Food Chemistry 160 (2014) 346356

Contents lists available at ScienceDirect

Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

Review

Effect of fermentation on the antioxidant activity in plant-based foods

Sun Jin Hur a, Seung Yuan Lee a, Young-Chan Kim b, Inwook Choi b, Geun-Bae Kim a,
a
Department of Animal Science and Technology, Chung-Ang University, 4726 Seodong-daero, Daedeok-myeon, Anseong-si, Gyeonggi-do 456-756, Republic of Korea
b
Korea Food Research Institute, 1201-62 Anyangpangyo-ro, Bundang-gu, Gyeonggi-do 463-746, Republic of Korea

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

Article history: This study provides an overview of the factors that inuence the effect of fermentation on the antioxidant
Received 1 October 2013 activity and the mechanisms that augment antioxidative activities in fermented plant-based foods. The
Received in revised form 24 February 2014 ability of fermentation to improve antioxidant activity is primarily due to an increase in the amount of
Accepted 24 March 2014
phenolic compounds and avonoids during fermentation, which is the result of a microbial hydrolysis
Available online 1 April 2014
reaction. Moreover, fermentation induces the structural breakdown of plant cell walls, leading to the lib-
eration or synthesis of various antioxidant compounds. These antioxidant compounds can act as free rad-
Keywords:
ical terminators, metal chelators, singlet oxygen quenchers, or hydrogen donors to radicals. The
Fermentation
Antioxidative activity
production of protease, a-amylase and some other enzymes can be inuenced by fermentation that
Plant-based foods may have metal ion chelation activity. Because the mechanisms that affect antioxidant activity during
fermentation are extremely varied, further investigation is needed to establish the precise mechanisms
for these processes.
2014 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 346
2. Antioxidant activity of phytochemicals and fermentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 347
3. Effect of various microorganisms on antioxidative activity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 347
4. Effect of proteins and peptides on antioxidative activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 349
5. Effect of pH on antioxidative activity during fermentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 349
6. Effect of temperature on antioxidative activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 353
7. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 353
Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354
Acknowledgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354

1. Introduction (Frias, Miranda, Doblado, & Vidal-Valverde, 2005). Many biochem-

ical changes occur during fermentation, leading to an altered ratio
Fruits and vegetables contain many antioxidant compounds, of nutritive and anti-nutritive components and, consequently, af-
including phenolic compounds, carotenoids, anthocyanins and toc- fects the products properties, such as bioactivity and digestibility
opherols (Naczk & Shahidi, 2006). Most antioxidants are polyphe- (Zhang et al., 2012). Recently, this bioprocess has been applied to
nolic compounds, which act as reducing agents (free radical the production and extraction of bioactive compounds in the food,
terminators), metal chelators, singlet oxygen quenchers (Mathew chemical and pharmaceutical industries (Martins et al., 2011;
& Abraham, 2006) and hydrogen donors (Miller & Rice-Evans, Torino et al., 2013). For example, fermentation has been applied to
1997). Fermentation is an ancient technology used to enhance increase the content of bioactive phenolic compounds in legumes,
the shelf-life and nutritional and organoleptic qualities of food thus enhancing their antioxidant activity (Lee, Hung, & Chou,
2008; Torino et al., 2013). Torino et al. (2013) reported that the
Corresponding author. Tel.: +82 31 670 3027; fax: +82 31 676 5986. bioconversion of the conjugated forms of phenolic compounds into
E-mail address: kimgeun@cau.ac.kr (G.-B. Kim). their free forms during fermentation improves their health-linked

http://dx.doi.org/10.1016/j.foodchem.2014.03.112
0308-8146/ 2014 Elsevier Ltd. All rights reserved.
 S.J. Hur et al. / Food Chemistry 160 (2014) 346356
functionality. Lactic acid bacteria have been employed in foods to
produce angiotensin converting enzyme (ACE)-inhibitory peptides
and c-aminobutyric acid, both of which are useful in the preven-
tion and treatment of hypertension (Kono & Himeno, 2000; Torino
et al., 2013). In general, antioxidants prevent the auto-oxidation of
food components and neutralise the plethora of free radicals that
are generated within the human body (He et al., 2012). Many lig-
ninolytic and carbohydrate-metabolising enzymes hydrolyse phe-
nolic glycosides and release free aglycones, which have the
potential for high antioxidative activity and are thus very useful
for applications in the food and beverage industries (Vattem &
Shetty, 2003). For the reasons discussed above, the fermentation
of food materials is a useful tool to improve the antioxidative activ-
ity of food products. This study provides an overview of the factors
during fermentation that inuence antioxidative activity and the
mechanisms that augment antioxidative activities in fermented
plant-based foods.
2. Antioxidant activity of phytochemicals and fermentation
Antioxidants are molecules that inhibit the oxidation of other
molecules, and they are widely used in dietary supplements. Anti-
oxidant activity is the total capacity of antioxidants for eliminating
free radicals in the cell and in food. Polyphenols are excellent anti-
oxidants due to a 30 -40 dihydroxy group in their B ring and the gal-
loyl ester in the C ring of avonoids, which are also important
structures in metal ion chelation (Chu & Chen, 2006; Khokhar &
Owusu Apenten, 2003). Tocopherols have their own antioxidative
activity, including hydrogen atom transfer at the 6-hydroxyl group
on the chroman ring and scavenging of singlet oxygen and other
reactive species (Lee, Koo, & Min, 2004). In general, ascorbic acid
is an excellent electron donor because of its low standard 1-elec-
tron reduction potential (282 mV), allowing for the conversion of
the relatively stable semi-dehydroascorbic acid to ascorbic acid
(Lee et al., 2004). The antioxidant mechanisms of ascorbic acid
are based on hydrogen atom donation to lipid radicals, quenching
of singlet oxygen and the removal of molecular oxygen (Lee et al.,
2004). Quercetin is also a strong antioxidant. Its resonance struc-
tures, such as the 40 keto group and 23 double bond, or modica-
tions, such as methylation of the 3-OH and 5-OH groups, determine
its iron chelation efciency (Chu & Chen, 2006; Khokhar & Owusu
Apenten, 2003). Lee et al. (2004) reported that avonoids have the
most potent antioxidative activity because their chemical struc-
tures contain an o-diphenolic group, a 23 double bond conjugated
with the 4-oxo function and hydroxyl groups in positions 3 and 5
(Lee et al., 2004). Flavonoids effectively scavenge hydroxyl and
peroxyl radicals, form complexes with metals, and inhibit metal-
initiating lipid oxidation (Lee et al., 2004). The antioxidant
activity of phenolic acids depends on the number and orientation
of the hydroxyl groups relative to the electron-withdrawing
CO2H, CH2CO2H, or (CH)2CO2CH functional groups (Rice-Evans,
Miller, & Paganga, 1996). The aromatic OH is a critical determinant
of hydrogen donation and free radical scavenging by phenolic
compounds (Ng, Liu, & Wang, 2000) and Fenton-induced oxidation
is strongly inhibited by avonoids with the 30 ,40 -catechol, 4-oxo,
and 5-OH arrangement (Cheng & Breen, 2000). Free radical
scavenging capacity is primarily attributed to the high reactivities
of hydroxyl substituents that participate in the following reaction:
F  OH R ! F  O RH
The avonoid heterocycle contributes to the antioxidant activ-
ity by (i) the presence of a free 3-OH, and (ii) permitting conjuga-
tion between the aromatic rings (Heim, Tagliaferro, & Bobilya,
2002).
347
Because fermentation improves antioxidative activity by
increasing the release of avonoids from plant-based foods, it is
a useful method for increasing the supply of natural antioxidants.
The fermentation-induced structural breakdown of the cereal cell
walls may also liberate and/or induce the synthesis of various bio-
-
active compounds (Katina et al., 2007; ordevic, iler-Marinkovic,
& Dimitrijevic-Brankovic, 2010). Ng, Wang, Wang, Tzeng, and Shyu
(2011) also reported that plant parts have an increase in total phe-
nols after fermentation, and that the observed antioxidative activ-
ity may be due to the increase in the total phenolic compounds.
Phenolic compounds can act as reducing agents, hydrogen donors
and singlet oxygen quenchers (Miller & Rice-Evans, 1997). Vinegar
is a fermented food produced from a variety of cereals and fruits,
and therefore its antioxidative activity due to a high concentration
of polyphenolic compounds. Verzelloni, Tagliazucchi, and Conte
(2007) reported that the antioxidant capacity of wines and vine-
gars is highly correlated with their phenolic content. Seki et al.
(2008) also found that rice vinegar contains tyrosol and ferulic
acid, both have LOO-scavenging activity. Microbial enzymes, such
as glucosidase, amylase, cellulase, chitinase, inulinase, phytase,
xylanase, tannase, esterase, invertase or lipase produced by fer-
mentation can hydrolyse glucosides, and break down plant cell
walls or starch. These enzymes play a role in disintegrating the
plant cell wall matrix and consequently facilitating the avonoids
extraction.Another possible mechanism for increasing the antioxi-
dative activity of plant-based foods using fermentation may be
structural changes in phytochemicals. The presence of lactic acid
bacteria in controlled fermentation contributes to the simple
phenolic conversion and the depolymerization of high molecular
weight phenolic compounds (Othman, Roblain, Chammen,
Thonart, & Hamdi, 2009). Hubert, Berger, Nepveu, Paul, and Dayd
(2008) reported that the health benets of fermented soy foods
have been attributed to the antioxidative activity of particular
compounds that are structurally modied or released after bacte-
rial hydrolysis; furthermore, these authors found that the conver-
sion of glycosylated isoavones into their aglycones occurs by
fermentation. Compared with unfermented soybean, fermented
soybean foods contain more aglycones as the predominant isoav-
one structures (Tsangalis, Ashton, McGill, & Shah, 2002). Thus, the
conversion of glucosides into their aglycone form by fermentation
is a principal means of increasing antioxidative activity in plant-
based foods. In contrast, Kim, Goodner, Park, Choi, and Talcott
(2011) reported that the amount of avonol glycosides, which ac-
count for up to 18% of the total phenolic compounds present in
green tea, were reduced during tea fermentation and that this
reduction in the avonol glycosides might be due to oxidative deg-
radation. As a result of fermentation, tea catechins were signi-
cantly reduced by the transformation to theaavins and
thearubigins, resulting in the loss of the total soluble phenolic con-
tent and antioxidative activity (Kim et al., 2011). The total antiox-
idative activity of the extract from plant-based foods (cereals,
fruits and vegetables) cannot be predicted on the basis of its total
phenolic content alone; synergism between polyphenolic com-
pounds and/or other components present in an extract may con-
tribute to the overall observed antioxidative activity (Naczk &
Shahidi, 2006). We propose that increasing the antioxidative activ-
ity of plant-based foods by fermentation may be inuenced by var-
ious factors, including the microorganism species, pH,
temperature, solvent, water content, fermentation time, kind of
food and aerobic conditions.
3. Effect of various microorganisms on antioxidative activity
The antioxidative activity can be inuenced by the microbial
species present during the fermentation of plant-based foods.
348 S.J. Hur et al. / Food Chemistry 160 (2014) 346356
As determined by an assay using rat liver microsomes and thiobar-
bituric acid, 19 strains of lactic acid bacteria have antioxidant
activity (Kaizu, Sasaki, Nakajima, & Suzuki, 1993). Fermentation has
a positive inuence on the total phenolic content and antioxidant
activity of cereals; however, the degree of inuence depends on
the species of microorganism. Lactic acid bacteria are widely used
in food fermentation (Ng et al., 2011), and Lactobacillus plantarum
is the species most frequently used to ferment food products of
plant origin (Rodrguez et al., 2009). Lactic acid bacteria with b-glu-
cosidase activity (including Lactobacillus acidophilus, Lactobacillus
casei, L. plantarum, Lactobacillus fermentum, Bidobacterium animal-
is subsp. lactis, and Bidobacterium longum) increase the isoavone
aglycone content of soymilk during fermentation (Marazza, Garro,
& Savoy de Giori, 2009). This ability may be due to their high
a-galactosidase activity (Marazza et al., 2009), and the released
isoavone aglycone can act as an antioxidant.
L. plantarum is a lactic acid species that degrades tannins. L.
plantarum produces tannase after 24 h of growth on minimal med-
ia containing tannic acid (Rodrguez et al., 2009). Tannase catalyses
the hydrolysis of ester bonds in hydrolysable tannins and gallic
acid esters; it is used in the food industry as a substrate for the syn-
thesis of propylgallate, a potent antioxidant (Rodrguez et al.,
2009). Ciafardini, Marsilio, Lanza, and Pozzi (1994) studied oleu-
ropein hydrolysis by b-glucosidase, which is produced by strains
of L. plantarum. The formation of the oleuropein aglycone by L.
plantarum may improve the antioxidative activity.
Natural and induced fermentation by L. plantarum are sufcient
to improve the concentration of phenolic compounds in fermented
cowpea our; complex polyphenols are hydrolysed to simpler and
more biologically active compounds during fermentation (Dueas,
Fernndez, Hernndez, Estrella, & Muoz, 2005). p-Coumaric, caf-
feic, ferulic and m-coumaric acids are also metabolised by L. plan-
tarum (Rodrguez et al., 2009). L. plantarum growth in fresh olive
mill wastewaters leads to phenolic hydrolysis and depolymeriza-
tion (Lamia & Moktar, 2003). There is higher antioxidative activity
in samples fermented with L. rhamnosus compared with samples
fermented with Saccharomyces cerevisiae. For example, the per-
centage of lipid peroxidation inhibition in liposomes is 50.8% in
unfermented barley, 52.4% in barley fermented with S. cerevisiae,
and 60.9% in barley fermented with Lactobacillus rhamnosus
-
(ordevic et al., 2010). The effects of lactic acid bacteria on antiox-
idative activity could be explained by the liberation of simple
phenolic compounds after acid and enzymatic hydrolysis of
polymerised phenolic compounds during fermentation.
Another possible explanation is that lactic acid bacteria them-
selves have antioxidant activity. Many lactic acid bacteria possess
enzymatic and non-enzymatic antioxidative mechanisms and min-
imize the generation of reactive oxygen species to levels that are
not harmful to cells (Lee et al., 2006). L. casei strains have different
Fe2+ and Cu2+ chelating abilities that ranges from 1.1 to 10.6 ppm
and from 1.35 to 21.8 ppm, respectively (Lee et al., 2006). This re-
sult indicates not only the increasing polyphenol content due to
fermentation but also these lactic acid bacteria have their own
antioxidative activities. When microorganisms are exposed to
reactive oxygen species, they evolve mechanisms to protect them-
selves against oxidative damage, including the formation of enzy-
matic antioxidants that may directly scavenge reactive oxygen
species and non-enzymatic antioxidants (Farr & Kogoma, 1991;
Kim et al., 2005). Lactobacillus bulgaricus LB207 inhibits lipid perox-
idation by its high hydroxyl radical scavenging activity and reduc-
ing power (Kim et al., 2005). Kullisaar et al. (2002) and Chang and
Hassan (1997) reported that two strains of L. fermentum and Strep-
tococcus thermophilus had signicant antioxidative activity via
superoxide dismutase (SOD), and that SOD decreases oxidative
stress. Probiotic bacteria release and promote the production of
the major non-enzymatic antioxidants and the free-radical
scavengers, glutathione or catalase (Spyropoulos, Misiakos,
Fotiadis, & Stoidis, 2011). Moreover, probiotic bacteria promote
the production of certain antioxidant biomolecules, such as the
exopolysaccharides; additionally, probiotic bacteria exhibit metal
chelating activities (Spyropoulos et al., 2011).
The enzymatic hydrolysis could depolymerize polysaccharides
during fermentation. Bacteria belonging to Clostridium, Cellulomon-
as, Bacillus, Thermomonospora, Ruminococcus, Bacteriodes, Erwinia,
Acetovibrio, Microbispora and Streptomyces can produce cellulases
(Sun & Cheng, 2002). Fungi that have been reported to produce cel-
lulases include Sclerotium rolfsii, Phanerochaete chrysosporium and
species of Trichoderma, Aspergillus, Schizophyllum and Penicillium
(Sun & Cheng, 2002). Enzymatic hydrolysis of cellulose consists
of three steps: adsorption of the cellulase enzymes onto the surface
of cellulose, the biodegradation of cellulose to fermentable sugars,
and desorption of cellulose (Sun & Cheng, 2002). At least three ma-
jor groups of cellulases are involved in the hydrolysis process: (1)
endoglucanase which attacks regions of low crystallinity in the cel-
lulose bre, creating free chain-ends; (2) exoglucanase or cellobio-
hydrolase which degrades the molecule further by removing
cellobiose units from the free chain-ends; (3) b-glucosidase which
hydrolyses cellobiose to produce glucose (Sun & Cheng, 2002).
Enzymatic hydrolysis is the most promising means to yield antiox-
idant activity compounds from plant based foods during fermenta-
tion. a-amylases are extracellular enzymes that catalyse the
hydrolysis of a-1,4-glycosidic linkages in starch liberating linear
and branched oligosaccharides of varying chain lengths as well as
glucose; the endo products have an a-conformation at C1 (Sharma
and Satyanarayana, 2013). Aglycones are more potent antioxidant
than their corresponding glycosides. For example, luteolin and
quercetin aglycones signicantly exceeded their 3-,40 - and 7-O-
glucosides in retarding the accumulation of hydroperoxides in
membrane bilayers, but a 40 -sugar was more suppressive than
3- or 7-substitution (Heim et al., 2002). During fermentation, the
enzyme b-glucosidase (b-D-glucoside glucohydrolase) catalyses
the hydrolysis of glycosidic linkages in alkyl and aryl b-D-glucosides,
as well as glycosides containing only carbohydrate residues
(Vattem & Shetty, 2003). This enzyme might help the cleavage of
inter-sugar linkages, releasing the corresponding glycosides that
were hydrolysed liberating the phenolic aglycon moieties (Martins
et al., 2011).
Fungi have a great potential for the production of bioactive
compounds, such as antioxidants (Martins et al., 2011). The total
phenolics and anthocyanin contents and antioxidative activity of
black beans are enhanced after fermentation by lamentous fungi
(Lee et al., 2008). Fungi produce many different types of enzymes
during fermentation, e.g., glycoside hydrolase, cellulose- or xy-
lan-degrading enzymes, and esterase, which soften the kernel
structure, break down cereal cell walls, and release esteried and
insoluble-bound nutrients (Cai et al., 2012). These enzymes hydro-
lyse the b-glucosidic bonds of several phenolic compounds that oc-
cur mainly as conjugates with one or more sugar residues linked to
hydroxyl groups (Georgetti et al., 2009). Enzymatic hydrolysis of
phenolic glucosides is a promising way to increase the concentra-
tion of free polyphenols and to enhance the nutraceutical activity
of various foods (Georgetti et al., 2009). Furthermore, the liberation
of lipophilic aglycones from isoavone glucosides, such as genistin,
by the catalytic action of b-glucosidase during fermentation by
fungi increases antioxidant activity in extracts (Lin, Wei, & Chou,
2006).
Upon fermentation, the degradation of phenolic compounds
takes place, and the rate of this phenolic loss is responsible for
the decreased antioxidant activity (Othman et al., 2009). Fermenta-
tion processing, such as olive processing, induces an important
phenolic loss leading to the reduction of antioxidant value (Othman
et al., 2009). This result indicates that certain fermentation
 S.J. Hur et al. / Food Chemistry 160 (2014) 346356
processing have a negative effect on the antioxidant activity. More
studies of microbes and the activities of their relevant enzymes are
needed to establish the precise mechanisms that occur during
the fermentation of foods.
4. Effect of proteins and peptides on antioxidative activity
Many amino acids, such as histidine, tyrosine, methionine and
cysteine, have antioxidant activity; histidine exhibits an especially
strong radical scavenging activity due to the decomposition of its
imidazole ring (He et al., 2012). The antioxidative activity of rape-
seed peptides may be due to amino acids (histidine, tyrosine,
methionine and cysteine), although the amino acid sequence of
the peptides is also an important contributing factor (He et al.,
2012). A Lactobacillus jensenii strain shows high antioxidant poten-
tial, as it has a high concentration of the hydrophobic amino acids,
including valine, leucine, phenylalanine and tryptophan (Virtanen,
Pihlanto, Akkanen, & Korhonen, 2007). These amino acids also pos-
sess excess electrons that can be donated and used to quench free
radicals or reduce metal cations (He et al., 2012). In general, amino
acids with aromatic residues can donate protons to electron-de-
cient radicals; this property improves the radical-scavenging abil-
ity of the amino acid residues (Coda, Rizzello, Pinto, & Gobbetti,
2012; Sarmadi & Ismail, 2010). The antioxidative activity of histi-
dine-containing peptides is related to the hydrogen-donating, lipid
peroxyl radical-trapping, and/or the metal ion-chelating ability of
the imidazole group (Rajapakse, Mendis, Jung, Je, & Kim, 2005).
Histidine at the N-terminus acts mainly as a metal ion chelator,
while at the C-terminus, it is an effective scavenger against various
radicals (Chen, Muramoto, Yamauchi, Fujimoto, & Nokihara, 1998;
Coda et al., 2012). Park, Lee, Baek, and Lee (2010) reported that
phenylalanine is the main active component which shows antiox-
idant activity. Its antioxidant activity could be attributed to the fact
that when phenylalanine is exposed to hydroxyl radicals, it is con-
verted to tyrosine, and tyrosine scavenges hydroxyl radicals (Park
et al., 2010; Togashi et al., 2000). The SH group of cysteine has a
crucial antioxidative activity due to its direct interaction with rad-
icals (Pasini, Simonato, Giannattasio, Peruffo, & Curioni, 2001).
Moreover, the sulfur groups of cysteine and methionine neutralise
reactive free radical species to form stable oxidation products and
methionine sulfoxide, respectively (He et al., 2012). Thus, the anti-
oxidative properties of amino acids and peptides may be related to
their composition, structure and hydrophobicity (Chen et al.,
1998).
Recent studies have shown that the antioxidative activity of
protein hydrolysate and peptides can be produced during fermen-
tation by microbial proteases (Ricci, Artacho, & Olalla, 2010). Thus,
we assume that peptides hydrolysed by fermentation can act as
antioxidants. Rapeseed proteins are hydrolysed to amino acids
and peptides by proteases produced by Bacillus subtilis during fer-
mentation (He et al., 2012); in this case, fermentation leads to the
production of peptides and amino acids with free radical scaveng-
ing activity. A previous study (Hernandez-Ledesma, Davalos,
Bartolome, & Amigo, 2005) observed a peptide (tryptophan, tyrosine,
serine, leucine, alanine, methionine, alanine, serine, asparagine and
isoleucine) with radical scavenging activity is higher than that of
butylated hydroxyanisole. The cleavage of peptide bonds by
hydrolysis enhances the levels of free amino and carboxyl groups,
resulting in increased solubility (Sarmadi & Ismail, 2010). This
enhanced solubility may improve the antioxidant activity of the
peptide. Protein hydrolysis involves major structural changes, such
as the gradual cleavage of protein molecules into smaller peptide
units, as the degree of hydrolysis increases, the solubility of the
hydrolysed protein also increases (Balakrishnan et al., 2011). Many
Bacillus species produce large amounts of proteases during
349
fermentation, and the peptides liberated by these enzymes are
partially responsible for their antioxidant properties.
In this regard, the effect of peptides on antioxidative activity
could be summarised by the following features: metal chelating
amino acid residues, such as methionine, glutamic acid, glutamine,
lysine or arginine, within the sequences of these peptides contrib-
uted to the superior Fe2+-chelating ability of the antioxidant pep-
tides as well as their high radical scavenging potential (Zhu,
Zhang, Kang, Zhou, & Xu, 2014). These amino acid, containing
non polar groups, have a high binding capacity for polyunsaturated
fatty acids, which contribute to the antioxidant activity of the pep-
tides (Jung, Kim, & Kim, 1995). Lipid oxidation is thought to pro-
ceed via a radical-mediated abstraction of hydrogen atoms from
methylene carbons in polyunsaturated fatty acid (Rajapakse
et al., 2005), and the aromatic side chains of peptide can easily do-
nate hydrogen atoms (Zhu et al., 2014). Hydrophobic amino acids
might play an important role in the lipid oxidation inhibition by
increasing the solubility of peptides in lipids (Chen, Muramoto,
Yamauchi, & Nokihara, 1996). The hydrophobic side chain of pep-
tide might also increase the accessibility of the peptide to the non-
polar phase, allowing for full antioxidant capacity (Chen,
Muramoto, & Yamauchi, 1995). Moreover, the presence of phenyl-
alanine and histidine at the N-terminus might contribute to the
high radical-scavenging activity of the peptide via its ability to do-
nate a proton from the benzene ring and imidazole group, respec-
tively (Lapsongphon & Yongsawatdigul, 2013). Low-molecular
weight peptides have been reported to exhibit better radical-scav-
enging activities than their high-molecular weight counterparts
(Ajibola, Fashakin, Fagbemi, & Aluko, 2011). Thus, increasing the
low-molecular weight peptides by enzymatic hydrolysis may inu-
ence the antioxidative activity during fermentation. In this review,
the authors propose that one of the main mechanisms for the effect
of fermentation on antioxidative activity in food may be the pro-
duction of antioxidative peptides or amino acids during fermenta-
tion by bacilli.
5. Effect of pH on antioxidative activity during fermentation
pH is one of the most important environmental parameters
affecting food fermentation. pH is closely related to microbial
growth and the structural changes in phytochemicals during fer-
mentation. For example, anthocyanin breakdown is dependent on
the pH in the presence of oxygen, is also directly related to the le-
vel of pseudobase, and is inversely related to the cation concentra-
tion (Su & Chien, 2007). Several studies (Cabrita, Fossen, &
Andersen, 2000; Nielsen, Haren, Magnussen, Dragsted, & Rasmussen,
2003) have shown that anthocyanins are stable at low pH.
Anthocyanins exhibit the highest stability, with the red avylium
cation stable around pH 12 (Nielsen et al., 2003). The stability
of anthocyanins is dependent on their structure; for instance, acyl-
ated anthocyanins are more stable than the non-acylated forms
(Devi & Mohandas, 2012). pH is a dominant factor in the radical
scavenging capacity of wine anthocyanins, as an increase in pH
often increases the capacity for radical scavenging (Borkowski,
Szymusiak, Gliszczynska-Swiglo, Rietjens, & Tyrakowska, 2005).
The retention of anthocyanin is also largely affected by changes
in pH (from 2 to 7.5) (Tagliazucchi, Verzelloni, Bertolini, & Conte,
2010).
Catechins are among the major natural phenols and antioxi-
dants. The stability of catechins in green tea is pH-dependent; they
are very unstable in alkaline solutions but stable in acidic solutions
(Chu & Chen, 2006; Zhu, Zhang, Tsang, Huang, & Chen, 1997). For
example, the contents of catechin derivatives in green or black
tea extracts rapidly diminish by 7080% at pH 7.4 for 60 min, but
the antioxidant activity and concentration of polyphenols
350 S.J. Hur et al. / Food Chemistry 160 (2014) 346356
Fig. 1. Examples of natural antioxidants structures.
Fig. 2. Mechanism for the antioxidant activity of phenolic.
Fig. 3. A schematic diagram of the conversion of glucosides into the aglycone form.
decreases by approximately 25% (Record & Lane, 2001). Thus, pH
changes during fermentation could inuence the antioxidant activ-
ity by changing the contents and structure of the phenolic
compounds. The radical scavenging capacities of polyhydroxylav-
ones and catechins increase with the pH of the medium due to an
increase in the electron-donating ability upon deprotonation
(Muzolf, Szymusiak, Gliszczynska-Swigo, Rietjens, & Tyrakowska,
2008). The increase in the electron-donating ability upon deproto-
nation could explain the increase in the trolox equivalent antioxi-
dant capacity (TEAC) values of catechins with increasing pH value,
and we can propose that electron donation via deprotonation of
catechins is the dominant mechanism of antioxidant action.
Quercetin is the aglycone form of a number of other avonoid
glycosides in buckwheat and onions, and it has antioxidant activ-
ity. A low initial pH (pH 5.5) causes deep insertion of quercetin
in the hydrophobic core of the lipid bilayer, because in its undisso-
ciated form it is completely liposoluble and would therefore pre-
vail at this low pH (Movileanu, Neagoe, & Flonta, 2000).
Therefore, quercetin can act as an antioxidant in the lipid bilayer.
It has been suggested that the antioxidative activity of quercetin
is responsible for some of the positive effects observed in other lac-
tic acid bacteria, such as extended growth in Lactobacillus hilgardii
(Figueiredo, Campos, de Freitas, Hogg, & Couto, 2008). Quercetin
improves the fermentation performance of L. plantarum in a pH-
and dose-dependent manner (Curiel, Muoz, & Lpez de Felipe,
2010). Lactic acid production is accelerated by quercetin, which
is important to accelerate wine deacidication and acidication
 S.J. Hur et al. / Food Chemistry 160 (2014) 346356 351

Fig. 4. A schematic diagram of the effect of pH on antioxidant activity.

of various other fermentation processes in which L. plantarum

Fig. 5. A schematic diagram of the effect of temperature on antioxidant activity.
plays a key role as a starter (Curiel et al., 2010). Phenolic com-
pounds act as pro-oxidants under certain conditions, such as when
high concentrations of phenolic compounds or metal ions are pres-
ent and at a high pH (Lee et al., 2004). As mentioned above, the
types of fermentation (by different microorganisms) can modify
some of the bioactive compounds in plant-based food. This effect
might be due to the difference in the pH of different fermentations,
as the optimum pH inuences the degradation of the cell wall-
degrading enzymes (Boskov Hansen et al., 2002). Presumably, the
liberation of the cell wall components by fermentation induces
the release of phenolic compounds from food, and these phenolic
compounds affect the consequent antioxidative activity.
The antioxidative activity of polyphenolic antioxidants is not
only based on the number and position of the hydroxyl moieties
in the molecule but also their protonation state, which is inu-
enced by the pKa of the hydroxyl moieties, the pH of the surround-
ing medium, intramolecular hydrogen bridges and O-methylated
hydroxyl groups (Tyrakowska, Lemanska, Szymusiak, Borkowski,

Fig. 6. The primary mechanisms for the effects of fermentation on the antioxidative activity in plant-based foods.
352 S.J. Hur et al. / Food Chemistry 160 (2014) 346356

Table 1
Main microorganisms and enzymatic activity used in food fermentation.

Microorganisms Species Active enzymes

Lactic acid bacteria Lactobacillus acidophilus Amylase, lactate dehydrogenases, peptidases, proteinase
Lactobacillus casei Amylase, lactate dehydrogenases, peptidases, proteinase
Lactobacillus fermentum Amylase, lactate dehydrogenases, peptidases, proteinase
Lactobacillus lactis Amylase, aminotransferases, decarboxylase, esterase, lactate dehydrogenases, peptidases, proteinase
Lactobacillus plantarum Amylase, b-glucosidase, decarboxylase, lactate dehydrogenases, peptidases, phenolic acid decarboxylases,
phenol reductase, proteinase, tannase
Lactobacillus rhamnosus Amylase, cellulases, esterase, glucoamylase, b-glucosidase, lactate, dehydrogenases, peptidases, proteinase
Fungi Bacillus cereus Amylase, cellulases, tannase
Bacillus subtilis Amylase, cellulases, hydrolases, levansucrase, peptidase, proteases, xylanase
Bacillus thuringiensis Amylase, cellulases, tannase
Aspergilus niger Amylase, cellulases, estrase, fucoidanase, glucoamylase, b-glycosidase, invertase, lipase, mannanase,
pectinases, phytase, protease, tannase, b-xylosidase, xylanase
Aspergilus oryzae Acid protease, a-galactosidase, amylase, invertase, lignin peroxidase, tannase
Yeast Cryptococcus avus Amylase, b-glucanases, b-glucosidase, catalase, esterase, lipase, proteases, xylanases
Cryptococcus sp. S-2 Amylase, b-glucanases, b-glucosidase, catalase, esterase, lipase, proteases, xylanases
Rhodotorula glutinis Alcohol dehydrogenase, amylase, b-glucosidase, epoxide hydrolases, invertase, lipase, pectinase,
tannase, thiamine hydroxylase
Saccharomyces cerevisiae Alcohol dehydrogenase, amylase, b-glucosidase, invertase, maltase, proteases

Table 2
Effect of fermentation on antioxidative activity in various plant-based foods.

Food sources Fermentation process Enzymatic activity Antioxidative activity & factors References
Cereal ours Sourdough fermentation using Hydrolysis of protein Peptides released Coda et al. (2012)
lactobacilli
Soybean germ Fermentation using lactic acid bacteria Hydrolysis of isoavone Isoavones and saponin levels increased Hubert et al. (2008)
and soyasaponins
Wine Model wild fermentation using Catabolism of quercetin Quercetin stability improved Curiel et al. (2010)
Lactobacillus plantarum
Cowpeas Fermentation using Lactobacillus Hydrolysis of glycosides Phenolic compound (gallic acid, vanillic Dueas et al. (2005)
plantarum and Maillards reaction acid, quercetin, ferulic acid, p-
hydroxybenzoic acid) concentration
improved
Lupin seeds Fermentation using Lactobacillus Vitamin C and E content increased Frias et al. (2005)
plantarum
Olive Fermentation using Lactobacillus Hydrolysis of glucosides Phenolic compound loss Othman et al. (2009)
plantarum
Lentil Liquid-state fermentation (LSF) using Hydrolysis of peptide bond Free amino acid and angiotensin Torino et al. (2013)
Lactobacillus plantarum and solid-state or proteolytic activity I-converting enzyme inhibitory increased
fermentation using Bacillus subtilis (SSF) by LSF, and c-aminobutyric acid increased
by SSF
Rapeseed Solid-state fermentation using Bacillus Hydrolysis of protein Soluble peptides increased He et al. (2012)
subtilis
Black soybean Fermentation using Bacillus subtilis Total phenolic, avonoids and vitamin K2 Juan and Chou (2010)
increased and aglycone contents
enhanced
Peanut Fermentation using Bacillus subtilis Hydrolysis of protein Peanut peptides possessed metal Zhang et al. (2014)
chelating capacity and reducing power
Soybean natto Fermentation using Bacillus natto Hydrolysis of protein, Protease, b-glucosidase activities, total Hu et al. (2010)
caseinolytic activity, phenolic and anthocyanin increased
b-glucosidase activity
Soyben Kinema Fermentation using Bacillus subtilis Hydrolysis of soy protein Total phenolic compound content Moktan, Saha, and
increased Sarkar (2008)
Soybean Fermentation using Aspergillus oryzae Hydrolysis of soybean by Metal chelating ability of saponins and Huang et al. (2011)
a-amylase, b-amylase, isoavones improved
protease, b-glucosidase,
lipase
Cranberry pomace Solid-state fermentation using Lentinus Hydrolysis of glycosidic Extractable phenolic contents increased Vattem and Shetty
edodes linkages by b-glucosidase (2003)
Apple pomace Solid-state fermentation using Hydrolysis of phenolic Polyphenol concentration increased Ajila et al. (2011)
Phanerochaete chrysosporium glycosides
Wheat Fermentation using Cordyceps militaris Hydrolysis of polyphenols Polyphenols and rutin increased Zhang et al. (2012)
mycelium
Rye bran Fermentation using Bakers yeast Hydrolysis of rye by Folates increased, and easily extractable Katina et al. (2007)
xylanases, proteases, phenolic compounds, ferulic acid and
a-amylase solubilised pentosans
Brown alga Fermentation using yeast strain YM-1 Hydrolysis of brown alga Total phenolic increased Eom et al. (2011)
Ashwagandharishtha Fermentation using Saccharomyces. Phenolic compounds increased Manwar, Mahadik,
Cerevisiae Jm.20 Sathiyanarayanan,
Paradkar, and Patil
(2013)
 S.J. Hur et al. / Food Chemistry 160 (2014) 346356
Table 2 (continued)
Food sources Fermentation process
Mulberry Solid-state fermentation using by
Saccharomyces. cerevisiae IFI240 A
Blueberry Fermentation using Saccharomyces.
Bayanus
Bush tea Tea fermentation at different
temperatures
Tea Tea fermentation
Blueberry Skin-contact fermentation
& Rietjens, 2003). Perron and Brumaghim (2009) reported pKa val-
ues in the range of 79 for the most acidic phenolic hydrogen, and
that polyphenols are easily deprotonated at or below physiological
pH in the presence of iron and form very stable complexes. Thus,
the metal ion chelation effects of phenolic compounds are largely
inuenced by pH. The chelation effect may be dependent on the
combination of foods and fermentation methods, and fermentation
methods can be modied appropriately according to their various
purposes.
6. Effect of temperature on antioxidative activity
Changes in temperature also affect fermentation. Maintaining
the optimal temperature during fermentation results in improved
microbial growth and enzymatic activity, and consequently, the
benets of fermentation are improved. Moreover, the antioxidant
activity of plant-based foods may be inuenced by changes in tem-
perature during fermentation, as the production of antioxidants,
such as phenolic compounds, can be inuenced by changes in tem-
perature. Temperature increases can increase the polyphenol con-
tent, which could be because the solvent viscosity decreases and
the movement of molecules is accelerated, leading to the dissolu-
tion of polyphenols and an increase in the diffusion coefcient
and stability (Ajila, Brar, Verma, Tyagi, & Valro, 2011). Increased
extraction of polyphenolic groups with increasing temperature
can be attributed to the rapid mass transfer of solutes and in-
creased solubility, especially of polymeric fractions, at higher tem-
peratures (Ajila et al., 2011). Sufu ripened at 45 C has enhanced
antioxidative activity and aglycone content, followed in descend-
ing order by those samples ripened at 37 and 25 C (Huang, Lai,
& Chou, 2011). However, an overly high temperature causes sol-
vent loss, resulting in a lower yield and promoting the oxidation
of polyphenols, which in turn affects the free radical scavenging
activity of the extraction of apple pomace (Ajila et al., 2011). The
rate of anthocyanin monomer loss in lowbush blueberry juice in-
creases with increasing temperature (Simard, Bourzeix, & Heredia,
1982). A fermentation temperature of 30 C signicantly increases
polyphenols (followed by fermentation temperatures of 34 and
38 C); the lowest levels are obtained at 24 and 42 C in bush tea
(Hlahla, Mudau, & Mariga, 2010). Polyphenolic content, colour,
and antioxidative activity in red grape pomace peels are fairly
heat-stable (Su & Silva, 2006). However, a drying temperature of
100 C or above is not recommended because of the loss of antiox-
idative activity (Larrauri, Ruprez, & Saura-Calixto, 1997). These
studies indicate that optimal temperature control plays an impor-
tant role in the improvement of antioxidative activity by
fermentation.
Temperature plays an important role in controlling the growth
of microorganisms during fermentation, and the growth of micro-
organisms can inuence the antioxidative activity. Microbial fer-
mentation induces enzymatic changes in antioxidants, such as
353
Enzymatic activity Antioxidative activity & factors References
Hydrolysis of mulberry Anthocyanin content increased Prez-Gregorio et al.
phenolics by enzymes, acid, (2011)
alkaline
Hydrolysis of blueberry by Total phenolic and anthocyanin Johnson, Lucius,
a-amylase, a-glucosidase content increased Meyer, and Mejia
(2011)
Polyphenols and tannin content increased Hlahla et al. (2010)
Antioxidative activity of saponin Li, Du, and Zou (2009)
increased at pH 8
Anthocyanin content increased Su and Chien (2007)
phenolic compounds. The b-glucosidase activity of L. casei is max-
imal at 35 C (Coulon, Chemardin, Gueguen, Arnaud, & Galzy,
1998), and the b-glucosidase activity in L. plantarum is reduced
by 50% after heating to 50 C for 5 min (Sestelo, Poza, & Villa,
2004). b-glucosidase activity during microbial fermentation causes
the hydrolysis of phenolic glycosides and the release of free agly-
cones, which can have a high antioxidant activity. It is well known
that the antioxidant activity of phenols is affected by their chemi-
cal structure, and this activity can be decreased or increased
depending upon the functional group attached to a basic aglycon
(Prez-Gregorio, Regueiro, Alonso-Gonzlez, Pastrana-Castro, &
Simal-Gndara, 2011). The presence of glycosides attached to
avonoid aglycons, such as a avonol or anthocyanidin, decreases
the antioxidative activity of the avonoid (Prez-Gregorio et al.,
2011). In this case, the glucoside moiety interferes with the
co-planarity of the avonoid molecule, decreasing its ability to
delocalize electrons and thereby decreasing the antioxidative
activity of the avonoid (Jakobek, eruga, eruga, Novak, &
Medvidovic-Kosanovic, 2009). In a review, Thavasi, Bettens, and
Leong (2009) concluded that temperature is the primary factor in
affecting antioxidant activity during fermentation. The radical
scavenging ability of phenols is increased upon an increase in
temperature. As more kinetic energy is imparted by increasing
the temperature, the OH group of the phenols becomes more labile,
and the H atom readily dissociates (Thavasi et al., 2009). The rates
of chemical reactions are accelerated with increasing temperature
by the faster moving of atoms. Consequently, the release of antiox-
idative compounds is accelerated by the increased degradation of
the plant cell walls. However, extremely high or low temperatures
reduce antioxidant activity during fermentation. As shown above,
the effect of temperature on antioxidant activity during fermenta-
tion varies between many different types of foods and strains of
microorganisms. Thus, more research is needed to improve the
benets of fermentation, including the increase in antioxidative
activity and to clarify the mechanisms that drive changes in
antioxidative activity in response to temperature changes.
7. Conclusion
In summary, increased antioxidative activity in fermented
plant-based foods is due to an increase in the release of antioxidant
compounds (Fig. 1). The improvement of antioxidative activity by
fermentation is mainly due to an increase in phenolic compounds
and avonoids via microbial hydrolysis. Microbial enzymes hydro-
lyse phenolic glycosides and release the aglycone, which has anti-
oxidative activity. The effect of bacterial fermentation on
antioxidative activity can be summarised with enzymatic and
non-enzymatic antioxidative activities. Moreover, fermentation in-
duces the structural breakdown of plant cell walls, leading to
the liberation or synthesis of various antioxidant compounds. These
antioxidant compounds can donate hydrogen atoms or scavenge
354 S.J. Hur et al. / Food Chemistry 160 (2014) 346356
free radicals, and prevent lipid oxidation. In addition, fermentation
by bacillus can induce the formation of protease or a-amylase, en-
zymes that may chelate metal ions. When microorganisms are ex-
posed to oxidative stress during fermentation, the cells may evolve
protective mechanisms involving enzymatic antioxidation, which
may contribute to the antioxidative effect of fermentation (Figs. 26).
Fermentation is a good technology with great potential for
application on the production or extraction of antioxidant active
compounds from natural sources. New bioactive compounds could
be found during fermentation. Moreover, modication of fermen-
tation process could be tailored so as to increase the bioaccessibil-
ity of bioactive compounds. Production of bioactive compounds yet
remains a quite unexplored potential, which could be accom-
plished by utilising the new fermentation process. Therefore, in
the future, it can be anticipated that fermentation could be used
to design food with health effects. Some fermentation processes
are available on the applications of production of antioxidant activ-
ity compounds. However, the underlying mechanisms affecting
antioxidative activity during fermentation are varied, and the pro-
duction of antioxidant activity compounds during fermentation
may vary depending on the microorganisms, cultivation medium,
times, temperature, pH, inhibitors, stimulators or atmosphere.
Thus, it is very hard to make the decision, which fermentation is
better for improving the production of antioxidant activity com-
pounds. Moreover, conicting results between the positive and
negative effects of fermentation may also arise from confusion in
the production or degradation of antioxidant activity compounds.
The choice of microorganism used in the fermentation process de-
pends on the desired end product, and mostly the production
yields of antioxidant activity compounds can be improved with a
suitable choice and microorganism or substrate. In conclusion, fu-
ture work is needed to understand the effect of various factors (e.g.,
microorganisms, cultivation medium, times, temperature, pH,
inhibitor or atmosphere) that occur during fermentation and how
these factors relate to changes of production of antioxidant activity
compounds (Tables 1 and 2).
Conict of interest
The authors have no conicts of interest to declare.
Acknowledgment
This study was supported by agenda project (Grant No.
PJ009376012014) of the Rural Development Administration,
Republic of Korea.
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