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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 Biotechnology Applied to Cereal Industry By-Products: Nutritional and Functional Insights

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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