Fermentation Biotechnology Applied to Cereal Industry By-Products: Nutritional and Functional Insights
Introduction: Overview of the Fate of Cereal Industry By-Products
Cereals are the edible seeds of the grass family of Poaceae, also known as Gramineae, and their cultivation dates to thousands of years ago. Wheat, maize, rice, barley, sorghum, millet, oat, and rye are the cereals most important on a global scale (1). Among them, wheat and rice represent the dominant crops, in Western and Asian countries, respectively (2, 3). Cereals are one of the most important food sources for human consumption, with a production of more than 2 billion tons/year. However, unfortunately, roughly 30% of this amount is wasted or lost due to several reasons (2, 4). Overall, food losses include all the edible parts discarded during the supply chain, while food wastes are residues of high organic load, removed during raw materials processing to foodstuff (5). In developing countries, substantial food losses occur during agricultural production, whereas in industrialized countries losses also include processed products during the distribution and consumption stages (5). Considering the unused food matrix as waste does not enforce the possibility of re-utilizing it in the food chain. For this reason, the use of the term “by-product” is increasing and identifies those wastes that become substrates for the recapture of functional compounds and the development of new products with a market value (6).
Introduction: Overview of the Fate of Cereal Industry By-Products
Cereals are the edible seeds of the grass family of Poaceae, also known as Gramineae, and their cultivation dates to thousands of years ago. Wheat, maize, rice, barley, sorghum, millet, oat, and rye are the cereals most important on a global scale (1). Among them, wheat and rice represent the dominant crops, in Western and Asian countries, respectively (2, 3). Cereals are one of the most important food sources for human consumption, with a production of more than 2 billion tons/year. However, unfortunately, roughly 30% of this amount is wasted or lost due to several reasons (2, 4). Overall, food losses include all the edible parts discarded during the supply chain, while food wastes are residues of high organic load, removed during raw materials processing to foodstuff (5). In developing countries, substantial food losses occur during agricultural production, whereas in industrialized countries losses also include processed products during the distribution and consumption stages (5). Considering the unused food matrix as waste does not enforce the possibility of re-utilizing it in the food chain. For this reason, the use of the term “by-product” is increasing and identifies those wastes that become substrates for the recapture of functional compounds and the development of new products with a market value (6).
Fermentation of the Milling By-Products
Wheat Bran
The multiple outer layers of wheat (outer and inner pericarp, seed coat, and nucellar epidermis) are commonly referred to as bran (20). During conventional wheat roller milling, most of the endosperm is separated and further ground to wheat flour. Therefore, bran, together with the aleurone layer and remnants of endosperm, becomes a milling by-product. Different types of bran (i.e., coarse bran or regular bran, coarse weatings or fine bran, fine weatings or middlings or shorts, and low-grade flour or “red dog”) can be distinguished depending on the particle size and the endosperm content (21). The most abundant polysaccharides of the bran layers, arabinoxylans and β-glucans, have a role in lowering the risk of type II diabetes and colorectal cancer as well as cardiovascular and diverticular diseases (8). However, bioactive compounds such as dietary fibers and phenolic acids are trapped in the cell wall structures resisting conventional milling and thus having low bioaccessibility (22). Thereby, new milling techniques, enzymatic treatments and fermentation processes targeting the structure of bran, have been studied with the aim of enhancing its nutritional potential (23). Over the last years, the interest of the scientific community toward wheat bran fermentation, alone or combined with other approaches, markedly increased. Fermentation with two selected microbial strains (Lactobacillus brevis E95612 and Kazachstania exigua C81116) combined with hydrolytic enzymes, mainly
xylanase, endoglucanase, and β-glucanase was employed to obtain bran with higher nutritional quality than the native one (24).
Wheat Germ
Wheat germ is a high nutritional value by-product separated
during the milling process. It is the primary source of vitamin
E in wheat kernel and a rich source of vitamins of the group B,
proteins, dietary fiber and minerals (30, 42). Most of the essential
amino acids are present in wheat germ proteins at concentrations
higher than in the reference egg protein pattern (43, 44). Wheat
germ is also rich in unsaturated fatty acids, mainly oleic, linoleic
and α-linoleic acids and functional phytochemicals especially
flavonoids, sterols, octacosanols, and glutathione (45). However,
its consumption is limited by some anti-nutritional factors
(raffinose, phytic acid, and wheat germ agglutinin) and by the
high lipase and lipoxygenase activity that favor lipid oxidation,
negatively affecting the stability of wheat germ (15).
To solve this issue, the effects of sourdough fermentation on
wheat germ stabilization were studied. Two lactic acid bacteria
(Lactobacillus plantarum LB1 and Lactobacillus rossiae LB5)
isolated from wheat germ were used as starters for sourdough
fermentation (46). After 40 days of storage, compared to the
raw germ, the fermented one had very low percentage of the
aldehydes usually responsible for the rancidity perception, as well
as of alcohols, ketones, furanones, and lactones, other volatile
compounds occurring in lipid oxidation. The low pH achieved
with fermentation was indeed responsible of the lower lipase
activity. Fermentation also increased of ca.
50% the concentration
of total free amino acids, more specifically Lys, the major
limiting amino acid of wheat flour, and GABA were present
in fermented wheat germ at the concentration of almost 2
g/kg (46). During sourdough fermentation of wheat germ, the
phytase activity increased and an enhanced the bioaccesibility
of Ca++, Fe++, K+, Mn++, Na+, and Zn++. Concomitantly,
raffinose concentration decreased by 45% and a 33% increase in
phenol content occurred, which resulted in higher scavenging
activity toward free radical DPPH and ABTS (46). Antioxidant
activity in food matrixes is often due to the presence of
phenolic compounds; nonetheless, this functional property can
also be ascribed to bioactive peptides. Biologically active peptides,
often encrypted in the native sequence, can be produced from
their protein precursor by digestive enzymes or during food
processing (47). The interest toward bioactive peptides from
vegetable sources has increased thanks to the recent evidence
of their wide potential functional effects (antihypertensive,
antioxidant, antitumoral, antiproliferative, hypocholesterolemic,
antinflammatory activities) (48). After 48 h of fermentation of a
medium composed by 5% of defatted wheat germ, the maximum
yield of peptides was obtained. The protein hydrolysate showed
high antioxidant activity, determined as scavenging activity on
DPPH, hydroxyl, and superoxide radicals (49).
Rye Bran
Rye, one of the most important sources of dietary fiber in
European Nordic countries, is often used as whole grain flour
in the making of cereal based products. Nonetheless, rye
bran is also a by-product of conventional milling and can
be used as ingredient to increase food nutritional value (56).
Besides fibers, the bran fraction is rich in many other bioactive
compounds (phenolic acids, phytosterols, tocopherols), among
which alkylresorcinols and steryl ferulates have been studied for
their cancer preventive and antioxidant potential (7, 57, 58). The
influence of fermentation conditions and type of bran (native
or peeled) on the levels of bioactive compounds was studied
(59). Bran fractions, deriving from native or peeled grains were
Rice Germ and Bran
Asian Countries are the major producers of rice, representing
50% of the daily energy supply of the diet of the local population
(68). From the commercial white rice, germ and bran are
removed because the oils they contain are quickly subjected to
rancidity, reducing its shelf-life (7). It is estimated that every
year 120,000 tons of rice husks alone are wasted worldwide
(10). Rice milling by-products are currently underutilized, since
their further exploitation is possible. Rice bran oils and proteins
have demonstrated antioxidant properties and chronic disease
preventing activity, particularly toward cardiovascular disease
and certain cancers (69–71). However, the content of these
bioactive compounds is not equally distributed among rice
varieties (72). Microbial fermentation of rice by-products is an
emerging area of scientific and industrial research. Rice bran
fermented with S. cerevisiae was shown to exert anti-stress and
anti-fatigue effects on rats (73). Moreover, water-soluble extracts
of fermented rice bran had an anti-photoaging effect on human
skin fibroblasts cultures (74). During the last decade, solidstate fungal fermentation of rice bran was extensively studied.
The main results achieved concerned the increase of protein
content and antioxidant activity (75–77), particularly efficient
when the substrate had small particle size (0.18 mm) (78).
When defatted rice bran was fermented with Rhizopus sp.
and
Aspergillus oryzae, a high amino acids release and consequently
a substantial (from 37.5 to 54.3%) chemical score increase (79)
were obtained. Apart from proteins, fibers and minerals, rice
bran is a good source of oil, which can reach up to 20% of
its weight (70). Fermentation with either Rhizopus oryzae or A.
oryzae significantly increased palmitic and linoleic acids content,
causing a decrease in saturated fatty acids and an increase in the
unsaturated ones (80, 81), thus improving the overall nutritional
quality; additionally, when R. oryzae was used as starter for rice
bran fermentation, a 10% reduction of total lipid content was also
observed (80).
Milling By-Products From Other Cereals
Barley and oat significantly differ in their chemical composition
from other cereals; their cell walls are rich in the non-starchy
polysaccharide β-glucan, which is the major component of
the soluble dietary fiber, and has been associated with the
reduction of plasma cholesterol and glycemic index, and a
decreased risk of colon cancer (91). Despite the beneficial
advantages deriving from the consumption of barley and
oat dietary fibers, very little information in the literature
deals with the fermentation of their by-products. Catechin
and proanthocyanidins are among the polyphenol compounds
contained in barley bran. Hordeumin, an anthocyanidin-tannin
purple pigment produced from barley bran fermented using
Salmonella typhimurium, was found to have antimutagen
properties (92). Barley bran hydrolysates were used to obtain
xylitol through bioconversion of xylose-containing solutions
by the yeast Debaryomyces hansenii under microaerophilic
conditions (93). Xylitol is employed in the food industry
to manufacture sugar-free products because of its high
sweetening power, anticaries properties, and its tolerance by
diabetics (94).
Fermentation was used as means to enrich oat bran with
folate. Folate is a generic name for several derivatives of
pteroylglutamic acid (folic acid) and is necessary for methylation
reactions in cell metabolism and for neural development
of fetus during pregnancy (95). Oat bran was fermented
with yeasts isolated from barley kernels and selected for the
ability to synthesize folate, alone or together with lactic acid
bacteria isolated from oat bran. The best folate producers
were S. cerevisiae, followed by Pseudozyma sp., Rhodotorula
glutinis, and Kluyveromyces marxianus. Many yeasts, beyond
the considerable amount of folate produced, caused a decrease
in the viscosity, suggesting a possible generation of soluble
fibers, with positive repercussion on the nutritional effect.
When inoculated together with Streptococcus thermophilus or
L. rhamnosus, S. cerevisiae and Candida milleri produced
significant amount of folates reaching 120 ng/g, suggesting
that the consumption of 100 g of fermented oat bran could
represents 15% of the recommended folates daily intake (95).
Fermentation of oat bran with rye sourdough, previously
obtained with a commercial starter culture containing lactobacilli
and Candida milleri, allowed to double protein and β-glucan
solubility (96).
Trends and Perspectives
The future bio-economy concept, based on a more sustainable
use of agricultural by-products, will require a more efficient
utilization of side streams and waste from food processing
industry to reduce the environmental burden of their generation
and disposal. The exploitation of cereal by-products for
the extraction of their functional compounds, whether for
food, cosmetics, or pharmaceutical industry, offers promising alternative to synthetic compounds and it is an increasing
trend. Nevertheless, this approach implies that more by-products
will be generated once the specific compound is extracted.
Furthermore, if the generation of by-products from food industry
is unavoidable, the best possible valorization of these by-products
should be sought which, in the case of by-products still fit for
human consumption, as described in this review, implies their
re-utilization within the food chain.
As recently pointed out by the EAT Lancet report1
, a diet
rich in plant-derived food and less relying on animal derived
foods is the most beneficial for human health and environment1
.
In this context, the use of the fiber and protein rich part
of cereal by-products in food formulations represents a very
good opportunity to enrich our diet with beneficial compounds.
To contribute to the above objective, the development of
technologies allowing the use of the whole by-product, without
the undesirable features and with improved nutritional quality is
a crucial step.
AUTHOR CONTRIBUTIONS
MV, CR, and RC wrote and critically evaluated the manuscript
making substantial, direct and intellectual contribution to
the work.
FUNDING
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
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