Industrial Crops and Products 69 (2015) 137–142

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Industrial Crops and Products

journal homepage: www.elsevier.com/locate/indcrop

Changes in antioxidant capacity, levels of soluble sugar, total

polyphenol, organosulfur compound and constituents in garlic
clove during storage
Fei Meng LI ∗ , Tong LI, Wei LI, Long De Yang
Gansu Provincial Key Lab of Aridland Crop Science/College of Life Science and Technology, Gansu Agricultural University, Lanzhou 730070, PR China

a r t i c l e i n f o a b s t r a c t

Article history: The present study was designed to study the effect of storage duration on changes of antioxidant capacities
Received 15 September 2014 and bioactive compounds in garlic clove by DPPH and FRAP assays and GC–MS analysis. Both DPPH and
Received in revised form 11 January 2015 FRAP assays displayed that the antioxidant capacities in garlic clove extracts reached maximum values at
Accepted 11 February 2015
8 weeks. The levels of soluble sugar decreased during storage, and the contents of total polyphenols and
Available online 19 February 2015
organosulfur compounds reached maximum value at 6 and 8 weeks, respectively, and then decreased
significantly. The GC–MS analysis results of ethyl acetate extract showed that among of the eighteen
Keywords:
typical organosulfur compounds, ten compounds reached maximum levels at 8 weeks. The present study
Garlic (Allium sativum L.)
Storage duration
indicated that organosulfur compounds in garlic cloves might play a key role in antioxidant capacities due
Antioxidant capacity to their positive relationship during storage. The results in this study would provide beneficial information
Organosulfur compounds for garlic processing industries and consumers to make full use of garlic during storage.
Soluble sugar Crown Copyright © 2015 Published by Elsevier B.V. All rights reserved.
Polyphenols

1. Introduction responsible for the anticancer effect for garlic eaters (Seki et al.,
2008). Moreover, garlic contained stable organosulfur compounds,
Garlic (Allium sativum L.) belongs to the vegetables of the Allium flavonoids and polyphenols, which had potent antioxidant prop-
genus, it has a long history as being a food having a unique taste erties (Nencini et al., 2011; Beato et al., 2011). In addition, garlic
and odor (Ariga and Seki, 2006; Ngo et al., 2007). Nowadays, Garlic polysaccharide, mainly consisted of water-soluble fructose poly-
has been not only widely used in antibacterial, antiviral, antifungal mers, displayed bioactivity in many aspects, such as controlling
and antiprotozoal, but also beneficial effects on the cardiovascular blood lipids, lowering blood sugar and promoting the absorbability
and immune systems (Harris et al., 2001). Researchers have proved of minerals (Huang et al., 2012).
that there are more than 200 components identified from garlic, The flavor compounds that are important quality parameters
such as vitamins, proteins, lipids, trace elements Se, flavonoids and will be affected by many factors, such as storage temperature, culti-
at least 33 different organosulfur compounds (Stajner et al., 2006; var, storage duration, etc (Randle and Lancaster, 2002; Bloem et al.,
Ngo et al., 2007). 2011). Bloem et al. (2011) demonstrated that sulfur fertilization
Garlic clove contains a surprisingly large amount of alliinase was shown to significantly increase the alliin concentration in gar-
(10 mg/g fresh weight), alliinase in the bundle sheath cells and lic cloves, while high nitrogen levels had an adverse effect, and
alliin in the storage cells are separated, and only they encounter best quality in terms of high alliin contents was obtained during
each other once garlic is damaged, then generate chemical reaction the entire storage time at an sulfur level of at minimum 30 kg/ha if
and convert alliin immediately to the alk(en)yl sulfinyl compounds no nitrogen was applied. Montaño et al. (2011) presented that there
(Ellmore and Feldberg, 1994). Alk(en)yl sulfides are characteris- was a significant effect of the location, cultivar, and garlic ecotype
tic flavor components of garlic. Modern scientific research has on individual organosulfur compound contents.
revealed that the wide variety of dietary and medicinal functions of Generally, garlic cloves are stored for varying lengths of time
garlic can be attributed to the sulfur compounds from garlic (Ariga before being consumed, so it is important for garlic processing
and Seki, 2006). Studies suggested that diallyl trisulfide (DATS) was industries and consumers to know the changes of chemical con-
stituents and antioxidant capacities during storage, but so far
these have not yet been investigated. In the present study, the
changes of antioxidant capacities, soluble sugar, total polyphenols
∗ Corresponding author. Tel.: +86 931 7631742. and organosulfur compounds were determined and identified by
E-mail address: limengfei0921@163.com (M.L. Fei).

http://dx.doi.org/10.1016/j.indcrop.2015.02.021
0926-6690/Crown Copyright © 2015 Published by Elsevier B.V. All rights reserved.
138 M.L. Fei et al. / Industrial Crops and Products 69 (2015) 137–142

Fig. 1. Changes in antioxidant capacities of different solvent extracts in garlic by the assays of DPPH (A) and FRAP (B) during storage. The data are the means of triplicate
measurements. Different lowercase and uppercase letters on top of the column were considered significant at P < 0.05 level among different solvent extracts and storage
times, respectively.

DPPH and FRAP assays and GC–MS (gas chromatography–mass 2.3. Antioxidant assays
spectrometry), with the aim of gaining insight into metabolism and
evaluating the effect of storage duration on antioxidant capacity in 2.3.1. DPPH assay
garlic cloves. The measurement was performed according to the literature (Li
et al., 2012, 2013), and the specific steps as follows. The extracts
of H2 O, ethanol and ethyl acetate in Section 2.2 were diluted with
2. Experimental
80% methanol with concentration of 10 mg/mL, and then 50 ␮l of
sample solution was added into 950 ␮l of 10−4 M DPPH methanol
2.1. Plant material
solution. After shaking and incubating in dark at room temperature
for 30 min. The absorbance was evaluated at 515 nm, and 500 ␮M
Fresh garlic cloves, harvested from the Gansu Provincial Key
90% methanol ASA was tested as a positive control. The assay was
Lab Foundation of Aridland Crop Science, Lanzhou, China, in June
carried out in triplicate, and the capability to scavenge the DPPH
2012, were used for the present study. Garlic cloves were stored in
radicals was calculated as:
an incubator at 20 ± 2 ◦ C with 45% relative humidity on a 1000 lx
light/dark (12 h/12 h) cycle, for detecting the changes of antioxi-  (A − A) 
0
dant capacities, soluble sugar, total polyphenols and organosulfur Scavenging effect(I%, Percentage of inhibition) = × 100
A0
compounds and chemical constituents during storage duration.
where A0 and A were the absorbance of DPPH without and with
sample, respectively.
2.2. Extracts preparation

The extracts preparation was performed according to the lit- 2.3.2. FRAP assay
erature (Brankovic et al., 2011) with slightly modification, and The measurement was described by the literature (Benzie and
the specific steps as follows. Garlic cloves were peeled, weighed Strain, 1996; Li et al., 2012), and the specific steps as follows.
(50.0 g), and pulverized into a fine juice by a laboratory blender, The 300 ␮L FRAP reagent [prepared ex tempore by mixing 10 vol-
extracted separately with 200 mL of H2 O, 80% methanol, ethanol umes of 300 mmol/L acetate buffer, pH 3.6, with 10 mmol/L TPTZ in
and ethyl acetate, respectively, for 4 h at room temperature in a 40 mmol/L HCl, and 20 mmol/L FeCl3 ·6H2 O at 10:1:1 (v/v/v)] and
shaker, carried out in an ultrasonic vibration for 30 min, and then the 10 ␮l standard samples (FeSO4 ·7H2 O, 500 ␮M) or test sam-
filtered three times through cheesecloth. The filtrate was added ples of H2 O, ethanol and ethyl acetate in section 2.2 (10 mg/mL
10 mL of cold 1.0% saline solution and stirred at high speed for 80% methanol) were mixed. The mixture reacted at 37 ◦ C and the
20 min. The mixture was centrifuged at 12000 rpm for 15 min, and absorbance was taken at 593 nm immediately and 4 min later. And
then the supernatant was evaporated and condensed in a rotary 500 ␮M 90% methanol ASA was tested as a positive control. The
evaporator at 35 ◦ C. The obtained extracts were stored at −20 ◦ C. assay was carried out in triplicate. The FRAP value of the test
 M.L. Fei et al. / Industrial Crops and Products 69 (2015) 137–142 139

Table 1
Percentage of different constituents in garlic cloves at 2 weeks. The data are the means of triplicate measurements.

Percentage (%) 37.11 ± 2.38 21.16 ± 2.70 12.35 ± 1.90 4.29 ± 0.57 5.64 ± 1.13 19.45 ± 2.51
Chemical constituents Organosulfur compounds Polyphenol Terpenoids Saponins Cardiac glycoside Others (such as organic acids, amino acids)

samples was calculated on the basis of 500 ␮M Fe2+ (FeSO4 ·7H2 O)

as follows:
 
ÄA593nm testsample
FRAPvalue(M) = × 500(M)
ÄA593nm standardsample

where ÄA593nm is the absorbance of the sample minus the

absorbance of the blank at the 4th min.

2.4. Determination of soluble sugar and total polyphenols

2.4.1. Determination of soluble sugar

The soluble sugar in garlic cloves were estimated by the descrip-
tion (Dubois et al., 1956) with slightly modification. The extracts of
H2 O in Section 2.2 were diluted with 80% methanol with concentra-
tion of 10 mg/mL, 1.0 mL diluted extracts and 1.0 mL of 5% phenol
were mixed in a thick test tube, then 5.0 H2 SO4 was added and
mixed thoroughly. After the test tube was cooled, absorbance was
recorded at 485 nm. All determinations were carried out in tripli-
cate. The concentration of soluble sugar was determined against a
standard curve prepared by using a glucose solution (concentra-
tion range from 50 to 1000 ␮g/mL). Results were expressed as ␮g
of glucose equivalents for g of garlic cloves.

2.4.2. Determination of total polyphenols

Total polyphenols in garlic cloves were measured with the
Folin–Ciocateu reagent according to the literature (Beato et al.,
2011; Nencini et al., 2011). The extracts of 80% methanol in Sec-
tion 2.2 were diluted with 80% methanol with concentration of
10 mg/mL, and 1.0 mL of freshly prepared 0.2 M Folin–Ciocateu
reagent was then added. After 3 min, 800 ␮l of a 7.5% sodium
carbonate solution was added and incubated for 30 min at room
temperature, the absorbance was measured at 760 nm. All determi-
nations were carried out in triplicate. Quantification was obtained
by reporting the absorbance in the standard curve of garlic acid used
as standard phenol (concentration range from 50 to 1000 ␮g/mL).
Results were expressed as ␮g of garlic acid equivalents for g of garlic
cloves.

2.5. Analysis of organosulfur compounds by GC–MS

Fig. 2. Changes in water (A), soluble sugar (B) and total polyphenols (C) in garlic
during storage. The data are the means of triplicate measurements. Different letters
The extract of ethyl acetate mentioned in Section 2.2 was used to on top of the column were considered significant at P < 0.05 level.
identify the constituents of typical organosulfur compounds. Trace
DSQ GC–MS from American Finnigan Company was used. The GC
and MS conditions were described by the literature (Li et al., 2012)
with slightly modification, and the specific steps as follows. 1N 3. Results
NOWAX quartz capillary column: 30 m × 0.32 cm × 0.25 mm; col-
umn temperature: 50–190 ◦ C; procedure temperature: 5 ◦ C/min; 3.1. Changes in antioxidant capacity during storage
carrier gas: He; vaporizer temperature: 280 ◦ C; the MS conditions
were: Ion source: EI; temperature: 200 ◦ C; ionizing voltage: 70 eV; The results of DPPH (A) and FRAP (B) assays are shown in Fig. 1.
electric current of collection: 300 ␮A; electric current of emis- It was clear that the antioxidant capacities of ethyl acetate extract
sion: 1 mA; resolution: 500; mass: 10–500. The changes level of were significantly higher than that of H2 O and ethanol extracts
organosulfur compound were expressed as percentage (%) and cal- under both DPPH and FRAP assays during storage. The DPPH radical
culated from the sum of all peak areas. scavenging effects of ethanol were significantly higher than that of
H2 O extracts up to 4 weeks, then exhibited no significant differ-
2.6. Statistical analysis ence. The antioxidant activities of ethanol under FRAP assay were
significantly lower than that of H2 O extracts before 6 weeks, but
Statistical analysis was carried out using one-way analysis of opposite after 8 weeks. During storage, the extracts of H2 O, ethanol
variance (ANOVA) followed by Duncan test. Statistical P < 0.05 was and ethyl acetate under both DPPH and FRAP assays displayed
considered significant. the strongest antioxidant capacities at 8 weeks, except for the
140 M.L. Fei et al. / Industrial Crops and Products 69 (2015) 137–142

Fig. 3. Chemical structures of typical organosulfur compounds in garlic cloves.

Fig. 4. Changes level of typical organosulfur compounds in garlic at different storage times. The data are the means of triplicate measurements. Different letters on top of
the column were considered significant at P < 0.05 level.

Fig. 5. Changes level of total typical organosulfur compounds in garlic cloves during storage. The data are the means of triplicate measurements. Different letters on top of
the column were considered significant at P < 0.05 level.
 M.L. Fei et al. / Industrial Crops and Products 69 (2015) 137–142 141

antioxidant capacities of the H2 O extract decreased under FRAP reported that a dual function protein (25–26 kDa) was isolated from
assay with storage. A. sativum bulbs which exhibited proteolytic and hemagglutinating
activities. Hadji et al. (2007) demonstrated that crude garlic extract
3.2. Changes in water, soluble sugar and total polyphenols during contained one Mn-superoxide dismutase designated as SOD1 and
storage two Cu, Zn superoxide dismutases as SOD2 and SOD3. Ichikawa
et al. (2006) reported that the properties of garlic were attributed
The levels of water (A), soluble sugar (B) and total polyphenols to organosulfur compounds, a newly developed analytical method
(C) in garlic during storage are shown in Fig. 2. Analysis results with a rapid and simple sample preparation to determine four sul-
showed that storage duration had a significant effect on levels foxides and three ␥-glutamyl peptides in garlic. In addition, the
of water, soluble sugar and total polyphenols. At early weeks, no studies on selenium speciation in garlic and its anti-cancer were
differences of water content in garlic were presented, and then also investigated (Dumont et al., 2006; Shukla and Kalra, 2007).
significantly decreased. The level of soluble sugar decreased sig- Almost no information is available about if and how storage
nificantly after 4 weeks. The level of total polyphenols reached duration affects the changes of chemical constituents and antioxi-
maximum value (839.96 ± 31.38 ␮g/g DW) at 6 weeks, and then dant capacities in garlic. In the present study, we found that storage
decreased significantly. had a significant influence on changes levels of soluble sugar, total
polyphenols, organosulfur compounds, including the antioxidant
3.3. Chemical constituents in garlic bulbs capacities of extracts. The levels of soluble sugar decreased during
storage, and that of total polyphenols and organosulfur compounds
The analyzed results of chemical constituents in the ethyl reached maximum value at 6 and 8 weeks, respectively. The GC–MS
acetate extract of garlic cloves by GC–MS were divided into results of ethyl acetate extract showed that among of the eighteen
five categories, involved in organosulfur, polyphenol, terpenoids, typical organosulfur compounds, ten compounds involved in DAS,
saponins, cardiac glycoside, and other compounds (such as organic DADS, DATS, etc reached maximum levels at 6 or 8 weeks. Both
acids and amino acids). The average percentage of the five cat- DPPH and FRAP assays almost displayed the strongest antioxidant
egories was 37.11%, 21.16%, 12.35%, 4.29%, 5.64% and 19.45%, capacities at 8 weeks.
respectively, which showed that organosulfur compounds occu- Imai et al. (1994) and Hsu et al. (2004) demonstrated that SAC,
pied the largest part of the constituents in the ethyl acetate extract SAMC possess anti-oxidative. Dillon et al. (2003) reported that
of garlic cloves (Table 1). DAS, DADS, DATS extracted from aged garlic exhibited antioxidant
capacities and could effectively suppress low density lipoproteins
3.4. Changes level of typical organosulfur compounds in garlic oxidation in vitro. Nencini et al. (2011) demonstrated that the con-
during storage tent of polyphenol in garlic was directly correlated with antioxidant
activity in vitro. In this study, we found that the levels of organosul-
The Identified results of organosulfur compounds and the struc- fur compounds, especially correlation with the DAS, DADS, DATS,
tures in garlic cloves at 2 weeks storage by GC–MS are shown DATTS, AMS, AMDS, 6-(methylthio) hexa-1,5-dien-3-ol were con-
in Fig. 3, mainly involved in eighteen typical organosulfur com- sistent with the changes of antioxidant capacities.
pounds. The changes level of every compound are shown in Fig. 4.
Among of the eighteen typical organosulfur compounds, ten com-
5. Conclusions
pounds involved in diallyl sulfide (DAS), diallyl disulfide (DADS),
diallyl trisulfide (DATS), diallyl tetrasulfide (DATTS), allyl methyl
Our results indicated that storage duration significantly affected
sulfide (AMS), allyl methyl disulfide (AMDS), allyl methyl trisulfide
the content of water, changes levels of soluble sugar, total polyphe-
(AMTS), 1-propenyl sulfide, 6-(methylthio) hexa-1,5-dien-3-ol and
nols, organosulfur compounds and chemical constituents, which
5,5-dimethyl-1,3-dithian-2-one, reached maximum levels at 6 or 8
consequently had an effect on the antioxidant capacities in garlic
weeks; two compounds S-allylcysteine (SAC) and S-allyl-mercapto
colves. The total changes of organosulfur compounds, especially
cysteine (SAMC) increased during storage; four compounds 2,5-
the DAS, DADS, DATS, DATTS, AMS, AMDS, 6-(methylthio) hexa-
dimethylthiophene, 1,3-dithiane, 3-vinyl-3,6-dihydro-1, 2-dithiine
1,5-dien-3-ol, reached maximum level at 8 weeks, which showed
and 3-vinyl-3,4-dihydro-1,2-dithiine decreased during storage;
positive relationship with the antioxidant capacities that also
The remaining two compounds allylsulfanyl acetonitrile and 2-
exhibited maximum level at 8 weeks. The metabolism of substances
vinyl-1, 3-dithiane did not show a regular variation. Among of
in garlic is complex, the specific antioxidant capacities among of the
which the maximum level of DATS reached 10.15 ± 0.02% at 8
organosulfur compounds are still not clear, which need to further
weeks, and 1-propenyl sulfide was only 0.18 ± 0.01% at 8 weeks.
investigations.
The changes level of the total eighteen organosulfur compounds
during storage are shown in Fig. 5. The levels increased but not
present significant at P < 0.05 level from 2 to 6 weeks, reached max- Acknowledgements
imum level 41.36 ± 2.34% at 8 weeks, then decreased significantly.
We would like to thank the Project of Biotechnology Applica-
4. Discussions tions and Research (GNSW-2013-20) of Department of Agriculture
and Animal Husbandry of Gansu Provincial, P.R. China, for finan-
The quality parameters of garlic to consumption are mainly the cial support during the course of this study. We thank Yongzhong
content of water, nutrients or bioactivities such as pungency sub- Huang, College of Chemistry and Chemical Engineering, Lanzhou
stances. In this study, the water content decreased significantly at University, P.R. China, for the GC–MS analysis.
6 weeks, the results may be that the drying process starts from the
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