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Bran bioprocessing for enhanced functional properties
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ScienceDirect Bran bioprocessing for enhanced functional properties Rossana Coda1, Kati Katina1 and Carlo G Rizzello2 Bran is the nutritious outer layer of the cereal grain, too often discarded during milling, since its use in the food industry poses several technological problems. However, bran provides dietary fiber and many different bioactive substances, including phenolic compounds, which can exert a beneficial effect on human health. The biological value of bran can also be enhanced by different processing techniques, while at the same time also improving some of the technological drawbacks, such as loss of volume in bread and unappealing taste. This review will summarize recent bioprocessing technologies such as enzymatic processing and fermentation, aimed at enhancing the nutritional and technological functionality of bran. Addresses 1 Department of Food and Environmental Sciences, University of Helsinki, Finland 2 Department of Soil, Plant and Food Sciences, University of Bari, 70126 Bari, Italy Corresponding author: Coda, Rossana ([email protected])
Current Opinion in Food Science 2015, 1:50–55 This review comes from a themed issue on Food bioprocessing Edited by Fidel Toldra´ For a complete overview see the Issue and the Editorial Available online 26th November 2014 http://dx.doi.org/10.1016/j.cofs.2014.11.007 2214-7993/# 2014 Elsevier Ltd. All rights reserved.
Introduction Bran is a by-product of the milling process and an important source of fiber, vitamins, minerals and phytochemicals. Although its use in the food and feed industry has increased in the past decade, the major part of bran is still used as livestock feed and only a small percentage is employed for food purposes [1]. The potential health benefits of consuming more whole grain foods have been quite extensively studied in the last years and nowadays the importance of cereal bran is firmly recognized, due to its high content of dietary fiber (DF) and antioxidant compounds [2]. Most consumers still prefer refined white flour to whole grain products, since the textural and flavor properties of bran are perceived as less attractive in comparison with products made with refined flour [3], and, despite the evidence of positive effects on health, the intake of DF is still less than the recommended 25 g/day, according to WHO/FAO suggestions [4]. Current Opinion in Food Science 2015, 1:50–55
During the last years, the research focused on the development of novel technologies, including dry milling and fractionation, leading to new cereal fractions with increased health-promoting compounds [5]. Nevertheless, one of the most important challenges to overcome is to increase the consumption of whole grains by improving their perceived attractiveness. According to a recent study, the major reasons behind a poor consumption are consumer preferences about color, texture, and taste. Therefore, there is an evident need for more appealing whole-grain products to improve consumer acceptance [6]. The use of bran in food applications is more challenging and limited than refined grains also due to some technological drawbacks. In bread, for instance, bran supplementation usually weakens the structure and baking quality of the dough and decreases bread volume and elasticity of the crumb, reducing the overall quality [5,7,8]. Supplementation of bran in bread is successfully accomplished only when processing techniques, such as pre-fermentation, aimed at improving the quality of the baked product, are employed. The development of innovative transformation processes is therefore necessary to increase the value and the usage of this nutritious food matrix by improving the bioaccessibility of health promoting compounds and decreasing the negative technological effects. Bran is indeed a matrix with very complex structure, formed by multiple layers in which arabinoxylans (AX) and b-glucans represent the most abundant cell wall polysaccharides. However, the amount and size of pericarp, aleurone, and the thickness of cell walls and the amount of b-glucan, can vary between different cereals (ex. wheat versus rye) [9]. In these layers, bioactive compounds such as DF and phenolic acids are trapped in the strong cell wall structures resisting conventional milling and thus having low bioaccessibility [5]. Bioaccessibility, which is the release of the compound from its natural matrix to be available for intestinal absorption, is in fact the first limiting factor to bioavailability [10]. Overall, bioprocessing is now considered an efficient tool to improve the nutritional and technological functionality of bran. Bioprocessing commonly refers to the use of biological activity of cells, or their parts, to obtain desirable changes in the matrix. Bioprocessing affects the structure of cereal grains and, by allowing the specific targeting or modifications of components it enhances their health-promoting and technological properties. This review aims at exploring the most recent advances in bioprocessing of bran with a main focus on the effects on www.sciencedirect.com
Bran bioprocessing Coda, Katina and Rizzello 51
the improvement of nutritional and technological functionality. Table 1 summarizes some of these achievements, obtained by the use of microbial enzymes and fermentation.
Enzymatic bioprocessing The intake of DF through whole grains and bran was shown to have beneficial effects on health, including colon cancer, type 2 diabetes and cardiovascular diseases risk [11,12]. In bran, DF polysaccharides are linked through ester bonds with phenolic compounds (PC) [2]. The use of enzymes to solubilize DF and to overall modify the complex structure of the cell walls, is one of the most studied approaches to improve the nutritional and technological functionality of bran [13]. The current
research suggests, in fact, that the positive action of gut microflora is favored when the DF-PC is more accessible, therefore when the DF is less cross-linked [2]. Wheat bran DF consists mainly of arabinoxylan, cellulose, lignin, and some mixed-linkage b-D-glucans [14]. Arabinoxylans (AX) are the major component, exerting a beneficial effect on health and a major impact on the functional properties of wheat bran [5]. The increase of AX solubility has been an important target for selective enzymatic modification in these last years. The use of hydrolytic enzymes such as endoxylanase to hydrolyze water-insoluble AX, causes a cleavage in the backbone structure, allowing more water to be absorbed by the cell wall material [15]. Endoxylanases have been employed to
Table 1 Main nutritional and technological effects of the use of microbial enzymes and fermentation in bioprocessing of bran and whole grain or bran-enriched flours. Bran bioprocessing Cell wall degrading enzymes and yeast fermentation Saccharomyces cerevisiae, Lactobacillus brevis, enzymes mixture (amylase, xylanase and lipase) Endoxylanases Endoxylanases, xylosidases, arabinofurosidases, ferulic acid esterases (enzyme preparation from Humicola insolens) Xylanases (Gryndamyl S100 and from Aspergillus niger, Talaromyces emersonii, Bacillus subtilis) Xylanase (from Bacillus subtilis) Thricoderma spp. enzymes
Xylanase (from Bacillus subtilis) Xylanase (from Bacillus subtilis) Commercial enzyme preparations Viscozyme L, Pectinex 3XL, Ultraflo L, Flavourzyme 500L, Celluclast 1.5L Phytases (from Bifidobacteria) Lactobacillus brevis and Kazachstania exigua fermentation (with or without addition of enzyme mixture with various carbohydrase activities) Yeast and lactic acid bacteria (sourdough) fermentation Yeast fermentation and xylanases Yeast fermentation followed by cell-wall hydrolysing enzymes Sourdough fermentation
Lactobacillus sanfranciscensis and Lactobacillus plantarum fermentation
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Effects
References
Improvement of phenolic compound bioaccessibility. Increase of the levels of human metabolites possessing anti-inflammatory properties as measured ex vivo Improvement of the technological properties
[13,27]
DF solubilization Release of ferulic and p-coumaric acids
[15] [20,21]
Arabinoxylans solubilization
[17]
Arabinoxylans solubilization, improvement of the technological properties Increase of the amount of soluble DF, hydroxycinnamic acids, free phenolic concentration, water-soluble antioxidant activity, and phenol compounds bioavailability Production of oligosaccharides and feruloylated oligosaccharides Production of feruloyl oligosaccharides Improvement of the bioaccessibility of wheat antioxidants
[16,18]
Improvement of mineral bioaccessibility Improvement of technological properties and bioavailability of healthpromoting compounds in bran (folates, phenolic compounds, ferulic acid, antioxidant and phytase activities, content of peptides and total free amino acids and in vitro digestibility of proteins) Increase of folates, free phenolic acids, soluble arabinoxylans. Improvement of structural and technological properties of bread Improvement of physical and chemical properties of dough and bread texture Increase of soluble fiber content, increase of soluble protein content and in vitro digestibility, release of short chain fatty acids Improvement of technological and nutritional properties, overall flavor and sensory aspect; decrease of the starch digestibility and low glycemic response Increase of free amino acids, total phenols, dietary fiber, phytase and antioxidant activities. Improvement of nutritional, textural and sensory properties of breads and decreased the value of hydrolysis index (HI)
[7] [25,30]
[37]
[38]
[39] [19] [24]
[29] [30] [23] [27]
[28]
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52 Food bioprocessing
hydrolyze internal b-1,4 bonds in the main-chain, generating soluble xylooligosaccharides which are suitable substrates for b-xylosidases and leading to the formation of AX oligosaccharides. Arabinoxylan oligosaccharides are important beneficial compounds which act as prebiotic components and their enzymatic release from bran has been extensively studied, as reviewed by Delcour et al. [5]. Xylanases have been applied mostly to solubilize rye and wheat AX [16,17,18], and for the production of oligosaccharides and feruloylated oligosaccharides, which were shown to protect against oxidative stress [19]. Other enzymes, such as a-L-arabinofuranosidases and feruloyl esterases have been used to target a-1,2 and/or a-1,3 bonds that link arabinose to xylose, and ester bonds between ferulic acid and arabinose, respectively [20,21]. Bran is also an important source of low-molecular weight phenolic compounds, among which, ferulic acid (FA) is the most abundant and one of the most interesting, since it exhibits a number of potential biological activities: natural antioxidant, antimicrobial, anti-inflammatory [22]. Most of the FA is however esterified to AX, limiting its bioaccessibility and bioavailability [23]. The release of FA has been obtained with different enzymatic treatments. Feruloyl esterases and glycosyl hydrolases were successfully employed to release almost all the FA from bran [20], while with b-glucanase treatment of wheat bran 50% of the insoluble bound FA was converted into the bioaccessible soluble form [24]. Considering the technological aspect, it was already mentioned that the use of native bran as ingredient for making leavened baked goods was detrimental, showing negative effects on bread volume and crumb, mostly due to alteration in the gluten matrix, and finally on the overall flavor [8,24]. Therefore enzymatic treatments of bran have been applied to bread making in order to solve some of these issues. For instance, the addition of endoxylanases was beneficial to the dough properties and bread quality. Xylanases had a positive impact on dough and bread properties by converting water-unextractable AX into solubilized AX [5], and, in particular, the use of a thermophilic xylanase counteracted the reduction in bread volume when wheat bran was added to bread [26]. Moreover, it was shown [18] that both structural and physicochemical properties of bran are affected by the way of processing, including the water content, probably due to mechanisms related to the bran–water mixture. In detail, mixing bran treated with xylanase at low water content (40%) led to a significant modification of the structure and enhanced AX solubilization as a consequence of the physical breakdown of bran cell walls due to shear forces, in comparison with the same process at high water content (90%) [18]. A future trend might thus include the evaluation of water content in the enzymatic modification, since reduced Current Opinion in Food Science 2015, 1:50–55
water content could be more sustainable and economically convenient, especially if directed to dry products. In this sense, hybrid processing could be a very promising technology to improve functionality of bran [16].
Lactic acid bacteria and yeast fermentation From the nutritional point of view, the efforts made in these last years on bran bioprocessing were directed mostly toward the increase of in vitro and in vivo bioaccessibility of phenolic acids [13,27], and of soluble DF [28]. For this purpose, lactic acid bacteria and yeasts were successfully used for bran fermentation, very often in enzyme-combined bioprocessing. Overall, fermentation favored the enhancement of the bioactive potential of bran and the increase of the concentration of folates, phenolic compounds, FA and solubilized pentosans [29]. This effect was even more evident when bioprocessing was carried out by microbial fermentation and hydrolytic enzymes [13,29,30]. In addition to DF and phenolic compounds, bran is also considered as important source of minerals and of phytic acid, which is the major anti-nutritional factor for micronutrient absorption. It has been widely reported in the literature that during sourdough fermentation (involving a microbial consortium of lactic acid bacteria and yeasts), the action of endogenous enzymes together with microbial phytase activity, results in an improvement of mineral bioavailability [31]. This is also shown in a recent study, where bioprocessing of wheat bran with Lactobacillus brevis E95612 and Kazachstania exigua C81116 improved the antioxidant and phytase activities, the content of peptides and total free amino acids and the in vitro digestibility of proteins [30]. Enzyme addition during fermentation further enhanced the positive effects of the microbial starters [29,30,32]. In particular, the presence of a mixture of enzymes with various carbohydratedegrading activities favored the growth of L. brevis by increasing the content of fermentable sugars. As a consequence, the lower pH and enhanced microbial and bran endogenous enzymatic activities, promoted proteolytic and phytase activities [29]. An enzyme mixture containing xylanase, b-glucanase, a-amylase, cellulase and ferulic acid esterase in combination with Saccharomyces cerevisiae (baker’s yeast), a microbial source of the same enzymatic activities, was used for bioprocessing of wheat bran, leading to an enhanced in vitro and in vivo bioaccessibility of phenolic acids and their circulating metabolites, compounds which have immunomodulatory effects ex vivo [27]. Analogous positive effects were observed also in bioprocessing of rye bran when the use of cell-wall hydrolyzing enzymes was followed by S. cerevisiae fermentation, resulting in higher soluble fiber and soluble protein content, higher in vitro protein digestibility, and faster release of short chain fatty acids through fermentation www.sciencedirect.com
Bran bioprocessing Coda, Katina and Rizzello 53
Figure 1
(a)
(b)
500 µm
(c)
500 µm
500 µm Current Opinion in Food Science
Microstructure of native bran (50 mm particle size) before bioprocessing (a), after fermentation with Lactobacillus brevis and Kazachstania exigua without (b) or with (c) the addition of enzymes having carbohydrase activities (c). b-Glucan in aleurone cell walls and endosperm is stained in blue, the pericarp layer is stained in green, and proteins are stained in red and reddish brown. The pigment strand (between pericarp and aleurone layer) is stained in orange. Starch is unstained and appears black. Adapted from [30].
[28]. Besides the improvement of the protein digestibility, sourdough technology was also effective in reducing the starch digestibility and lowering the glycemic response when applied to the production of baked goods containing whole grain and bran as ingredient [33,34]. The extent of these modifications as well as the metabolite profile can be modulated and tailored by changing the dimension of the bran particles during milling prior to fermentation [28,30], and by adjusting aeration conditions during fermentation [32]. It was reported that bioprocessing induced modifications in cell wall structure, mainly in the aleurone layer, that affected bran composition [30]. Indeed, a partial disruption of the structures of the different layers was observed after fermentation, as the consequence of the extensive breakdown of the cell wall structures caused by the combined activities of added, endogenous, and microbial enzymes during bioprocessing of bran [30]. In particular, a release of protein and the degradation of fructans and b-glucans were observed [28]. A representative image obtained by epifluorescence microscopy, concerning the modification of bran structure through bioprocessing, is shown in Figure 1. Bioprocessing of wheat and rye bran with selected lactic acid bacteria or yeasts before baking was a successful strategy to improve loaf volume, crumb structure, flavor and shelf life of bread [25,35]. Sourdough fermentation has shown several positive effects on the technological and nutritional functionality of bran. It improved the texture and palatability of whole grain and fiber-rich products and was particularly effective in increasing the intensity of flavor attributes [25,35]. In comparison with the native, bioprocessed bran did not increase pungent flavor or bitter aftertaste of bread [25]. Overall, as www.sciencedirect.com
already observed by Poutanen et al. [31], sourdough fermentation has shown several positive effects on the nutritional and technological functionality of bran. In high fiber baking, it exerted positive effects on bread structure, texture and flavor, as well as on the glycemic response [33]. The presence of DF in bread was shown to reduce the glycemic response by effecting starch state, water distribution in the matrix, and by increasing the viscosity of digesta [31]. In particular, the preservation of starch from the access of human amylases, as well as the reduced pH during sourdough fermentation that may delay gastric emptying or create a barrier to starch digestion, seems to be more effective than DF per se in improving glucose metabolism [36].
Conclusions The current knowledge about the importance of exploiting more of the cereal bran in healthy food is promoting the development of new technologies to be employed for the next generation of cereal-based food with high content of dietary fiber, phytonutrients and added protein sources [31]. Despite the increased awareness for the potential health benefits derived from whole grain foods consumption, consumer barriers have not yet been overcome. So far, bran addition to food has been a difficult task when considering the technological and sensory performance of the final product. Native bran is not suitable to be directly used in food application for different reasons, like its high water-holding capacity that alters the volume and elasticity of the dough in bread making, and the negative sensory attributes, such as bitterness and gritty mouthfeel [1]. Both chemical composition and food structure must be considered for the development of palatable and health-promoting food added with bran. This aspect seems to be still particularly important since the sensory Current Opinion in Food Science 2015, 1:50–55
54 Food bioprocessing
quality is driving the consumer’s choice. Bioprocessing is considered an efficient and environmentally friendly tool to obtain desired changes in the bran matrix, and the most recent findings show that it is an important pre-requisite for improving bran functionality and usability. The targeted modification of specific structures is able to positively affect both the nutritional and technological performances of bran. As a consequence, the changes in the structure, and the new interactions between different molecules, enhance the bioaccessibility and bioavailability of health promoting compounds, exploiting more of bran functional potential. Together with new milling techniques, bioprocessing by fermentation and enzyme technologies represent a new possibility for improved whole grain food.
References Pru¨ckler M, Siebenhandl-Ehn S, Apprich S, Ho¨ltinger S, Haas C, Schmid E, Kneifel W: Wheat bran-based biorefinery 1: composition of wheat bran and strategies of functionalization. LWT-Food Sci Technol 2014, 56:211-221. A state-of-the-art of the technological approaches, including enzymatic treatment, used to modify the functional properties of wheat bran.
[1.
[2]. Vitaglione P, Napolitano A, Fogliano V: Cereal dietary fibre: a natural functional ingredient to deliver phenolic compounds into the gut. Trends Food Sci Technol 2008, 19:451-463. [3]. Bakke A, Vickers Z: Consumer liking of refined and whole wheat breads. J Food Sci 2007, 72:S473-S480. [4]. WHO: Diet, Nutrition and the Prevention of Chronic Diseases. Technical Report Series; 2003:: 916. Delcour JA, Rouau X, Courtin CM, Poutanen K, Ranieri R: Technologies for enhanced exploitation of the healthpromoting potential of cereals. Trends Food Sci Technol 2012, 25:78-86. This review describes the novel technologies for whole grain processing considering also the modification of bran matrix and the health potential.
[5.
[6]. McKeown NM, Jacques PF, Seal CJ, de Vries J, Jonnalagadda SS, Clemens R, Webb D, Murphy LA, van Klinken J-W, Topping D, Murray R, Degeneffe D, Marquart LF: Whole grains and health: from theory to practice. J Nutr 2013, 143:744S-758S. [7]. Sanz Penella J, Collar C, Haros M: Effect of wheat bran and enzyme addition on dough functional performance and phytic acid levels in bread. J Cereal Sci 2008, 48:715-721. [8]. Noort MW, van Haaster D, Hemery Y, Schols HA, Hamer RJ: The effect of particle size of wheat bran fractions on bread quality — evidence for fibre–protein interactions. J Cereal Sci 2010, 52:59-64. [9]. Kamal-Eldin A, Lærke HN, Bach Knudsen K-E, Lampi A-M, Piironen V, Adlercreutz H, Katina K, Poutanen K, Man P: Physical, microscopic and chemical characterisation of industrial rye and wheat brans from the Nordic countries. Food Nutr Res 2009, 53 http://dx.doi.org/10.3402/fnr.v53i0.1912. [10]. Stahl W, van den Berg H, Arthur J, Bast A, Dainty J, Faulks RM, Ga¨rtner C, Haenen G, Hollman P, Holst B: Bioavailability and metabolism. Mol Aspects Med 2002, 23:39-100. [11]. Aune D, Chan DSM, La R, Vieira R, Greenwood DC, Kampna E, Norat T: Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose–response meta-analysis of prospective studies. BMJ 2011, 343:d6617. [12]. Ye EQ, Chacko SA, Chou EL, Kugizak M, Liu S: Greater wholegrain intake is associated with lower risk of type 2 diabetes, cardiovascular disease, and weight gain. J Nutr 2012, 142:1304-1313. Current Opinion in Food Science 2015, 1:50–55
[13]. Mateo Anson N, van den Berg R, Havenaar R, Bast A, Haenen GR: Bioavailability of ferulic acid is determined by its bioaccessibility. J Cereal Sci 2009, 49:296-300. [14]. DuPont MS, Selvendran RR: Hemicellulosic polymers from the cell walls of beeswing wheat bran: part I, polymers solubilised by alkali at 2-. Carbohydr Res 1987, 163:99-113. [15]. Petersson K, Nordlund E, Tornberg E, Eliasson AC, Buchert J: Impact of cell wall-degrading enzymes on water-holding capacity and solubility of dietary fibre in rye and wheat bran. J Sci Food Agric 2013, 93:882-889. [16]. Santala O, Lehtinen P, Nordlund E, Suortti T, Poutanen K: Impact of water content on the solubilisation of arabinoxylan during xylanase treatment of wheat bran. J Cereal Sci 2011, 54:187-194. [17]. Figueroa-Espinoza M-C, Poulsen C, Borch Søe J, Zargahi MR, Rouau X: Enzymatic solubilization of arabinoxylans from native, extruded, and high-shear-treated rye bran by different endo-xylanases and other hydrolyzing enzymes. J Agric Food Chem 2004, 52:4240-4249. [18. Santala OK, Nordlund EA, Poutanen KS: Treatments with xylanase at high (90%) and low (40%) water content have different impacts on physicochemical properties of wheat bran. Food Bioprocess Technol 2013, 6:3102-3112. This paper describes the different effects of water content on the enzymatic processing of bran. [19]. Yuan X, Wang J, Yao H: Production of feruloyl oligosaccharides from wheat bran insoluble dietary fibre by xylanases from Bacillus subtilis. Food Chem 2006, 95:484-492. [20]. Faulds C, Mandalari G, LoCurto R, Bisignano G, Waldron K: Arabinoxylan and mono-and dimeric ferulic acid release from brewer’s grain and wheat bran by feruloyl esterases and glycosyl hydrolases from Humicola insolens. Appl Microbiol Biotechnol 2004, 64:644-650. [21]. Sørensen HR, Jørgensen CT, Hansen CH, Jørgensen CI, Pedersen S, Meyer AS: A novel GH43 a-L-arabinofuranosidase from Humicola insolens: mode of action and synergy with GH51 a-L-arabinofuranosidases on wheat arabinoxylan. Appl Microbiol Biotechnol 2006, 73:850-861. [22]. Graf E: Antioxidant potential of ferulic acid. Free Radic Biol Med 1992, 13:435-448. [23. Mateo Anson N, Hemery YM, Bast A, Haenen GR: Optimizing the bioactive potential of wheat bran by processing. Food Funct 2012, 3:362-375. Overview dealing with the bioactive potential of bran and its improvement by processing. [24]. Moore J, Liu JG, Zhou K, Yu L: Effects of genotype and environment on the antioxidant properties of hard winter wheat bran. J Agric Food Chem 2006, 54:5313-5322. [25]. Coda R, Ka¨rki I, Nordlund E, Heinio¨ R-L, Poutanen K, Katina K: Influence of particle size on bioprocess induced changes on technological functionality of wheat bran. Food Microbiol 2014, 37:69-77. [26]. Bram Damen B, Pollet A, Dornez E, Willem FB, Van Haesendonck I, Trogh I, Arnaut F, Delcour JA, Courtin CM: Xylanase-mediated in situ production of arabinoxylan oligosaccharides with prebiotic potential in whole meal breads and breads enriched with arabinoxylan rich materials. Food Chem 2012, 131:11-118. [27]. Mateo Anson N, Aura AM, Selinheimo E, Mattila I, Poutanen K, van den Berg R, Havenaar R, Bast A, Haenen GR: Bioprocessing of wheat bran in whole wheat bread increases the bioavailability of phenolic acids in men and exerts antiinflammatory effects ex vivo. J Nutr 2011, 141:137-143. [28]. Nordlund E, Katina K, Aura A-M, Poutanen K: Changes in bran structure by bioprocessing with enzymes and yeast modifies the in vitro digestibility and fermentability of bran protein and dietary fibre complex. J Cereal Sci 2013, 58:200-208. [29. Katina K, Juvonen R, Laitila A, Flander L, Nordlund E, Kariluoto S, Piironen V, Poutanen K: Fermented wheat bran as a functional ingredient in baking. Cereal Chem 2012, 89:126-134. This article describes the effects of fermentation and type of bran on technological functionality. www.sciencedirect.com
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[30. Coda R, Rizzello CG, Curiel JA, Poutanen K, Katina K: Effect of bioprocessing and particle size on the nutritional properties of wheat bran fractions. Innov Food Sci Emerg 2013 http:// dx.doi.org/10.1016/j.ifset.2013.11.012. This article describes the effect of bioprocessing on several nutritional features of wheat bran having different particle size. [31. Poutanen K, Sozer N, Della Valle G: How can technology help to deliver more of grain in cereal foods for a healthy diet? J Cereal Sci 2014, 59:327-336. Review reporting new technologies in cereal processing with an emphasis on whole grain foods. [32]. Savolainen OI, Coda R, Suomi K, Katina K, Juvonen R, Hanhineva K, Poutanen K: The role of oxygen in the liquid fermentation of wheat bran. Food Chem 2014, 153:424-431. [33]. Poutanen K, Flander L, Katina K: Sourdough and cereal fermentation in a nutritional perspective. Food Microbiol 2009, 26:693-699. [34]. Rizzello CG, Coda R, Mazzacane F, Minervini D, Gobbetti M: Micronized by-products from debranned durum wheat and
www.sciencedirect.com
sourdough fermentation enhanced the nutritional, textural and sensory features of bread. Food Res Int 2012, 46:304-313. [35]. Hartikainen K, Poutanen K, Katina K: Influence of bioprocessed wheat bran on the physical and chemical properties of dough and on wheat bread texture. Cereal Chem 2014, 91:115-123. [36]. Scazzina F, Siebenhandl-Ehn S, Nicoletta Pellegrini N: The effect of dietary fibre on reducing the glycaemic index of bread. Br J Nutr 2013, 109:1163-1174. [37]. Katina K, Salmenkallio-Marttila M, Partanen R, Forssell P, Autio K: Effects of sourdough and enzymes on staling of high-fibre wheat bread. LWT-Food Sci Technol 2006, 39:479-491. [38]. Napolitano A, Lanzuise S, Ruocco M, Arlotti G, Ranieri R, Knutsen SH, Lorito M, Fogliano V: Treatment of cereal products with a tailored preparation of Trichoderma enzymes increases the amount of soluble dietary fiber. J Agric Food Chem 2006, 54:7863-7869. [39]. Swennen K, Courtin CM, Delcour JA: Non-digestible oligosaccharides with prebiotic properties. Crit Rev Food Sci 2006, 46:459-471.
Current Opinion in Food Science 2015, 1:50–55
ScienceDirect Bran bioprocessing for enhanced functional properties Rossana Coda1, Kati Katina1 and Carlo G Rizzello2 Bran is the nutritious outer layer of the cereal grain, too often discarded during milling, since its use in the food industry poses several technological problems. However, bran provides dietary fiber and many different bioactive substances, including phenolic compounds, which can exert a beneficial effect on human health. The biological value of bran can also be enhanced by different processing techniques, while at the same time also improving some of the technological drawbacks, such as loss of volume in bread and unappealing taste. This review will summarize recent bioprocessing technologies such as enzymatic processing and fermentation, aimed at enhancing the nutritional and technological functionality of bran. Addresses 1 Department of Food and Environmental Sciences, University of Helsinki, Finland 2 Department of Soil, Plant and Food Sciences, University of Bari, 70126 Bari, Italy Corresponding author: Coda, Rossana ([email protected])
Current Opinion in Food Science 2015, 1:50–55 This review comes from a themed issue on Food bioprocessing Edited by Fidel Toldra´ For a complete overview see the Issue and the Editorial Available online 26th November 2014 http://dx.doi.org/10.1016/j.cofs.2014.11.007 2214-7993/# 2014 Elsevier Ltd. All rights reserved.
Introduction Bran is a by-product of the milling process and an important source of fiber, vitamins, minerals and phytochemicals. Although its use in the food and feed industry has increased in the past decade, the major part of bran is still used as livestock feed and only a small percentage is employed for food purposes [1]. The potential health benefits of consuming more whole grain foods have been quite extensively studied in the last years and nowadays the importance of cereal bran is firmly recognized, due to its high content of dietary fiber (DF) and antioxidant compounds [2]. Most consumers still prefer refined white flour to whole grain products, since the textural and flavor properties of bran are perceived as less attractive in comparison with products made with refined flour [3], and, despite the evidence of positive effects on health, the intake of DF is still less than the recommended 25 g/day, according to WHO/FAO suggestions [4]. Current Opinion in Food Science 2015, 1:50–55
During the last years, the research focused on the development of novel technologies, including dry milling and fractionation, leading to new cereal fractions with increased health-promoting compounds [5]. Nevertheless, one of the most important challenges to overcome is to increase the consumption of whole grains by improving their perceived attractiveness. According to a recent study, the major reasons behind a poor consumption are consumer preferences about color, texture, and taste. Therefore, there is an evident need for more appealing whole-grain products to improve consumer acceptance [6]. The use of bran in food applications is more challenging and limited than refined grains also due to some technological drawbacks. In bread, for instance, bran supplementation usually weakens the structure and baking quality of the dough and decreases bread volume and elasticity of the crumb, reducing the overall quality [5,7,8]. Supplementation of bran in bread is successfully accomplished only when processing techniques, such as pre-fermentation, aimed at improving the quality of the baked product, are employed. The development of innovative transformation processes is therefore necessary to increase the value and the usage of this nutritious food matrix by improving the bioaccessibility of health promoting compounds and decreasing the negative technological effects. Bran is indeed a matrix with very complex structure, formed by multiple layers in which arabinoxylans (AX) and b-glucans represent the most abundant cell wall polysaccharides. However, the amount and size of pericarp, aleurone, and the thickness of cell walls and the amount of b-glucan, can vary between different cereals (ex. wheat versus rye) [9]. In these layers, bioactive compounds such as DF and phenolic acids are trapped in the strong cell wall structures resisting conventional milling and thus having low bioaccessibility [5]. Bioaccessibility, which is the release of the compound from its natural matrix to be available for intestinal absorption, is in fact the first limiting factor to bioavailability [10]. Overall, bioprocessing is now considered an efficient tool to improve the nutritional and technological functionality of bran. Bioprocessing commonly refers to the use of biological activity of cells, or their parts, to obtain desirable changes in the matrix. Bioprocessing affects the structure of cereal grains and, by allowing the specific targeting or modifications of components it enhances their health-promoting and technological properties. This review aims at exploring the most recent advances in bioprocessing of bran with a main focus on the effects on www.sciencedirect.com
Bran bioprocessing Coda, Katina and Rizzello 51
the improvement of nutritional and technological functionality. Table 1 summarizes some of these achievements, obtained by the use of microbial enzymes and fermentation.
Enzymatic bioprocessing The intake of DF through whole grains and bran was shown to have beneficial effects on health, including colon cancer, type 2 diabetes and cardiovascular diseases risk [11,12]. In bran, DF polysaccharides are linked through ester bonds with phenolic compounds (PC) [2]. The use of enzymes to solubilize DF and to overall modify the complex structure of the cell walls, is one of the most studied approaches to improve the nutritional and technological functionality of bran [13]. The current
research suggests, in fact, that the positive action of gut microflora is favored when the DF-PC is more accessible, therefore when the DF is less cross-linked [2]. Wheat bran DF consists mainly of arabinoxylan, cellulose, lignin, and some mixed-linkage b-D-glucans [14]. Arabinoxylans (AX) are the major component, exerting a beneficial effect on health and a major impact on the functional properties of wheat bran [5]. The increase of AX solubility has been an important target for selective enzymatic modification in these last years. The use of hydrolytic enzymes such as endoxylanase to hydrolyze water-insoluble AX, causes a cleavage in the backbone structure, allowing more water to be absorbed by the cell wall material [15]. Endoxylanases have been employed to
Table 1 Main nutritional and technological effects of the use of microbial enzymes and fermentation in bioprocessing of bran and whole grain or bran-enriched flours. Bran bioprocessing Cell wall degrading enzymes and yeast fermentation Saccharomyces cerevisiae, Lactobacillus brevis, enzymes mixture (amylase, xylanase and lipase) Endoxylanases Endoxylanases, xylosidases, arabinofurosidases, ferulic acid esterases (enzyme preparation from Humicola insolens) Xylanases (Gryndamyl S100 and from Aspergillus niger, Talaromyces emersonii, Bacillus subtilis) Xylanase (from Bacillus subtilis) Thricoderma spp. enzymes
Xylanase (from Bacillus subtilis) Xylanase (from Bacillus subtilis) Commercial enzyme preparations Viscozyme L, Pectinex 3XL, Ultraflo L, Flavourzyme 500L, Celluclast 1.5L Phytases (from Bifidobacteria) Lactobacillus brevis and Kazachstania exigua fermentation (with or without addition of enzyme mixture with various carbohydrase activities) Yeast and lactic acid bacteria (sourdough) fermentation Yeast fermentation and xylanases Yeast fermentation followed by cell-wall hydrolysing enzymes Sourdough fermentation
Lactobacillus sanfranciscensis and Lactobacillus plantarum fermentation
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Effects
References
Improvement of phenolic compound bioaccessibility. Increase of the levels of human metabolites possessing anti-inflammatory properties as measured ex vivo Improvement of the technological properties
[13,27]
DF solubilization Release of ferulic and p-coumaric acids
[15] [20,21]
Arabinoxylans solubilization
[17]
Arabinoxylans solubilization, improvement of the technological properties Increase of the amount of soluble DF, hydroxycinnamic acids, free phenolic concentration, water-soluble antioxidant activity, and phenol compounds bioavailability Production of oligosaccharides and feruloylated oligosaccharides Production of feruloyl oligosaccharides Improvement of the bioaccessibility of wheat antioxidants
[16,18]
Improvement of mineral bioaccessibility Improvement of technological properties and bioavailability of healthpromoting compounds in bran (folates, phenolic compounds, ferulic acid, antioxidant and phytase activities, content of peptides and total free amino acids and in vitro digestibility of proteins) Increase of folates, free phenolic acids, soluble arabinoxylans. Improvement of structural and technological properties of bread Improvement of physical and chemical properties of dough and bread texture Increase of soluble fiber content, increase of soluble protein content and in vitro digestibility, release of short chain fatty acids Improvement of technological and nutritional properties, overall flavor and sensory aspect; decrease of the starch digestibility and low glycemic response Increase of free amino acids, total phenols, dietary fiber, phytase and antioxidant activities. Improvement of nutritional, textural and sensory properties of breads and decreased the value of hydrolysis index (HI)
[7] [25,30]
[37]
[38]
[39] [19] [24]
[29] [30] [23] [27]
[28]
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52 Food bioprocessing
hydrolyze internal b-1,4 bonds in the main-chain, generating soluble xylooligosaccharides which are suitable substrates for b-xylosidases and leading to the formation of AX oligosaccharides. Arabinoxylan oligosaccharides are important beneficial compounds which act as prebiotic components and their enzymatic release from bran has been extensively studied, as reviewed by Delcour et al. [5]. Xylanases have been applied mostly to solubilize rye and wheat AX [16,17,18], and for the production of oligosaccharides and feruloylated oligosaccharides, which were shown to protect against oxidative stress [19]. Other enzymes, such as a-L-arabinofuranosidases and feruloyl esterases have been used to target a-1,2 and/or a-1,3 bonds that link arabinose to xylose, and ester bonds between ferulic acid and arabinose, respectively [20,21]. Bran is also an important source of low-molecular weight phenolic compounds, among which, ferulic acid (FA) is the most abundant and one of the most interesting, since it exhibits a number of potential biological activities: natural antioxidant, antimicrobial, anti-inflammatory [22]. Most of the FA is however esterified to AX, limiting its bioaccessibility and bioavailability [23]. The release of FA has been obtained with different enzymatic treatments. Feruloyl esterases and glycosyl hydrolases were successfully employed to release almost all the FA from bran [20], while with b-glucanase treatment of wheat bran 50% of the insoluble bound FA was converted into the bioaccessible soluble form [24]. Considering the technological aspect, it was already mentioned that the use of native bran as ingredient for making leavened baked goods was detrimental, showing negative effects on bread volume and crumb, mostly due to alteration in the gluten matrix, and finally on the overall flavor [8,24]. Therefore enzymatic treatments of bran have been applied to bread making in order to solve some of these issues. For instance, the addition of endoxylanases was beneficial to the dough properties and bread quality. Xylanases had a positive impact on dough and bread properties by converting water-unextractable AX into solubilized AX [5], and, in particular, the use of a thermophilic xylanase counteracted the reduction in bread volume when wheat bran was added to bread [26]. Moreover, it was shown [18] that both structural and physicochemical properties of bran are affected by the way of processing, including the water content, probably due to mechanisms related to the bran–water mixture. In detail, mixing bran treated with xylanase at low water content (40%) led to a significant modification of the structure and enhanced AX solubilization as a consequence of the physical breakdown of bran cell walls due to shear forces, in comparison with the same process at high water content (90%) [18]. A future trend might thus include the evaluation of water content in the enzymatic modification, since reduced Current Opinion in Food Science 2015, 1:50–55
water content could be more sustainable and economically convenient, especially if directed to dry products. In this sense, hybrid processing could be a very promising technology to improve functionality of bran [16].
Lactic acid bacteria and yeast fermentation From the nutritional point of view, the efforts made in these last years on bran bioprocessing were directed mostly toward the increase of in vitro and in vivo bioaccessibility of phenolic acids [13,27], and of soluble DF [28]. For this purpose, lactic acid bacteria and yeasts were successfully used for bran fermentation, very often in enzyme-combined bioprocessing. Overall, fermentation favored the enhancement of the bioactive potential of bran and the increase of the concentration of folates, phenolic compounds, FA and solubilized pentosans [29]. This effect was even more evident when bioprocessing was carried out by microbial fermentation and hydrolytic enzymes [13,29,30]. In addition to DF and phenolic compounds, bran is also considered as important source of minerals and of phytic acid, which is the major anti-nutritional factor for micronutrient absorption. It has been widely reported in the literature that during sourdough fermentation (involving a microbial consortium of lactic acid bacteria and yeasts), the action of endogenous enzymes together with microbial phytase activity, results in an improvement of mineral bioavailability [31]. This is also shown in a recent study, where bioprocessing of wheat bran with Lactobacillus brevis E95612 and Kazachstania exigua C81116 improved the antioxidant and phytase activities, the content of peptides and total free amino acids and the in vitro digestibility of proteins [30]. Enzyme addition during fermentation further enhanced the positive effects of the microbial starters [29,30,32]. In particular, the presence of a mixture of enzymes with various carbohydratedegrading activities favored the growth of L. brevis by increasing the content of fermentable sugars. As a consequence, the lower pH and enhanced microbial and bran endogenous enzymatic activities, promoted proteolytic and phytase activities [29]. An enzyme mixture containing xylanase, b-glucanase, a-amylase, cellulase and ferulic acid esterase in combination with Saccharomyces cerevisiae (baker’s yeast), a microbial source of the same enzymatic activities, was used for bioprocessing of wheat bran, leading to an enhanced in vitro and in vivo bioaccessibility of phenolic acids and their circulating metabolites, compounds which have immunomodulatory effects ex vivo [27]. Analogous positive effects were observed also in bioprocessing of rye bran when the use of cell-wall hydrolyzing enzymes was followed by S. cerevisiae fermentation, resulting in higher soluble fiber and soluble protein content, higher in vitro protein digestibility, and faster release of short chain fatty acids through fermentation www.sciencedirect.com
Bran bioprocessing Coda, Katina and Rizzello 53
Figure 1
(a)
(b)
500 µm
(c)
500 µm
500 µm Current Opinion in Food Science
Microstructure of native bran (50 mm particle size) before bioprocessing (a), after fermentation with Lactobacillus brevis and Kazachstania exigua without (b) or with (c) the addition of enzymes having carbohydrase activities (c). b-Glucan in aleurone cell walls and endosperm is stained in blue, the pericarp layer is stained in green, and proteins are stained in red and reddish brown. The pigment strand (between pericarp and aleurone layer) is stained in orange. Starch is unstained and appears black. Adapted from [30].
[28]. Besides the improvement of the protein digestibility, sourdough technology was also effective in reducing the starch digestibility and lowering the glycemic response when applied to the production of baked goods containing whole grain and bran as ingredient [33,34]. The extent of these modifications as well as the metabolite profile can be modulated and tailored by changing the dimension of the bran particles during milling prior to fermentation [28,30], and by adjusting aeration conditions during fermentation [32]. It was reported that bioprocessing induced modifications in cell wall structure, mainly in the aleurone layer, that affected bran composition [30]. Indeed, a partial disruption of the structures of the different layers was observed after fermentation, as the consequence of the extensive breakdown of the cell wall structures caused by the combined activities of added, endogenous, and microbial enzymes during bioprocessing of bran [30]. In particular, a release of protein and the degradation of fructans and b-glucans were observed [28]. A representative image obtained by epifluorescence microscopy, concerning the modification of bran structure through bioprocessing, is shown in Figure 1. Bioprocessing of wheat and rye bran with selected lactic acid bacteria or yeasts before baking was a successful strategy to improve loaf volume, crumb structure, flavor and shelf life of bread [25,35]. Sourdough fermentation has shown several positive effects on the technological and nutritional functionality of bran. It improved the texture and palatability of whole grain and fiber-rich products and was particularly effective in increasing the intensity of flavor attributes [25,35]. In comparison with the native, bioprocessed bran did not increase pungent flavor or bitter aftertaste of bread [25]. Overall, as www.sciencedirect.com
already observed by Poutanen et al. [31], sourdough fermentation has shown several positive effects on the nutritional and technological functionality of bran. In high fiber baking, it exerted positive effects on bread structure, texture and flavor, as well as on the glycemic response [33]. The presence of DF in bread was shown to reduce the glycemic response by effecting starch state, water distribution in the matrix, and by increasing the viscosity of digesta [31]. In particular, the preservation of starch from the access of human amylases, as well as the reduced pH during sourdough fermentation that may delay gastric emptying or create a barrier to starch digestion, seems to be more effective than DF per se in improving glucose metabolism [36].
Conclusions The current knowledge about the importance of exploiting more of the cereal bran in healthy food is promoting the development of new technologies to be employed for the next generation of cereal-based food with high content of dietary fiber, phytonutrients and added protein sources [31]. Despite the increased awareness for the potential health benefits derived from whole grain foods consumption, consumer barriers have not yet been overcome. So far, bran addition to food has been a difficult task when considering the technological and sensory performance of the final product. Native bran is not suitable to be directly used in food application for different reasons, like its high water-holding capacity that alters the volume and elasticity of the dough in bread making, and the negative sensory attributes, such as bitterness and gritty mouthfeel [1]. Both chemical composition and food structure must be considered for the development of palatable and health-promoting food added with bran. This aspect seems to be still particularly important since the sensory Current Opinion in Food Science 2015, 1:50–55
54 Food bioprocessing
quality is driving the consumer’s choice. Bioprocessing is considered an efficient and environmentally friendly tool to obtain desired changes in the bran matrix, and the most recent findings show that it is an important pre-requisite for improving bran functionality and usability. The targeted modification of specific structures is able to positively affect both the nutritional and technological performances of bran. As a consequence, the changes in the structure, and the new interactions between different molecules, enhance the bioaccessibility and bioavailability of health promoting compounds, exploiting more of bran functional potential. Together with new milling techniques, bioprocessing by fermentation and enzyme technologies represent a new possibility for improved whole grain food.
References Pru¨ckler M, Siebenhandl-Ehn S, Apprich S, Ho¨ltinger S, Haas C, Schmid E, Kneifel W: Wheat bran-based biorefinery 1: composition of wheat bran and strategies of functionalization. LWT-Food Sci Technol 2014, 56:211-221. A state-of-the-art of the technological approaches, including enzymatic treatment, used to modify the functional properties of wheat bran.
[1.
[2]. Vitaglione P, Napolitano A, Fogliano V: Cereal dietary fibre: a natural functional ingredient to deliver phenolic compounds into the gut. Trends Food Sci Technol 2008, 19:451-463. [3]. Bakke A, Vickers Z: Consumer liking of refined and whole wheat breads. J Food Sci 2007, 72:S473-S480. [4]. WHO: Diet, Nutrition and the Prevention of Chronic Diseases. Technical Report Series; 2003:: 916. Delcour JA, Rouau X, Courtin CM, Poutanen K, Ranieri R: Technologies for enhanced exploitation of the healthpromoting potential of cereals. Trends Food Sci Technol 2012, 25:78-86. This review describes the novel technologies for whole grain processing considering also the modification of bran matrix and the health potential.
[5.
[6]. McKeown NM, Jacques PF, Seal CJ, de Vries J, Jonnalagadda SS, Clemens R, Webb D, Murphy LA, van Klinken J-W, Topping D, Murray R, Degeneffe D, Marquart LF: Whole grains and health: from theory to practice. J Nutr 2013, 143:744S-758S. [7]. Sanz Penella J, Collar C, Haros M: Effect of wheat bran and enzyme addition on dough functional performance and phytic acid levels in bread. J Cereal Sci 2008, 48:715-721. [8]. Noort MW, van Haaster D, Hemery Y, Schols HA, Hamer RJ: The effect of particle size of wheat bran fractions on bread quality — evidence for fibre–protein interactions. J Cereal Sci 2010, 52:59-64. [9]. Kamal-Eldin A, Lærke HN, Bach Knudsen K-E, Lampi A-M, Piironen V, Adlercreutz H, Katina K, Poutanen K, Man P: Physical, microscopic and chemical characterisation of industrial rye and wheat brans from the Nordic countries. Food Nutr Res 2009, 53 http://dx.doi.org/10.3402/fnr.v53i0.1912. [10]. Stahl W, van den Berg H, Arthur J, Bast A, Dainty J, Faulks RM, Ga¨rtner C, Haenen G, Hollman P, Holst B: Bioavailability and metabolism. Mol Aspects Med 2002, 23:39-100. [11]. Aune D, Chan DSM, La R, Vieira R, Greenwood DC, Kampna E, Norat T: Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose–response meta-analysis of prospective studies. BMJ 2011, 343:d6617. [12]. Ye EQ, Chacko SA, Chou EL, Kugizak M, Liu S: Greater wholegrain intake is associated with lower risk of type 2 diabetes, cardiovascular disease, and weight gain. J Nutr 2012, 142:1304-1313. Current Opinion in Food Science 2015, 1:50–55
[13]. Mateo Anson N, van den Berg R, Havenaar R, Bast A, Haenen GR: Bioavailability of ferulic acid is determined by its bioaccessibility. J Cereal Sci 2009, 49:296-300. [14]. DuPont MS, Selvendran RR: Hemicellulosic polymers from the cell walls of beeswing wheat bran: part I, polymers solubilised by alkali at 2-. Carbohydr Res 1987, 163:99-113. [15]. Petersson K, Nordlund E, Tornberg E, Eliasson AC, Buchert J: Impact of cell wall-degrading enzymes on water-holding capacity and solubility of dietary fibre in rye and wheat bran. J Sci Food Agric 2013, 93:882-889. [16]. Santala O, Lehtinen P, Nordlund E, Suortti T, Poutanen K: Impact of water content on the solubilisation of arabinoxylan during xylanase treatment of wheat bran. J Cereal Sci 2011, 54:187-194. [17]. Figueroa-Espinoza M-C, Poulsen C, Borch Søe J, Zargahi MR, Rouau X: Enzymatic solubilization of arabinoxylans from native, extruded, and high-shear-treated rye bran by different endo-xylanases and other hydrolyzing enzymes. J Agric Food Chem 2004, 52:4240-4249. [18. Santala OK, Nordlund EA, Poutanen KS: Treatments with xylanase at high (90%) and low (40%) water content have different impacts on physicochemical properties of wheat bran. Food Bioprocess Technol 2013, 6:3102-3112. This paper describes the different effects of water content on the enzymatic processing of bran. [19]. Yuan X, Wang J, Yao H: Production of feruloyl oligosaccharides from wheat bran insoluble dietary fibre by xylanases from Bacillus subtilis. Food Chem 2006, 95:484-492. [20]. Faulds C, Mandalari G, LoCurto R, Bisignano G, Waldron K: Arabinoxylan and mono-and dimeric ferulic acid release from brewer’s grain and wheat bran by feruloyl esterases and glycosyl hydrolases from Humicola insolens. Appl Microbiol Biotechnol 2004, 64:644-650. [21]. Sørensen HR, Jørgensen CT, Hansen CH, Jørgensen CI, Pedersen S, Meyer AS: A novel GH43 a-L-arabinofuranosidase from Humicola insolens: mode of action and synergy with GH51 a-L-arabinofuranosidases on wheat arabinoxylan. Appl Microbiol Biotechnol 2006, 73:850-861. [22]. Graf E: Antioxidant potential of ferulic acid. Free Radic Biol Med 1992, 13:435-448. [23. Mateo Anson N, Hemery YM, Bast A, Haenen GR: Optimizing the bioactive potential of wheat bran by processing. Food Funct 2012, 3:362-375. Overview dealing with the bioactive potential of bran and its improvement by processing. [24]. Moore J, Liu JG, Zhou K, Yu L: Effects of genotype and environment on the antioxidant properties of hard winter wheat bran. J Agric Food Chem 2006, 54:5313-5322. [25]. Coda R, Ka¨rki I, Nordlund E, Heinio¨ R-L, Poutanen K, Katina K: Influence of particle size on bioprocess induced changes on technological functionality of wheat bran. Food Microbiol 2014, 37:69-77. [26]. Bram Damen B, Pollet A, Dornez E, Willem FB, Van Haesendonck I, Trogh I, Arnaut F, Delcour JA, Courtin CM: Xylanase-mediated in situ production of arabinoxylan oligosaccharides with prebiotic potential in whole meal breads and breads enriched with arabinoxylan rich materials. Food Chem 2012, 131:11-118. [27]. Mateo Anson N, Aura AM, Selinheimo E, Mattila I, Poutanen K, van den Berg R, Havenaar R, Bast A, Haenen GR: Bioprocessing of wheat bran in whole wheat bread increases the bioavailability of phenolic acids in men and exerts antiinflammatory effects ex vivo. J Nutr 2011, 141:137-143. [28]. Nordlund E, Katina K, Aura A-M, Poutanen K: Changes in bran structure by bioprocessing with enzymes and yeast modifies the in vitro digestibility and fermentability of bran protein and dietary fibre complex. J Cereal Sci 2013, 58:200-208. [29. Katina K, Juvonen R, Laitila A, Flander L, Nordlund E, Kariluoto S, Piironen V, Poutanen K: Fermented wheat bran as a functional ingredient in baking. Cereal Chem 2012, 89:126-134. This article describes the effects of fermentation and type of bran on technological functionality. www.sciencedirect.com
Bran bioprocessing Coda, Katina and Rizzello 55
[30. Coda R, Rizzello CG, Curiel JA, Poutanen K, Katina K: Effect of bioprocessing and particle size on the nutritional properties of wheat bran fractions. Innov Food Sci Emerg 2013 http:// dx.doi.org/10.1016/j.ifset.2013.11.012. This article describes the effect of bioprocessing on several nutritional features of wheat bran having different particle size. [31. Poutanen K, Sozer N, Della Valle G: How can technology help to deliver more of grain in cereal foods for a healthy diet? J Cereal Sci 2014, 59:327-336. Review reporting new technologies in cereal processing with an emphasis on whole grain foods. [32]. Savolainen OI, Coda R, Suomi K, Katina K, Juvonen R, Hanhineva K, Poutanen K: The role of oxygen in the liquid fermentation of wheat bran. Food Chem 2014, 153:424-431. [33]. Poutanen K, Flander L, Katina K: Sourdough and cereal fermentation in a nutritional perspective. Food Microbiol 2009, 26:693-699. [34]. Rizzello CG, Coda R, Mazzacane F, Minervini D, Gobbetti M: Micronized by-products from debranned durum wheat and
www.sciencedirect.com
sourdough fermentation enhanced the nutritional, textural and sensory features of bread. Food Res Int 2012, 46:304-313. [35]. Hartikainen K, Poutanen K, Katina K: Influence of bioprocessed wheat bran on the physical and chemical properties of dough and on wheat bread texture. Cereal Chem 2014, 91:115-123. [36]. Scazzina F, Siebenhandl-Ehn S, Nicoletta Pellegrini N: The effect of dietary fibre on reducing the glycaemic index of bread. Br J Nutr 2013, 109:1163-1174. [37]. Katina K, Salmenkallio-Marttila M, Partanen R, Forssell P, Autio K: Effects of sourdough and enzymes on staling of high-fibre wheat bread. LWT-Food Sci Technol 2006, 39:479-491. [38]. Napolitano A, Lanzuise S, Ruocco M, Arlotti G, Ranieri R, Knutsen SH, Lorito M, Fogliano V: Treatment of cereal products with a tailored preparation of Trichoderma enzymes increases the amount of soluble dietary fiber. J Agric Food Chem 2006, 54:7863-7869. [39]. Swennen K, Courtin CM, Delcour JA: Non-digestible oligosaccharides with prebiotic properties. Crit Rev Food Sci 2006, 46:459-471.
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