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Impact of Fermentation on the Phenolic Compounds and Antioxidant Activity

of Whole Cereal Grains: A Mini Review

Article in Molecules · February 2020

DOI: 10.3390/molecules25040927

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 molecules
Review
Impact of Fermentation on the Phenolic Compounds
and Antioxidant Activity of Whole Cereal Grains:
A Mini Review
Oluwafemi Ayodeji Adebo 1, * and Ilce Gabriela Medina-Meza 2
1 Department of Biotechnology and Food Technology, Faculty of Science, University of Johannesburg,
Doornfontein Campus, P.O. Box 17011, Gauteng, South Africa
2 Department of Biosystems and Agricultural Engineering, Michigan State University, 524 South Shaw Lane,
East Lansing, MI 48824-1323, USA; [email protected]
* Correspondence: [email protected]; Tel.: +27-11-559-6261

Academic Editor: María Dolores Torres




Received: 22 December 2019; Accepted: 14 February 2020; Published: 19 February 2020
Abstract: Urbanization, emergence, and prominence of diseases and ailments have led to conscious
and deliberate consumption of health beneficial foods. Whole grain (WG) cereals are one type of
food with an array of nutritionally important and healthy constituents, including carotenoids, inulin,
β-glucan, lignans, vitamin E-related compounds, tocols, phytosterols, and phenolic compounds,
which are beneficial for human consumption. They not only provide nutrition, but also confer health
promoting effects in food, such as anti-carcinogenic, anti-microbial, and antioxidant properties.
Fermentation is a viable processing technique to transform whole grains in edible foods since
it is an affordable, less complicated technique, which not only transforms whole grains but also
increases nutrient bioavailability and positively alters the levels of health-promoting components
(particularly antioxidants) in derived whole grain products. This review addresses the impact of
fermentation on phenolic compounds and antioxidant activities with most available studies indicating
an increase in these health beneficial constituents. Such increases are mostly due to breakdown
of the cereal cell wall and subsequent activities of enzymes that lead to the liberation of bound
phenolic compounds, which increase antioxidant activities. In addition to the improvement of these
valuable constituents, increasing the consumption of fermented whole grain cereals would be vital
for the world’s ever-growing population. Concerted efforts and adequate strategic synergy between
concerned stakeholders (researchers, food industry, and government/policy makers) are still required
in this regard to encourage consumption and dispel negative presumptions about whole grain foods.

Keywords: fermentation; fermented foods; whole grains; health benefits; phenolic compounds;
antioxidant activity

1. Introduction
Foods in the past were known to conventionally provide nutrients necessary for basic physiological
functions. This assumption has changed with available knowledge at the disposal of consumers,
changes in food regulations, and an ever-growing health-conscious population, which are factors
resulting in an increasing desire for foods with additional physiological benefits. The 2500-year-old
concept of “Let food be thy medicine and medicine be thy food” by Hippocrates is now being embraced
better than ever as consumers are gradually becoming aware of the importance of diet in health
promotion and disease prevention. Such a concept of food as medicine could have led to the trend of
what is now known as “functional foods,” which is a concept first created in Japan in the 1980s [1].
Supporting this perspective of food as medicine are several studies on whole grains (WGs) and
WG-diets having positive effects on disease markers such as blood pressure, diabetes, and obesity [2–11].

Molecules 2020, 25, 927; doi:10.3390/molecules25040927 www.mdpi.com/journal/molecules

Molecules 2020, 25, 927 2 of 19

WGs are essentially made up of the germ, bran, and endosperm and contains all the important parts
of the entire grain seed in their original proportions. A more detailed and approved definition by
the American Association of Cereal Chemists (AACC) says “WGs shall consist of the intact, ground,
cracked, or flaked caryopsis, whose principal anatomical components—the starchy endosperm, germ,
and bran—are present in the same relative proportions as they exist in the intact caryopsis” [12]. On the
contrary, refined grains (RGs) are products obtained after the refining process involving the removal of
the most potent protective components of the grains found in the bran and germ. This consequently
leaves only the starchy-rich endosperm. The retained protective components in WGs make them better
constituents of beneficial components as compared to their refined counterparts.
Health beneficial constituents of WGs include phytochemicals, bioactive carbohydrate fractions,
peptides, and other phytonutrients [11,13–16]. WGs contain high amounts of phytochemicals, which are
plant secondary metabolites that have shown biological activity and have been broadly investigated as
health beneficial groups of compounds in food [17–19]. Particularly important are phenolic constituents,
which are major forms of these phytochemicals and vital with reference to their unique contribution to
the health benefits of WGs. The major sources of these phytochemicals are phenolic compounds (PCs)
due to the high concentrations of bioactive constituents in the bran and germ layer [17,20,21] and the
fact that they are largely one of the most important dietary sources of energy intake worldwide.

2. Phenolic Compounds in WG Foods

The overall benefit derived from three major components of WG (germ, bran, and endosperm)
altogether is higher than any of the individual fractions [22,23]. A combination of these components
makes WG contain physiologically important components including vitamins, fatty acids, phytosterols,
PCs, fatty acids, dietary fiber, carotenoids, lignans, and sphingolipids (Figure 1), which can promote
health either singly or in synergy with each other [18,24]. A series of meta analyses and multiple scientific
studies have equally reported an association between increasing intake of WG-foods and reduced risk
of non-communicable diseases such as cardiovascular diseases, coronary heart diseases, stroke [24–26],
metabolic syndrome [27], and cancers [28,29] as well as a positive effect on gut microbiota [30]. Phenolic
compounds are subsequently discussed in this review as it is of vital importance in WG-cereals [16]
and the fact that they are the most studied phytochemicals [31]. Usually, WGs may be consumed as
food after it has been incorporated as an ingredient into other food products or as food itself after
processing. One type of such a food processing technique adopted for the transformation of WGs into
diets is fermentation, which is a process that yields products that are not only shelf stable, but also
better in sensorial qualities and health beneficial constituents [32–36]. The cereal bran is a major source
of these PCs and this paper seeks to review available scientific literature on fermented WG-products to
understand the influence and role of fermentation on PCs and antioxidant activity (AA) thereof.
Phenolic compounds (also called phenolics) are derived from several biosynthetic precursors
including pyruvate, acetate, some amino acids (phenylalanine and tyrosine), malonyl CoA, acetyl
CoA through the action of pentose phosphate, shikimate, and phenylpropanoid metabolism
pathways [37–39]. The term ‘phenolic acids’ refers to phenolic compounds having one carboxylic
acid group and are mainly divided into two subgroups, i.e., hydroxybenzoic acids (such as gallic,
p-hydroxybenzoic, protocatechuic, syringic, and vanillic acids) and hydroxycinnamic acids (caffeic,
ferulic, p-coumaric, and sinapic acids) (Figure 2). Flavonoids are an equally well-known class of
frequently occurring phenolics in WGs. Major phenolics found in WGs are phenolic acids (PAs),
flavonoids, and tannins. These plant-derived constituents are bioactive and involved in potentiating
the redox defense of the body, prevention, and counteracting oxidative stress and reducing free
radical-related cellular damage.
 Molecules 2020, 25, 927 3 of 19
Molecules 2020, 25, x FOR PEER REVIEW 3 of 18

Phenolic
compounds
Molecules 2020, 25, x FOR PEER REVIEW 3 of 18
Phytosterols Carotenoids

Phenolic
compounds

Tocols
Whole grain CarotenoidsInulin
Phytosterols

phytochemicals

Tocols
Whole grain Inulin
Vitamin E- phytochemicals
related β-glucan
compounds

Vitamin E- Lignans
related β-glucan
compounds
Lignans
Figure
Figure 1. Whole
1. Whole grain grain phytochemicals.
phytochemicals.

As stated
As stated by Singhby Singh et al.flavonoids
et al. [40], [40], flavonoids
are theare the largest
largest group of group of phenolics
phenolics and account
and account for the for
Figure 1. Whole grain phytochemicals.
the half of known PCs in plants. These compounds are
half of known PCs in plants. These compounds are equally low molecular weight compoundsequally low molecular weight compounds
consisting
consisting Asofstated
of two two aromatic
aromatic rings
by Singh etrings
(A (Aflavonoids
and
al. [40], and
B) B) joined
joined a by
by the
are a three-carbon
three-carbon
largest group of bridge bridge
(C6–C
phenolics (C3–C
and –C 3 –C6for
structure)
the [40]. [40].
6 structure)
6account
Tannins,
Tannins, on on
halfthe the other
of other
known PCs hand,
hand, inare areThese
plants.
high high molecular
compounds
molecular weight weight
are polymeric
equally
polymeric low phenolicphenolic
molecular compounds
weight
compoundscompounds
known known
to to
contribute to
consisting the
of pericarp
two aromatic(seed coat)
rings (A color
and B) of cereals.
joined by a These
three-carbonpolyphenolic
bridge
contribute to the pericarp (seed coat) color of cereals. These polyphenolic compounds have molecular (C 6–Ccompounds
3–C6 structure)have
[40].molecular
Tannins,
weights on the other
of between hand, are
500–3000 high molecular
g/mol, containing weight polymeric
sufficient phenolic compounds
hydroxyls and other known
groups toincluding
weights of between 500–3000 g/mol, containing sufficient hydroxyls and other groups including
contribute to the pericarp (seed coat) color of cereals. These polyphenolic compounds have molecular
carboxyl
carboxyl [41–43].
[41–43]. TanninsTanninsbe canbroadly
be broadly classified into two, which include hydrolysable tannins
weights of betweencan 500–3000 classified
g/mol, containing into two,
sufficient which
hydroxyls include
and otherhydrolysable
groups including tannins
[esters of ellagic
[esters of carboxyl
ellagic acid acid (ellagitannins)
(ellagitannins) or gallic acid (gallotannins)] and condensed tannins [(called
[41–43]. Tannins can beorbroadly gallic classified
acid (gallotannins)]
into two, which and condensed
include tannins
hydrolysable [(called
tannins
polymeric
polymeric [esters proanthocyanidins)
proanthocyanidins) and known
and known
of ellagic acid (ellagitannins) togallic
or toacid
be (gallotannins)]
be composed composed ofand
of flavonoid flavonoid units)
units) [41,44].
condensed [41,44].
tanninsA [(calledA plethora
plethora of
of excellent
polymeric reviews and scientific
proanthocyanidins) and literature
known to are
be available
composed of in the
flavonoidliterature
units)
excellent reviews and scientific literature are available in the literature on detailed classifications, on detailed
[41,44]. A classifications,
plethora of
forms,excellent reviewsand
occurrences, and formation/generation
scientific literature are available
of these incompounds
the literature[15,16,40,41,45–50].
on detailed classifications,
forms, occurrences, and formation/generation of these compounds [15,16,40,41,45–50].
forms, occurrences, and formation/generation of these compounds [15,16,40,41,45–50].

Figure 2.2.Classification
Figure Classification ofofmajor
major phenolic
phenolic compounds
compounds in grains.
in whole whole grains.

Figure 2. Classification of major phenolic compounds in whole grains.

Molecules 2020, 25, 927 4 of 19

3. Fermentation of WG Foods
Food processing is essential for the transformation of food crops into edible forms. Fermentation
is an old food processing technique that has been adopted for centuries around the world, especially
in developing nations. It involves an intentional conversion/modification of a substrate through
activities of microorganisms to get a desired product. This is usually completed through microbial
actions, which positively alter the appearance, flavor, functionalities, nutritional composition, color,
and texture. The fermentation process itself yields beneficial effects through direct microbial action
and production of metabolites and other complex compounds [51–53]. Conventional techniques of
fermentation include (i) natural (also called spontaneous) occurrences through the actions of endogenous
microorganisms, (ii) back slopping involves utilizing plenty of successful previous fermentation
batches) and (iii) controlled fermentation, which entails the inoculation of starter cultures/specific
strains. Subsequent fermented products are not only shelf stable through the preservative effect of this
process, but fermentation also improves bioavailability and palatability, confers desirable organoleptic
characteristics that impact aroma, texture, and flavor and improves the health beneficial components
in food [32–36]. Irrespective of the food substrate (cereal, legume, vegetable, fruit, RG, or WG),
fermentation results in the modification of inherent constituents, secondary metabolites, detoxification
of toxic components/residues, and improvement in the functionality of the food product [35,36,53–55].
The incorporation of WG into diet which, is influenced by cultural beliefs, disadvantages of longer
cooking time, the presence of phytates, tannins, and a limited variety of products made from them [56].
Additionally, some of their components may adversely affect the functional characteristics, taste, texture,
and sensory appeal of subsequent formulations. Viable options for addressing this and incorporating
WGs into diet would be completed through appropriate transformation into various other beneficial
food forms, which would ensure the possibility of obtaining various value-added products. Although
RGs are mostly used in fermented foods, the use of WGs as staple foods equally has a long history
of human consumption [23]. Findings from epidemiological studies and discoveries, therefore, have
triggered renewed interest among governmental bodies of different nations that WG should form part
of cereal servings [24,57,58]. Table 1 summarizes common fermented WG products obtained through
both solid-state fermentation (SSF) and liquid/submerged fermentation (SmF). While the former occurs
in the absence or near-absence of free water, the latter occurs in the presence of free flowing water (more
fluids compared to SSF). Subsequent fermented products are relatively few in contrast to numerous
other studies reporting the use of RGs for similar food products, which necessitates further intensified
research on the development of WG-fermented food products.

Table 1. Some reported fermented food products from whole grains.

Whole Grain(s) Food Type of Fermentation Reference

Barley and oat Tempe SSF Eklund-Jonsson et al. [59]
Oyarekua [60],
Maize Akamu/Ogi SSF
Obinna-Echem et al. [61]
Millet Koji SSF Salar et al. [62]
Millet Probiotic drink SmF Di Stefano et al. [63]
Millet Fermented milk SmF Sheela et al. [64]
Millet Sourdough bread SSF Wang et al. [65]
Oat Fermented oat SSF Wu et al. [66]
Oat, wheat Bread SSF Gamel et al. [67]
Quinoa Yoghurt SmF Zannini et al. [68]
Molecules 2020, 25, 927 5 of 19

Table 1. Cont.

Whole Grain(s) Food Type of Fermentation Reference

Quinoa, wheat Fermented product SSF Ayyash et al. [69]
Rye, oat, wheat Bread SSF Buddrick et al. [70]
Rye, wheat Sourdough bread SSF Koistinen et al. [71]
Johansson et al. [72],
Rye Bread SSF
Raninen et al. [73]
Rye Porridge SSF Lee et al. [74]
Beckmann et al. [75],
Rye Sourdough bread SSF
Zamaratskaia et al. [76]
Sorghum Burukutu SmF Ikediobi et al. [77]
Sorghum Fermented balls SSF Ragaee and Abdel-Aal [78]
Sorghum Fermented porridge SSF Dlamini et al. [79]
Sorghum Injera SSF Taylor and Taylor [80]
Sorghum Ogi SmF Akingbala et al. [81]
Sorghum Omuramba SmF Mukuru et al. [82]
Kruger et al. [83],
Sorghum Ting SSF
Adebo et al. [84,85]
Sorghum Uji SmF Taylor and Taylor [80]
Tef Injera SSF Tamene et al. [86]
Wheat Boza SmF Gotcheva et al. [87]
Mustafa and Adem [88],
Wheat Bread SSF
Struyf et al. [89]
Wheat Sourdough bread SSF García-Mantrana et al. [90]
Dey and Kuhad [91],
Wheat Tempe SSF
Starzyńska-Janiszewska et al. [92]
SSF—solid-state fermentation. SmF—submerged/liquid fermentation.

Due to the protective pericarp/seed coat, the fermentation process might be slightly hindered.
Such has been reported in the literature and attributed to some of the antimicrobials and bioactive
constituents in the seed coat that might mitigate the activity of fermenting microorganisms [55,90,93,94].
The protective pericarp layer of cereal tends to alter the diffusion of nutrients such as amino acids and
sugars necessary for the growth of fermenting microorganisms. While this might result in a slightly
higher pH and likely longer fermentation periods (in the absence of a starter culture), fermentation still
modifies the phenolic constituents in WGs.

4. Impact of Fermentation on Phenolic Compounds in WGs

The fermentation process can have multiple effects on WG phenolics leading to modifications in
inherent levels and/or formation of subsequent monomers or polymers. Adebo et al. [84] reported
higher bioactive compounds (catechin, gallic acid, and quercetin) after fermentation in a study on ting
from fermented WG-sorghum with a concurrent decrease in total flavonoid content (TFC), total tannin
content (TNC), and total phenolic content (TPC). Reported decreases in levels of TPC, TFC, and TNC
were attributed to degradation and hydrolysis of the phenolic compounds, while a corresponding
increase in catechin, gallic acid, and quercetin was attributed to a release of these bioactive compounds
after fermentation with Lactobacillus strains.
Through fungal fermentation of WG-wheat into tempe, an increase in the sum of PAs was observed
with up to a 382% increase in ferulic acid recorded after fermentation [92]. A similar trend of increase
in investigated PCs and TPC during the fermentation of WG-tempe with Rhizopus oryzae RCK2012 had
been reported earlier [91]. Salar et al. [62] equally reported an increase in TPC of the WG-millet-koji and
attributed this to mobilization of PCs from their bound form to a free state through enzymes produced
Molecules 2020, 25, 927 6 of 19

during fermentation. Similar authors earlier reported an increase in TPC during the fermentation of
WG-maize [95], reportedly through the activities of β-glucosidase, which is capable of hydrolyzing
phenolic phucosides to release free phenolics. Increased extractability of PCs, synthesis of new bioactive
compounds, and consequent liberation of PCs due to structural breakdown of cereal cell walls have all
been attributed to such increases in WG-PCs after fermentation (Table 2). Through metabolic activities
of microbes, fermentation also induces structural breakdown of the cell wall, which leads to synthesis
of various bioactive compounds [65]. Equally important are the roles of proteases, amylases, xylanases
derived from fermenting microorganisms, and the cereal grain that contributes to modification of the
grain and distorting of chemical bonds, which, consequently, releases bound phenolics (Figure 3).

Table 2. Documented studies on the effect of fermentation on phenolics of whole grains.

Whole Fermented Phenolics Analytical

Findings References
Grain Product Investigated Method
Increase in total content of bound PAs
in flours from WG-barley related to
increased content of bound
Barley and Fermented Free and bound Colorimetric; Hole et al.
p-coumaric acid, ferulic acid, and
oat groat product PAs HPLC [96]
dimers of ferulic acid (5,50 - diferulic,
8-o-4-diferulic, and
8,50 -diferulic acids).
Increase in TPC after fermentation
attributed to the activities of
Fermented Salar et al.
Maize TPC Colorimetric β-glucosidase, capable of hydrolyzing
product [95]
phenolic phucosides to release free
phenolics
Increase in TPC of fermented product
due to mobilization of PCs from their
Salar et al.
Millet Koji TPC Colorimetric bound form to a free state through
[62]
enzymes produced during
fermentation
Increase and decrease in soluble and
bound phenolic content. Slight
decrease in TPC observed. Increment
of soluble phenolic content may be
Sourdough Wang et al.
Millet TPC Colorimetric due to acidification, production of
bread [65]
hydrolytic enzymes by LAB, and/or
activation of indigenous cereal
enzymes, which broke down the bran
cell wall structure
Increase in TPC may be attributed to
hydrolytic activities (e.g., esterases) of
Bifidobacteria strains that released
Quinoa, Fermented Ayyash et al.
TPC Colorimetric more PCs via the hydrolysis of
wheat product [69]
complexed forms, possibly the
synthesis of new bioactive
compounds detected as PCs
Fermentation phase more than
Baked Colorimetric, Liukkonen et
Rye TPC, PAs doubled the levels of easily
sourdough HPLC al. [97]
extractable PCs
Increased level of total PCs due to
increases in methanol-extractable PCs.
Modification in levels of bioactive
compounds during fermentation by
Colorimetric, the metabolic activity of microbes. Katina et al.
Rye Sourdough TPC, PAs
HPLC Fermentation-induced structural [98]
breakdown of cereal cell walls might
have also occurred and led to
liberation and/or synthesis of various
bioactive compounds
Molecules 2020, 25, 927 7 of 19

Table 2. Cont.

Whole Fermented Phenolics Analytical

Findings References
Grain Product Investigated Method
Increase in PAs due to activities of
Whole meal Skrajda-Brdak
Rye, wheat PAs HPLC phenolic acid esterases during the
bread et al. [99]
fermentation stage
Reduction in TNC and TPC.
Reduction in TNC could be due to
Fermented binding of tannins with protein and Dlamini et al.
Sorghum TPC, TNC Colorimetric
porridge other components, which reduces [79]
their extractability and tannin
degradation by microbial enzymes
Fermented Mohapatra et
Sorghum TPC, TNC Colorimetric Increase in TPC, decrease in TNC
product al. [100]
Decrease in TFC, TNC, and TPC
attributed to possible degradation of
PCs and hydrolysis of bioactive
compounds. Breakdown of
tannin-related compounds to lower
Flavonoids, PA, Colorimetric, molecular weight compounds, which Adebo et al.
Sorghum Ting
TFC, TNC, TPC LC-MS/MS affected extractability. Increase in PA [84,85]
and flavonoids could be due to
decarboxylation, hydrolysis,
microbial oxidation, and reduction as
well as esterification reactions that
occurred during fermentation
Increase in TPC through modification
Fermented in levels of bioactive compounds Ðordevic et
Wheat TPC Colorimetric
product during fermentation by the metabolic al. [101]
activity of microbes
Degradation, reduction of some PAs
and content of some remain
unchanged. Release of PAs from
LC-MS/MS, Ripari et al.
Wheat Sourdough PAs bound fraction, metabolism of PA by
UPLC [102]
LAB strains and action of enzymes
(decarboxylases, esterases, and
reductases)
Increase in TPC after fermentation,
Colorimetric, Dey and
Wheat Tempe TPC, PCs possibly due to release of bound
TLC, UPLC Kuhad [91]
compounds from the wheat matrix
Increase in the sum of PA could be Starzyńska-
Free and
Wheat Tempe HPLC linked to an increase in their Janiszewska
condensed PAs
extractability after fermentation et al. [92]
TPC of all fermented samples
increased except for Rhizopus
oligosporus fermented maize. Increase
Wheat, as well as decrease in PA levels.
Fermented Colorimetric, Dey and
brown rice, TPC, PAs Decreases was attributed to
product HPLC Kuhad [103]
maize, oat strain/specie specificity and/or grain
composition. General increases were
alluded to enhanced bioavailability of
cereal phenolics.
HPLC—high performance liquid chromatography. LAB—lactic acid bacteria. LC-MS/MS – liquid chromatography
tandem mass spectrometry. PA—phenolic acid. PC—phenolic compound. TFC—total flavonoid content. TLC—thin
layer chromatography. TNC—total tannin content. TPC—total phenolic content. UPLC—ultra high-performance
liquid chromatography.
 Wheat, maize. Increase as well as decrease in PA
brown Fermented Colorimetric, levels. Decreases was attributed to Dey and
TPC, PAs
rice, product HPLC strain/specie specificity and/or grain Kuhad [103]
maize, oat composition. General increases were
alluded to enhanced bioavailability of
cereal phenolics.

HPLC—high performance liquid chromatography. LAB—lactic acid bacteria. LC-MS/MS – liquid

Molecules 2020, 25, 927chromatography tandem mass spectrometry. PA—phenolic acid. PC—phenolic compound. TFC— 8 of 19
total flavonoid content. TLC—thin layer chromatography. TNC—total tannin content. TPC—total
phenolic content. UPLC—ultra high-performance liquid chromatography.

- Activities of enzymes (β-glucosidase, decarboxylases, esterases,

hydrolases, reductases)
Fermentation
- Breakdown of cereal cell wall

- Enhanced bioavailability

- Increased extractability after fermentation

- Metabolic activities of fermenting microorganisms

Increase
- Mobilization/release of bound phenolics to free forms
WG-phenolics - Synthesis/liberation of new bioactive compounds
Decrease

- Binding with other constituents

- Fermenting microbial strain specificity to PC-metabolism

- Degradation by microbial enzymes

Fermentation
- Hydrolysis of bioactive compounds

- Reduced extractability

Figure 3. A summary of ways by which whole grain phenolic compounds are modified during
Figure 3. Afermentation.
summary of ways by which whole grain phenolic compounds are modified
during fermentation.
During fermentation, PCs are metabolized and modified by fermenting organisms into other
conjugates, glucosides, and/or related forms. Such a metabolism of PCs during fermentation have
During fermentation, PCs are
been reported to increase theirmetabolized and modified
bioavailability [104,105] by fermenting
and lead to generation organisms
of compounds that into other
impact flavor [106,107]. Fermentation of sorghum into sourdough using LAB strains [singly and in
conjugates, glucosides, and/or related forms. Such a metabolism of PCs during fermentation have
two binary combinations (L. plantarum and L. casei or L. fermentum and L. reuteri)] was reported to
been reportedhaveto increase their
resulted in the bioavailability
metabolism [104,105]
of PAs, PA-esters, andglucosides
and flavonoid lead to[108].generation
Most PCs inof compounds that
this
study were metabolized and most notable were the transformation of caffeic
impact flavor [106,107]. Fermentation of sorghum into sourdough using LAB strains [singly and in acid  dihydrocaffeic

two binary combinations (L. plantarum and L. casei or L. fermentum and L. reuteri)] was reported to
have resulted in the metabolism of PAs, PA-esters, and flavonoid glucosides [108]. Most PCs in this
study were metabolized and most notable were the transformation of caffeic acid → dihydrocaffeic
acid, ethylcatechol, vinylcathechol, ferulic acid → dihydroferulic acid and naringenin-7-O-glucoside →
naringenin, reportedly an indication of the presence of esterase (tannase), glucosidase, PA decarboxylase,
and PA reductase [108]. The authors also suggested that the strains might have used different pathways
for PA and flavonoid metabolism. Fermentation of WG-sorghum have also been reported to have led
to the modification of PCs (catechin, gallic acid, and quercetin) into structurally related compounds,
which were not identified [85]. The authors suggested that the observed modification could be
attributed to decarboxylation, hydrolysis, and esterification reactions that might have occurred during
fermentation [85]. In a study on the metabolism of PAs in whole wheat and rye malt sourdoughs,
L. plantarum was observed to have metabolized free ferulic acid in wheat and rye malt sourdoughs,
while a strain of L. hammesii (DSM 16381) metabolized syringic and vanillic acids and reduced
levels of bound ferulic acid in wheat sourdoughs [102]. Co-fermentation of the LAB strains was also
noted to have aided the conversion of resultant-free ferulic acid to dihydroferulic acid and volatile
metabolites (vinyl-guaiacol and ethyl-guaiacol), which suggests that PA metabolism in sourdoughs
is more enhanced by co-fermentation due to complementary metabolic activities [102]. Carboxylase,
decarboxylase, esterase, and reductase activities in the LABs were reportedly responsible for PA
metabolism in this study [102]. It should, however, be noted that such metabolism could lead to an
increase in antimicrobial activities of resulting metabolic products [109], a decrease in antimicrobial
activities [104,110], or no alteration in antimicrobial activity levels [108].
According to Gänzle [104], metabolism of PCs may involve the removal of noxious compounds
as well as the release of hexosides as a source of metabolic energy. This metabolism could, however,
be influenced by composition and intrinsic factors of the matrices/substrate and can, thus, influence
the metabolic pathway, i.e., enzymatic activities can shift from decarboxylase action to reductase to
glucosidase activity [111]. Glycosyl hydrolases have also been implicated as a group of enzymes
responsible for such metabolism of PCs [104]. For example, L. hammesii was reported to have
metabolized hydroxybenzoic acids in wheat but not in rye malt sourdoughs, which possibly reflects
that the fermentation substrate influences the expression of enzymes active on PAs [111]. Likewise, in
a study on sorghum sourdough, the accumulation of dihydrocaffeic acid by only L. fermentum indicates
Molecules 2020, 25, 927 9 of 19

that decarboxylase and reductase enzymes of the other strains (L. fermentum and L. plantarum) have
different substrate specificities [108]. The study of Gaur et al. [112] also suggests that availability of
genes necessary for the metabolism of these PCs is also of importance and a significant contributor to
the metabolic potential of fermenting microorganisms.

5. Impact of Fermentation on Antioxidant Activity in WGs

Antioxidants are endogenous or exogenous molecules that mitigate any form of
oxidative/nitrosative stress or its consequences [113]. According to Slavin [114], the primary protective
role of antioxidants in the body is through their reaction with free radicals. Antioxidants function as free
radical scavengers, quenchers of singlet oxygen formation, and reducing agents [115,116] through their
inhibitory activity of prooxidant enzymes. A potential mechanism by which PCs confer AA involves
the induction of detoxification mechanisms through phase II conjugation reactions, which prevents the
formation of carcinogens from precursors as well as by blocking the reaction of carcinogens with critical
cellular macromolecules [117,118]. Phenolic compounds also modify some cellular signaling processes
and donate an electron/transfer hydrogen atom to free radicals, activate endogenous antioxidant
mechanisms, which increases the levels of antioxidant enzymes, and act as chelators of trace metals
involved in free radical protection [116,119,120].
As evident in Table 3, most available studies in the literature investigating the influence of
fermentation on phenolic compounds have majorly focused on AAs as its health benefit. This might be
unsurprising as PCs, particularly PAs, have been reported as one of the most abundant metabolites
of cereal crops with AAs [121–123]. While the role of other bioactive constituents in WGs cannot be
disregarded, PCs equally play a huge role in the antioxidant properties it confers to WG-foods.

Table 3. Documented studies on the effect of fermentation on antioxidant activity of whole grains.

Whole Fermented
Assay Mechanism(s) Reported References
Grain Product
Increase in ABTS and DPPH due to the
role of the hydrolytic enzyme that
Maize Fermented product ABTS, DPPH Salar et al. [95]
released/mobilized bound polyphenolic
compounds, which enhanced AAs.
Koji showed increased scavenging of
ABTS and DPPH radicals due to the
Millet Koji ABTS, DPPH release of a bound form of Salar et al. [62]
phytochemicals present and high levels of
TPC modulated during fermentation.
Increase in DPPH radical inhibition after
sourdough fermentation. The conversion
Millet Sourdough bread DPPH of bound to soluble PCs improved the Wang et al. [65]
health-related functionality of the final
products.
An increase in ABTS and DPPH values
was attributed to the soluble
Quinoa, Ayyash et al.
Fermented product ABTS, DPPH phytochemicals released during
wheat [69]
fermentation and to bioactive peptides
formed as a result of proteolytic activity.
The fermentation stage increased AA
Liukkonen et al.
Rye Baked sourdough DPPH likely due to an increased level of
[97]
extractable PCs.
Molecules 2020, 25, 927 10 of 19

Table 3. Cont.

Whole Fermented
Assay Mechanism(s) Reported References
Grain Product
Reduction in antioxidant levels after
fermentation attributed to changes
during processing that affected the
Fermented extraction of total phenols and tannins. Dlamini et al.
Sorghum ABTS, DPPH
porridge Such changes were hypothesized to have [79]
likely involved associations between the
tannins, phenols, proteins, and other
compounds in the grain.
Mohapatra et al.
Sorghum Fermented product CUPRAC, DPPH Increase in AAs investigated.
[100]
Increase in AA due to regenerated and
released bioactive compounds (including
non-phenolic components after
Adebo et al.
Sorghum Ting ABTS fermentation with the L. fermentum
[85]
strains), which might have contributed to
the radical scavenging properties of the
product.
Ðordevic et al.
Wheat Fermented product DPPH, FRAP, TBA Increase in the investigated AAs.
[101]
Increase in antioxidant properties
investigated attributed to the composition
ABTS, DPPH, FRAP, of PCs, unidentified compounds, and
Dey and Kuhad
Wheat Tempe HP-scavenging and other water-soluble bioactive compounds
[91]
OH-scavenging assays like small peptides and
xylo-oligosaccharides produced during
fermentation.
Increase in soluble antioxidant potential
as fermentation increased extractable
Starzyńska-
ABTS, OH-scavenging antiradical activity scavenging potential,
Wheat Tempe Janiszewska et
and FCRS-RP assays which might be due to the release of
al. [92]
peptides and other compounds during
fermentation.
Both ABTS and DPPH scavenging
properties were enhanced after
fermentation of the WG-cereals by all the
Wheat,
four micro-organisms (except R. Dey and Kuhad
brown rice, Fermented product ABTS, DPPH
oligosporus-fermented maize). Increases [103]
maize, oat
related to release of more soluble
bioactive compounds, such as peptides
and oligosaccharides.
ABTS-2,20 -azino-bis(3-ethylbenzothiazoline-6-sulfonic acid). CUPRAC—cupric reducing antioxidant capacity.
DPPH—2,2-diphenyl-1-picrylhydrazyl. FCRS-RP—Folin-Ciocalteu reacting substances-reducing power.
FRAP—ferric reducing antioxidant property. HP—hydrogen peroxide. HPLC—high performance liquid
chromatography. OH—hydroxyl.

Although the majority of the studies reviewed herein reported increases in PCs, this is not
always the case, as decreases in these health beneficial constituents have also been reported (Table 2).
Studies on fermented WG-sorghum reported a decrease in TNC and TPC with this attributed to the
ability of tannins to bind with proteins and other components, which reduces extractability as well
as tannin degradation [79,85]. Investigations into the metabolism of sourdough by Ripari et al. [102]
also suggested that reduction in some investigated PAs might be due to metabolism of PAs by lactic
acid bacteria (LAB) and the activities of decarboxylases, esterases, and reductases. In the study of
Dey and Kuhad [103] on fermentation of different WGs, both an increase and a decrease in TPC
was observed. While increases alluded to enhanced bioavailability of cereal phenolics, a decrease
observed in maize was associated with the specificity of the microbial strain to act on the PCs as well
as the grain composition. The effect of the microbial activity on the levels of individual phenolics
can differ, depending on the microbial strain. The genome of certain microorganisms might encode
genes responsible for the metabolism and/or degradation of phenolic compounds while some do
not [92,96,102]. This might, however, be difficult to ascertain or distinguish in spontaneous fermentation
processes or back-slopping that is characterized by a wide range of fermenting microorganisms.
Molecules 2020, 25, 927 11 of 19

During the estimation of AA of food products, using more than one analytical method is
better because food contains a myriad of constituents [92]. The frequently used techniques are
spectrophotometric assays and the 2, 20 -Azino-bis (3-ethylbenzothiazoline-6-sulfate) (ABTS) (also
called ABTS-radical cation depolarization) assay as well as the cupric-reducing antioxidant capacity
(CUPRAC), 2,2-Diphenyl-1-picrylhydrazyl (DPPH) and ferric-reducing antioxidant power (FRAP)
assay. Less frequently used techniques found in the course of this review are the lipid peroxidation
technique adopting the thiobarbituric acid (TBA) assay, which was used to determine the TBA reactive
substance from lipid peroxidation [101], as well as OH- and H2 O2 -scavenging assays. These are
both concerning due to their role in causing tissue damage and cell death, and could combine with
nucleotides to cause carcinogenesis [124].
Considering the general trend of increase in WG-PCs after fermentation and associated
mechanisms, it could, thus, be hypothesized that this should be tantamount to an increase in AAs.
While such increases were reported, some studies noted decreases in AAs of WG-fermented products.
As documented by Ðordevic et al. [101] and Sun and Ho [125], possible explanations for this ambiguous
relationship between AA and PCs are that: (i) quantified TPC values do not include other components
that can equally confer AAs, (ii) synergy in a mixture makes AA not only dependent on antioxidant
concentration but also on the structure and interactions among antioxidants, and (iii) different methods
used for measuring AA based on different mechanisms may lead to different observations. Such an
observation has also been buttressed by other authors suggesting that directly linking AAs in food and
a responsible component might be somewhat difficult, as methods of extraction, identification, and/or
quantification of AAs vary [126,127], which makes comparisons and, subsequently, extrapolating
conclusions quite tricky.
General increases in AA of fermented foods have been attributed to a release of bound PC due
to activities of hydrolytic enzymes and contents modulated during fermentation of a maize-based
product and koji from millet [62,95]. A likely conversion of bound PCs into health-related components,
a release of soluble phytochemicals and other non-PCs as well as increased extractability of AA-related
PCs have equally been implicated to have led to an increase in AA during the fermentation of WGs
into tempe, ting, and sourdough (from millet and rye) [65,69,85,92,97]. An addition to these could be
that the fermentation process facilitated cleavage/dissociation of the bonds between PCs and other
constituents leading to a release of PC-monomers, which yield AAs. Equally important and implicated
in other studies are products of protein hydrolysis through proteolytic actions through fermentation,
which could have led to components that contribute to increased PC and consequent antioxidant
potential of fermented WGs. Available enzymes during fermentation and/or produced by fermenting
microorganisms could also break down ester bonds, hydrolyse β-glucosidic bonds, and distort the
hydroxyl groups in phenolic structures liberating free PCs and other antioxidant-related compounds.
On the contrary, a decrease in AA after fermentation was attributed to modifications that influenced
the extractability of compounds that confer AAs, especially the association between tannins, phenols,
proteins, and other compounds in the grain [79].
Although in vitro studies reflect potential AAs of WG-fermented cereals, these in vitro techniques
could underestimate physiological antioxidants, which necessitates in vivo studies. The use of in vivo
models in investigating the influence of fermentation on AA is largely desirable. According to
Benedetti et al. [128] and Alam et al. [129], in vivo protocols involve the administration of antioxidants
to testing animals for a specified period of time, after which the animals are sacrificed, and blood or
tissues are analyzed. Subsequently done are assays such as lipid peroxidation (LPO), thioredoxin
reductase activities, and glutathione peroxidase (GSHPx) in human patients [128,130]. Although such
in vivo studies are largely desirable, challenges related to ethical approvals, high costs, and daunting
logistics have led to the adoption of in vitro techniques. Few studies are available on in vivo assays
on fermented WG-cereal products with such studies focusing on AAs of the product. Breads made
from WG-Kamut Khorasan wheat and WG-durum wheat were both reported to protect rat liver from
Molecules 2020, 25, 927 12 of 19

oxidative stress [128]. An earlier study by similar authors reported a lower oxidative state in rats fed
with experimental diets of sourdough bread for seven weeks [131].
Phenolic compounds usually occur in an esterified form linked to the cell wall matrix in the
cereal bran and, as such, not readily available. Fermentation is considered a possible strategy to
not only increase AAs but also to release the insoluble bound phenolic acids and, thus, to improve
the poor bioavailability of grain phenolics [132]. This is particularly important as the antioxidant
potential of WGs could be restricted by low availability of compounds during digestion. Not
only does fermentation increases PCs and AA of WG-fermented products (Tables 2 and 3), it also
positively influences bioavailability, bio-accessibility, and PAs as demonstrated in a study on flours
from WG-barley fermented with probiotic strains [96].

6. Future Perspective
Fermentation positively alters food quality, confers organoleptic characteristics, and improves
phenolic constituents and antioxidant activity of WGs. Could this then translate to consumption
of more whole grains? Possibly not, considering the grittiness and associated sensory challenges
associated with whole grain foods. This might also contribute to fewer whole grain fermented foods
as compared to those from refined grains. This is in tandem with a study on the consumption of
WGs foods from brewers’ spent grain, which indicates that hereditary consumers of whole grain
foods will be more receptive to its consumption as compared to their refined foods counterpart [133].
Some studies have also indicated barriers for consuming WG foods such as the lack of knowledge about
its health benefits, challenges with cooking/preparation time, negative sensory perception, perceived
cost, and the lack of availability of whole grains [134–136].

7. Conclusions
Increasing whole grain consumption should, therefore, be a target for health organizations with
recommendations for intake proposed in many countries. As such, new strategies and partnerships
between researchers, industry, and relevant agencies are further needed to promote whole grain
consumption. Future studies are necessary in the area of phenolic compounds in fermented whole
grains along with effective techniques such as whole genome sequencing to investigate genes responsible
for the conversion of phenolic constituents and improvements in AAs. Such would largely assist in
choosing starter cultures that would further improve the quality of fermented WG foods. Deeper
investigation into the mechanisms of different forms of fermentation (solid state and liquid) on
single/pure phenolic compounds (in isolation) and antioxidant activities should equally be explored.
Additionally, studies are needed into the absorption and bioavailability of these phenolics in the gut,
preferably through in vivo models.

Funding: The University of Johannesburg Global Excellence and Stature (GES) 4.0 Catalytic Initiative Grant and the
National Research Foundation (NRF) of South Africa Thuthuka funding (Grant no: 121826) are duly acknowledged.
Conflicts of Interest: The authors declare no conflict of interest.

References
1. Arai, S. Studies on functional foods in Japan-state of the art. Biosci. Biotechnol. Biochem. 1996, 60, 9–15.
[CrossRef] [PubMed]
2. Hallfrisch, J.; Scholfield, D.J.; Behall, K.M. Blood pressure reduced by whole grain diet containing barley
or whole wheat and brown rice in moderately hypercholesterolemic men. Nutr. Res. 2003, 23, 1631–1642.
[CrossRef]
3. Juntunen, K.S.; Laaksonen, D.E.; Poutanen, K.S.; Niskanen, L.K.; Mykkanen, H.M. High-fiber rye bread and
insulin secretion and sensitivity in healthy postmenopausal women. Am. J. Clin. Nutr. 2003, 77, 385–391.
[CrossRef] [PubMed]
Molecules 2020, 25, 927 13 of 19

4. Behall, K.M.; Scholfield, D.J.; Hallfrisch, J. Diets containing barley significantly reduce lipids in mildly
hypercholesterolemic men and women. Am. J. Clin. Nutr. 2004, 80, 1185–1193. [CrossRef] [PubMed]
5. Behall, K.M.; Scholfield, D.J.; Hallfrisch, J. Whole-grain diets reduce blood pressure in mildly
hypercholesterolemic men and women. J. Am. Diet. Assoc. 2006, 106, 1445–1449. [CrossRef] [PubMed]
6. Marquart, L.; Jones, J.M.; Chohen, E.A.; Poutanen, K. The future of whole grains. In Whole Grains and Health;
Marquart, L., Jacobs, D.R., McIntosh, G.H., Poutanen, K., Reicks, M., Eds.; Blackwell Publishing: Ames, IA,
USA, 2007; pp. 3–16.
7. Priebe, M.G.; van Binsbergen, J.J.; de Vos, R.; Vonk, R.J. Whole grain foods for the prevention of type 2
diabetes mellitus. Cochrane Database Syst. Rev. 2008, 23, CD006061. [CrossRef]
8. Maki, K.C.; Beiseigel, J.M.; Jonnalagadda, S.S.; Gugger, C.K.; Reeves, M.S.; Farmer, M.V.; Kaden, V.N.;
Rains, T.M. Whole-grain ready-to-eat oat cereal, as part of a dietary program for weight loss, reduces
low-density lipoprotein cholesterol in adults with overweight and obesity more than a dietary program
including low-fiber control foods. J. Am. Diet. Assoc. 2010, 110, 205–214. [CrossRef]
9. Tighe, P.; Duthie, G.; Vaughan, N.; Brittenden, J.; Simpson, W.G.; Duthie, S.; Mutch, W.; Wahle, K.; Horgan, G.;
Thies, F. Effect of increased consumption of whole-grain foods on blood pressure and other cardiovascular
risk markers in healthy middle-aged persons: A randomized controlled trial. Am. J. Clin. Nutr. 2010, 92,
733–740. [CrossRef]
10. Ross, A.B.; Bruce, S.J.; Blondel-Lubrano, A.; Oguey-Araymon, S.; Beaumont, M.; Bourgeois, A.;
Nielsen-Moennoz, C.; Vigo, M.; Fay, L.B.; Kochhar, S.; et al. A whole-grain cereal-rich diet increases
plasma betaine and tends to decrease total and LDL-cholesterol compared with a refined-grain diet in healthy
subjects. Br. J. Nutr. 2011, 105, 1492–1502. [CrossRef]
11. Seal, C.J.; Brownlee, I.A. Whole-grain foods and chronic disease: Evidence from epidemiological and
intervention studies. Proc. Nutr. Soc. 2015, 74, 313–319. [CrossRef]
12. AACC. Definition of Whole Grain. Available online: https://www.cerealsgrains.org/initiatives/definitions/
Pages/WholeGrain.aspx (accessed on 8 November 2019).
13. Jonnalagadda, S.S.; Harnack, L.; Liu, R.H.; McKeown, N.; Seal, C.; Liu, S.; Fahey, G.C. Putting the whole grain
puzzle together: Health benefits associated with whole grains-Summary of American Society for Nutrition
2010 satellite symposium. J. Nutr. 2011, 141, 1011S–1022S. [CrossRef] [PubMed]
14. Borneo, R.; León, A.E. Whole grain cereals: Functional components and health benefits. Food Funct. 2012, 3,
110–119. [CrossRef] [PubMed]
15. McRae, M.P. Health benefits of dietary whole grains: An umbrella review of meta-analyses. J. Chiroprac.
Med. 2017, 16, 10–18. [CrossRef] [PubMed]
16. Călinoiu, L.F.; Vodnar, D.C. Whole grains and phenolic acids: A review on bioactivity, functionality, health
benefits and bioavailability. Nutrients 2018, 10, 1615. [CrossRef] [PubMed]
17. Liu, R.H. Whole grain phytochemicals and health. J. Cereal. Sci. 2007, 46, 207–219. [CrossRef]
18. Okarter, N.; Liu, R.H. Health benefits of whole grain phytochemicals. Crit. Rev. Food Sci. Nutr. 2011, 50,
193–208. [CrossRef]
19. Zhu, Y.; Sang, S. Phytochemicals in whole grain wheat and their health-promoting effects. Mol. Nutr. Food
Res. 2017, 61, 1600852. [CrossRef]
20. Koistinen, V.M.; Katina, K.; Nordlund, E.; Poutanen, K.; Hanhineva, K. Changes in the phytochemical profile
of rye bran induced by enzymatic bioprocessing and sourdough fermentation. Food Res. Int. 2016, 89,
1106–1115. [CrossRef]
21. Idehen, E.; Tang, Y.; Sang, S. Bioactive phytochemicals in barley. J. Food Drug Anal. 2017, 25, 148–161.
[CrossRef]
22. Harvard Health Letter. The whole is greater than the sum of the parts. I. Whole grain. Harv. Health Lett.
1999, 25, 8.
23. Schaffer-Lequart, C.; Lehmann, U.; Ross, A.B.; Roger, O.; Eldridge, A.L.; Ananta, E.; Bietry, M.F.; King, L.R.;
Moroni, A.V.; Srichuwong, S.; et al. Whole grain in manufactured foods: Current use, challenges and the
way forward. Crit. Rev. Food Sci. Nutr. 2017, 57, 1562–1568. [CrossRef] [PubMed]
24. Jones, J.M.; Reicks, M.; Adams, J.; Fulcher, G.; Weaver, G.; Kanter, M.; Marquart, L. The importance of
promoting a whole grain foods message. J. Am. Coll. Nutr. 2002, 21, 293–297. [CrossRef] [PubMed]
25. Mellen, P.B.; Walsh, T.F.; Herrington, D.M. Whole grain intake and cardiovascular disease: A meta-analysis.
Nutr. Metab. Cardiovasc. Dis. 2008, 18, 283–290. [CrossRef] [PubMed]
Molecules 2020, 25, 927 14 of 19

26. Ye, E.Q.; Chacko, S.A.; Chou, E.L.; Kugizaki, M.; Liu, S. Greater whole-grain intake is associated with lower
risk of type 2 diabetes, cardiovascular disease, and weight gain. J. Nutr. 2012, 142, 1304–1313. [CrossRef]
[PubMed]
27. Esmaillzadeh, A.; Mirmiran, P.; Azizi, F. Whole-grain consumption and the metabolic syndrome: A favorable
association in Tehranian adults. Eur. J. Clin. Nutr. 2005, 59, 353–362. [CrossRef] [PubMed]
28. Jacobs, D.; Marquart, L.; Slavin, J.; Kushi, L.H. Whole grain intake and cancer: An expanded review and
meta-analysis. Nutr. Cancer 1998, 30, 85–96. [CrossRef]
29. Mourouti, N.; Papavagelis, C.; Plytzanopoulou, P.; Kontogianni, M.; Vassilakou, T.; Malamos, N.; Linos, A.;
Panagiotakos, D. Dietary patterns and breast cancer: A case-control study in women. Eur. J. Nutr. 2015, 54,
609–617. [CrossRef]
30. Vanegas, S.M.; Maydani, M.; Barnett, J.B.; Goldin, B.; Kane, A.; Rasmussen, H.; Brown, C.; Vangay, P.;
Knights, D.; Jonnalagadda, S.; et al. Substituting whole grains for refined grains in a 6-wk randomized trial
has a modest effect on gut microbiota and immune and inflammatory markers of healthy adults. Am. J. Clin
Nutr. 2017, 105, 635–650. [CrossRef]
31. Boudet, A.M. Evolution and current status of research in phenolic compounds. Phytochemistry 2007, 68,
2722–2735. [CrossRef]
32. Arendt, E.K.; Moroni, A.; Zannini, E. Medical nutrition therapy: Use of sourdough lactic acid bacteria as a
cell factory for delivering functional biomolecules and food ingredients in gluten free bread. Microb. Cell
Fact. 2011, 10, S15. [CrossRef]
33. Coda, R.; Cagno, R.D.; Gobbetti, M.; Rizzello, C.G. Sourdough lactic acid bacteria: Exploration of non-wheat
cereal-base fermentation. Food Microbiol. 2014, 37, 51–58. [CrossRef]
34. Adebo, O.A.; Njobeh, P.B.; Adeboye, A.S.; Adebiyi, J.A.; Sobowale, S.S.; Ogundele, O.M.; Kayitesi, E.
Advances in fermentation technology for novel food products. In Innovations in Technologies for Fermented
Food and Beverage Industries; Panda, S.K., Shetty, P.H., Eds.; Springer: Cham, Switzerland, 2018; pp. 71–87.
35. Adebo, O.A.; Kayitesi, E.; Tugizimana, F.; Njobeh, P.B. Differential metabolic signatures in naturally and
lactic acid bacteria (LAB) fermented ting (a Southern African food) with different tannin content, as revealed
by gas chromatography mass spectrometry (GC–MS)-based metabolomics. Food Res. Int. 2019, 121, 326–335.
[CrossRef]
36. Adebiyi, J.A.; Kayitesi, E.; Adebo, O.A.; Changwa, R.; Njobeh, P.B. Food fermentation and mycotoxin
detoxification: An African perspective. Food Cont. 2019, 106, 106731. [CrossRef]
37. Robards, K.; Prenzler, P.D.; Tucker, G.; Swatsitang, P.; Glover, W. Phenolic compounds and their role in
oxidative process in fruits. Food Chem. 1999, 66, 401–436. [CrossRef]
38. Shadidi, F. Phytochemicals in oilseeds. In Phytochemicals in Nutrition and Health; CRC Press: Boca Raton, FL,
USA, 2002; pp. 139–156.
39. Randhir, R.; Lin, Y.-T.; Shetty, K. Phenolics, their antioxidant and antimicrobial activity in dark germinated
fenugreek sprouts in response to peptide and phytochemical elicitors. Asia Pac. J. Clin. Nutr. 2004, 13,
295–307.
40. Singh, B.; Singh, J.P.; Kaur, A.; Singh, N. Phenolic composition and antioxidant potential of grain legume
seeds: A review. Food Res. Int. 2017, 101, 1–16. [CrossRef]
41. Awika, J.M.; Rooney, L.W. Sorghum phytochemicals and their potential impact on human health.
Phytochemistry 2004, 65, 1199–1221. [CrossRef]
42. Ghosh, D. Tannins from foods to combat diseases. Int. J. Pharm. Res. Rev. 2015, 4, 40–44.
43. Adebo, O.A. Metabolomics, Physicochemical Properties and Mycotoxin Reduction of Whole Grain ting (a
Southern African Fermented Food) Produced via Natural and Lactic Acid Bacteria (LAB) Fermentation.
Ph.D. Thesis, University of Johannesburg, Johannesburg, South Africa, October 2018.
44. Goel, G.; Puniya, A.K.; Aguliar, C.N.; Singh, K. Interaction of gut microflora with tannins in feeds.
Naturwissenschaften 2005, 92, 497–503. [CrossRef]
45. Clifford, M.N. Chlorogenic acids and other cinnamates-nature, occurrence, and dietary burden. J. Sci. Food
Agric. 1999, 79, 362–372. [CrossRef]
46. Bondia-Pons, I.; Aura, A.M.; Vuorela, S.; Kolehmainen, M.; Mykkanen, H.; Poutanen, K. Rye phenolics in
nutrition and health. J. Cereal Sci. 2009, 49, 323–336. [CrossRef]
47. Shadidi, F.; Chandrasekara, A. Millet grain phenolics and their role in disease risk reduction and health
promotion: A review. J. Funct. Food 2013, 5, 570–581. [CrossRef]
Molecules 2020, 25, 927 15 of 19

48. Shadidi, F.; Yeo, J. Insoluble-bound phenolics in food. Molecules 2016, 21, 1216. [CrossRef]
49. Gong, L.; Cao, W.; Chi, H.; Wang, J.; Zhang, H.; Liu, J.; Sun, B. Whole cereal grains and potential health
effects: Involvement of the gut microbiota. Food Res. Int. 2018, 103, 84–102. [CrossRef]
50. Kumar, N.; Goel, N. Phenolic acids: Natural versatile molecules with promising therapeutic applications.
Biotechnol. Rep. 2019, 24, e00370. [CrossRef]
51. Masebe, K.M.; Adebo, O.A. Production and quality characteristics of a probiotic beverage from watermelon
(Citrullus lanatus). In Engineering, Technology and Waste Management (SETWM-19), Proceedings of the
17th Johannesburg International Conference on Science, Johannesburg, South Africa, 18–19 November 2019;
Fosso-Kankeu, E., Waanders, F., Bulsara, H.K.P., Eds.; Eminent Association of Pioneers and North-West
University: Johannesburg, South Africa, 2019; pp. 42–49.
52. Marsh, A.J.; Hill, C.; Ross, R.P.; Cotter, P.D. Fermented beverages with health-promoting potential: Past and
future perspectives. Trend Food Sci. Technol. 2014, 38, 113–124. [CrossRef]
53. Adebo, O.A.; Njobeh, P.B.; Adebiyi, J.A.; Gbashi, S.; Phoku, J.Z.; Kayitesi, E. Fermented pulse-based foods in
developing nations as sources of functional foods. In Functional Food-Improve Health through Adequate Food;
Hueda, M.C., Ed.; InTech: Rijeka, Croatia, 2017; pp. 77–109.
54. Kaushik, G.; Satya, S.; Naik, S.N. Food processing a tool to pesticide residue dissipation—A review. Food Rev.
Int. 2009, 42, 26–40. [CrossRef]
55. Adebiyi, J.A.; Njobeh, P.B.; Kayitesi, E. Assessment of nutritional and phytochemical quality of Dawadawa
(an African fermented condiment) produced from Bambara groundnut (Vigna subterranea). Microchem. J.
2019, 149, 104034. [CrossRef]
56. Llopart, E.E.; Drago, S.R.; De Greef, D.M.; Torres, R.L.; Gonzalez, A.R. Effects of extrusion conditions on
physical and nutritional properties of extruded whole grain red sorghum (Sorghum spp.). Int. J. Food Sci.
Nutr. 2014, 65, 34–41. [CrossRef]
57. Kantor, L.S.; Variyam, J.N.; Allshouse, J.E.; Putnam, J.J.; Lin, B.H. Choose a variety of grains daily, especially
whole grains: A challenge for consumers. J. Nutr. 2001, 131, 473S–486S. [CrossRef]
58. Kyrø, C.; Skeie, G.; Dragsted, L.O.; Christensen, J.; Overvad, K.; Hallmans, G.; Johansson, I.; Lund, E.;
Slimani, N.; Johnsen, J.F.; et al. Intake of whole grain in Scandinavia: Intake, sources and compliance with
new national recommendations. Scand J. Public Health 2012, 40, 76–84. [CrossRef]
59. Eklund-Jonsson, C.; Sanderg, A.S.; Alminger, M.L. Reduction of phytate content while preserving minerals
during whole grain cereal tempe fermentation. J. Cereal Sci. 2006, 44, 154–160. [CrossRef]
60. Oyarekua, M.A. Effect of co-fermentation on nutritive quality and pasting properties of maize/cowpea/sweet
potato as complementary food. Afr. J. Food Agric. Nutr. Dev. 2013, 13, 7171–7191. [CrossRef]
61. Obinna-Echem, P.C.; Beal, P.; Kuri, V. Effect of processing method on the mineral content of Nigerian
fermented maize infant complementary food-akamu. LWT-Food Sci. Technol. 2015, 61, 145–151. [CrossRef]
62. Salar, R.J.; Purewal, S.S.; Bhatti, M.S. Optimization of extraction conditions and enhancement of phenolic
content and antioxidant activity of pearl millet fermented with Aspergillus awamori MTCC-54. Resour. Effic.
Technol. 2016, 2, 148–157. [CrossRef]
63. Di Stefano, E.; White, J.; Seney, S.; Hekmat, S.; McDowell, T.; Sumarah, M.; Reid, G. A novel millet-based
probiotic fermented food for the developing world. Nutrients 2017, 9, 529. [CrossRef]
64. Sheela, P.; UmaMaheswari, T.; Kanchana, S.; Kamalasundari, S.; Hemalatha, G. Development and evaluation
of fermented millet milk based curd. J. Pharmacog. Phytochem. 2018, 7, 714–717.
65. Wang, Y.; Compaoré-Sérémé, D.; Sawadogo-Lingani, H.; Coda, R.; Katina, K.; Maina, N.J. Influence of
dextran synthesized in situ on the rheological, technological and nutritional properties of whole grain pearl
millet bread. Food Chem. 2019, 285, 221–230. [CrossRef]
66. Wu, H.; Rui, X.; Li, W.; Xiao, Y.; Zhou, J.; Dong, M. Whole-grain oats (Avena sativa L.) as a carrier of lactic acid
bacteria and a supplement rich in angiotensin I-converting enzyme inhibitory peptides through solid-state
fermentation. Food Funct. 2018, 9, 2270–2281. [CrossRef]
67. Gamel, T.H.; Abdel-Aal, E.M.; Tosh, S.M. Effect of yeast-fermented and sour-dough making processes on
physicochemical characteristics of β-glucan in whole wheat/oat bread. LWT-Food Sci. Technol. 2015, 60, 78–85.
[CrossRef]
68. Zannini, E.; Jeske, S.; Lynch, K.M.; Arendt, E.K. Development of novel quinoa-based yoghurt fermented with
dextran producer Weissella cibaria MG1. Int. J. Food Microbiol. 2018, 268, 19–26. [CrossRef]
Molecules 2020, 25, 927 16 of 19

69. Ayyash, M.; Johnson, S.K.; Liu, S.Q.; Al-Mheiri, A.; Abushelaibi, A. Cytotoxicity, antihypertensive, antidiabetic
and antioxidant activities of solid-state fermented lupin, quinoa and wheat by Bifidobacterium species:
In vitro investigations. LWT-Food Sci. Technol. 2018, 95, 295–302. [CrossRef]
70. Buddrick, O.; Jones, O.A.H.; Cornell, H.J.; Small, D.M. The influence of fermentation processes and cereal
grains in wholegrain bread on reducing phytate content. J. Cereal Sci. 2014, 59, 3–8. [CrossRef]
71. Koistinen, V.M.; Mattila, O.; Katina, K.; Poutanen, K.; Aura, A.M.; Hanhineva, K. Metabolic profiling of
sourdough fermented wheat and rye bread. Sci. Rep. 2018, 8, 5684. [CrossRef]
72. Johansson, D.P.; Lee, I.; Risérus, U.; Langton, M.; Landberg, R. Effects of unfermented and fermented whole
grain rye crisp breads served as part of a standardized breakfast, on appetite and postprandial glucose and
insulin responses: A randomized cross-over trial. PLoS ONE 2015, 10, e0122241. [CrossRef]
73. Raninen, K.; Lappi, J.; Kolehmainen, M.; Kolehmainen, M.; Mykkanen, H.; Poutanen, K.; Raatikainen, O.
Diet-derived changes by sourdough-fermented rye bread in exhaled breath aspiration ion mobility
spectrometry profiles in individuals with mild gastrointestinal symptoms. Int. J. Food Sci. Nutr. 2017, 8,
987–996. [CrossRef]
74. Lee, I.; Shi, L.; Webb, D.L.; Hellström, P.M.; Risérus, U.; Landberg, R. Effects of whole-grain rye porridge
with added inulin and wheat gluten on appetite, gut fermentation and postprandial glucose metabolism:
A randomised, cross-over, breakfast study. Br. J. Nutr. 2017, 116, 2139–2149. [CrossRef]
75. Beckmann, M.; Lloyd, A.J.; Haldar, S.; Seal, C.; Brandt, K.; Draper, J. Hydroxylated phenylacetamides
derived from bioactive benzoxazinoids are bioavailable in humans after habitual consumption of whole
grain sourdough rye bread. Mol. Nutr. Food Res. 2013, 57, 1859–1873. [CrossRef]
76. Zamaratskaia, G.; Johansson, D.P.; Junqueira, M.A.; Deissler, L.; Langton, M.; Hellstrom, P.M.; Landberg, R.
Impact of sourdough fermentation on appetite and postprandial metabolic responses—A randomised
cross-over trial with whole grain rye crispbread. Br. J. Nutr. 2017, 118, 686–697. [CrossRef]
77. Ikediobi, C.O.; Olugboji, O.; Okoh, P.N. Cyanide profile of component parts of sorghum (Sorghum bicolor L.
Moench) sprouts. Food Chem. 1988, 27, 167–175. [CrossRef]
78. Ragaee, S.; Abdel-Aal, E.M. Pasting properties of starch and protein in selected cereals and quality of their
food products. Food Chem. 2006, 95, 9–18. [CrossRef]
79. Dlamini, N.R.; Taylor, J.R.N.; Rooney, L.W. The effect of sorghum type and processing on the antioxidant
properties of African sorghum-based foods. Food Chem. 2007, 105, 1412–1419. [CrossRef]
80. Taylor, J.; Taylor, J.R.N. Protein biofortified sorghum: Effect of processing into traditional African foods on
their protein quality. J. Agric. Food Chem. 2011, 59, 2386–2392. [CrossRef]
81. Akingbala, J.O.; Rooney, L.W.; Fauboin, J.M. Physical, chemical, and sensory evaluation of ogi from sorghum
of differing kernel characteristics. J. Food Sci. 1981, 76, 1532–1536. [CrossRef]
82. Mukuru, S.Z.; Butler, L.G.; Rogler, J.C.; Kirleis, A.W.; Ejeta, G.; Axtell, J.D.; Mertz, E.T. Traditional processing
of high-tannin sorghum grain in Uganda and its effect on tannin, protein digestibility, and rat growth. J. Agric.
Food Chem. 1992, 40, 1172–1175. [CrossRef]
83. Kruger, J.; Taylor, J.R.N.; Oelofse, A. Effects of reducing phytate content in sorghum through genetic
modification and fermentation on in vitro iron availability in whole grain porridges. Food Chem. 2012, 131,
220–224. [CrossRef]
84. Adebo, O.A.; Njobeh, P.B.; Adebiyi, J.A.; Kayitesi, E. Co-influence of fermentation time and temperature on
physicochemical properties, bioactive components and microstructure of ting (a Southern African food) from
whole grain sorghum. Food Biosci. 2018, 25, 118–127. [CrossRef]
85. Adebo, O.A.; Njobeh, P.B.; Kayitesi, E. Fermentation by Lactobacillus fermentum strains (singly and in
combination) enhances the properties of ting from two whole grain sorghum types. J. Cereal Sci. 2018, 82,
49–56. [CrossRef]
86. Tamene, A.; Kariluoto, S.; Baye, K.; Humblot, C. Quantification of folate in the main steps of traditional
processing of tef injera, a cereal based fermented staple food. J. Cereal Sci. 2019, 87, 225–230. [CrossRef]
87. Gotcheva, V.; Pandiella, S.S.; Angelov, A.; Roshkova, Z.; Webb, C. Monitoring the fermentation of the
traditional Bulgarian beverage boza. Int. J. Food Sci. Technol. 2001, 36, 129–134. [CrossRef]
88. Mustafa, K.D.; Adem, E. Comparison of autoclave, microwave, IR and UV-stabilization of whole wheat flour
branny fractions upon the nutritional properties of whole wheat bread. J. Food Sci. Technol. 2014, 51, 59–66.
Molecules 2020, 25, 927 17 of 19

89. Struyf, N.; Laurent, J.; Verspreet, J.; Verstrepen, K.J.; Coutrin, C.M. Saccharomyces cerevisiae and Kluyveromyces
marxianus cocultures allow reduction of fermentable oligo-, di-, and monosaccharides and polyols levels in
whole wheat bread. J. Agric. Food Chem. 2017, 65, 8704–8713. [CrossRef] [PubMed]
90. García-Mantrana, I.; Yebra, M.J.; Haros, M.; Monedero, V. Expression of bifidobacterial phytases in Lactobacillus
casei and their application in a food model of whole-grain sourdough bread. Int. J. Food Microbiol. 2016, 216,
18–24. [CrossRef] [PubMed]
91. Dey, T.B.; Kuhad, R.C. Enhanced production and extraction of phenolic compounds from wheat by solid-state
fermentation with Rhizopus oryzae RCK2012. Biotechnol. Rep. 2014, 4, 120–127.
92. Starzyńska-Janiszewska, A.; Stodolak, B.; Socha, R.; Mickowska, B.; Wywrocka-Gurgul, A. Spelt wheat tempe
as a value-added whole-grain food product. LWT-Food Sci. Technol. 2019, 113, 108250. [CrossRef]
93. Nuobariene, L.; Cizeikiene, D.; Gradzeviciute, E.; Hansen, A.S.; Rasmussen, S.K.; Juodeikiene, G.;
Vogensen, F.K. Phytase-active lactic acid bacteria from sourdoughs: Isolation and identification. LWT-Food
Sci. Technol. 2015, 63, 766–772. [CrossRef]
94. Adebo, O.A.; Njobeh, P.B.; Mulaba-Bafubiandi, A.F.; Adebiyi, J.A.; Desobgo, Z.S.C.; Kayitesi, E. Optimization
of fermentation conditions for ting production using response surface methodology. J. Food Proc. Preserv.
2018, 42, e13381. [CrossRef]
95. Salar, R.K.; Certik, M.; Brezova, V. Modulation of phenolic content and antioxidant activity of maize by
solid state fermentation with Thamnidium elegans CCF 1456. Biotechnol. Bioprocess Eng. 2012, 17, 109–116.
[CrossRef]
96. Hole, A.S.; Rud, I.; Grimmer, S.; Sigl, S.; Narvhus, J.; Sahlstrøm, S. Improved bioavailability of dietary
phenolic acids in whole grain barley and oat groat following fermentation with probiotic Lactobacillus
acidophilus, Lactobacillus johnsonii, and Lactobacillus reuteri. J. Agric. Food Chem. 2012, 60, 6369–6375. [CrossRef]
97. Liukkonen, K.H.; Katina, K.; Wilhelmsson, A.; Myllymaki, O.; Lampi, A.M.; Kariluoto, S.; Piironen, V.;
Heinonen, S.M.; Nurmi, T.; Adlercreutz, H.; et al. Process-induced changes on bioactive compounds in
whole grain rye. Proc. Nutr. Soc. 2003, 62, 117–122. [CrossRef]
98. Katina, K.; Liukkonen, K.H.; Kaukovirta-Norja, A.; Adlercreutz, H.; Heinonen, S.M.; Lampi, A.M.;
Pihlava, J.M.; Poutanen, K. Fermentation-induced changes in the nutritional value of native or germinated
rye. J. Cereal Sci. 2007, 46, 348–355. [CrossRef]
99. Skrajda-Brdak, M.; Konopka, I.; Tańska, M.; Czaplicki, S. Changes in the content of free phenolic acids and
antioxidative capacity of wholemeal bread in relation to cereal species and fermentation type. Eur. Food Res.
Technol. 2019, 245, 2247–2256. [CrossRef]
100. Mohapatra, D.; Patel, A.S.; Kar, A.; Deshpande, S.S.; Tripathi, M.K. Effect of different processing conditions
on proximate composition, anti-oxidants, anti-nutrients and amino acid profile of grain sorghum. Food Chem.
2019, 271, 129–135. [CrossRef] [PubMed]
101. Ðordevic, T.M.; Šiler-Marinkovic, S.S.; Dimitrijevic-Brankovic, S.I. Effect of fermentation on antioxidant
properties of some cereals and pseudo cereals. Food Chem. 2010, 119, 957–963. [CrossRef]
102. Ripari, V.; Bai, Y.; Gänzle, M.G. Metabolism of phenolic acids in whole wheat and rye malt sourdoughs. Food
Microbiol. 2019, 77, 43–51. [CrossRef]
103. Dey, T.B.; Kuhad, R.C. Upgrading the antioxidant potential of cereals by their fungal fermentation under
solid-state cultivation conditions. Lett. Appl. Microbiol. 2014, 59, 493–499.
104. Gänzle, M.G. Enzymatic and bacterial conversions during sourdough fermentation. Food Microbiol. 2014, 37,
2–10. [CrossRef]
105. Katina, K.; Juvonen, R.; Laitila, A.; Flander, L.; Nordlund, E.; Kariluoto, S.; Piironen, V.; Poutanen, K.
Fermented wheat bran as a functional ingredient in baking. Cereal Chem. 2012, 89, 126–134. [CrossRef]
106. Czerny, M.; Schieberie, P. Important aroma compounds in freshly ground whole meal and white wheat
flour-identification and quantitative changes during sourdough fermentation. J. Agric. Food Chem. 2002, 50,
6835–6840. [CrossRef]
107. Rodríguez, H.; Curiel, J.A.; Landete, J.M.; de las Rivas, B.; de Felipe, F.L.; Gomez-Cordoves, C.; Mancheno, J.M.;
Munoz, R. Food phenolics and lactic acid bacteria. Int. J. Food Microbiol. 2009, 132, 79–90. [CrossRef]
108. Svensson, L.; Sekwati-Monang, B.; Lutz, D.L.; Schieber, A.; Gänzle, M.G. Phenolic acids and flavonoids in
nonfermented and fermented red sorghum (Sorghum bicolor (L.) Moench). J. Agric. Food Chem. 2010, 58,
9214–9220. [CrossRef] [PubMed]
Molecules 2020, 25, 927 18 of 19

109. Sánchez-Maldonado, A.F.; Schieber, A.; Gänzle, M.G. Structure-function relationships of the antibacterial
activity of phenolic acids and their metabolism by lactic acid bacteria. J. Appl. Microbiol. 2011, 111, 1176–1184.
[CrossRef] [PubMed]
110. Raccach, M. The antimicrobial activity of phenolic antioxidant in food: A review. J. Food Saf. 1984, 6, 141–170.
[CrossRef]
111. Filannino, P.; Bai, Y.; Di Cagno, R.; Gobbetti, M.; Gänzle, M.G. Metabolism of phenolic compounds by
Lactobacillus spp. during fermentation of cherry juice and broccoli puree. Food Microbiol. 2015, 46, 272–279.
[CrossRef] [PubMed]
112. Gaur, G.; Oh, J.H.; Filannino, P.; Gobbetti, M.; van Pijkeren, J.P.; Gänzle, M.G. Genetic determinants of
hydroxycinnamic acid metabolism in heterofermentative lactobacilli. Appl. Environ. Microbiol. 2019.
[CrossRef] [PubMed]
113. Kurutas, E.B. The importance of antioxidants which play the role in cellular response against
oxidative/nitrosative stress: Current state. Nutr. J. 2016, 15, 71. [CrossRef] [PubMed]
114. Slavin, J. Why whole grains are protective: Biological mechanisms. Proc. Nutr. Soc. 2003, 62, 129–134.
[CrossRef]
115. Verma, B.; Hucl, P.; Chibbar, R.N. Phenolic content and antioxidant properties of bran in 51 wheat cultivars.
Cereal Chem. 2008, 85, 544–549. [CrossRef]
116. Sevgi, K.; Tepe, B.; Sarikurkcu, C. Antioxidant and DNA damage protection potentials of selected phenolic
acids. Food Chem. Toxicol. 2015, 77, 12–21. [CrossRef]
117. Wattenberg, L.W. Chemoprevention of cancer. Cancer Res. 1985, 45, 1–8. [CrossRef]
118. Slavin, J.L. Mechanisms for the impact of whole grain foods on cancer risk. J. Am. Coll. Nutr. 2000, 19,
300S–307S. [CrossRef] [PubMed]
119. Ghasemzadeh, A.; Ghasemzadeh, N. Flavonoids and phenolic acids: Role and biochemical activity in plants
and human. J. Med. Plants Res. 2011, 5, 6697–6703. [CrossRef]
120. Juurlink, B.H.J.; Azouz, H.J.; Aldalati, A.M.Z.; AlTinawi, B.M.H.; Ganguly, P. Hydroxybenzoic acid isomers
and the cardiovascular system. Nutr. J. 2014, 13, 63. [CrossRef] [PubMed]
121. Beta, T.; Nam, S.; Dexter, J.E.; Sapirstein, H.D. Phenolic content and antioxidant activity of pearled wheat
and roller-mill fractions. Cereal Chem. 2005, 82, 390–393. [CrossRef]
122. Kim, K.H.; Tsao, R.; Yang, R.; Cui, S.W. Phenolic acid profiles and antioxidant activities of wheat bran extracts
and the effect of hydrolysis conditions. Food Chem. 2006, 95, 466–473. [CrossRef]
123. Li, L.; Shewry, P.R.; Ward, J.L. Phenolic acids in wheat varieties in the HEALTHGRAIN diversity screen.
J. Agric. Food Chem. 2008, 56, 9732–9739. [CrossRef]
124. Khan, R.A.; Khan, M.R.; Sahreen, S.; Ahmed, M. Evaluation of phenolic contents and antioxidant activity of
various solvent extracts of Sonchus asper (L.) Hill. Chem. Central J. 2012, 6, 12. [CrossRef]
125. Sun, T.; Ho, C.T. Antioxidant activities of buckwheat extracts. Food Chem. 2005, 90, 743–749. [CrossRef]
126. Dai, J.; Mumper, R. Plant phenolics: Extraction, analysis and their antioxidant and anticancer properties.
Molecules 2010, 15, 7313–7352. [CrossRef]
127. Žilić, S.; Serpen, A.; Akıllıoğlu, G.; Janković, M.; Gökmen, V. Distributions of phenolic compounds, yellow
pigments and oxidative enzymes in wheat grains and their relation to antioxidant capacity of bran and
debranned flour. J. Cereal Sci. 2012, 56, 652–658. [CrossRef]
128. Benedetti, S.; Primiterra, M.; Tagliamonte, M.C.; Carnevali, A.; Gianotti, A.; Bordoni, A.; Canestrari, F.
Counteraction of oxidative damage in the rat liver by an ancient grain (Kamut brand khorasan wheat).
Nutrition 2012, 28, 436–441. [CrossRef] [PubMed]
129. Alam, M.N.; Bristi, N.J.; Rafiquzzaman, M. Review on in vivo and in vitro methods evaluation of antioxidant
activity. Saudi Pharm. J. 2013, 21, 143–152. [CrossRef] [PubMed]
130. Verni, M.; Verardo, V.; Rizzello, C.G. How fermentation affects the antioxidant properties of cereals and
legumes. Foods 2019, 8, 362. [CrossRef] [PubMed]
131. Gianotti, A.; Danesi, F.; Verardo, V.; Serrazanetti, D.I.; Valli, V.; Russo, A.; Riciputi, Y.; Tossani, N.; Caboni, M.F.;
Guerzoni, M.E.; et al. Role of whole grain in the in vivo protection from oxidative stress. Front. Biosci. 2011,
16, 1609–1618. [CrossRef] [PubMed]
132. Moore, J.; Cheng, Z.; Hao, J.; Guo, G.; Liu, J.G.; Lin, C.; Yu, L.L. Effects of solid state yeast treatment on the
antioxidant properties and protein and fiber compositions of common hard wheat bran. J. Agric. Food Chem.
2007, 55, 10173–10182. [CrossRef] [PubMed]
 Molecules 2020, 25, 927 19 of 19

133. Combest, S.; Warren, C. Perceptions of college students in consuming whole grain foods made with brewers’
spent grain. Food Sci. Nutr. 2018, 7, 225–237. [CrossRef]
134. Kuznesof, S.; Brownlee, I.A.; Moore, C.; Richardson, D.P.; Jebb, S.A.; Seal, C.J. WHOLEheart study participant
acceptance of wholegrain foods. Appetite 2012, 59, 187–193. [CrossRef]
135. Kamar, M.; Evans, C.; Hugh-Jones, S. Factors influencing adolescent whole grain intake: A theory-based
qualitative study. Appetite 2016, 101, 125–133. [CrossRef]
136. Chea, M.; Mobley, A.R. Factors associated with identification and consumption of whole-grain foods in a
low-income population. Curr. Dev. Nutr. 2019, 3, nzz064. [CrossRef]

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