this article in press as: Mozaffari-Khosravi H, et al. The effect of ginger powder supplementation on insulin
resistance and glycemic indices in patients with type 2 diabetes: A randomized, double-blind, placebo-controlled trial.
Complement Ther Med (2014), http://dx.doi.org/10.1016/j.ctim.2013.12.017
+Model
YCTIM-1300; No. of Pages 8 ARTICLE IN PRESS
Ginger supplementation and insulin resistance in diabetes mellitus 5
Table 2 Comparison of daily dietary intake of energy and some nutrients before and after the intervention in ginger and
placebo groups.
Energy (kcal)
Ginger 1331.74 ± 329.70 1321.22 ± 452.99 0.36
Placebo 1363.35 ± 457.28 1389.14 ± 549.28 0.60
P-value 0.79
Carbohydrate (g)
Ginger 151.04 ± 60.93 145.85 ± 76.99 0.18
Placebo 170.07 ± 72.77 158.07 ± 70.05 0.06
P-value 0.28
Protein (g)
Ginger 54.22 ± 21.44 52.03 ± 16.63 0.58
Placebo 50.91 ± 24.24 54.37 ± 24.94 0.47
P-value 0.62
Fat (g)
Ginger 58.52 ± 14.22 61.04 ± 19.56 0.66
Placebo 55.34 ± 15.65 61.76 ± 26.83 0.06
P-value 0.66
Cholesterol (mg)
Ginger 250.18 ± 362.66 177.58 ± 232.84 0.17
Placebo 170.54 ± 252.64 168.76 ± 179.60 0.15
P-value 0.78
Fiber (g)
Ginger 8.65 ± 4.26 8.31 ± 6.64 0.25
Placebo 9.29 ± 4.01 7.99 ± 4.97 0.07
P-value 0.84
Salt (g)
Ginger 3.47 ± 0.54 3.51 ± 0.65 0.99
Placebo 3.39 ± 0.47 3.63 ± 0.97 0.31
P-value 0.85
the PG thereby showing the effect of ginger in controlling with [6]-gingerol (100 mg/kg bw) for 12 days can significantly
diabetes. On the other hand, among the insulin resistance (p < 0.05) lower FBG and improve the glucose tolerance,
indices, a significant decrease was found in fasting insulin decrease plasma triglycerides, total cholesterol, free fatty
and HOMA-IR index in both groups, a significant increase in acid, low-density lipoprotein cholesterol, and plasma insulin
S% in both groups, and a significant increase of QUICKI index concentration. The study is thus consistent with the FBS
in the GG. Therefore, considering the results of these indices results in our study.
especially OUICKI index, FBS and HbA1c related to which the Also Goyal et al. (2006) in India studied the impact of gin-
mean of their differences (Table 3), it can be concluded that ger on goldthioglucose-induced obesity in mice.19 Treatment
ginger is effective in glycemic control and in lowering insulin with 250 mg/kg of methanol and ethyl acetate extracts of
resistance. ginger for 8 weeks produced significant reduction in body
As to the effect of ginger consumption, several studies weight, glucose, insulin and lipid concentration as com-
have been carried out on human and animals the results pared to controlled obese mice. The reduction in elevated
of which are comparable to those of us. In a study con- glucose along with elevated insulin levels indicated that
ducted by Shirdel et al. in Iran (2009), the antidiabetic and ginger improves insulin sensitivity thus being in line with
antilipidemic effects of ginger on diabetic mice affected FBS results of our study. Al-amin et al. (2006) in Kuwait21
by aloxanmonohydrate and their comparison with gliben- indicated that an aqueous extract of raw ginger adminis-
clamide were investigated the result of which represented tered daily (500 mg/kg, intraperitoneally) for a period of
a significant decrease of serum glucose by ginger in the 7 weeks to streptozotocin-induced diabetic rats produces
diabetic mice17 thus being in line with our FBS results. In hypoglycaemic, hypocholesterolaemic and hypolipidaemic
another study accomplished by Singh et al. (2009) in India, properties. The glucose-lowering effect of ginger in this
the blood glucose lowering, lipid lowering, and antioxidant study is consistent with what we detected in relation to FBS.
effect of [6]-gingerol in type 2 diabetic db/db mice was Also in Bhandari’s study (2005) in India, the effect of oral gin-
investigated.18 The results depicted that treatment of mice ger ethanolic extract on diabetic mice was investigated the
Please cite this article in press as: Mozaffari-Khosravi H, et al. The effect of ginger powder supplementation on insulin
resistance and glycemic indices in patients with type 2 diabetes: A randomized, double-blind, placebo-controlled trial.
Complement Ther Med (2014), http://dx.doi.org/10.1016/j.ctim.2013.12.017
+Model
YCTIM-1300; No. of Pages 8 ARTICLE IN PRESS
6 H. Mozaffari-Khosravi et al.
Table 3 Comparison of glycemic indices, QUICKI index, and body mass index before and after the intervention in ginger and
placebo groups.
Table 4 Comparison of insulin resistance indices before and after the intervention in ginger and placebo groups.
Percentiles Percentiles
Please cite this article in press as: Mozaffari-Khosravi H, et al. The effect of ginger powder supplementation on insulin
resistance and glycemic indices in patients with type 2 diabetes: A randomized, double-blind, placebo-controlled trial.
Complement Ther Med (2014), http://dx.doi.org/10.1016/j.ctim.2013.12.017
+Model
YCTIM-1300; No. of Pages 8 ARTICLE IN PRESS
Ginger supplementation and insulin resistance in diabetes mellitus 7
results of which indicated its significant antihyperglycemic therefore, for the forthcoming similar investigation a longer
effect and significant lipid lowering activity after 20 days.22 duration of the study is suggested. Moreover, the efficacy
In a counter-evidence study by Bordia et al. (1997) in examination of a longer use of ginger supplement and its
India23 the effect of ginger and fenugreek on blood sugar impact on parameters pertinent to inflammation and hor-
and lipid concentration was investigated. For the subjects mones which are related to inflammation are suggested as
subsuming healthy individuals, patients with coronary artery well.
disease (CAD), and diabetic patients (with CAD or without
CAD), 4-gram consumption of ginger powder for 3 months Conclusions
was not effective on lipids and blood sugar, thereby being
inconsistent with our results on FBS and HbA1c.
This study demonstrated that daily consumption of 3 g of gin-
For assessing insulin resistance, our study focused on
ger in capsules for 8 weeks by patients with type 2 diabetes
indices such as fasting insulin, HOMA-IR, S%, ˇ%, and OUICKI,
leads to lowering FBS and HbA1c means as well as variation
the results of which were not the same. That is, although
in fasting insulin, insulin resistance, increase of sensitivity
median of fasting insulin and HOMA-IR index showed sig-
to insulin and QUICKI index. Therefore, consumption of this
nificant decrease before the intervention compared with
supplement is appropriate for patients; for identifying its
the end in each group, no such median significant differ-
other effects, however, some further studies are needed.
ence was detected between the groups (both before and
after the intervention). Moreover, median of S% was not
significantly different between the two groups. ˇ% had a Conflict of interests
significant decrease in the PG; in this regard a significant
difference was identified between the groups at the outset. Nothing to declare.
Therefore, considering the results of these indices espe-
cially OUICKI index in which the mean and the mean of its Funding
difference have significantly increased in the GG it can be
concluded that ginger is effective in lowering insulin resis- This work has been funded by Shahid Sadoughi University of
tance. The fact that all the indices did not come to the same Medical Sciences.
consequences may be due to the disparity in sensitivity or
properties of these indices or due to other causes.
Overall, the reexamination of the previous studies indi-
Acknowledgements
cated that research to date as to the impact of ginger
powder on sugar indices of the diabetic patients has been We hereby appreciate the participation of the patients as
very constrained. Moreover the results of the researches well as the cooperation of the staff in diabetes research
conducted on human and animals have turned out to be center of Yazd specially Dr. Farzaneh Dehghan, Dr. Sima
contradictory. This contradiction may be the consequence of Mohammad Zadeh, Mrs. Azod, Mrs. Ghiasi, Mrs. Karimi, and
disparity in people’s response. And this disparity of response Mrs Barzegari.
can be the sequel of the patients’ difference at the onset
of research, experimental group weight, severity of insulin References
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resistance and glycemic indices in patients with type 2 diabetes: A randomized, double-blind, placebo-controlled trial.
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Please cite this article in press as: Mozaffari-Khosravi H, et al. The effect of ginger powder supplementation on insulin
resistance and glycemic indices in patients with type 2 diabetes: A randomized, double-blind, placebo-controlled trial.
Complement Ther Med (2014), http://dx.doi.org/10.1016/j.ctim.2013.12.017