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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.
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 . . .
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
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.
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
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.
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
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