Eur J Nutr (2016) 55:2129–2136
DOI 10.1007/s00394-015-1027-6
ORIGINAL CONTRIBUTION
Changes of serum adipocytokines and body weight
following Zingiber officinale supplementation in obese women: a
RCT
Vahideh Ebrahimzadeh Attari1 · Alireza Ostadrahimi2 ·
Mohammad Asghari Jafarabadi3 · Sajjad Mehralizadeh1 · Sepideh Mahluji1
Received: 19 March 2015 / Accepted: 19 August 2015 / Published online: 29 August 2015
© Springer-Verlag Berlin Heidelberg 2015
Abstract area, ongoing clinical trials are needed to further explore
Purpose The present randomized, double-blind, placebo- ginger’s effectiveness.
controlled study aimed to evaluate the effect of Zingiber
officinale (ginger) consumption on some metabolic and Keywords Zingiber officinale Roscoe · Obesity ·
clinical features of obesity. Adipocytokines
Methods Eighty eligible obese women (aged 18–45 years)
were randomly assigned to either ginger or placebo groups
(receiving 2 g/day of ginger powder or corn starch as two 1 g Introduction
tablets) for 12 weeks. Body mass index (BMI) and body com-
position were assessed every 4 weeks, and serum levels of lep- Obesity, the excessive accumulation of body fat, is a major
tin, adiponectin, resistin, insulin and glucose were determined risk factor for the global prevalence of chronic diseases [1].
before and after intervention. The homeostasis model assess- In fact, the adipose tissue contributes to these comorbidities
ment of insulin resistance (HOMA-IR) and quantitative insu- through the secretion of signaling molecules, termed adi-
lin sensitivity check index (QUICKI) were also calculated. pokines [1–3]. Adiponectin as the most abundant adipokine
Results Ginger consumption significantly decreased BMI, exerts both insulin-sensitizing and anti-atherogenic effects,
serum insulin and HOMA-IR index, along with increasing and its concentration increases with weight loss [4]. In con-
QUICKIs as compared to the placebo. Moreover, signifi- trast, leptin and resistin have been implicated in the patho-
cant reductions in serum leptin, resistin and glucose were genesis of insulin resistance and atherosclerosis along with
observed in both groups, especially in ginger group with their pro-inflammatory properties. Leptin has also a pri-
nonsignificant differences between groups. The body com- mary role in the body weight regulation through controlling
position and serum levels of adiponectin were not signifi- food intake and energy expenditure. Despite the elevated
cantly changed in study groups. levels of leptin in obese patients, its efficiency is low, most
Conclusion In conclusion, our findings demonstrate a likely due to the increased leptin resistance. Moreover,
minor beneficial effect of 2 g ginger powder supplemen- the circulating levels of these hormones decrease as body
tation for 12 weeks on weight loss and some metabolic weight declines [1, 5, 6].
features of obesity. However, given the lack of data in this To date, several strategies have been investigated to
manage this public health issue, particularly the use of
* Alireza Ostadrahimi medicinal plants as a possible effective way for weight loss
[email protected] and also correction of metabolic imbalance of adipokines
1
Student Research Committee, Tabriz University of Medical [7].
Sciences, Tabriz, Iran Ginger (Zingiber officinale Roscoe, family Zingiber-
2
Nutrition Research Center, Tabriz University of Medical aceae) is one of the most widely used spices and medici-
Sciences, Tabriz, Iran nal plants around the world. There are some scientific
3
Road Traffic Injury Research Center, Tabriz University evidences regarding its various pharmacological activities
of Medical Sciences, Tabriz, Iran including anti-inflammatory and antioxidant [8, 9], glucose
13
2130 Eur J Nutr (2016) 55:2129–2136
and lipid lowering [10, 11], antiemetic [12] and anticancer weight of ginger tablet. The tablets were placed in the iden-
effects [13]. tical containers and were labeled with two codes by a third
The anti-obesity and weight-lowering effect of ginger person not directly involved in our study. In addition, for
and its components has also been recently considered, and blinding of subjects, a slight amount of ginger powder was
there are some promising results from in vitro and rodent added to the placebo tablets’ container to give ginger odor
in vivo studies [14–19]. In addition, evidences from experi- during opening the door.
mental studies indicate that ginger maybe affect the cir-
culating level of cytokines [19–23]. However, scientific Study design
research in humans is very limited [24, 25]. To the best of
our knowledge, the effect of ginger consumption on adi- This study utilized a randomized, double-blind, placebo-
pocytokines levels has been investigated just in one pilot controlled design. The sample size was calculated based
study [24]. Accordingly, the aim of the present randomized, on a 90 % power and a 5 % significance level, consider-
double-blind, placebo-controlled study was to investigate ing the leptin variables from the study of Mansour et al.
the effect of ginger supplementation on weight loss and [24], which necessitated at least 28 cases in each group.
some serum adipocytokines in obese women. But assuming a 40 % dropout, 40 cases were assigned in
each group. Participants (n = 80) were randomly assigned
to the ginger or placebo group (n = 40) using a random
Methods and materials number table and were instructed to take two tablets per
day (30 min before meal) for 12 weeks. Tablets were given
Subjects to the participants every 4 weeks. The subjects were also
instructed to maintain their usual dietary and exercise
Eighty eligible healthy obese women, aged 18–45 years pattern throughout the study. Besides, the subjects were
and BMI of 30–40 kg/m2, were voluntarily participated in instructed to precisely record their food intake for three
our study, through a general call schedule across the city of consecutive days at baseline, weeks 6 and 12. Dietary data
Tabriz, Iran. (energy values and macronutrient content) were analyzed
Subjects were excluded in the case of clinically diag- using Nutritionist 4 software (First Databank; Hearst, San
nosed diabetes mellitus, cardiovascular disease, gallstone, Bruno, CA, USA).
hypo- or hyperthyroidism, deep depression, pregnancy,
breast feeding or menopause, being on a weight-lowering Clinical parameters
diet, taking medications that could influence weight, smok-
ing, subjects with high physical activity, taking nutritional Blood samples were obtained from all subjects at the begin-
supplements and being hypersensitive to ginger. ning and end of intervention after a 12-h overnight fasting
The study was approved by the Ethics Committee of (water permitted). Serum samples were separated by cen-
Tabriz University of Medical Science (reference number trifugation and stored at −80 °C until analysis.
92154), and the study was registered on the Iranian Regis- Serum levels of leptin, resistin and total adiponectin
try of Clinical Trials (http://www.irct.ir) with the identifica- were measured using the human ELISA kits (leptin and
tion No. 201311172017N18. All subjects were made aware resistin: BioVendor-Laboratorni Medicina, Brno, Czech
of the content of the study and signed a written consent Republic and adiponectin: Orgenium Laboratories, Vantaa,
form, at the beginning of study. Finland), according to the manufacturers’ instructions.
Fasting serum glucose enzymatically analyzed with a
Supplements preparation commercial kit (Pars Azmun Co., Tehran, Iran). Serum
insulin concentration was also determined using the human
Dried rhizomes of ginger (Zingiber officinale Roscoe, Chi- ELISA kit (Monobind Inc., Lake Forest, CA, USA). Insulin
nese yellow ginger) were purchased from a local market resistance index was estimated by the homeostasis model
in Tabriz. They were authenticated by morphologic com- assessment of insulin resistance (HOMA-IR) using the fol-
parison with different standard texts by Nutrition Research lowing formula: [fasting serum insulin (µU/ml) × fasting
Center, Tabriz University of Medical Science (Tabriz, Iran). serum glucose (mg/dl)/405] [17]. Moreover, insulin sensi-
The ginger rhizomes were finely ground and then prepared tivity was determined using quantitative insulin sensitivity
as tablets containing 1 g ginger powder in each (Pharma- check index (QUICKI) by the following formula: [1/log
ceutics Laboratory, Faculty of Pharmacy, Tabriz University insulin (µU/ml) + log glucose (mg/dl)] [26].
of Medical Science). Besides, the placebo tablet consisted Furthermore, BMI (weight (kg)/height (m2)) was cal-
of corn starch and other excipients in order to match the culated from the height and weight, using the calibrated
13
Eur J Nutr (2016) 55:2129–2136 2131
80 healthy
obese women
Randomization
Ginger group Placebo group
(n=40) (n=40)
9 withdrew because of:
1 withdrew because of travelling (n= 2), using
antidepressant agents (n= 2),
pregnancy during study Follow up diagnosed hypothyroidism
12 weeks (n= 1), pregnancy (n=3) and
rheumatoid arthritis (n=1)
Completed trial Completed trial
Analysis
n= 39 subjects n= 31 subjects
Fig. 1 Study participant flow diagram
equipment, every 4 weeks. Body composition [total body paired-sample t test and the nonparametric Wilcoxon
fat mass (FM), total body fat-free mass (FFM) and total signed-rank test were employed. The repeated-measures
body water (TBW)] was also assessed by an 8-electrode analysis of variance was also performed to assess within-
bioelectrical impedance analyzer with a 0.1 kg precision group differences of BMI and fat mass in time trend.
(Tanita BC-418 MA; Tanita Co., Tokyo, Japan), every Results are reported as mean ± SD, if not otherwise stated.
4 weeks. The percent changes were also calculated as follows: (after-
before/before) × 100. The significance level was set at
Statistical analyses p < 0.05.
Data were analyzed using SPSS software, version 21.0
(IBM Corp., Armonk, NY, USA). The normal distribution Results
of variables was tested by the Kolmogorov–Smirnov test,
and also considering the mean and SD. Possible differences From eighty volunteer women who were recruited the
at baseline among treatment groups were assessed by inde- study, ten participants did not complete the study as shown
pendent sample t test for normally distributed parameters in Fig. 1. One person from the ginger group withdrew
and the Mann–Whitney test for nonparametric data. because of pregnancy, and nine participants from the pla-
At the end of intervention, differences between groups cebo group dropped out because of traveling (n = 2), preg-
were analyzed using the analysis of covariance (ANCOVA) nancy (n = 3), using antidepressant agents (n = 2), diag-
for normally distributed parameters (the baseline values nosed hypothyroidism (n = 1) and taking corticosteroids
and BMI differences employed as covariates) and Mann– for rheumatoid arthritis (n = 1). None of the subjects dis-
Whitney test for nonparametric variables. Moreover, to continued the study because of the adverse effects of ginger
assess within-group differences of biochemical parameters, or placebo.
13
2132 Eur J Nutr (2016) 55:2129–2136
Table 1 Baseline Parameters Ginger group (n = 39)b Placebo group (n = 31)b p value**
characteristics of the
participants in both groups Age (years) 35.25 ± 7.30 34.54 ± 7.91 0.699
BMI (kg/m2) 34.34 ± 3.61 35.46 ± 3.41 0.192
Body fat mass (kg) 36.63 ± 6.14 37.50 ± 7.80 0.605
Body fat-free mass (kg) 50.58 ± 3.65 50.84 ± 4.22 0.781
Glucose (mg/dl) 94.20 ± 13.50 94.48 ± 15.31 0.936
Insulin (µU/ml)a 5.20 (2.30, 8.50) 3.40 (1.40, 5.50) 0.066
Leptin (ng/ml) 33.05 ± 14.75 35.61 ± 13.89 0.461
Adiponectin (µg/ml)a 2.00 (1.00, 3.00) 3.00 (1.00, 5.00) 0.014
Resistin (ng/ml) 6.97 ± 1.63 6.05 ± 1.48 0.017
Values are mean ± SD
** p values are based on the independent sample t test for normally distributed parameters and Mann–
Whitney test for nonparametric variables
a
Values are presented as median (25th, 75th percentiles) for the nonparametric variables
b
Baseline data are shown just for study subjects who completed the study
The baseline characteristics of the participants are a 36
shown in Table 1. At the beginning of study, there was no
significant difference between groups in aforesaid param- 35.5
eters, except for adiponectin (p = 0.014) and resistin con-
35
centration (p = 0.017).
* *†
BMI
Consumption of ginger for 12 weeks significantly 34.5 *
reduced BMI (p = 0.019) (see Fig. 2), serum insu-
34
lin (p = 0.021) and HOMA-IR index (p = 0.014), while
increasing QUICKIs (p = 0.045) as compared to the pla- 33.5 Ginger
cebo (see Table 2), whereas there was no significant dif- Placebo
ference in changes of body composition (Fig. 2), fasting 33
0 4 8 12
blood glucose and circulating levels of adipokines between
Time
groups (p > 0.05, see Table 2).
Furthermore, within-group analyses showed that BMI, b 39
serum glucose, insulin, leptin and resistin levels signifi- 38.5
cantly decreased in ginger group (p < 0.0001), along with
38
significant reduction in the HOMA-IR and increase in
QUICKIs (p < 0.0001), whereas in the placebo group, 37.5
Fat mass
there was only a significant reduction in serum glucose 37
(p = 0.008), leptin (p = 0.001) and resistin (p < 0.0001)
36.5
levels (Table 2). However, these decreases were more
pronounced in the ginger group than those in the placebo 36
Ginger
group (percent changes of glucose: −7.51 vs. −6.16 %, 35.5 Placebo
leptin: −20.25 vs. −11.42 % and resistin level: −38.64 vs. 35
−36.11 %). 0 4 8 12
The circulating level of total adiponectin was also Time
slightly decreased in both groups, particularly in placebo
group (p > 0.05). Our results revealed a slight and nonsig- Fig. 2 Effect of ginger compared to the placebo supplementation on
nificant increase in fat mass in both groups (Fig. 2) which BMI (a) and fat mass (b). †p < 0.05 based on the repeated-measures
was mainly due to the total body water (TBW) changes analysis of variance. *p < 0.05, the comparison between groups by
analysis of covariance (ANCOVA) with the baseline values and
during measurements. Hence, TBW was utilized as a energy intake differences, employed as covariates for BMI and the
covariate during ANCOVA test (Fig. 2). baseline values, energy intake differences and total body water differ-
ences, as covariates for body composition data
13
Table 2 Effect of ginger compared to the placebo supplementation on some biochemical parameters in obese women
Eur J Nutr (2016) 55:2129–2136
Parameters Ginger group Placebo group p value Effect Observed
a a
sizea powera
Before interven- After intervention Changes (%) p value** Before interven- After intervention Changes (%) p value**
tion tion
Glucose (mg/dl) 94.20 ± 13.50 86.17 ± 8.25 −7.51 ± 9.67 <0.0001 94.48 ± 15.31 87.54 ± 10.51 −6.16 ± 12.12 0.008 0.669† 0.003 0.071
Leptin (ng/ml) 33.05 ± 14.75 26.00 ± 12.44 −20.25 ± 23.75 <0.0001 35.61 ± 13.89 30.21 ± 11.84 −11.42 ± 26.15 0.001 0.495† 0.007 0.104
Resistin (ng/ml) 6.97 ± 1.63 4.32 ± 1.33 −38.64 ± 9.96 <0.0001 6.05 ± 1.48 3.79 ± 1.12 −36.11 ± 18.33 <0.0001 0.869† 0.000 0.053
Adiponectinb 2.00 (1.00, 3.00) 1.5 (1.00, 3.00) – 0.711 3.00 (1.00, 5.00) 1.00 (0.0, 3.00) – 0.216 0.242†† – –
(µg/ml)
Insulinb (µU/ml) 5.20 (2.30, 8.50) 2.40 (1.80, 4.00) – <0.0001 3.40 (1.40, 5.50) 2.30 (1.80, 3.70) – 0.501 0.021†† – –
HOMA-IRb 1.20 (0.55, 1.82) 0.53 (0.38, 0.84) – <0.0001 0.83 (0.28, 1.26) 0.49 (0.39, 0.86) – 0.256 0.014†† – –
QUICKIb 0.37 (0.34, 0.42) 0.42 (0.39,0.45) – <0.0001 0.39 (0.36, 0.48) 0.43 (0.39, 0.45) – 0.901 0.045†† – –
Ginger group: n = 39; Placebo group: n = 31
** p values are based on the paired-sample t test for normally distributed parameters and Wilcoxon signed-rank test for nonparametric data
†
p values indicate the comparison between groups by analysis of covariance (ANCOVA) with the baseline values and BMI differences, employed as covariates
††
p values indicate the comparison between groups by Mann–Whitney test
a
Percent changes, effect size and observed power are presented just for normally distributed parameters
b
Values are presented as median (25th, 75th percentiles) for the nonparametric variables
13
2133
2134 Eur J Nutr (2016) 55:2129–2136
Discussion Our results are in agreement with some earlier reports.
More recently, Li et al. [17] demonstrated that gin-
The present randomized, double-blind, placebo-controlled ger extract treatment (100 and 200 mg/kg) significantly
study was designed to determine whether 12-week gin- decreased serum insulin and HOMA-IR in the high-fat,
ger supplementation could influence some of the obesity- high-carbohydrate (HFHC) diet-fed rats over 10 weeks,
related features and serum adipocytokines levels. Our while a marked reduction in blood glucose was observed
results revealed that ginger consumption resulted in a just in the high-dose ginger extract treatment group
slight, but statistically significant decrease in BMI along (200 mg/kg) compared to HFHC controls. Likewise,
with nonsignificant reductions in serum leptin and resistin Beattie et al. [30] revealed a significant decrease in insu-
as compared to the placebo group. However, body fat mass lin in mice feeding with a high-fat diet plus 6-gingerol for
and serum total adiponectin level had no significant change 8 weeks, but there was not significant difference between
in any groups. groups in serum glucose lowering effect.
Our findings are partly supported by the existing exper- Our results are also supported by some previous clini-
imental studies. Saravanan et al. [19] and Okamoto et al. cal trials that ginger powder supplementation in type 2 dia-
[22] demonstrated that rodents treated with a high-fat diet betic patients significantly decreased fasting blood glucose,
(HFD) containing [6] gingerol had significant lower weight insulin and HOMA-IR and increased the QUICKI versus
gain, fat accumulation, and circulating level of leptin, com- placebo [11, 31]. However, contrary to our results, ginger
pared to the HFD control. In another study, ginger aqueous consumption (1 g/day) for 10 weeks did not cause any sig-
extracts significantly decreased body weight, body fat mass nificant change in fasting serum insulin and glucose levels
and serum leptin levels in obese diabetic rats compared to in obese men [25].
the control group [23]. In contrast, Wadikar and Premav- Although the mechanisms responsible for these ben-
alli [27] showed that ginger juice significantly increased eficial effects of ginger are not entirely clear, they might
weight gain and decreased leptin levels in rats. As there result from the increased expression of GLUT-4 and glu-
are very limited clinical studies in this regard, it is difficult cose uptake by cells, increased insulin receptors, enhanced
to compare our results. However, contrary to our findings, pancreatic beta cells’ functions and also modifying the adi-
Mansour et al. [24] reported that intake of a single-dose hot pokines’ levels as described before [10, 32].
ginger beverage (with 2 g ginger powder) before a standard Taken together, this is the first clinical trial aimed to
breakfast meal had no significant effect on serum leptin, investigate the effect of ginger on some metabolic features
adiponectin and other cytokines levels, as compared to the of obesity. A potential limitation of this study is that accord-
control group. In another study, ginger consumption (1 g/ ing to our facilities, we used the bioelectrical impedance
day) for 10 weeks did not cause any significant change in analyzer for body composition assessment that although is
BMI and body composition of obese men [25]. a safe and valuable clinical tool to measure body compo-
Overall, it seems that ginger could influence body sition, it is very sensitive to body water changes through
weight and body composition through some mechanisms some confounders such as drinking water before measure-
such as (1) increasing thermogenesis and energy expendi- ment, drinking tea or coffee 24 h ago [33]. However, we
ture by catecholamine-releasing action [18, 24, 28], (2) adjusted total body water changes for fat mass and fat-free
increasing the lipolysis of white adipose tissue [18, 20, 29] mass analyses. Moreover, based on experimental studies, it
and (3) inhibition of the lipase enzyme and the intestinal seems that treatment with ginger maybe need higher dose
absorption of dietary fat [16]. of powder form or using standard extracts to reach more
Although the mechanisms of ginger effect on adipokines effectiveness, just as a suggestion for future researches,
level have not been clarified, there are evidences from since it is a safe herbal medicine according to existing data
in vitro studies that ginger components can increase the and also the FDA’s report on its safety [10].
gene expression of some adipokines such as adiponectin In conclusion, our findings demonstrate a minor ben-
[21] and inhibit the gene expression of resistin [20]. eficial effect of 2 g ginger powder supplementation for
The other findings of the present study were significant 12 weeks on weight loss and some metabolic features of
reduction in serum insulin and HOMA-IR index along with obesity. However, given the lack of data in this area, it is
significant increase in QUICKI in ginger compared to the difficult to explicitly talk about the effectiveness of gin-
placebo group. Interestingly, these are in accordance with ger and further well-designed clinical trials are needed to
decrease in serum leptin and resistin, as two pro-inflam- explore ginger’s potential in management of obesity.
matory adipokines. Furthermore, serum glucose level was
significantly decreased in both groups especially in ginger Acknowledgments We wish to express our appreciation to the sub-
jects who participated in the study. We also would like to thank Dr.
group, without a significant difference between them. Samira Pormoradian for technical assistance on biochemical analyses.
13
Eur J Nutr (2016) 55:2129–2136 2135
This study was supported by a Grant from the Research Vice Chancel- 16. Mahmoud RH, Elnour WA (2013) Comparative evaluation of the
lor and Nutrition Research Center, Tabriz University of Medical Sci- efficacy of ginger and orlistat on obesity management, pancre-
ences (Tabriz, Iran), with Grant Number (5/71/1353). The results of atic lipase and liver peroxisomal catalase enzyme in male albino
this article are derived from Ph.D. thesis of Vahideh Ebrahimzadeh rats. Eur Rev Med Pharmacol Sci 17(1):75–83
Attary (NO, D/32). 17. Li Y, Tran VH, Kota BP, Nammi S, Duke CC, Roufogalis BD
(2014) Preventative effect of Zingiber officinale on insulin
Compliance with ethical standards resistance in a high-fat high-carbohydrate diet-fed rat model
and its mechanism of action. Basic Clin Pharmacol Toxicol
Conflict of interest The authors have declared that there is no con- 115(2):209–215
flict of interest. 18. Pulbutr P, Thunchomnang K, Lawa K, Mangkhalathon A, Sae-
nubol P (2011) Lipolytic effects of Zingerone in adipocytes iso-
lated from normal diet fed rats and high fat diet fed rats. Int J
Pharmacol 7:629–634
References 19. Saravanan G, Ponmurugan P, Deepa MA, Senthilkumar B (2014)
Anti-obesity action of gingerol: effect on lipid profile, insulin,
1. Jung UJ, Choi MS (2014) Obesity and its metabolic complica- leptin, amylase and lipase in male obese rats induced by a high-
tions: the role of adipokines and the relationship between obe- fat diet. J Sci Food Agric 94(14):2972–2977
sity, inflammation, insulin resistance, dyslipidemia and nonalco- 20. Ahn EK, Oh JS (2012) Inhibitory effect of Galanolactone iso-
holic fatty liver disease. Int J Mol Sci 15(4):6184–6223 lated from Zingiber officinale Roscoe extract on adipogenesis in
2. Yoo HJ, Choi KM (2014) Adipokines as a novel link between 3T3-L1 Cells. J Korean Soc Appl Biol Chem 55:63–68
obesity and atherosclerosis. World J Diabetes 5(3):357–363 21. Isa Y, Miyakawa Y, Yanagisawa M, Goto T, Kang MS, Kawada
3. Lafontan M (2014) Adipose tissue and adipocyte dysregulation. T, Morimitsu Y, Kubota K, Tsuda T (2008) 6-Shogaol and
Diabetes Metab 40(1):16–28 6-gingerol, the pungent of ginger, inhibit TNF-alpha mediated
4. Tilg H, Moschen AR (2008) Role of adiponectin and PBEF/vis- down regulation of adiponectin expression via different mecha-
fatin as regulators of inflammation: involvement in obesity-asso- nisms in 3T3-L1 adipocytes. Biochem Biophys Res Commun
ciated diseases. Clin Sci 114(4):275–288 373(3):429–434
5. Koleva DI, Orbetzova MM, Atanassova PK (2013) Adipose tis- 22. Okamoto M, Irii H, Tahara Y, Ishii H, Hirao A, Udagawa H,
sue hormones and appetite and body weight regulators in insulin Hiramoto M, Yasuda K, Takanishi A, Shibata S, Shimizu I (2011)
resistance. Folia Med 55(1):25–32 Synthesis of a new [6]-gingerol analogue and its protective effect
6. Al-Suhaimi EA, Shehzad A (2013) Leptin, resistin and visfatin: with respect to the development of metabolic syndrome in mice
the missing link between endocrine metabolic disorders and fed a high-fat diet. J Med Chem 54(18):6295–6304
immunity. Eur J Med Res 18:12 23. Shalaby MA, Saifan HY (2014) Some pharmacological effects
7. Derdemezis CS, Kiortsis DN, Tsimihodimos V, Petraki MP, of cinnamon and ginger herbs in obese diabetic rats. J Intercult
Vezyraki P, Elisaf MS, Tselepis AD (2011) Effect of plant poly- Ethnopharmacol 3(4):144–149
phenols on adipokine secretion from human SGBS adipocytes. 24. Mansour MS, Ni YM, Roberts AL, Kelleman M, Roychoud-
Biochem Res Int 2011:285618 hury A, St-Onge MP (2012) Ginger consumption enhances the
8. Grzanna R, Lindmark L, Frondoza CG (2005) Ginger-an herbal thermic effect of food and promotes feelings of satiety without
medicinal product with broad anti-inflammatory actions. J Med affecting metabolic and hormonal parameters in overweight
Food 8(2):125–132 men: a pilot study. Metabolism 61(10):1347–1352
9. Mashhadi NS, Ghiasvand R, Askari G, Hariri M, Darvishi L, 25. Atashak S, Peeri M, Azarbayjani MA, Stannard SR, Mosalman
Mofid MR (2013) Anti-oxidative and anti-inflammatory effects Haghighi M (2011) Obesity-related cardiovascular risk factors
of ginger in health and physical activity: review of current evi- after long- term resistance training and ginger supplementation. J
dence. Int J Prev Med 4(S1):36–42 Sports Sci Med 10:685–691
10. Li Y, Tran VH, Duke CC, Roufogalis BD (2012) Preventive and 26. Henríquez S, Jara N, Bunout D, Hirsch S, de la Maza MP, Leiva
protective properties of Zingiber officinale (Ginger) in diabetes L, Barrera G (2013) Variability of formulas to assess insulin sen-
mellitus, diabetic complications, and associated lipid and other sitivity and their association with the Matsuda index. Nutr Hosp
metabolic disorders: a brief review. Evid Based Complement 28(5):1594–1598
Alternat Med 2012:516870 27. Wadikar DD, Premavalli KS (2011) Appetizer administration
11. Mahluji S, Attari VE, Mobasseri M, Payahoo L, Ostadrahimi stimulates food consumption, weight gain and leptin levels in
A, Golzari S (2013) Effects of ginger (Zingiber officinale) on male Wistar rats. Appetite 57(1):131–133
plasma glucose level, HbA1c and insulin sensitivity in type 2 28. Fujisawa F, Nadamoto T, Fushiki T (2005) Effect of intake of
diabetic patients. Int J Food Sci Nutr 64(6):682–686 ginger on peripheral body temperature. J Jpn Soc Nutr Food Sci
12. Palatty PL, Haniadka R, Valder B, Arora R, Baliga MS (2013) 58(1):3–9
Ginger in the prevention of nausea and vomiting: a review. Crit 29. Iwasaki Y, Morita A, Iwasawa T, Kobata K, Sekiwa Y, Morimitsu
Rev Food Sci Nutr 53(7):659–669 Y, Kubota K, Watanabe T (2006) A nonpungent component of
13. Pereira MM, Haniadka R, Chacko PP, Palatty PL, Baliga MS steamed ginger—[10]-shogaol—increases adrenaline secretion
(2011) Zingiber officinale Roscoe (ginger) as an adjuvant in can- via the activation of TRPV1. Nutr Neurosci 9(3–4):169–178
cer treatment: a review. J BUON 16(3):414–424 30. Beattie JH, Nicol F, Gordon MJ, Reid MD, Cantlay L, Horgan
14. Goyal RK, Kadnur SV (2006) Beneficial effects of Zingiber GW, Kwun IS, Ahn JY, Ha TY (2011) Ginger phytochemicals
officinale on goldthioglucose induced obesity. Fitoterapia mitigate the obesogenic effects of a high-fat diet in mice: a pro-
77:160–163 teomic and biomarker network analysis. Mol Nutr Food Res
15. Malik ZA, Sharmaa PL (2011) Attenuation of high-fat diet 55(Suppl 2):S203–S213
induced body weight gain, adiposity and biochemical anomalies 31. Mozaffari-Khosravi H, Talaei B, Jalali BA, Najarzadeh A,
after chronic administration of Ginger (Zingiber officinale) in Mozayan MR (2014) The effect of ginger powder supplementa-
Wistar Rats. Int J Pharmacol 7:801–812 tion on insulin resistance and glycemic indices in patients with
13
2136 Eur J Nutr (2016) 55:2129–2136
type 2 diabetes: a randomized, double-blind, placebo-controlled 33. Faria SL, Faria OP, Cardeal MD, Ito MK (2014) Validation
trial. Complement Ther Med 22(1):9–16 study of multi-frequency bioelectrical impedance with dual-
32. Roufogalis BD (2014) Zingiber officinale (Ginger): a future out- energy X-ray absorptiometry among obese patients. Obes Surg
look on its potential in prevention and treatment of diabetes and 24(9):1476–1480
prediabetic states. New J Sci 2014:674684
13