You are on page 1of 12

Hypotheses in Food Science

Composition and Nutrient Value Proposition


Concise Reviews &

of Brewers Spent Grain


Sana Ikram, LianYan Huang, Huijuan Zhang, Jing Wang , and Meng Yin

Abstract: Brewer’s spent grain (BSG), a major brewing industry byproduct, is generated in large quantities annually.
This review summarizes research into the composition and preservation of BSG, different extraction techniques for BSG
proteins and phenolic acids, and the bioactivities of these phenolic components. Moreover, this article also highlights
BSG integration into foodstuff for human consumption and animal feed supplements. BSG is considered a rich source
of fiber, protein, and phenolic compounds. The phenolic acids present in BSG are hydroxycinnamic acids (ferulic, p-
coumaric, and caffeic acids), which have many biofunctions, such as antioxidant, anticarcinogenic, antiatherogenic, and
antiinflammatory activities. Previously, attempts have been made to integrate BSG into human food, such as ready-to-eat
snacks, cookies and bread, to increase fiber and protein contents. The addition of BSG to animal feed leads to increased
milk yields, higher fat contents in milk, and is a good source of essential amino acids. Therefore, many studies have
concluded that integrating the biofunctional compounds in BSG into human food and animal feed has various health
benefits.

Keywords: antioxidant activity, Brewer’s spent grain, phenolic compound

Introduction fractions and its hydrolysates has shown anti-inflammatory impact


Brewer’s spent grain (BSG) is an insoluble solid residue obtained in Jurkat T cells.
after wort production, and is the most abundant brewing indus- In the last few years, BSG for human consumption has gained
try byproduct (Aliyu and Bala 2011), comprising 85% of total attention, mainly because of its health-related bioactive compo-
byproducts generated (Tang and others 2009). Almost 3.4 million nents. These bioactive compounds include secondary metabolites,
tons of BSG are produced annually by the brewing industry in the such as alkaloids, antibiotics, plant growth factors, food-grade pig-
European Union (Stojceska and Ainsworth 2008). Despite being ments, and phenolic acids (Martins and others 2011). BSG is con-
readily available, BSG receives little attention in industry and is sidered the major source of phenolic compounds, particularly hy-
traditionally only used in animal feed (Xiros and others 2008). droxycinnamic acids (HCAs), which include ferulic, p-coumaric,
This underutilization is due to its complex composition and high sinapic, and caffeic acids (Faulds and others 2002; Szwajgier and
moisture content, which make it difficult to store and transport. others 2010). These phenolic compounds are considered natu-
Moreover, it is commonly considered a waste material because of ral antioxidants, which have been associated with prevention of
the risk of rapid microbiological degradation (Robertson and oth- Crowley age-associated chronic diseases, such as cardiovascular
ers 2010). The shelf life of BSG ranges from 7 to 10 d in warm cli- diseases, neurogenerative diseases, diabetes (types І and ІІ), and
mates because of its high water content, of around 70% (Mussatto certain cancers (Naczk and Shahidi 2004; Barbosa-Pereira and
and others 2006). As readily available low-cost biomass, BSG re- others 2013; Connolly and others 2014). The importance of BSG
mains an important resource in industrial development (Robertson antioxidant phenolic acids and a integration of BSG as an in-
and others 2010). BSG is considered a lignocellulosic material, gredient into human and animal food stuff were also highlighted
containing approximately 20% protein and 70% fiber (Mussatto (Aliyu and Bala 2011; Mccarthy and others 2013c). BSG is also
and others 2006). Recently, Vieira and others (2014) treated BSG considered a source of dietary fiber for humans, especially viscous
with increasing concentrations of 0.1M, 0.5M, and 4M alkali fibers, which aid in an increasing cholesterol and fat excretion, ac-
(NaOH or KOH) solutions to obtain the protein-rich isolates and celerating transit time, increasing fecal weight (Zhang and others
arabinoxylans (AX), which result a yield of 82% to 85% of the 1991), and improving ulcerative colitis (UC) symptoms (Kanauchi
total BSG proteins and 66% to 73% of total AX. Moreover, BSG and Agata 1997). The incorporation of BSG as an ingredient in
protein and its hydrolysates have shown selective immunomodu- the formulation of extruded snacks and breadsticks products also
latory effects, which may be useful in controlling inflammatory have shown increased levels of bioactive antioxidants and AX and
diseases (McCarthy and others 2013a). In addition, Crowley and with low glycaemic index (Reis and Abu-Ghannam 2014). Scien-
others (2015) also reported that simulated gastrointestinal diges- tists are now searching for natural resources, such as agroindustrial
tion (SGID) milk product supplemented with BSG protein rich residues, plants, vegetables, and fruits, which are efficient sources
of phenolic compounds. Furthermore, there is an increasing in-
terest in efficiently replacing some synthetic antioxidants that are
JFDS-2017-0096 Submitted 1/15/2017, Accepted 5/30/2017. Authors Ikram, carcinogenic and toxic with natural plant resources (Bouayed and
Huang, Zhang, Wang, and Yin are with Innovation Center for Food Nutrition Bohn 2010).
and Human Health, China. Author Wang is also with Beijing Engineering and This review aims to present potential extraction techniques used
Technology Research Center of Food Additives, Beijing Technology & Business Univ. to obtain proteins and phenolic compounds from BSG, to increase
(BTBU), Beijing 100048, China. Direct inquiries to authors Zhang and Wang
(E-mail: zhanghuijuan@th.btbu.edu.cn and wangjing@th.btbu.edu.cn). the novel applications of antioxidant phenolic compounds, such as
ferulic acid and p-coumaric acid, found in BSG. We also discuss the
feasibility of introducing BSG into different foodstuffs, along with

C 2017 Institute of Food Technologists


 R

2232 Journal of Food Science r Vol. 82, Nr. 10, 2017 doi: 10.1111/1750-3841.13794
Further reproduction without permission is prohibited
Hypotheses in Food Science
Composition and preservation of BSG . . .

Concise Reviews &


its use as a food supplement for both humans and animals. Several 21.5% of the total protein content. Previously, glutelin proteins
studies have been conducted to investigate the health benefits of were little known because of difficulties in separating the pure
BSG, and this review endeavors to summarize the recent advances undenatured fraction under the complex extraction conditions
regarding the potential health benefits of BSG. required. Traditionally, dilute alkali is used to separate glutelins in
the presence of a reducing agent, but chaotropic agents and/or
BSG Composition detergents have also been used (Shewry 1993; Celus and others
BSG is mainly composed of the husk pericarp and seed coat, 2006; Tatham and Shewry 2012). The most abundant proteins in
which is a rich source of lignin, cellulose, hemicellulose, lipids, BSG are hordeins, also known as prolamins because of their high
and protein (Mussatto and Roberto 2006; Aliyu and Bala 2011). proline and glutamine contents, which represent 43% of the pro-
According to Mussatto and Roberto (2006), BSG can be re- tein content and are traditionally separated with alcohols in the
garded as a lignocellulosic material, with cellulose (a linear ho- presence of a reducing agent. Hordeins have been further classi-
mopolymer of glucose units), hemicellulose, and lignin (a polyphe- fied, according to their molecular weights, as B (30 to 50 kDa),
nolic macromolecule) containing almost 50% (w/w) BSG, as C (55 to 80 kDa), and D hordeins (95 kDa). D hordeins are
reflected in Table 1. Components, on a dry-weight basis, include a found in barley grain, but not in BSG, because of their rapid
large amount of monosaccharides, including appreciable quantities degradation during the malting process. BSG is also a good source
of glucose, xylose, and arabinose (Table 1). Hemicellulose, which of essential and nonessential amino acids (Huige 2006; Mussatto
mainly consists of arabinoxylan (AX), is the prime component of and others 2006). The essential amino acids in BSG are methion-
BSG and can be present up to 40% on dry weight basis (Mandalari ine, phenylalanine, tryptophan, histidine, and lysine, whereas the
and others 2005). AX is the major noncellulose polysaccharide nonessential amino acids are serine, alanine, glycine, and proline
in cereals and grasses. The reported study has proposed the at- is the most abundant amino acids present in barley (B, C, and D)
tachment of AX with the cellulose fibrils via hydrogen bonding hordeins (Huige 2006; Mussatto and others 2006). Other authors
(Mandalari and others 2005). β-(1,4)-Linked xylose residues are also mentioned the presence of a high amount of leucine (Leu) as
said to be the backbone of AX, and arabinose residues can sub- an essential amino acid and glutamine (Glx) and asparagines (Asx)
stitute this backbone, where ferulic acid can be esterified to ara- as nonessential amino acids in BSG (Mussatto and others 2006;
binose (Mendis and Simsek 2014). AX chains can be cross-linked Coelho and others 2016). As mentioned above, BSG is a ligno-
via Diferulic acid bridges (Mandalari and others 2005). Moreover, cellulosic material rich in dietary fiber, which comprises polysac-
Coelho and others (2016) discovered that AX in BSG contains ara- charides and lignin resistant to hydrolysis by small bowel digestive
binose residues at terminals and that additional functional groups enzymes. Dietary fiber consists of complex groups of compounds
can be present, substituents like, uronic acid, hexose, methylated that are further classified by solubility; the soluble dietary fiber
uronic acid, and acetyl groups are worth mentioning additional includes β-glucans, pectic polysaccharides, arabinogalactans, high
groups here. Another abundant polysaccharide in BSG is cellu- branched AX, and xyloglucans, although insoluble dietary fiber
lose (β-(1,4)-linked glucose residues) and (1-3,1-4)-β-d-glucan includes lignin, cellulose, and low branched AX, xyloglucans, and
and starch may also present in low levels. Xylose, glucose, and galactomannans (Kanauchi and Agata 1997).
arabinose are the most abundant monoglycans in BSG, whereas In the last few years, much research has been conducted on
lesser amounts of rhamnose and galactose have also been found germinated barley foodstuff (GBF), a BSG product that is milled
(Mandalari and others 2005; Forssell and others 2008). Lignin is and sieved to obtain a glutamine-rich protein and dietary fiber-
another noteworthy constituent of BSG, forming 10% to 28% enriched product. Kanauchi and Agata (1997) have described the
of the total dry weight. The structural integrity and rigidity of process in detail. GBF is used to treat patients with inflamma-
plant cell wall is maintained by lignin which is a poly-phenolic tory bowel diseases (IBDs), particularly UC, GBF showed anti-
macromolecule (Mussatto and Teixeira 2010; Mussatto 2014). The inflammatory effect by changing microflora, such asEubacterium,
complex lignin is constituted from 3 monomers sinapyl alcohol, Bifidobacterium, and Lactobacillus species increases the level of bu-
coniferyl alcohol, and p-coumaryl alcohol that are linked to- tyrate production, which is instant fuel for mucosa (Jacobasch
gether by radical induced condensation reactions in a branched and others 1999; Bamba and others 2002; Kanauchi and others
network structure (Niemi and others 2013). In addition, Lignin 2003). Faghfoori and others (2011) reported that a short-chain
also contains a considerable amount of phenolic components, in- fatty acid (butyrate) can inhibit the production and release of cy-
cluding mainly ferulic, p-coumaric, vanillic, hydroxybenzoic, and tokines Tumor Necrosis Factor-α (TNF-α), contributing to the
syringic acids (Bartolome and Gomez-Cordoves 1999; Mussatto antiinflammatory impact of fiber.
and Roberto 2006). The barley grain husk also contains a large
amount of silica. Kunze (1996) reported that about 25% of min- Vitamins and Minerals
erals present in barley are represented as silicates. BSG contains a considerable quantity of vitamins, including
folic acid, niacin, biotin, thiamine, choline, pantothenic acid, ri-
BSG Fiber and Protein boflavin, and pyridoxine. Most studies performed on the vita-
BSG is considered a good source of protein and fiber. Mussatto mins of BSG focus on tocochromanols that comprise tocotrienols
and others (2006) have identified BSG as being 15% to 25% protein and tocopherols, commonly known as vitamin E. These vitamins
Santos and others (2003) found that, oven-dried BSG also con- form a class of lipid-soluble antioxidants that are only synthesized
tained 15% to 24.2% protein and 3.9% ash, similar to the original by plants and other photosynthetic organisms. Tocochromanols
barley grain, including globulins, albumins, glutelins, and hordeins. act as antioxidants (Burton and Traber 1990), decreasing serum
These proteins were subdivided by their sequential extractabilities LDL cholesterol in swine, chickens, and humans (Qureshi and
(Osborne 1924). Using the aqueous wort extraction technique others 1986; Qureshi and others 1991a, b). They can also act
during the brewing process, small amounts of salt- and water- as anticarcinogenic agents and exhibit neuroprotective properties
soluble globulins and albumins are extracted from BSG (7.5% (Pryma and others 2007; Sen and others 2010). According to
of the total protein content). In BSG, glutelins represent about Meneses and others (2013), the most abundant minerals in BSG

Vol. 82, Nr. 10, 2017 r Journal of Food Science 2233


Hypotheses in Food Science
Concise Reviews & Composition and preservation of BSG . . .

Table 1–BSG’s composition.

Components on (g/kg) dry weight basis


Cellulose Hemicellulose
Proteins Ashes Lignin (glucose) (Xyl) (Ara) Study conducted
153 46 278 168 199 85 (Mussatto and Roberto 2006)
240 24 119 254 NR NR (Kanauchi and others 2001)
246 12 217 219 206 90 (Carvalheiro and others 2004)
NR 46 169 253 NR NR (Silva and others 2004)
247 42 194 217 136 56 (Moreira and others 2013)
Ara, arabinose; NR, not reported; Xyl, xylose.

are calcium (3600 mg/kg), magnesium (1900 mg/kg), phospho- 2 d dropped moisture to about 10%. Moreover, researchers noted
rus (6000 mg/kg), and (2900 mg/kg), and sodium (137 mg/kg). no bacterial growth when the resultant BSG cakes were stored in
Other minerals present in BSG include iron, copper, potassium, open air for 6 mo after this process.
and manganese (Mussatto 2009). More research is needed to develop economically viable meth-
BSG also contains waxes, resins, tannins, essential oils, and lipid ods for drying-up BSG without compromising flavor and aroma,
contents of between 5.8% and 11.0% (Brigas and others 1981). or affecting the BSG nutritional quality. Furthermore, novel tech-
Among these lipids, triglyceride levels are the highest (approxi- niques should be established to improve the shelf-life of BSG
mately 55%), followed by fatty acids (approximately 30%; Mussatto without affecting its composition.
and Roberto 2005).
Protein Extraction from BSG
BSG Preservation and Storage Techniques Many protein extraction studies conducted on BSG involved
Recently, several methods have been suggested for prolonged sodium dodecyl sulfate (SDS) and alkali as the extraction solvent at
BSG storage, to make BSG an economically viable and commer- high temperatures, followed by ethanol precipitation or isoelectric
cially viable product. BSG has a water content of around 77% to precipitation. Furthermore, nitrogenous materials in BSG have
81% (w/w), but different portions of the grain contain different been solubilized by using different solvents, such as water, aqueous
moisture levels (Santos and others 2003; Russ and others 2005; solution, alkaline and acidic solutions. Diptee and others (1989)
Mussatto and others 2006). used dried BSG to extract a 60% protein-enriched isolate using
BSG is considered an unstable material, deteriorating quickly 0.6% Na2 HPO4 for 95 min at 95 °C.
because of its high moisture and sugar content. Therefore, drying BSG has also been used to obtain a protein-enriched isolate via
is considered the most effective preservation method for reducing a mechanical process, using sieving combined with pressing in the
storage and transportation costs (Santos and others 2003; Tang presence of water, to separate 60% protein and dietary fiber from
and others 2004; Mussatto and others 2006; Tang and others BSG (Kishi and others 1992a, b). Townsley (1979) used a num-
2009). Currently, brewing companies use special plants to per- ber of milling steps to produce a protein-enriched isolate, which
form “drying up,” a 2-step drying process. The 1st step uses a was further modified by Kanauchi and Agata (1997), who added
pressing technique to reduce the moisture level to 65% or below, sieving and drying processes to produce GBF with a 46% protein
whereas the second step uses a drying-up technique to further de- content. Protein isolate was also extracted using a sieving process
creases the moisture content to below 10% (Tang and others 2004; with different combinations of solvents, such as SDS, dithiothre-
Mussatto and others 2006). This conventional method uses drum itol, 1-propanol and urea, to obtain 60% protein-enriched isolates
rotary dryers, an energy-intensive technique (Tang and others (Celus and others 2006). As a further modification, Celus and
2004). Bartolome and others (2002) compared 3 methods to pre- others (2007) treated BSG with 0.1 mM NaOH alkaline solu-
serve BSG, namely freezing, freeze drying, and oven drying. Their tion to extract protein-enriched isolate that had 60% total protein
study showed that preservation by freeze drying and oven drying content. Jay and others (2008) studied extracting protein isolate
decreased the product volume without changing its composition. from BSG with a combination of sieving processes to separate
Freezing was not an economical method, with a large volume re- about (<53 µm) protein-rich particles. Tang and others (2009)
quired for storage, although oven drying technique had also some also investigated the impact of ultrafiltration on protein recovery
limitations, with temperatures above 60 °C leading to flavor de- from BSG, which resulted in a lower protein content of about
terioration and brown discoloration (Mussatto and others 2006). 20.90%. Recently, Vieira and others (2014) also treated BSG with
Tang and others (2005) used a cost-effective preservation tech- increasing concentrations of 0.1M, 0.5M, and 4M alkali (NaOH
nique involving a superheated system for thin layer drying. This or KOH) solutions for 24 h at room temperature to obtain the
technique saved energy by circulating the superheated steam in protein-rich isolates the alkaline extracts were acidified with cit-
a closed loop. The superheated steam method also has additional ric acid to pH3 and AX were recovered by ethanol precipitation,
advantages, such as efficient drying, low carbon emissions, no ex- which result a yield of 82% to 85% of the total BSG proteins and
plosion risk, and vital organic compound recovery (Tang and oth- 66% to 73% of total AX.
ers 2004; Tang and others 2005). In a pilot plant study, El-Shafey Protein extraction from BSG was also achieved using enzymatic
and others (2004) proposed a new method using a membrane filter hydrolysis, in which BSG was treated with commercially available
press. During this process, BSG is thoroughly mixed in water, fil- proteinases to extract about 77% protein isolates at pH 8.0 (Forssell
tered at a pressure of 45 to 75 psi, and washed with water at 65 °C. and others 2008; Treimo and others 2008). Recently, Niemi and
Then filtered through nylon membrane and vacuum-dried to re- others (2012) reported treating BSG with alkaline proteinase, pro-
duce the moisture levels up to 20% to 30% and then air drying for ducing approximately 76% protein-enriched isolate. To enhance

2234 Journal of Food Science r Vol. 82, Nr. 10, 2017


Hypotheses in Food Science
Composition and preservation of BSG . . .

Concise Reviews &


Table 2–Major phenolic acids in BSG. Techniques and Treatments used to Release Pheno-
Concentration of major phenolic acid (mg per 100g dry matter) lic Compounds and other Constituent Components
Phenolic compounds Mean SE
from BSG
In this section, common techniques and treatments used for
Ferulic acid 336.3 16 the extraction and recovery of major phenolic acids and other
p-Coumaric acid 64.4 4.6
Sinapic acid 42 1.1
components from BSG are discussed. Contemporary studies have
Caffeic acid 9.9 0.7 relied on advanced extraction methods, such as microwave-assisted
Syringic acid 6.5 0.1 extraction (Mallouchos and others 2007), acid hydrolysis, saponi-
fication with 1 to 4 M NaOH, and liquid–liquid or solid–liquid
extraction techniques (Stalikas 2007). Acid hydrolysis and saponifi-
Table 3–Free and bound phenolic acids in BSG.
cation methods have been used more frequently in natural plants to
Concentration of free and bound acid (µg per 100 g dry matter) separate, detect, and extract proteins, carbohydrates, and phenolic
Phenolic acids Free phenolic acids Bound phenolic acids acids (Stalikas 2007; Xiros and Christakopoulos 2012). Tradition-
ally, solid–liquid extraction was used to extract phenolic acids from
Catechin 1.08 ± 0.04 NR BSG, because of its ease of use, high efficiency, and wide appli-
Epicatechin NR NR
Quinic acid 2.50 ± 0.07 1.30 ± 0.40 cability (Bonoli and others 2004; Teixeira and others 2006; Vatai
Gallic acid 0.42 ± 0.03 NR and others 2009; Guo and Beta 2013). Hot water bath extraction
p-Coumaric acid 0.48 ± 0.06 652.27 ± 160.5 was another method used by Meneses and others (2013) to extract
Ferulic acid 0.72 ± 0.51 3739.42 ± 270.80 phenolic acids from BSG, using different mixed solvents, includ-
NR, not reported. ing methanol, acetone, ethanol, hexane, ethyl acetate, and water.
The extract produced with acetone: water 60% (v/v) contained
the highest total content of phenols (9.90 ± 0.41 mgGAE /g dry
matter). Enzymatic hydrolysis was another solid–liquid technique
used for the extraction of phenolic compounds and other compo-
nents of BSG. Moreover, enzymatically produced fractions were
more possible to retain bioactivity and their novel food applica-
tions would be seen more favorably compared with chemically
extracted compounds. In addition, another advantage was that
they were more environmentally friendly as they did not create
any toxics (Mussatto 2014). Considering the complex structure of
Ferulic Acid (C10H10O4) R = OCH3 BSG polymers, for example, hemicellulose fractions (presence of
p-Coumaric Acid (C9H8O3) R = H many substituted groups and bond linkages on polymer), a wide
range of enzymes was needed to complete the process of hydrol-
ysis. For example, feruloyl esterases, acetyl esterases, xylanases,
Figure 1–Structures of major phenolic acids present in BSG (p-coumaric
and ferulic acids). β-xylosidases, α-L-arabinofuransidases, and glucuronoyl esterases
were the main enzymes needed for the process of hemicellulose
the possible applications of insoluble proteins separated from BSG, degradation. Many studies used enzymatic hydrolysis for major
protein hydrolysis has proved to be an effective technique for ex- phenolic compounds and various fractions of BSG are shown in
traction. Table 4 (Szwajgier and others 2010) reported that phenolic acid
was released from BSG using ferulic acid esterase from lactobacillus
acidophilus K1, although ferulic acid and p-coumaric acid con-
Phenolic Profile of BSG tents were 7.00 ± 0.07 and 1.88 ± 0.10 mg, respectively, from
Phenolic acids, mainly hydroxybenzoic acids (HBAs), and hy- 100 g of BSG. In a recent study, Coelho and others (2014) used
droxycinnamic acids (HCAs), are plant secondary metabolites microwave super-heated water and dilute alkali extraction tech-
mostly found in plant foods. Phenolic acids are popular subjects of nique to extract AX and arabinoxylo-oligosaccharides (AXOS)
research because of their anticarcinogenic, antiinflammatory, and from BSG, which were also effective antioxidants and potent rad-
antioxidant properties (Mussatto and others 2006). ical scavengers. The obtained results showed that the yield of AX
BSG is considered an important source of phenolic acids because and AXOS was 43% at 140 °C. Meanwhile, the total content of
the barley grain husk contains good quantities of phenolic com- polyphenols was 0.34 µM/mg and the antioxidant activity was
pounds (Mussatto and others 2006; Figure 1), with p-coumaric 208 µM/mg.
and ferulic acids present in high concentrations (Table 2). Studies A review of extraction and quantification methods for pheno-
reported that ferulic acid in BSG ranges from 1860 to 1948 µg/g, lic compounds in foods showed that alkaline hydrolysis (Table 5)
although p-coumaric acid content ranges from 565 to794 µg/g is also commonly used to extraction phenolic acids (Naczk and
(Hernanz and others 2001). The phenolic content of BSG also Shahidi 2004). Rich phenolic acid extracts from BSG have the
depends on the type of malt used (Moreira and others 2013; ability to act against genotoxic and oxidant effects in human lym-
McCarthy and others 2013b). Recent literature has shown that phocytic U937 cells (McCarthy and others 2012). BSG provided
most bioactive phenolic acids were present in bound form in BSG the highest ferulic acid content (27.31 ± 0.69 µg/mL) and to-
(Forssell and others 2008). Another Study have also reported that, tal phenolic content (0.732 ± 0.020 mgGAE /mL) when extracted
ferulic acid and p-coumaric acid were present in high concentra- with alkaline hydrolysis using 1 M NaOH.
tions in linked to AX and BSG also contains catechin, quinic and A new method used to extract free and bound phenolic acids
galic, and syringic acids in high quantity (Ktenioudaki and others from cereals, including barley, which applies an inexpensive and
2015; Table 3). simple solid-phase extraction method along with HPLC-diode

Vol. 82, Nr. 10, 2017 r Journal of Food Science 2235


Hypotheses in Food Science
Concise Reviews & Composition and preservation of BSG . . .

Table 4–Representing the effectiveness of enzyme preparations used to extract the phenolic acids and other components from
BSG by using enzymatic hydrolysis.

Hydrolysis
Enzyme preparation conditions Product released Yields (%) Study conducted
Viscozyme L (commercial 37 °C for 3 h Hydroxycinnamic acids FA(33) and p-CA(0.80) (Bartolome and
enzyme) Gomez-Cordoves
1999)
Lallzyme (commercial enzyme) 37 °C for 3 h Hydroxycinnamic acids FA(55) and p-CA(1.60)
Feruloyl esterase from (Aspergillus 37 °C for 3 h Hydroxycinnamic acids FA(3.30) and (Bartolome and others
niger) p-CA(NR) 2003)
Feruloyl esterase from (Aspergillus 37 °C for 3 h Hydroxycinnamic acids FA(30) and p-CA(NR)
niger) along with xylanase from
(Trichoderma viride)
Ultraflo L, α β-glucanase 37 °C for 3 h Hydroxycinnamic acids FA(65) and p-CA(9) (Faulds and others 2002,
preparation from (Humicola Faulds and others
insolens) 2004)
Feruloyl esterase from 37 °C for 3 h Hydroxycinnamic acids FA (7.00 ± 0.07
(Lactobacillus acidophilus) K1 mg/100g) and p-CA
(1.9 ±0.1 mg/100g)
Monoenzymes feruloyl esterase 37 °C for 3 h Hydroxycinnamic acids FA (49) and p-CA (NR) (Xiros and others 2013)
(ferulic acid esterase,
FoFaeC-12213) and xylanase
(Trichodemalongibrachiatum M3)
Crude enzyme extract from 37 °C for 3 h Ferulic acid FA (49) and p-CA (NR)
(Fusarium oxysporum)
Ultraflo L (commercial enzyme) 37 °C for 3 h Hydroxycinnamic acids FA (70) and p-CA (8) (Bartolome and others
2015)
Ferulic acid esterase along with 37 °C for 3 h Hydroxycinnamic acids FA (43) and p-CA (<9)
(xylanase) from (Sterptomyces
avermitilis CECT 3339)
Econase CE, Spezyme CP 50 °C for 5 h Hydroxycinnamic acids, FA (75) and (Forssell and others
(Dupont Genencor, USA) AXOS, Monosaccharides Monosaccharides(26 2008)
Depol 740 and 686 to 28)
Ultraflo N, Alcalase, Promod 40 °C for 24 h Solubilised BSG and Protein (50) and FA (Faulds and others 2008)
24L,184P,278P, and 439L Hydroxycinnamic acids (8.6)
crude enzyme extract from N/A Hydroxycinnamic acids and 8% of total content (Napolitano and others
(Trichoderma T. harzianuma XOS 2006)
and T. reesei)
NR, not reported.

Table 5–Summary of phenolic acids extract mainly ferulic acid and p-coumaric acid from BSG by alkaline extraction method.

Extraction conditions Ferulic acid content p-Coumaric acid content Reference


2M NaOH,16 h under N2 at 1948 ± 143 µg/g 794 ± 58 µg/g (Hernanz and others 2001)
20 °C
1MNaOH,16 h under N2 at 0.24% dry weight 0.121% dry weight (Bartolome and others 2002)
20 °C,
pre-treatment with H2 SO4 + 9.65 mg/g solubilized lignin 9.22 mg/g solubilized lignin (Mussatto and others 2007)
2% (0.5 M) NaOH, 120
°C, 90 min
1M NaOH,16 h RT, 27.3 ± 0.7 mg/mL NR (McCarthy and others 2013)
RT, room temperature; NR, not reported.

array detection analysis, has been explored, yielding accurate re- phenolic (0.35 ± 0.01 mg/g BSG) content and good antioxidant
coveries. Studies have shown that reverse-phase HPLC provides a properties (2.09 ± 0.04 %/g BSG). These results demonstrated
greater degree of separation and quantification of phenolic com- that reusing BSG is also a viable economic method for large-scale
pounds, with the most recent research using Luna C18 reverse extraction.
phase columns. This HPLC method established that ferulic acid Different extraction methods used for BSG have also been
is the most abundant phenolic acid in BSG, with p-coumaric used on other food materials, including rich wheat bran extracts
acid the second most abundant, although saponification with 1 (Table 6; Kim and others 2006) and apple waste extracts (McCann
to 4 M NaOH has been commonly used to extract HCAs from and others 2007).
BSG (Bartolome and Gomez-Cordoves 1999; Hernanz and others
2001; Faulds and others 2004). Spinelli and others (2016) devel- Novel Health Benefits of Major Phenolic Extracts
oped a new method to separate rich bioactive compounds from from BSG
BSG using supercritical carbon dioxide with EtOH cosolvent. In recent years, owing to the importance of natural bioactive
Results showed that an extraction temperature of 40 °C, time of compounds associated with human health, BSG has gained
240 min, and pressure of 35 MPa, with CO2 and 60% ethanol attention as a good source of natural phenolic acids because of
(v/v), were the best operating conditions for achieving a high its major phenolic acid contents. Ferulic acid has several possible

2236 Journal of Food Science r Vol. 82, Nr. 10, 2017


Table 6–Comparison of different extraction techniques used for BSG and other cereals.

Composition and preservation of BSG . . .


Individual phenolic content
Sample Methods Extraction conditions Total phenolic content (TPC) (IPC) Reference
BSG Solid–liquid extraction
Hot water bath extraction 60% acetone 9.90 mg GAE per dry BSG NR (Meneses and others 2013)
Alkaline hydrolysis Pre-treatment with H2 SO4 + NR FA (9.65 mg/g solubilized (Mussatto and others 2007)
2% (0.5 M) NaOH at lignin), p-CA (9.22 mg/g
120°C for 90 min solubilized lignin)
Supercritical-fluid 313 K, 35 Mpa NR Tocopherol (2 mg/L) (Fernández and others 2008)
extraction
Microwave-assisted water 140 °C for 2 min 0.34 µM/mg NR (Coelho and others 2014)
extraction
Barley Soxhlet extraction Ethyl acetate for 9 h 0.495 mgGAE /g extract 3,4-dihydroxybenzaldyde (3.07 (Conde and others 2008)
mg/g), Vanillin (2.23 mg/g),
p-CA (1.36 mg/g)
Solid-phase extraction Oasis HLB cartridges Free fraction (11.53 µg/g) Bound Free p-CA (0.97 µg/g); Bound (Irakli and others 2012)
fraction (485.06 µg/g) p-CA (75.9 6 µg/g)
Pressurized liquid 5 g sample, EtOH at 60 °C, 2.13 mgGAE /g NR (Bonoli and others 2004)
extraction 20 Mpa for10 min
Ultrasound assisted EtOH for 18 min at 50 °C 19.68 mgGAE /g NR (Wang and others 2013)
extraction
Accelerated solvent 4 g sample, 60% acetone, 60 Phenolic content (1346 µg/g), p-CA (374 µg/g), FA (696 (Holtekjølen and others 2006)
extraction °C, 200 bar Total DiFA (247 µg/g) µg/g), 5-5′ -DiFA (64 µg/g),
8-O-4′ -DiFA (79 µg/g),
8-5′ DiFA (104 µg/g), TriFA
(28 µg/g)
Barley roots Soxhlet extraction 0.3 g sample; 8 0% ethanol; 3.31 mg/g dry sample NR (Dudjak and others 2004)
20 h
Barley straw 50 g sample,1800mL hexane 2.05 % (wt/wt) Proto catechuic acid (0.12%), (Sun and Sun 2001)
acetone (2:1,vol/vol),12h p-CA (0.20%), FA (0.066%)
Out layers of barley Polyamide column 3618 µg/g 158 µg/g of Catechin fraction; (Quinde-Axtell and Baik 2006)
1339 µg/g dimeric fraction;
1455 µg/g of trimeric
fraction
Vol. 82, Nr. 10, 2017 r Journal of Food Science 2237

Roasted wheat germ Supercritical-fluid 2 g of sample, 240 bar, 6.63 mgGAE /g extract (4.8 mg/g) α-tocopherol, (Gelmez and others 2009)
extraction
at 56 °C, 20 min (2.4 mg/g) β-tocopherol,
(11.7 mg/g) γ -tocopherol
Distillers dried grains 0 12.02 mg/g NR (Inglett and others 2009)
Wheat bran Pressurized liquid 5 g, 0.5 M NaOH, NR (350 mg/100 g) p-CA, (Buranov and Mazza 2009)
extraction
at 180 °C, 5.2 Mpa, (2510 mg/100 g) FA
for 40 min
Microwave-assisted 10 g sample, 40 mL MeOH, Phenolic content (˃467.5 µg NR (Oufnac and others 2007)
extraction 20 min at 120 °C CE/g) tocopherol content
(19.5 µg/g)
Oat bran Microwave-assisted 10 g sample, 40mL n-Hexane, 1.98 mg GAE /g NR (Dar and Sharma 2013)
extraction 3.5 min at 60 °C, 2450
MHz
Rice bran 20 g sample, isopropanol, 15 NR (47.49 g/g) α-tocopherol, (7.29 (Zigoneanu and others 2008)
min at 120 °C g/g) γ -tocopherol
Corn bran Pressurized liquid 5 g, 0.5 M NaOH at 180 °C NR (350 mg/100 g) p-CA, (2510 (Buranov and Mazza 2009)
extraction for 40 min, 5.2 Mpa mg/100 g) FA
Brown black glutinous 2.5 g, 70% MeOH, RT, 1500 p-CA (1.06 mg/100 g), FA (Vichapong and others 2010)
rice psi at 15 min (5.27 mg/100 g)
NR, not reported.

Concise Reviews &


Hypotheses in Food Science
Hypotheses in Food Science
Concise Reviews & Composition and preservation of BSG . . .

applications because of its antioxidant, antiallergenic, anti- extracts, and exposed to the oxidants. The DNA damage was cal-
inflammatory, and preservative properties, whereas p-coumaric culated using the comet assay method. They found that ferulic
acid exhibits antioxidant and chemoprotectant properties (Bar- acid and black BSG extracts protected against oxidant-induced
tolome and others 2002; Mussatto and others 2007; Amarowicz DNA damage, demonstrating the potential antioxidant activity of
and others 2009; Dai and Mumper 2010; Barbosa-Pereira and oth- phenolic-rich BSG extracts. However, only a few in vivo studies
ers 2013; Meneses and others 2013; Connolly and others 2014). have attempted to clarify the antioxidant effects of HCAs. There-
fore, further studies are required to determine the biological role
Phenolic Acids as Antioxidants of these phenolic compounds (Shahidi and Chandrasekara 2010).
Recently, a beer study identified a direct association between
some phenolic compounds, including caffeic acid and syringic Phenolic Acids as Anticancer Agents
acid, and DPPH radical scavenging activity, metal chelation, su- In addition to their promising antioxidant effects, there is grow-
peroxide anions, and reducing power (Zhao and others 2010). ing evidence that these phenolic acids have anticarcinogenic activ-
Piazzon and others (2010) also found a link between the num- ities, with relevant animal studies having been conducted. Treating
ber of phenolic acids (ferulic, p-coumaric, caffeic, syringic, and a tumor breakthrough on the skin of mice with chlorogenic acid,
vanillic acids) and the ferric reducing antioxidant power assay. In ferulic acid, and caffeic acid blocked 60%, 28%, and 35% of 12-
addition, ferulic acid has attracted attention as an antioxidant, and O-tetradecanoylphorbol-13-acetate-induced tumors per mouse,
has been approved as a food preservative agent in many countries respectively (Huang and others 1988).
to prevent oxidation in certain foods (Itagaki and others 2009). Caffeic acid has been shown to have an antiproliferative effect on
Chen and Ho (1997) studied the antioxidant activity of ferulic cervical cancer cell lines using the 3-(4,5-dimethylthiazol-2-yl)-
acid in vitro and scavenged radicals using a superoxide anion and 2,5-diphenyltetra-zolium bromide (MTT) assay method (Chang
2,2-diphenyl-1-picrylhydrazyl assay. Kim and others (2006) used and others 2010), and on cancer cells in mammary glands, lym-
an alternative method (a model system of β-carotene and linoleic phoblastic leukemia, and adenocarcinoma (Gomes and others
acid) to determine the phenolic acids in wheat bran extracts and 2003). The presence of apoptosis (programmed cell death) in can-
their potential antioxidant activity, confirming that the acid with cer cell lines is a sign of conceivable anticarcinogenic effects, and
highest concentration, ferulic acid, exhibited the highest antiox- can be evaluated by the number of procedures containing DNA
idant activity. However, the antioxidant activities of caffeic acid splinters and Hoechst staining analysis. This apoptosis procedure
and α-tocopherol were found to be higher than that of ferulic was used to measure the development of emanating apoptosis by
acid (Kikuzaki and others 2002). Furthermore, phenolic com- cinnamic acid in human colon cancer (SW480) and leukemia
pounds also have potential applications as prooxidants under cer- (HL60) cell lines. Furthermore, the antiapoptotic impact on hu-
tain conditions, which could induce oxidative stress. Oxidative man peripheral blood mononuclear cells was examined, demon-
stress is the imbalance of antioxidants and prooxidants, chemicals strating the pretreatment of cells with phenolic mixtures contain-
that cause oxidative stress, either by producing reactive oxygen ing ferulic and caffeic acids, or ellagic acid, before exposing to
species or by inhibiting antioxidant activity, in an organism, and is H2 O2 constrained DNA splinters (Khanduja and others 2006).
thought to be the leading cause of degenerative conditions (Valko Cyclooxygenase isoform 2 (COX-2) analysis is another method
and others 2007; Shahidi and Chandrasekara 2010). Therefore, used to resolve the plausible anticancer effects of these compounds.
evidence suggests that phenolic compounds found in BSG, par- Overexpression of COX-2 boosts the modification of arachidonic
ticularly HBAs, can help to limit oxidative stress. In a recent study, acid to prostaglandins, which mediates the affliction and is linked
ferulic acid and caffeic acid were reported to scavenge free rad- with cancer cells. Ferulic acid has been shown to stop the appear-
icals at low concentrations. These phenolic acids can scavenge ance of COX-2, and thus reduce the chance of cancer (Kang and
reactive oxygen species and reactive nitrogen species, including others 2009). An NF-κB replication factor in the inflammation
2, 2’-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid), superox- process of raised stimulation has been proclaimed in many human
ide anions, and NO radicals, depending on the concentration cancer cells. Hole and others (2012) determined the ability of
to be scavenged (Maurya and Devasagayam 2010). Many phenolic potential phenolic compounds to attune the activity of NF-κB,
compounds exhibited pro-oxidant behavior at low concentrations, noting that, in many cereal grains, free phenolic acids (including
whereas α-tocopherol, a synthetic antioxidant, did not (Fukumoto ferulic acid and p-coumaric acid) adjusted the activity of NF-κB
and Mazza 2000). Ferulic and caffeic acids required higher concen- notably in U9373xkB-LUC cells, with the desired level of adjust-
trations to act as pro-oxidants (Maurya and Devasagayam 2010). ment accomplished by mutual action of the phenolic acids and
The high concentration of p-coumaric acid also caused greater other possible phenolic compounds.
H2 O2 -induced DNA damage in the comet assay method. This As mentioned above in the BSG composition section, that AX is
was probably due to the effect of ROS produced by p-coumaric the major constituent of hemicellulose fraction in BSG present up
acid as a result of its pro-oxidant activity (Ferguson and others to 40% which is higher than barley (4% to 8%) and wheat (4% to
2005). Morton and others (2000) suggested that the pro-oxidant 10%) AX content. Moreover, a major phenolic acid in BSG such
effect was directly correlated with the occurrence of metal ions in as ferulic acid can be esterifies to the residues of arabinose. The
the body (because of copper and iron released by tissue damage) solubility of AX can be affected by the ratio of arabinose to xylose,
and was significant for the bioactivity of phenolic acids in vivo. the formation of oxidative cross-linking by ferulic acids and the
Recently, McCarthy and others (2012) studied the ability of BSG degree and pattern of substitution of the xylan chain. This solubil-
phenolic extracts against oxidant-induced DNA damage in human ity of AX plays a vital role in the promotion of health (Steiner and
lymphocytic U937 cells. In this study, DNA damage was induced others 2015). The fractions of AX from BSG with different molec-
using wide range of oxidants, such as H2 O2 , 4-nitroquinoline ular weights were investigated to find out the prebiotic potential
1-oxide, 3-morpholinosydnonimine hydrochloride, and tert-butyl and the obtained results showed that fraction with low molecu-
hydroperoxide. The U937 cells were preincubated with 4 pale lar weight (66 kDa) was more effective for production of short
(P1, P2, P3, and P4) and 4 black (B1, B2, B3, and B4) BSG chain fatty acid (SCFA), mainly butyrate and health promoting

2238 Journal of Food Science r Vol. 82, Nr. 10, 2017


Hypotheses in Food Science
Composition and preservation of BSG . . .

Concise Reviews &


bacterial groups (Hughes and others 2007). Recently Gómez and products (Gupta and others 2013), and phytosterol and alkylre-
others (2015) presented that arabinoxylooligosaccharides (AXOS) sorcinol containing lipophilic fractions (del Rio and others 2013)
had higher prebiotic potential than fructoolgiosaccharides in BSG. could be investigated to identify natural food components with
Reis and Abu-Ghannam (2014) also found similar results of AX possible antioxidant abilities and other useful properties for phar-
fractions isolated with ultrasound assisted extraction method, and maceutical and nutraceutical applications. Therefore, further stud-
the obtained results was with noteworthy increase in bifidobacte- ies on the extraction and characterization of major phenolic acids
ria populations with high amount of SCFA. Grootaert and others from BSG are needed.
(2009) reported that the composition of microbial community did
not affect the xylooligosaccharides (XOS) fermentation, and the Integration of BSG into Feed/Foodstuffs
main site of colonic XOS fermentation was towards distal colon. Despite BSG being the major byproduct of the brewing industry,
This was beneficial as it was important to expand sugar fermenta- it has received little attention because of its chemical composition,
tion in the distal part of colon, where colon cancer usually occurs, abundance, and low market price. At present, BSG exploitation is
whereas increase production of SCFA at this site was more pro- limited in developing countries. However, several attempts have
tective and helpful. now been made to use this residue to benefit human health, with
some potential applications discussed in the literature.
Phenolic Acids as Anti-Inflammatory Agents
Cytokines are signaling molecules involved in inflammatory Use in Animal Feed
feedback, and include interferons (interferon-γ ) and interleukins. As previously mentioned, BSG contains 20% protein and
The ability of a compound to alter NO creation or stimulate 70% fiber. Because of this favorable chemical composition, BSG
cytokines indicates its potential as an immunomodulator. The ef- has potential applications as a food ingredient or raw material,
fects of a ferulic acid derivative (FA15) and rice-bran derived mainly for cattle (Mussatto and others 2006). The availability of
ferulic acid-rich extract on COX-2 and TNF-α were studied in this low-cost by-product makes it attractive as a feedstock for a
a RAW264·7 murine macrophage cell line and nitric oxide syn- wide range of animals, such as fish, chickens, pigs, and ruminants
thase. The results showed reduction in protein expression in both (Dhiman and others 2003; Mussatto and others 2006).The incor-
COX-2 and NO synthase, and TNF-α formation was inhibited poration of BSG into monogastric diets has shown positive results
(Murakami and others 2002). In addition, ferulic acid also con- on intestinal digestion, relieving both diarrhea, and constipation.
strained TNF-α and macrophage inflammatory protein-2 forma- Tang and others (2009) recognized these special effects, which
tion in a macrophage cell line driven by lipopolysaccharide. The were due to the high noncellulosic polysaccharide, glutamine-rich
dose-dependent effect was very weak compared with the effect of protein, and lower β-glucans contents. Kaur and Saxena (2004)
dexamethasone (a recognized inhibitor of interleukins; Sakai and investigated the effect of replacing rice bran in fish diet with 10%
others 1997). Ferulic acid has been demonstrated as being among to 40% BSG where the treatment group had gained more body
the prime phenolic acids in Cimicifuga heracleifolia, which is used weight than the control group, and the authors claimed that the
as an antiinflammatory medicine in Japanese oriental medicine. better growth performance was due to the high quality protein
Sakai and others (1999) investigated ferulic acid and isoferulic acid and essential amino acids present in the diet provided by BSG.
could reduce macrophage inflammatory protein-2 formation in A more recent study demonstrated the effect of BSG on the
a dose-dependent manner in RAW264·7 cells, with ferulic acid nutritive value of milk yield and blood composition in dairy cat-
and isoferulic acid shown to be accountable for the inflamma- tle. Cattle were fed with a diet containing maize silage, maize,
tory features of C. heracleifolia medicine. Recently, Kim and others wheat bran, and soya bean meal. From the treated group, re-
(2012) showed that ferulic acid and p-coumaric acid induced nitric searchers obtained enhanced total milk and milk fat relative to
oxide synthase in macrophages and inhibited lipopolysaccharide- the control group (Aliyu and Bala 2011), while the blood plasma
triggered NO production. concentrations of glucose, cholesterol, total protein, urea, albumin,
sodium, and triacylglyceride (Itagaki and others) were not affected
Phenolic Acids in Age-Associated Disease Prevention (Dhiman and others 2003; Mussatto and others 2006). Moreover,
Oxidized low-density lipoprotein (ox-LDL) is a well-known a contemporary study showed that biodegraded BSG contained
marker of cardiovascular disease, which is mainly caused by lysine, methionine, cysteine, and 14 other amino acids (Essien
atherosclerosis. Evidence exists for the impact of HCAs on the and Udotong 2008). Among them, alanine was found to have the
LDL oxidation inhibition. Nardini and others (1995) demon- highest concentration, although all were important in the poultry
strated the antioxidant effect of HCAs, such as caffeic, ferulic, diet. In summary, several attempts have been made to utilize whole
and p-coumaric acids, on LDL oxidation in vitro, using Cu2+ as a or part of BSG in mixed form in different animals, especially in
catalyst. At an accumulation of 100 µM, all phenolic acids, except dairy cattle, where it has many nutritional benefits.
p-coumaric acid, inhibited LDL oxidation. At an accumulation of
20 µM, ferulic acid inhibited about 92% of Cu-catalyzed human Use in Human Foodstuff
LDL oxidation, whereas only caffeic acid inhibited the LDL oxida- BSG is considered an ideal ingredient for human food be-
tion at a concentration of 5 µM. Subsequent research using same cause of being readily available, low-cost, and rich in nutrients. It
methodology also found that both ferulic acid and p-coumaric can be added to foodstuffs, such as breads, biscuits, muffins, and
acid demonstrated dose-dependent inhibition of human LDL ox- snacks, that need to improve their fiber and protein content while
idation in vitro when examined at 5, 10, and 20 µM (Meyer and minimizing calorie intake (Mussatto and others 2006). Initially,
others 1998). BSG was considered too coarse for direct consumption, requiring
In addition, BSG bioactive phenolic compound extracts milling. The brownish color and high moisture content limited its
(McCarthy and others 2012, 2013; Meneses and others 2013; usage in off-white food products, such as cookies, cakes, breads,
Moreira and others 2013), AX (Reis and Abu-Ghannam 2014), and pastas (Ozturk and others 2002). Moreover, the addition of
protein isolates (McCarthy and others 2013a), fermentation BSG to bakery products had some limitations due to the flavor

Vol. 82, Nr. 10, 2017 r Journal of Food Science 2239


Hypotheses in Food Science
Concise Reviews & Composition and preservation of BSG . . .

and texture (sensory properties) of the end products. Therefore, Bamba T, Kanauchi O, Andoh A, Fujiyama Y. 2002. A new prebiotic from germinated barley
for nutraceutical treatment of ulcerative colitis. J Gastroen Hepatol 17(8):818–24.
only a small amount (5% to 10%) can be added. Barbosa-Pereira L, Angulo I, Paseiro-Losada P, Cruz JM. 2013. Phenolic profile and antioxidant
Ozturk and others (2002) investigated the impact of 5% and properties of a crude extract obtained from a brewery waste stream. Food Res Int 51(2):663–9.
25% BSG in wheat flour when preparing cookies. The results Bartolome B, Faulds C, Williamson G. 1997. Enzymic release of ferulic acid from barley spent
grain. J Cereal Sci 25(3):285–8.
showed that the dietary fiber content increased with increasing Bartolome B, Gomez-Cordoves C. 1999. Barley spent grain: release of hydroxycinnamic acids
BSG content. These BSG-containing cookies provided various (ferulic and p-coumaric acids) by commercial enzyme preparations. J Sci Food Agr 79(3):
435–9.
human health benefits, such as increasing cholesterol and fat excre- Bartolomé B, Gómez-Cordovés C, Sancho AI, Dı́ez N, Ferreira P, Soliveri J, Copa-Patiño JL.
tion, increasing fecal weight, accelerating transit time, and decreas- 2003. Growth and release of hydroxycinnamic acids from brewer’s spent grain by Streptomyces
avermitilis CECT 3339. Enzyme Microb Technol 32(1):140–4.
ing gallstones (Mussatto and others 2006). According to Stojceska Bartolome B, Santos M, Jimenez JJ, del Nozal MJ, Gomez-Cordoves C. 2002. Pentoses and
and Ainsworth (2008), the incorporation of BSG with 4 different hydroxycinnamic acids in brewer’s spent grain. J Cereal Sci 36(1):51–8.
Bonoli M, Marconi E, Caboni MF. 2004. Free and bound phenolic compounds in barley
enzymes into wheat flour breads at different levels (0% to 30%) (hordeum vulgare L.) flours - evaluation of the extraction capability of different solvent
afforded breads with considerably improved fiber contents along mixtures and pressurized liquid methods by micellar electrokinetic chromatography and spec-
trophotometry. J Chromatogr A 1057(1-2):1–12.
with a increase in fat content. However, the degree of softness, Bouayed J, Bohn T. 2010. Exogenous antioxidants-double-edged swords in cellular redox state
shelf life, texture (sensory properties), and loaf volume were lower Health beneficial effects at physiologic doses versus deleterious effects at high doses. Oxid
Med Cell Longev 3(4):228–37.
than those of bread made with wheat flour. This can be improved Brigas D, Hough J, Stevens R, Young T. 1981. Malting and brewing science. Malt and sweet
using the right combination of BSG and enzymes (Stojceska and wort. UK: Chapman and Hall.
Buranov AU, Mazza G. 2009. Extraction and purification of ferulic acid from flax shives, wheat,
Ainsworth 2008). and corn bran by alkaline hydrolysis and pressurised solvents. Food Chem 115(4):1542–8.
Moreover, a study conducted in 2009 revealed that, in frank- Burton GW, Traber MG. 1990. Vitamin E: antioxidant activity, biokinetics, and bioavailability.
furter sausage production, BSG can be efficiently used in different Annu Rev Nutr 10(1):357–82.
Carvalheiro F, Esteves M, Parajó J, Pereira H, Gırio F. 2004. Production of oligosaccharides by
particle sizes, with the addition of BSG with increased particle sizes autohydrolysis of brewery’s spent grain. Bioresource Technol 91(1):93–100.
yielding products with high fiber contents without affecting their Celus I, Brijs K, Delcour JA. 2006. The effects of malting and mashing on barley protein
extractability. J Cereal Sci 44(2):203–11.
sensory attributes. BSG has also been used in low-fat high-fiber Celus I, Brijs K, Delcour JA. 2007. Enzymatic hydrolysis of brewers’ spent grain proteins and
meat products (Özvural and others 2009). In another study, on technofunctional properties of the resulting hydrolysates. J Agr Food Chem 55(21):8703–10.
Chang WC, Hsieh CH, Hsiao MW, Lin WC, Hung YC, Ye JC. 2010. Caffeic acid induces
the production of tarhana, BSG was utilized as a fermented wheat apoptosis in human cervical cancer cells through the mitochondrial pathway. Taiwan J Obstet
flour or yoghurt product. Milled BSG afforded satisfactory soup Gyne 49(4):419–24.
properties in tarhana production, and it was noted that the lower Chen JH, Ho CT. 1997. Antioxidant activities of caffeic acid and its related hydroxycinnamic
acid compounds. J Agr Food Chem 45(7):2374–8.
sensory properties, color, taste, and odor, could be compensated Coelho E, Rocha MAM, Moreira AS, Domingues MRM, Coimbra MA. 2016. Revisiting the
for by the increased fiber content in the end product, which can structural features of arabinoxylans from brewers’ spent grain. Carbohyd Polym 139:167–76.
Coelho E, Rocha MAM, Saraiva JA, Coimbra MA. 2014. Microwave superheated water and
provide health benefits (Ozboy-Ozbas and others 2010). Recently, dilute alkali extraction of brewers’ spent grain arabinoxylans and arabinoxylo-oligosaccharides.
the incorporation of increasing levels of BSG as an ingredient in the Carbohyd Polym 99:415–22.
Conde E, Moure A, Domı́nguez H, Parajó JC. 2008. Fractionation of antioxidants from auto-
formulation of extruded snacks (40/100g) and breadsticks products hydrolysis of barley husks. J Agr Food Chem 56(22):10651–9.
(35 g/100 g) have shown increased levels of bioactive antioxidants Connolly A, Piggott CO, FitzGerald RJ. 2014. In vitro alpha-glucosidase, angiotensin converting
enzyme and dipeptidyl peptidase-IV inhibitory properties of brewers’ spent grain protein
with (4- and 7-fold) and AX and with low glycaemic index (Reis hydrolysates. Food Res Int 56:100–7.
and Abu-Ghannam 2014). Ktenioudaki and others (2015) also re- Crowley DJ, Callaghan YO, Mccarthy AL, Connolly A, Piggott CO, Fitzgerald RJ, Brien
ported that, integration of 15% BSG flour into wheat flour breads NMO. 2015. Immunomodulatory potential of a brewers’ spent grain protein hydrolysate
incorporated into low-fat milk following in vitro gastrointestinal digestion. Int J Food Sci Nutr
improved the sensory, flavor, nutritional properties along with the 66(6):672–676.
antioxidant capacity. Xylanase and dough conditioner improved Dai J, Mumper RJ. 2010. Plant phenolics: extraction, analysis, and their antioxidant and anti-
cancer properties. Molecules 15(10):7313–52.
the mixing and pasting consistency of the wheat flours and also Dar B, Sharma S. 2011. Total phenolic content of cereal brans using conventional and microwave
enhanced the loaf volume and texture of breads and increases the assisted extraction. Am J Food Technol 6(12):1045–53.
del Rio JC, Prinsen P, Gutierrez A. 2013. Chemical composition of lipids in brewer’s spent
shelf life of breads when mixed with both sour dough and non- grain: a promising source of valuable phytochemicals. J Cereal Sci 58(2):248–54.
sour dough BSG breads. Dhiman TR, Bingham HR, Radloff HD. 2003. Production response of lactating cows fed dried
versus wet brewers’ grain in diets with similar dry matter content. J Dairy Sci 86(9):2914–21.
Diptee R, Smith J, Alli I, Khanizadeh S. 1989. Application of response surface methodology in
Conclusion protein extraction studies from brewer’s spent grain. J Food Process Pres 13(6):457–74.
This literature review demonstrates the attempts made to utilize Dudjak J, Lachman J, Miholová D, Kolihová D, Pivec V. 2004. Effect of cadmium on polyphenol
content in young barley plants (hordeum vulgare L.). Plant Soil Environ 50(11):471–7.
the readily available low-cost brewing byproduct, BSG, in poten- El-Shafey EI, Gameiro MLF, Correia PFM, de Carvalho JMR. 2004. Dewatering of brewer’s
tially valuable applications. BSG is gaining considerable attention spent grain using a membrane filter press: a pilot plant study. Sep Sci Technol 39(14):3237–61.
Essien J, Udotong I. 2008. Amino acid profile of biodegraded brewers spent grains (BSG). J Sci
as a source of fiber, protein, and potential bioactive phenolic com- Enivron Manage 12:109–11.
pounds, including ferulic, p-coumaric, and caffeic acids. BSG can Faghfoori Z, Navai L, Shakerhosseini R, Somi MH, Nikniaz Z, Norouzi MF. 2011. Effects of an
oral supplementation of germinated barley foodstuff on serum tumour necrosis factor-alpha,
act as an antioxidant, and has a range of potential bioactivities. interleukin-6 and -8 in patients with ulcerative colitis. Ann Clin Biochem 48:233–7.
Although efforts have been made to incorporate the bioactive Faulds CB, Mandalari G, LoCurto R, Bisignano G, Waldron KW. 2004. Arabinoxylan and
mono- and dimeric ferulic acid release from brewer’s grain and wheat bran by feruloyl
phenolic compounds, fiber, and protein in BSG into foodstuffs, esterases and glycosyl hydrolases from humicola insolens. Appl Microbiol Biot 64(5):644–50.
more studies are required to explore different applications of BSG Faulds CB, Robertson JA, Waldron KW. 2008. Effect of pH on the solubilization of brewers’
spent grain by microbial carbohydrates and proteases. J Agr Food Chem 56(16):7038–43.
and its components. Faulds CB, Sancho AI, Bartolome B. 2002. Mono- and dimeric ferulic acid release from brewer’s
spent grain by fungal feruloyl esterases. Appl Microbiol Biot 60(4):489–93.
Acknowledgment Ferguson LR, Zhu ST, Harris PJ. 2005. Antioxidant and antigenotoxic effects of plant cell wall
hydroxycinnamic acids in cultured HT-29 cells. Mol Nutr Food Res 49(6):585-93.
This work was supported by the Natl. Natural Science Foun- Fernández M, Rodriguez J, Garcı́a M, De Lucas A, Gracia I. 2008. Application of supercritical
dation of China (Nos. 31401522 and 31571940). fluid extraction to brewer’s spent grain management. Ind Eng Chem Res 47(5):1614–9.
Forssell P, Kontkanen H, Schols HA, Hinz S, Eijsink VGH, Treimo J, Robertson JA, Waldron
KW, Faulds CB, Buchert J. 2008. Hydrolysis of brewers’ spent grain by carbohydrate degrading
References enzymes. J I Brewing 114(4):306–14.
Aliyu S, Bala M. 2011. Brewer’s spent grain: a review of its potentials and applications. Afr J Fukumoto LR, Mazza G. 2000. Assessing antioxidant and prooxidant activities of phenolic
Biotechnol 10(3):324–31. compounds. J Agr Food Chem 48(8):3597–604.
Amarowicz R, Carle R, Dongowski G, Durazzo A, Galensa R, Kammerer D, Maiani G, Piskula Gelmez N, Kıncal NS, Yener ME. 2009. Optimization of supercritical carbon dioxide extrac-
MK. 2009. Influence of postharvest processing and storage on the content of phenolic acids tion of antioxidants from roasted wheat germ based on yield, total phenolic and tocopherol
and flavonoids in foods. Mol Nutr Food Res 53:S151–S83. contents, and antioxidant activities of the extracts. J Supercrit Fluid 48(3):217–24.

2240 Journal of Food Science r Vol. 82, Nr. 10, 2017


Hypotheses in Food Science
Composition and preservation of BSG . . .

Concise Reviews &


Gomes CA, da Cruz TG, Andrade JL, Milhazes N, Borges F, Marques MPM. 2003. Anticancer McCann MJ, Gill CIR, O’Brien G, Rao JR, McRoberts WC, HugheS P, McEntee R, Rowland
activity of phenolic acids of natural or synthetic origin: a structure-activity study. J Med Chem IR. 2007. Anti-cancer properties of phenolics from apple waste on colon carcinogenesis in
46(25):5395–401. vitro. Food Chem Toxicol 45(7):1224–30.
Gómez Bn, Mı́guez B, Veiga An, Parajó JC, Alonso JL. 2015. Production, purification, and in McCarthy AL, O’Callaghan YC, Connolly A, Piggott CO, FitzGerald RJ, O’Brien NM. 2012.
vitro evaluation of the prebiotic potential of arabinoxylooligosaccharides from brewer’s spent Phenolic extracts of brewers’ spent grain (BSG) as functional ingredients - assessment of their
grain. J Agr Food Chem 63(38):8429–38. DNA protective effect against oxidant-induced DNA single strand breaks in U937 cells. Food
Guo WW, Beta T. 2013. Phenolic acid composition and antioxidant potential of insoluble and Chem 134(2):641–6.
soluble dietary fiber extracts derived from select whole-grain cereals. Food Res Int 51(2): McCarthy AL, O’Callaghan YC, Connolly A, Piggott CO, FitzGerald RJ, O’Brien NM. 2013a.
518–25. In vitro antioxidant and anti-inflammatory effects of brewers’ spent grain protein rich isolate
Gupta S, Jaiswal AK, Abu-Ghannam N. 2013. Optimization of fermentation conditions for the and its associated hydrolysates. Food Res Int 50(1):205–12.
utilization of brewing waste to develop a nutraceutical rich liquid product. Ind Crop Prod McCarthy AL, O’Callaghan YC, Neugart S, Piggott CO, Connolly A, Jansen MAK, Krumbein
44:272–82. A, Schreiner M, FitzGerald RJ, O’Brien NM. 2013b. The hydroxycinnamic acid content of
Grootaert C, Van den Abbeele P, Marzorati M, Broekaert WF, Courtin CM, Delcour JA, Ver- barley and brewers’ spent grain (BSG) and the potential to incorporate phenolic extracts of
straete W, Van de Wiele T. 2009. Comparison of prebiotic effects of arabinoxylan oligosaccha- BSG as antioxidants into fruit beverages. Food Chem 141(3):2567–74.
rides and inulin in a simulator of the human intestinal microbial ecosystem. FEMS Microbiol Mccarthy AL, Ocallaghan YC, Piggott CO, Fitzgerald RJ, Obrien NM. 2013c. Brewers’ spent
Ecol 69(2):231–42. grain; bioactivity of phenolic component, its role in animal nutrition and potential for incor-
Hernanz D, Nunez V, Sancho AI, Faulds CB, Williamson G, Bartolome B, Gomez-Cordoves C. poration in functional foods: a review. Proceed Nutr Soc 72(01):117–25.
2001. Hydroxycinnamic acids and ferulic acid dehydrodimers in barley and processed barley. Mendis M, Simsek S. 2014. Arabinoxylans and human health. Food Hydrocoll 42:239–43.
J Agr Food Chem 49(10):4884–8. Meneses NGT, Martins S, Teixeira JA, Mussatto SI. 2013. Influence of extraction solvents on the
Hole AS, Grimmer S, Jensen MR, Sahistrom S. 2012. Synergistic and suppressive effects of recovery of antioxidant phenolic compounds from brewer’s spent grains. Sep Purif Technol
dietary phenolic acids and other phytochemicals from cereal extracts on nuclear factor kappa 108:152–8.
B activity. Food Chem 133(3):969–77. Meyer AS, Donovan JL, Pearson DA, Waterhouse AL, Frankel EN. 1998. Fruit hydroxycinnamic
Holtekjølen AK, Kinitz C, Knutsen SH. 2006. Flavanol and bound phenolic acid contents in acids inhibit human low-density lipoprotein oxidation in vitro. J Agr Food Chem 46(5):
different barley varieties. J Agr Food Chem 54(6):2253–60. 1783–7.
Huang MT, Smart RC, Wong CQ, Conney AH. 1988. Inhibitory effect of curcumin, chloro- Moreira MM, Morais S, Carvalho DO, Barros AA, Delerue-Matos C, Guido LF. 2013. Brewer’s
genic acid, caffeic acid, and ferulic acid on tumor promotion in mouse skin by 12-O- spent grain from different types of malt: evaluation of the antioxidant activity and identification
tetradecanoylphorbol-13-acetate. Cancer Res 48(21):5941–6. of the major phenolic compounds. Food Res Int 54(1):382–8.
Hughes S, Shewry P, Li L, Gibson G, Sanz M, Rastall R. 2007. In vitro fermentation by human Morton LW, Caccetta RA, Puddey IB, Croft KD. 2000. Chemistry and biological effects
fecal microflora of wheat arabinoxylans. J Agr Food Chem 55(11):4589–95. of dietary phenolic compounds: relevance to cardiovascular disease. Clin Exp Pharmacol P
Huige N. 2006. Brewery by-products and effluents. Food Sci Technol. New York: CRC Press. 27(3):152–9.
p 655–713. Murakami A, Nakamura Y, Koshimizu K, Takahashi D, Matsumoto K, Hagihara K, Taniguchi
Inglett GE, Rose DJ, Stevenson DG, Chen D, Biswas A. 2009. Total phenolics and antioxidant H, Nomura E, Hosoda A, Tsuno T, Maruta Y, Kim HW, Kawabata K, Ohigashi H. 2002.
activity of water and ethanolic extracts from distillers dried grains with soluble with or without FA15, a hydrophobic derivative of ferulic acid, suppresses inflammatory responses and skin
microwave irradiation. Cereal Chem 86(6):661–4. tumor promotion: comparison with ferulic acid. Cancer Lett 180(2):121–9.
Irakli MN, Samanidou VF, Biliaderis CG, Papadoyannis IN. 2012. Development and validation Mussatto SI. 2009. Biotechnological potential of brewing industry by-products. Biotechnology
of an HPLC-method for determination of free and bound phenolic acids in cereals after for agro-industrial residues utilisation. In: Nigam P, Pandey A, editors. Netherlands: Springer.
solid-phase extraction. Food Chem 134(3):1624–32. p 313–26.
Itagaki S, Kurokawa T, Nakata C, Saito Y, Oikawa S, Kobayashi M, Hirano T, Iseki K. 2009. In Mussatto SI. 2014. Brewer’s spent grain: a valuable feedstock for industrial applications. J Sci
vitro and in vivo antioxidant properties of ferulic acid: a comparative study with other natural Food Agr 94(7):1264–75.
oxidation inhibitors. Food Chem 114(2):466–71. Mussatto SI, Dragone G, Roberto IC. 2006. Brewers’ spent grain: generation, characteristics,
Jacobasch G, Schmiedl D, Kruschewski M, Schmehl K. 1999. Dietary resistant starch and chronic and potential applications. J Cereal Sci 43(1):1–14.
inflammatory bowel diseases. Int J Colorectal Dis 14(4-5):201–11. Mussatto SI, Dragone G, Roberto IC. 2007. Ferulic and p-coumaric acids extraction by alkaline
Jay AJ, Parker ML, Faulks R, Husband F, Wilde P, Smith AC, Faulds CB, Waldron KW. hydrolysis of brewer’s spent grain. Ind Crop Prod 25(2):231–7.
2008. A systematic micro-dissection of brewers’ spent grain. J Cereal Sci 47(2):357– Mussatto SI, Roberto IC. 2005. Acid hydrolysis and fermentation of brewer’s spent grain to
64. produce xylitol. J Sci Food Agr 85(14):2453–60.
Kanauchi O, Agata K. 1997. Protein, and dietary fiber-rich new foodstuff from brewer’s spent Mussatto SI, Roberto IC. 2006. Chemical characterization and liberation of pentose sugars from
grain increased excretion of feces and jejunum mucosal protein content in rats. Biosci Biotech- brewer’s spent grain. J Chem Technol Biot 81(3):268–74.
nol Biochem 61(1):29–33. Mussatto SI, Teixeira J. 2010. Lignocellulose as raw material in fermentation processes. Curr
Kanauchi O, Mitsuyama K, Araki Y. 2001. Development of a functional germinated barley Res, Technol, Educ Topics in Appl Microbiol Microb Biotechnol (Méndez-Vilas, A., Ed.)
foodstuff from brewer’s spent grain for the treatment of ulcerative colitis. J Am Soc Brew 2:897–907.
Chem 59(2):59–62. Naczk M, Shahidi F. 2004. Extraction and analysis of phenolics in food. J Chromatogr A
Kanauchi O, Serizawa I, Araki Y, Suzuki A, Andoh A, Fujiyama Y, Mitsuyama K, Takaki 1054(1-2):95–111.
K, Toyonaga A, Sata M, Bamba T. 2003. Germinated barley foodstuff, a prebiotic prod- Nardini M, D’Aquino M, Tomassi G, Gentili V, Di Felice M, Scaccini C. 1995. Inhibition
uct, ameliorates inflammation of colitis through modulation of the enteric environment. J of human low-density lipoprotein oxidation by caffeic acid and other hydroxycinnamic acid
Gastroenterol 38(2):134–41. derivatives. Free Radical Bio Med 19(5):541–52.
Kang NJ, Lee KW, Shin BJ, Jung SK, Hwang MK, Bode AM, Heo YS, Lee HJ, Dong ZG. Napolitano A, Lanzuise S, Ruocco M, Arlotti G, Ranieri R, Knutsen SH, Lorito M, Fogliano
2009. Caffeic acid, a phenolic phytochemical in coffee, directly inhibits Fyn kinase activity, V. 2006. Treatment of cereal products with a tailored preparation of Trichoderma enzymes
and UVB-induced COX-2 expression. Carcinogenesis 30(2):321–30. increases the amount of soluble dietary fiber. J Agr Food Chem 54(20):7863–9.
Kaur VI, Saxena PK. 2004. Incorporation of brewery waste in supplementary feed and its impact Niemi P, Aura A M, Maukonen J, Smeds AI, Mattila I, Niemelä K, Tamminen T, Faulds CB,
on growth in some carps. Bioresource Technol 91(1):101–4. Buchert J, Poutanen K. 2013. Interactions of a lignin-rich fraction from Brewer’s spent grain
Khanduja KL, Avti PK, Kumar S, Mittal N, Sohi KK, Pathak CM. 2006. Anti-apoptotic activity with gut microbiota in vitro. J Agr Food Chem 61(27):6754–62.
of caffeic acid, ellagic acid, and ferulic acid in normal human peripheral. Blood mononuclear Niemi P, Tamminen T, Smeds A, Viljanen K, Ohra-aho T, Holopainen-Mantila U, Faulds CB,
cells: a bcl-2 independent mechanism. Bba-Gen Subjects 1760(2):283–9. Poutanen K, Buchert J. 2012. Characterization of lipids and lignans in brewer’s spent grain
Kikuzaki H, Hisamoto M, Hirose K, Akiyama K, Taniguchi H. 2002. Antioxidant properties of and its enzymatically extracted fraction. J Agr Food Chem 60(39):9910–7.
ferulic acid and its related compounds. J Agr Food Chem 50(7):2161–8. Oufnac DS, Zhimin X, Ting S, Sabliov C, Prinyawiwatkul W, Godber JS. 2007. Extraction
Kim EO, Min KJ, Kwon TK, Um BH, Moreau RA, Choi SW. 2012. Antiinflammatory activity of antioxidants from wheat bran using conventional solvent and microwave-assisted methods.
of hydroxycinnamic acid derivatives isolated from corn bran in lipopolysaccharide-stimulated Cereal Chem 84(2):125–9.
Raw 264.7 macrophages. Food Chem Toxicol 50(5):1309–16. Osborne T. 1924. Classification of vegetable proteins. The vegetable proteins. New York:
Kim KH, Tsao R, Yang R, Cui SW. 2006. Phenolic acid profiles and antioxidant activi- Longmans, Green and Co. p 25–35.
ties of wheat bran extracts and the effect of hydrolysis conditions. Food Chem 95(3): Ozboy-Ozbas O, Hancer A, Gokbulut I. 2010. Utilization of sugar beet fiber and brewers’ spent
466–73. grain in the production of tarhana. Zuckerindustrie 135(8):496–501.
Kishi S, Kimura T, Minami T, Kobayashi H. 1992a. Process for producing protein-rich product, Ozturk S, Ozboy O, Cavidoglu I, Koksel H. 2002. Effects of brewer’s spent grain on the quality
fibrous product, and/or vegetable oil from brewer’s spent grain. Google Patents. and dietary fibre content of cookies. J I Brewing 108(1):23–7.
Kishi S, Kimura T, Minami T, Kobayashi H. 1992b. Protein-rich products of brewer’s spent Özvural EB, Vural H, Gökbulut I, Özboy-Özbaş Ö. 2009. Utilization of brewer’s spent grain in
grain origin. Google Patents. the production of frankfurters. Int J Food Sci Tech 44(6):1093–9.
Ktenioudaki A, Alvarez-Jubete L, Smyth TJ, Kilcawley K, Rai DK, Gallagher E. 2015. Applica- Piazzon A, Forte M, Nardini M. 2010. Characterization of phenolics content and antioxidant
tion of bioprocessing techniques (sourdough fermentation and technological aids) for brewer’s activity of different beer types. J Agr Food Chem 58(19):10677–83.
spent grain breads. Food Res Int 73:107–16. Pryma J, Ehrenbergerova J, Belcrediova N, Vaculova K. 2007. Tocol content in barley. Acta
Kunze W. 1996. Technology of malting and brewing. VLB, Berlin. p. 80. chim slov 54(1):102–5.
Mallouchos A, Lagos G, Komaitis M. 2007. A rapid microwave-assisted derivatization pro- Quinde-Axtell Z. 2006. Phenolic compounds of barley grain and their implication in food
cess for the determination of phenolic acids in brewer’s spent grains. Food Chem 102(3): product discoloration. J Agr Food Chem 54(26):9978–84.
606–11. Qureshi A, Qureshi N, Hasler-Rapacz J, Weber F, Chaudhary V, Crenshaw T, Gapor A,
Mandalari G, Faulds CB, Sancho AI, Saija A, Bisignano G, LoCurto R, Waldron KW. 2005. Ong A, Chong Y, Peterson D. 1991a. Dietary tocotrienols reduce concentrations of plasma
Fractionation and characterization of arabinoxylans from brewers’ spent grain and wheat bran. cholesterol, apolipoprotein B, thromboxane B2, and platelet factor 4 in pigs with inherited
J Cereal Sci 42(2):205–12. hyperlipidemias. Am J Clin Nutr 53(4):1042S–6S.
Martins S, Mussatto SI, Martinez-Avila G, Montanez-Saenz J, Aguilar CN, Teixeira JA. 2011. Qureshi AA, Burger WC, Peterson DM, Elson CE. 1986. The structure of an inhibitor of
Bioactive phenolic compounds: production and extraction by solid-state fermentation: a cholesterol biosynthesis isolated from barley. J Biol Chem 261(23):10544–50.
review. Biotechnol Adv 29(3):365–73. Qureshi AA, Qureshi N, Wright JJ, Shen Z, Kramer G, Gapor A, Chong YH, DeWitt G,
Maurya DK, Devasagayam TPA. 2010. Antioxidant and prooxidant nature of hydroxycinnamic Ong A, Peterson DM, et al. 1991b. Lowering of serum cholesterol in hypercholesterolemic
acid derivatives ferulic and caffeic acids. Food Chem Toxicol 48(12):3369–73. humans by tocotrienols (palmvitee). Am J Clin Nutr 53(4 Suppl.):1021S–6S.

Vol. 82, Nr. 10, 2017 r Journal of Food Science 2241


Hypotheses in Food Science
Concise Reviews & Composition and preservation of BSG . . .

Reis SF, Abu-Ghannam N. 2014. Antioxidant capacity, arabinoxylans content, and in vitro Tang ZW, Cenkowski S, Izydorczyk M. 2005. Thin-layer drying of spent grains in superheated
glycaemic index of cereal-based snacks incorporated with brewer’s spent grain. Lwt-Food Sci steam. J Food Eng 67(4):457–65.
Technol 55(1):269–77. Tatham AS, Shewry PR. 2012. The s-poor prolamins of wheat, barley and rye: revisited. J Cereal
Robertson JA, I’Anson KJA, Treimo J, Faulds CB, Brocklehurst TF, Eijsink VGH, Waldron Sci 55(2):79–99.
KW. 2010. Profiling brewers’ spent grain for composition and microbial ecology at the site Teixeira DM, Patao RF, Coelho AV, da Costa CT. 2006. Comparison between sample disruption
of production. Lwt-Food Sci Technol 43(6):890–6. methods and solid-liquid extraction (SLE) to extract phenolic compounds from ficus carica
Russ W, Mortel H, Meyer-Pittroff R. 2005. Application of spent grains to increase porosity in leaves. J Chromatogr A 1103(1):22–8.
bricks. Constr Build Mater 19(2):117–26. Townsley P. 1979. Preparation of commercial products from brewer’s waste grain and trub
Sakai S, Kawamata H, Kogure T, Mantani N, Terasawa K, Umatake M, Ochiai H. 1999. [protein flours]. Tech Quarterly MBAA 16:130–34.
Inhibitory effect of ferulic acid and isoferulic acid on the production of macrophage in- Treimo J, Aspmo SI, Eijsink VGH, Horn SJ. 2008. Enzymatic solubilization of proteins in
flammatory protein-2 in response to respiratory syncytial virus infection in RAW264.7 cells. brewer’s spent grain. J Agr Food Chem 56(13):5359–65.
Mediators Inflamm 8(3):173–5. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J. 2007. Free radicals and
Sakai S, Ochiai H, Nakajima K, Terasawa K. 1997. Inhibitory effect of ferulic acid on macrophage antioxidants in normal physiological functions and human disease. Int J Biochem Cell B
inflammatory protein-2 production in a murine macrophage cell line, RAW264.7. Cytokine 39(1):44–84.
9(4):242–8. Vatai T, Skerget M, Knez Z. 2009. Extraction of phenolic compounds from elder berry and
Santos M, Jimemez JJ, Bartolome B, Gomez-Cordoves C, del Nozal MJ. 2003. Variability of different grape marc varieties using organic solvents and/or supercritical carbon dioxide. J
brewer’s spent grain within a brewery. Food Chem 80(1):17–21. Food Eng 90(2):246–54.
Sen CK, Rink C, Khanna S. 2010. Palm oil-derived natural vitamin E α-tocotrienol in brain Vichapong J, Sookserm M, Srijesdaruk V, Swatsitang P, Srijaranai S. 2010. High performance
health and disease. J Am Coll Nutr 29(3):314S—23S. liquid chromatographic analysis of phenolic compounds and their antioxidant activities in rice
Shahidi F, Chandrasekara A. 2010. Hydroxycinnamates and their in vitro and in vivo antioxidant varieties. Lwt-Food Sci Technol 43(9):1325–30.
activities. Phytochem Rev 9(1):147–70. Vieira E, Rocha MAM, Coelho E, Pinho O, Saraiva JA, Ferreira IM, Coimbra MA. 2014.
Shewry P. 1993. Barley seed proteins. In: AW MacGregor, RS Bahatty, editors. Barley: chemistry Valuation of brewer’s spent grain using a fully recyclable integrated process for extraction of
and technology. St Paul, Minn., Amer Assoc Cereal Chemists. Inc. p 131–97 proteins and arabinoxylans. Ind Crop Prod 52:136–43.
Silva JP, Sousa S, Rodrigues J, Antunes H, Porter JJ, Gonçalves I, Ferreira-Dias S. 2004. Wang X, Qi J, Wang X, Cao L. 2013. Extraction of polyphenols from barley (hordeum vulgare
Adsorption of acid orange 7 dye in aqueous solutions by spent brewery grains. Sep Purif L.) grain using ultrasound-assisted extraction technology. Asian J Chem 25(3):1324–30.
Technol 40(3):309–15. Xiros C, Christakopoulos P. 2012. Biotechnological potential of brewers spent grain and its
Spinelli S, Conte A, Lecce L, Padalino L, Del Nobile MA. 2016. Supercritical carbon dioxide recent applications. Waste and Biomass Valorization 3(2):213–32.
extraction of brewer’s spent grain. J Supercrit Fluid 107:69–74. Xiros C, Moukouli M, Topakas E, Christakopoulos P. 2009. Factors affecting ferulic acid release
Stalikas CD. 2007. Extraction, separation, and detection methods for phenolic acids and from Brewer’s spent grain by Fusarium oxysporum enzymatic system. Bioresour Technol
flavonoids. J Sep Sci 30(18):3268–95. 100(23):5917–21.
Steiner J, Procopio S, Becker T. 2015. Brewer’s spent grain: source of value-added polysac- Xiros C, Topakas E, Katapodis P, Christakopoulos P. 2008. Hydrolysis and fermentation of
charides for the food industry in reference to the health claims. Eur Food Res and Technol brewer’s spent grain by neurospora crassa. Bioresource Technol 99(13):5427–35.
241(3):303–15. Zhang JX, Lundin E, Andersson H, Bosaeus I, Dahlgren S, Hallmans G, Stenling R, Aman P.
Stojceska V, Ainsworth P. 2008. The effect of different enzymes on the quality of high-fibre 1991. Brewer’s spent grain, serum lipids, and fecal sterol excretion in human subjects with
enriched brewer’s spent grain breads. Food Chem 110(4):865–72. ileostomies. J Nutr 121(6):778–84.
Sun R, Sun X F. 2001. Separation and characterization of lipophilic extracts from barley straw. Zhao HF, Chen WF, Lu J, Zhao MM. 2010. Phenolic profiles and antioxidant activities of
Sep Sci Technol 36(13):3027–48. commercial beers. Food Chem 119(3):1150–8.
Szwajgier D, Wasko A, Targonski Z, Niedzwiadek M, Bancarzewska M. 2010. The use of a Zigoneanu I, Williams L, Xu Z, Sabliov C. 2008. Determination of antioxidant compo-
novel ferulic acid esterase from lactobacillus acidophilus K1 for the release of phenolic acids nents in rice bran oil extracted by microwave-assisted method. Bioresource Technol 99(11):
from brewer’s spent grain. J I Brewing 116(3):293–303. 4910–8.
Tang DS, Yin GM, He YZ, Hu SQ, Li B, Li L, Liang HL, Borthakur D. 2009. Recovery of
protein from brewer’s spent grain by ultrafiltration. Biochem Eng J 48(1):1–5.
Tang Z, Cenkowski S, Muir WE. 2004. Modelling the superheated-steam drying of a fixed bed
of brewers’ spent grain. Biosyst Eng 87(1):67–77.

2242 Journal of Food Science r Vol. 82, Nr. 10, 2017

You might also like