Prebiotic Potential of oligosaccharides: A focus on xylan based oligosaccharides

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B i o a c t i v e C a r b o h y d r a t e s a n d D i e t a r y F i b r e 5 ( 2 0 1 5 ) 1 9 – 3 0

http://dx.doi.org/102212-6198/& 2014 El

nCorresponding autE-mail address: a

Prebiotic potential of oligosaccharides: A focuson xylan derived oligosaccharides

Ramkrishna D. Singh, Jhumur Banerjee, Amit Aroran

CTARA, Indian Institute of Technology Bombay, Powai, Mumbai, Maharashtra, India

a r t i c l e i n f o

Article history:

Received 8 July 2014

Received in revised form

7 October 2014

Accepted 19 November 2014

Keywords:

Lignocellulosic biomass

Xylan

Xylooligosaccharides

Prebiotics

.1016/j.bcdf.2014.11.003sevier Ltd. All rights rese

hor. Tel.: þ91 22 2576 [email protected] (A. Arora

a b s t r a c t

Xylan is available abundantly in nature as a major constituent of hemicellulose, a

component of lignocellulosic biomass. Agricultural wastes such as straw, stalk, cob, hull,

husk, bagasse and pulp of hardwood represent a major source of xylan. Xylooligosacchar-

ides (XOS), the hydrolysis product of xylan is substrate for colonic commensal bacterial

population, acting as potential prebiotic. Its fermentation produces short chain fatty acids,

improves gut epithelial health and regulates metabolic process. These oligosaccharides

possess bound phenolics including ferulic acid, coumaric acid, thus imparting additional

antioxidant effect and immunomodulatory activity. This paper deals with xylan based

oligosaccharides with an emphasis placed on the need of oligosaccharides and discusses in

detail the health benefits of xylooligosaccharides.

& 2014 Elsevier Ltd. All rights reserved.

rved.

3.).

Contents

1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192. Need for prebiotic supplementation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223. Xylooligosaccharides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 234. Health benefit of XOS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23

4.1. Effect of XOS on gut health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23

4.2. Effects on metabolic disorder . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244.3. Antioxidant activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244.4. Effect on immune system. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25

5. Economic aspects of XOS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256. Future prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267. Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

1. Introduction

With increased consumer awareness, there is distinct change inunderstanding of role of food in human health promotion.

Scientific investigations have also moved from primary role offood as source of energy, body forming substance to theirbiological activity on human health. The term “functional food”was first used in Japan, in the 1980s, for food products fortified

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with special constituents that possess advantageous physiolo-gical effects (Prapulla & Aachary, 2011; Hardy, 2000; Shahidi,2009). Functional foods can be considered as basic nutritionfoods which have demonstrated physiological benefit (Shahidi,2009). Functional food includes: i) food with natural bioactivesii) derived food e.g. prebiotics and iii) bioactives added to food assupplements e.g. probiotics, antioxidants (Grazek, Olejnik, &Sip, 2005). Table 1 provides the definition of probiotics, pre-biotics and synbiotics with some examples from this type offunctional foods.

Prebiotics are non-digestible or of low digestibility foodingredients which selectively stimulate growth of limited num-ber of species of gut microbiota, conferring health benefits tohost (Roberfroid et al., 2010; Vitali et al., 2012). It includesoligosaccharides and polysaccharides which are: 1) resistant togastric acidity and hydrolysis by mammalian enzyme, 2) fer-mented by intestinal microflora, and 3) selectively stimulategrowth of intestinal bacteria (Roberfroid, 2007; Broekaert et al.,2011). Cited examples of prebiotics include inulin, fructooligo-saccharides (FOS), galactooligosaccharides (GOS), isomaltooligo-saccharides, soybean oligosaccharides and lactulose (Macfarlane,Macfarlane, & Cummings, 2006). Xylooligosaccharides (XOS) area new class of prebiotics and consists of xylobiose, xylotriose andso on (Vazquez, Alonso, Dominguez, & Parajo, 2000; Chapla,Pandit, & Shah, 2012). They are naturally present in fruits,vegetables bamboo, honey and milk and can be produced fromxylan rich lignocellulosic wastes. Table 2 summarizes source,chemical characteristics, production process and marketed pro-ducts of different prebiotic oligosaccharides.

Lignocellulosic materials (LCM) are most abundant biomassand made up of: cellulose, a linear polymer of 1-4 linkedβ-glucose units; hemicellulose, a heteropolysaccharide compris-ing of monosaccharides (pentoses and hexoses); and lignin, Allthese constituents make a major portion of the plant cell wallmaterial (Parajo, Vazquez, & Alonso, 2000; Kobayashi & Fukuoka,2013). Annually tons of such biomass such as of corn stover,sugarcane bagasse, rice and wheat straw, pomace, peel aregenerated as a result of various post-harvest and processingactivities of grains, fruits and vegetables (Van Dyk, Gama,Morrison, Swart, & Pletscheke, 2013); most of this material isdiscarded, reducing the nutritional value of food (Martinez et al.,2012). Moreover, these agricultural wastes are rich in bioactiveswhich can be incorporated into foods to increase the nutritionalvalue and functional properties (O'Shea, Arendt, & Galaghar,2012, Carvalho, Neto, Fernandes da Silva, & Pastore, 2013).

Bioconversion of these LCM to usable products requirefermentation (Zha & Punt, 2013) and pretreatments includingmechanical (Cadoche & Lopez, 1989), chemical (Nguyen et al.,

Table 1 – Definition and examples of probiotics, prebiotics and

Name Definition

Probiotics Selected, viable microbial dietary supplements which inconfer health benefit to host

Prebiotics Non-digestible or low digestable food ingredients whichstimulate growth of limited number of species of gut michealth benefits to host

Synbiotics Combination of prebiotic with probiotic, where prebioticsthe probiotic

2010; Ramadoss & Muthukumar, 2014) and biological (Yin et al.,2011; Canam, Town, Iroba, Tabil, & Dumonceausx, 2013) toproduce higher value added products such as single cell protein,monosaccharides, xylitol, biofuel, aromatic compounds.

Hemicellulose (25–35%) is most abundant polymer only aftercellulose (45–55%) found in plant cell walls, in close associationwith lignin (Ebringerova & Heinze, 2000). Hemicelluloses have β-(1-4)-linked backbone and include xyloglucans, xylans, man-nans and glucomannans, and β-(1-3, 1-4)-glucans (Scheller &Ulvskov, 2010). Xylans have a linear β-(1-4)-D-xylopyrananbackbone with various substituents including arabinofuranosyl,glucopyranosyl and uronic acid derivatives, ferulic and couma-ric acid, acetyl and phenolic acids which are either ether or estersubstituted to the hydroxyl group of xylose units, as shown inFig. 1. Depending on the botanical source and the method ofextraction employed, xylans of various structural complexitiescan be obtained; also, different tissues of same plant may showdiversity in their structure and function (Suzuki, Kitamura, Kato,& Itoh, 2000, Jensen, Johnson, & Wilkerson, 2013). Most com-monly xylans are classified based on the substituents as shownin Fig. 2. These long chain carbohydrates and their oligosac-charides are major components of dietary fiber (Holloway,Tasman-Jones, & Bell, 1980) and play an important role asprebiotics (Otieno & Ahring, 2012).

According to IUP-IUPAC, oligosaccharides are defined asoligomers composed of 2–10 monosaccharide residues. Oligosac-charides are lowmolecular weight carbohydrate residues and areclassified as digestible or nondigestible (Mussatto & Mancilha,2007). As opposed to α-linkages which are digestible by humandigestive enzymes, the anomeric carbons in nondigestible oligo-saccharides have β-linkages and thus are resistant to hydrolysisby human digestive enzymes in most cases, except galactosides(e.g. lactose). Generally, the larger the molecular weight of thebulk sucrose substitute, the weaker the intensity of sweetness.Most oligosaccharides are water soluble, have sweet taste (0.3–0.6times of sucrose), good mouth feel and low calorific value(1.5 Kcal/g); hence they are used as bulking agent in foodproduction to enhance other food flavors (Roberfroid & Slavin,2000). The functional properties of oligosaccharides to be used inprocessed foods should be similar to that of sucrose in providingbulk properties and a good sweetness.

The focus of the review is to inform readers about needand role of XOS based prebiotics to manage the gastrointest-inal tract (GIT) ecosystem, antioxidant activity and positiveeffects on immune system. Wherever found feasible, exam-ples and selected citations have been given to demonstratethe application of XOS and other oligosaccharides prebioticsto manage the GIT ecosystem thereby improve the health and

synbiotics.

Examples References

sufficient quantity Bifidobacterium spp.,Lactobacillus spp., etc.

Sanders, 2008

selectivelyrobiota, conferring

Lactulose,fructooligosaccharides,Inulin etc.

Grazek et al.,2005

selectively favors Oligofructose andBifidobacteria

Schrezenmeir& de Vrese,2001

Table 2 – Dietary oligosaccharides with occurrence, chemical characteristics, production process, dose, calories, sweetness and marketed product.

Type of OS Naturaloccurrence

Chemicalstructure

Chemical composition Productionprocess

Daily dose(g/day)

Calorie(Kcal/g)

Sweetness(comparedto sucrose)

Marketedproduct

Reference

Lactulose Cow milk Ga–Fr 4-O-β-D-galactopyranosyl-D-fructose

Alkaliisomerization oflactose

10 – 48–62% Cephulac,Constillac

Mussatto & Mancilha,2007; Bouhnik et al.,2004

Inulin Chicoryroots,onion,asparagus,antichoke

GuFrn FOS having DP from 3–60.Fructosyl-glucose andfructosyl-fructose linked byβ-(2-1) & β-(1-2)respectively

Diffusion in hotwater, refiningand spray drying

10–20 1–2 30% Raftilose(Orafti, USA);Inulin FOS(JarrowFormulas,USA)

Niness, 1999; Kelly,2009; Costabile et al.,2010; Apolinario et al.,2014

FOS Antichoke,garlic,onion,asparagus,chicory

(Fr)n–Gu β-(2-1) linked fructosyl unitwith terminal glucose. Chainlength of 2–10 with averageDP of 4

Inulin hydrolysis,synthesis fromsucrose

10 2 20–40% Aktifit(Emmi,switzerland);probioplus(Migros,Switzerland

Guio, Rodriguez,Almeciga-Diaz, &Sanchez, 2009; Bornet,Brouns, Tashiro, &Duvillier, 2002

GOS Humanmilk, cowmilk

(Ga)n–Gu 2–8 galactose units withterminal glucose having 1-4, 1-6 linkages

Enzymatictranglycosylationfrom lactose

5–10 1.73 30–60% Oligomate(Yakult,Japan); Cup-Oligo (Nissin,Japan)

McVeagh & Miller,1997;Chockchaisawasdee,Athanasopoulos,Niranjan, & Rastall,2004; Lamsal, 2012

IMO Starch fromwheat,barley,potato, rice,cassava,honey

(Gu)n 4–7 units of α-(1,6) linked (6-O-α-D-glucopyranosyl-D-glucose)

Enzymaticallytransformed fromstarch

8–10 2.8–3.2 40% Vitafiber(BioNeurta,USA), IMO

Lee, Wang, & Lin, 2008;Goulas, Fisher, Grimble,Grandison, & Rastall,2004

Soybeanoligosaccharides

Soybean Raffinose,stachyose,

α-(1,6) linked galactosebonded via α-(1,3) toterminal sucrose

Extracted fromsoybean whey

3–10 – – Oligo CC(Calpis,Japan)

Espinosa-Martos &Ruperez, 2006

XOS Hardwood,corncob,wheatstraw, ricehull, barleystraw

Xyn β-(1-4) linked xylopyranose,with arabinofuranosyl, 4-O-methylglucuronic acid,acetyl, phenolics subsitutentat C2 or C3.

Hydrolysis ofxylans

2–5 – 30% -Oligo(Lifebridge,USA)

Moure et al., 2006;Vazquez et al., 2000

Gu: Glucose, Fr: fructose, Ga: Galactose, Xy: xylose, n: number of residues.DP: Degree of polymerization, RT: room temperature.

Bioactive

Carbohydrates

and

Dietary

Fibre

5(2015)19–30

21

Fig. 1 – Representative chemical structure of xylan showing the xylan backbone, substituents and corresponding sites ofenzyme hydrolytic action (Shallom & Shoham, 2003).

Xylan Glucuronoxylans: found in hardwood species (birch, poplar), are partly acetylated and have α-(1→2)-4-O-methyl-D-glucopyranosyl uronic acid (MeGLcUA) substituent

Arabinoxylan: found in cell wall of the starchy endosperm, and outer layer of cereals. These have arabinofuranosyl substituents partly esterfied withphenolic acids

(Arabino)glucuronoxylan: typical in softwoods (spruce, pine, cedar) and have α -(1→3)-L-arabinofuranosyl (ArbF) residues on glucuronoxylans”.

Heteroxylans: present in cereal bran, seeds and gum exudates. They consist of various mono-oligosaccharide residues.

(Glucurono)arabinoxylan: xylan backbone with disubsituted arabinofuranosyl residues, acetylated and esterfied with ferulic acid. Found in grasses and cereals

Homoxylans: Linear Polysaccharides found in seaweeds like red seaweed (Chaetangium fastigiatum), green seaweed (Caulerpa filiformis, C.lentillifera)

Fig. 2 – Classification of Xylan based polysaccharides (Ebringerova, 2006; Scheller & Ulvskov, 2010).

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nutritional status of the host. Review also emphasizes on theopportunities and challenges in XOS based functional foodproducts market.

2. Need for prebiotic supplementation

Diet is one of the factors which contribute to lifestyle diseasessuch as diabetes, hypertension, high cholesterol, gut disorderand infection etc (Sharma & Majumdar, 2009). Prebiotics havebeen shown to provide health benefits such as decrease ofcancer risk, improvement of heart health, enhancement ofimmune system, enhancement of gut health, diminution ofblood pressure and antiobese influences (Al-Sheraji et al.,2013). Prebiotics can be obtained from fruits and vegetablessuch as onions, garlic, artichoke, chicory etc. However, mostcommonly consumed foods are low in dietary fiber, providingabout 1–3 g of fiber per serving (Slavin, 2013). Hence largequantity of such food needs to be consumed to meet the dailyfiber requirement (25 g for a 2000 cal diet) which is difficult.

Thus, there is need to provide prebiotic fiber as supplementto meet the daily requirement and provide health benefits.

Prebiotics brings about a shift in composition of intesti-nal bacterial population; i.e. an increase in Lactobacillus andBifidobacterium spp. Fermentation of these prebiotics by gutbacteria results in short chain fatty acid (SCFA) such as acetate,propionate, butyrate and lactate (Cummings, Macfarlane, &Englyst, 2001). These SCFA lower pH (Campbell, Fahey, & Wolf,1997), act as electron sink for anaerobic respiration in gut andimprove bioavailability of minerals (Teitelbaum & Walker, 2002).They also reduce gut infection (Swennen, Courtin, & Delcour,2006), suppress colon cancer initiation (Topping & Clifton, 2001)and bring about an overall improvement in gut health.

The prebiotic effect of dietary fiber is dependent on itsfermentation by colonic bacteria, which in turn is stronglydependent on their structure and average degree of polymer-ization ((DP)ˉ) oligosaccharides with low value of degreeof polymerization (DP) i.e.r5 have the ability to increaseBifidobacteria concentration in contrast to oligosaccharides hav-ing higher (DP), which do not stimulate bacterial development(Van Craeyveld et al., 2008). Also, XOS hydrolysates from

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hardwood and rye were fermented by Bifidobacteria and Lacto-bacillus, whereas nontreated polymeric xylans were not utilizedby any of the strains (Falck et al., 2013). This is corroboratedwith studies on wheat arabinoxylans (Vardakou, Palop, Gasson,Narbad, and Christakopoulous, 2007) and maize arabinoxylans(Sugawara et al., 1990) wherein, the hydrolysis products arabi-noxylooligosaccharides (AXOS) and XOS exerted bifidogeniceffects in vitro and in vivo; in contrast, no increase in gutbacterial population was observed by their polymeric forms(Neyrinck et al., 2012). These data point to the need forproduction and consumption of oligosaccharides to exert theirprebiotic potential.

3. Xylooligosaccharides

Xylooligosaccharides, hydrolysis product of xylan, are oligo-mers of β-1, 4-linked xylose residues with various substitu-ents including acetyl, phenolic, and uronic acid. They arefound in fruits, vegetables, bamboo, honey, milk as well asxylan rich lignocellulosic material obtained from agricultural,forestal and industrial waste (Vazquez, Alonso, Dominguez,Garrote, & Parajo, 2003; Gupta, Agarwal, & Hegde, 2013). XOSsare available as white powder containing two to 10 xylosemolecules, however some researcher consider moleculeswith degree of polymerization (DP)r20 as XOS (Makelainenet al., 2010). However, for food application, XOS with DP 2–4are preferred (Loo et al., 1999; Vazquez et al., 2000).

These oligosaccharides are stable over a wide pH range of2.5–8.0, low gastric pH and temperatures up to 100 1C. XOSwith average DP ((DP)\overline) of 3–5 are more sensitive toalkaline decomposition as compared to longer chain XOS of((DP)\overline) 15 (Courtin, Swennen, Verjans, & Delcour,2009). XOS have good thermal stability during pasteurizationand autoclave sterilization at low pH (Wang, Sun, Cao, Tian, &Wang, 2009) as compared to FOS which are more susceptiblefor decomposition at low pH and higher temperature (Courtinet al., 2009). In food processing, XOS are advantageous overinulin in terms of heat and acidity resistance, allowing theirutilization in low pH juices (Vazquez et al., 2000).

Different bacteria inhabiting human gut, such asBifidobacterium spp, Bacteroides spp, Clostridium spp, utilizedifferent polysaccharides and oligosaccharides as source ofenergy (Voragen, Van Laere, Hartemink, Bosveld, & Schols,2000). Bifidobacteria, Bacteroides possess varying degree of spe-cificity for utilization of xylan as substrates. Bifidobacteria canproduce a broad range of glycosidases and are able to utilizestructurally complex oligosaccharides along with bifidogenicoligosaccharides such as FOS and XOS. Instead, Bacteroides sppwhich are the predominant intestinal bacteria are capable offermenting branched xylans such as rhamnogalacturono-oligosaccharides as well as different types of arabinogalactans.Lactobacilli are not able to utilize XOS as a sole carbon source(Jaskari et al., 1998) with the exception of Lactobacillus brevis,where moderate increase in growth was observed when fedwith XOS (Crittenden et al., 2002; Moura et al., 2007).

As a food ingredient, XOS are non-carcinogenic, stimulatebacterial growth and fermentation, and improves intestinalmineral absorption. They also possess antioxidant, antialler-genic, antimicrobial, immunomodulatory and selective

cytotoxic activity, as well as blood and skin health relatedeffects (Moure, Gullon, Dominguez, & Parajo, 2006).

4. Health benefit of XOS

4.1. Effect of XOS on gut health

XOS selectively stimulate growth or activity of specific groupof bacteria (Gibson & Roberfroid, 1995; Crittenden et al., 2002;Immerzeel et al., 2014), which is associated with theimproved health, reduced gut infection, and suppression ofcolon cancer (Macfarlane et al., 2006).

XOS are preferentially utilized by Bifidobacterium spp,especially Bifidobacterium adolescentis, Bifidobacterium longumin rat intestine (Okazaki, Fujikawa, & Matsumoto, 1990;Suwa et al., 1999). They are also shown to be used as carbonsource by strains of Weissella strains, thus increasing theprebiotic potential of XOS (Patel et al., 2013). Differences inmicrobial flora was observed when fed with XOS and FOS; FOSprimarily stimulated the growth of Lactobacilli, whereas XOSwas found to be more bifidogenic, both contributing to healthyenvironment of colon. Bifidogenic activity of XOS producesacetic acid and lactic acid, which was comparable to glucoseand more pronounced than inulin (a commercial prebiotic).Three fold increases in the population of Bifidobacterium specieswere noted following oral administration of 5 g/day XOSobtained from birch wood xylan to healthy volunteers for 2weeks (Okazaki, Fujikawa, & Matsumoto, 1990). The increase inBifidobacterium population was accompanied with decrease ofpH and maintenance of normal water content of feacesbetween 70% and 80%. These factors promote intestinal cellproliferation and peristalsis thus providing benefit againstconstipation. XOS intake was associated with reduction infeces hardness in healthy young women (Na & Kim, 2007,Iino et al., 1997), increased fecal water content in elderly withno effect on stool consistency and frequency (Chung, Hsu, Ko,& Chan, 2007). Moreover, 4.2 g/day XOS was found to be safeand effective in normalizing the bowel movements in pregnantwomen thus, providing an alternative intervention for treat-ment of severe constipation during the third trimester ofpregnancy (Kiso et al., 2005).

XOS and FOS reduced colonic aberrant crypt foci, an earlymarker of tumor diagnosis by 76% and 48% respectively,indicating better tumor suppressing activity of XOS over FOSin DMH induced colonic lesion (Hsu, Liao, Chung, Hsieh, &Chan, 2004). Supplementation of XOS and FOS improved colonhealth as indicated by increased cecal weight as a result of thebifidogenic activity of dietary fibers. A significant increase inbody weight, normalcy of colon epithelial cells, reduced coloniclipid peroxidation and restoration of antioxidant enzyme activ-ity was observed in DMH treated rats. In addition, XOS stimu-lated growth of bifidobacteria to higher extent as compared toFOS. A high concentration of acid in form of lactate, acetate andother fatty acid decreases the intestinal pH, thus hindering thegrowth of pathogenic and putrefactive bacterium. Butyrateproduced as a result of XOS fermentation inhibits colon cellcarcinoma via inhibition of histone hyperacetylation and p21gene induction (Archer et al., 1998). Butyrate is used as energy

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source for colonocytes (Roediger, 1982) and also improves abso-rptive capacity of colon epithelial cells (Topping & Clifton, 2001).

The effective daily dose of oligosaccharides (pure form) forXOS is 0.7 g and that for FOS is 3.0 g, indicating that XOS maybe effective at a lower dose as compared to FOS (Tomomatsu,1994). This is supported by a study wherein XOS at a dose of1.4 g/day in adults were found to be efficacious as prebiotic ascompared to FOS or GOS (Z10 g/day) (Bouhnik et al., 1999). Inaddition, consumption of FOS increases flatulence, intestinalbloating, and intestinal irritation (Ten Bruggencate, Bovee-Oudenhoven, Lettink-Wissink, Katan, & Van der Meer, 2006).XOS being given at lower dose compared to FOS have notbeen reported for such side effects and this physiologicaldifferentiation needs to be evaluated.

4.1.1. Effect of substitution on XOS on activityThe average degree of polymerization ((DP)ˉ) of XOS and AXOSinfluences the formed fermentation products and prebioticpotential. AXOS and XOS with low (DP) i.e. (less than 5)produces acetate and butyrate and have strong bifidogeniceffect, whereas those with (DP) above 5 resulted in markeddecrease of branched SCFA, indicating shift from proteinfermentation to carbohydrate fermentation (Van Craeyveldet al., 2008). Also, XOS with (DP) (2–3) have faster utilizationkinetics as compared to XOS with (DP)ˉ of 4 and 5 (Gullon et al.,2008). Substitution affects catalytic activity of enzymes, henceXOS fermentation by enzymes in human fecal inocula varywith degree of substitution. B. adolescentis are capable of utiliz-ing both unsubstituted and arabinose substituted XOS as sourceof carbon, in contrast to L. brevis, which ferments only unsub-stituted XOS (Falck et al., 2013). Linear XOS and arabino-XOSwere fermentated preferably andmore quickly to produce smallchain fatty acids and lactate as compared to highly substitutedXOS having acetyl and 4-o-methylglucuronic acid substituents(Voragen, Kabel, Kortenoveven, & Schols, 2002). Similarly, theprebiotic potential of XOS derived from wheat bran was foundto be better as compared to XOS from Bengal gram husk andthis was ascribed to relatively higher arabinose content ofwheat bran XOS (Madhukumar & Muralikrishna, 2012). Thus,the prebiotic effect of XOS is dependent on degree of polymer-ization, substitution, arabinose to xylose ratio as well as thebacterial strain tested.

4.2. Effects on metabolic disorder

Dietary fiber such as XOS could play interesting role inmanagement of metabolic syndrome through their ability tocontrol body weight, glucose and lipid homeostasis, insulinsensitivity and in regulation of inflammation markerinvolved in pathogenesis of metabolic syndrome (Galisteo,Duarte & Zarzuelo, 2008; Delzenne & Cani, 2005). The bene-ficial effect of XOS in metabolic condition of diabetes can beattributed to the production of SCFA in colon which increasessodium and water absorption in distal intestine improvingpolydipsia (Roediger & Moore, 1981). Also, acetic acid pro-duced as a result of fermentation is absorbed into systemiccirculation and transported to muscles where acetate is usedas source of energy thereby reducing degradation of muscleprotein for energy production (Knowles, Jarrett, Filsell, &Ballard, 1974; Skutches, Holroyde, Myers, & Reichard, 1979).

XOS included in diet of diabetic rats was found to improvegrowth, hyperphagia, polydipsia along with improving serumglucose and lipid profile (Imaizumi, Nakatsu, Sato,Sedarnawati, & Sugano, 1991).

Arabinoxylan (AX), as dietary fiber significantly improvesglycemic control in type II diabetes with no effect on serumlipid profile of normolipidemic subject (Lu, Walker, Muir, &O' Dea, 2004). In contrast, nonviscous wheat bran does notmodulate apparent glycemic response (Jenkins et al., 2002).Corncob XOS was observed to improve clinical conditionsassociated with diabetes, ameliorated function of nephrons,restored antioxidant enzymes activity while significantlydecreasing mortality rate in rodents (Prapulla, Gobinath,Madhu, Prashant, & Krishnapura, 2010). Wheat bran AXOSwas found to be useful in counteracting high fat induced bodyweight gain, fat mass development and hyperinsulinemia inrodent through increase in level of satietogenic peptides, andupregulation of gut barrier function. Thus, AXOS acts aspotential prebiotic nutrient in regulating obesity and relatedmetabolic disorders (Neyrinck et al., 2012). Similarly, wheat branXOS were found effective in protecting humans against high fatdiet induced oxidative stress (Wang, Cao, Wang & Sun, 2011).

XOS fed to humans for 8 weeks were found to improveblood glucose and lipid profile. In addition, there was increasein level of antioxidant enzymes such as superoxide dismu-tase and glutathione peroxidase (Sheu, Lee, Chen, & Chan,2008). Prebiotics such as XOS alter the structure, physico-chemical properties of membrane bilayer, bringing aboutchanges in sphingomyelin/cholesterol ratio in rat liverplasma membranes (Staneva et al., 2013). These effectsmodify the functioning of various membrane receptors andcell signaling, thus providing beneficial effect in glucose andlipid metabolism. These studies suggest the beneficial effectsof XOS in regulating glucose and lipid profile, thus XOS can beevaluated as a potential nutrient for their beneficial effect onhost energetic metabolism.

Stimulation of bifidogenic bacteria by oligosaccharides sup-presses protein fermentation in colon, thereby reducing thelevels of toxic catabolites like ammonia, amines, phenols,indoles and thiols; thus, reducing the risk of inflammatorydiseases of colon (Bone, Tamm, & Hill, 1976; Ramakrishna,Roberts-Thomson, Pannall, & Roediger, 1991). Protective activityagainst high protein diet induced genotoxicity and DNA strandbreakage in colonocytes was observed for XOS, however similarresults were not obtained for inulin (Conlon, Licht, Petersen, &Christophersen, 2013). The genoprotective effect was attributedto the production of short chain fatty acids, including acetateand butyrate. Acetate activates genes responsible for cellularenergy metabolism, anti-inflammatory response and also pre-vents reduction in transepithelial electrical resistance of colonepithelial cells (Ohno et al., 2011).

4.3. Antioxidant activity

In-vitro radical scavenging activity was found in water solublearabinoxylan extracted fromwheat bran comprising of phenolicresidues (Hromadkova, Paulsen, Polovka, Kostalova, andEbringerova, 2013). Similarly, in-vitro antioxidant activity hasbeen reported for enzymatically derived XOS from sunflowerand wheat stalk (Akpinar, Gunay, Yilmaz, Levent, and Bostanci,

Table 3 – Comparsion of xylan, arabinoxylan, XOS and AXOS for their Properties/biological activity.

Properties/biological activity

Xylan Arabinoxylan XOS AXOS Reference

Fermentability � þ þþ þ (Okazaki, Fujikawa, & Matsumoto, 1990; Patel et al., 2013; Hsu et al.,2004; Zhou et al., 2010 Walton, Lu, Trogh, Arnaut, & Gibson, 2012)

Metabolicregulation

� þ þ þ (Imaizumi et al., 1991; Ou et al., 2007, Torsdottir, Alspten, Holm,Sandberg, & Tolli, 1991)

Antioxidant activity þ þ þ þ (Akpinar et al., 2010; Barron, Surget & Rouau, 2007, Holvoet, Jenny,Schreiner, Tracy, & Jacobs, 2007, Renault et al., 2014)

Immunomodulation þ þþ þ * (Cao et al., 2011; Ogawa, Takeuchi, Nakamura, 2005; Shi, Dong &Ding, 2014; Zhou et al., 2010)

� : Absent, þ: present; þþ: high; *: Data not available.

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2010), XOS from endo-β-xylanase treated corncob (Yamani,Kristanti, & Puspaningsih, 2012) as well as for xylanase derivedXOS from sugarcane bagasse (Bian et al., 2013). XOS obtainedfrom ragi, wheat, rice and maize bran were evaluated for theirantioxidant activities (Veenashri & Muralikrishna, 2011). It wasobserved that antioxidant activity for ragi (12–70% at 10–60 mg)was higher as compared to XOS derived from wheat, rice andmaize (70% at 1000 mg), due to higher content of boundphenolics in the former.

The antioxidant activity is generally attributed to presenceof ester linked hydroxycinnamic acid derivatives, such asferulic acid and syringic acid residues on the xylan chain. Astudy on Wistar rat fed with wheat bran feruloyl oligosacchar-ides support the activity of ferulic acid as antioxidant (Wang,Sun, Cao, & Wang, 2010). Thus xylooligosaccharides withferulic acid substituents can be evaluated for their incorpora-tion in food products as antioxidant and as natural substitutesfor synthetic agents such as BHA and BHT.

4.4. Effect on immune system

The gastrointestinal tract is subjected to various foreign anti-genic stimuli from food and microbes. Thus, it is critical thatprotective immune responses are initiated to potential patho-gen while avoiding hypersensitivity reaction against dietaryantigens. Prebiotic fibers mediate immune response via produc-tion of SCFAs, direct contact of bifidobacteria, lactic acidbacteria and their fermentation product and modulating prop-erties of gut associated lymphoid tissues (GALT) (Schley & Field,2002, Vieira, Teixeira & Martins, 2013). XOS inhibited productionof inflammatory mediators in lipopolysaccharide stimulatedmacrophages, thus demonstrating anti-inflammatory andimmunomodulatory activity (Chen, Chen, Chang, & Lin, 2012).Water-soluble oligosaccharides obtained from wheat branshowed free radical scavenging properties and immunomodu-latory activity (Hromadkova et al., 2013). Similarly, XOS wasobserved to induce bifidogenesis and modulate markers ofimmune function in healthy adults, when given alone or incombination with probiotics i.e. Bifiobacterium animalis subsp.lactis (Childs et al., 2014). Partially O-acetylated XOS and theirdeacetylated form obtained from almond shell showed directmitogenic activity and enhancement of T-mitogen inducedproliferation of rat thymocytes, indicating immunostimulatoryactivity (Nabarlatz et al., 2007).

Wheat bran arabinoxylans were found to possess immu-nostimulatory activity, which contribute to antitumor activity.They promoted thymus and spleen indexes, splenocyte prolifer-ation, natural killer cell and macrophage phagocytosis activity,interleukin 2 production and delayed type hypersensitivity reac-tion. Furthermore, they significantly inhibited growth of trans-plantable tumors in S180 tumour bearing mice model (Cao et al.,2011). Extractions with chemical and enzymatic methods pro-duce end-products with different chemical groups which canaffect the functionality of the oligosaccharide. It was observedthat AX obtained by enzymatic treatment of wheat bran hadhigher macrophage phagocytosis and delayed hypersensitivityreaction as compared to AX derived by chemical method.However, no significant difference in enhancing lymphocyteproliferation was observed (Zhou et al., 2010). AX from greenleaves of Litsea glutinosa (Lauraceae) induced splenocyte andthymocyte proliferation at dose of 25 mg/ml and 50 mg/ml in amouse culture medium (Das, Maiti, Maiti, & Islam, 2013). Inaddition, a dose dependent increase in macrophage activationwas observed, indicating potential tumour inhibitory activity.However, low immunological activities were reported for arabi-noxylan and mixed-linked β-glucans from barley on cell cult-ures (Samuelsen, Rieder, Grimmer, Michaelsen, and Knutsen,2011). Contrasting results were obtained for XOS derived frombengalgram husk, wherein no mitogenic activity was observed.The reason was attributed to either low degree of polymeriz-ation or absence of ferulic or uronic moieties (Madhukumar,Chandrashekar, Venkatesh & Muralikrishna, 2011).

Thus, XOS, AXOS and their polymeric form differs in theirfermentability and utilization by gut microbiota, which cau-ses difference in their biological activity. Table 3 summarizesthe properties/biological activity of oligosaccharides and theirpolymeric form.

5. Economic aspects of XOS

The cost of raw material is an important factor to consider forproduct development. As previously mentioned, most of theoligosaccharides are either produced synthetically or obtainedfrom traditional food sources; XOS provides an exemption tothis category (as it obtained from LCM sources usually dis-carded as waste). Bikkle, a health drink comprising of XOS and

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bifidobacteria was launched by Suntory in 1993, it achieved asales of about 100 million USD (Staton et al., 2001). From 1997to 2008, about 32 products of XOS as dietary supplement, sugarand gum confectionery, non-alcoholic beverage and baby foodwere launched (Makelainen, Juntunen & Hasselwander, 2009).With increase in consumer's awareness regarding health andits relation to nutrition diet, the market of functional food hasincreased (Pizzoferrato, 2003). This is also applicable to XOSwhich is available at a market price of 1–200 U.S $/kg based onpurity level (suppliers survey and communication with ven-dor), which is higher as compared to other oligosaccharidessuch as FOS (1–20 U.S $/kg), GOS (5–100 U.S $/kg) and inulin(10–100 U.S $/kg). Our lab is working on producing pure form ofXOS in a costeffective manner from various substrates(Unpublished data).

6. Future prospects

XOS production is feasible as it can be obtained from variousagro-based wastes in comparison to other oligosaccharides,which are obtained from specific plant sources such as chicory,artichoke, cassava, milk or produced synthetically from sucrose(Vankova, Onderkova, Antosova & Polakovic, 2008). Hence,various underutilized LCM sources should be evaluated for theirxylan content, xylose to arabinose ratio, bound phenolics,structure-function relationships for high recovery and function-ality of purified XOS. It is also important to understand thefermentation kinetics of different microbiota at varyingarabinose–xylose ratio. It has been reported that XOS have beenutilized to improve the nutritive value of yoghurt (Semee,Rehman, Nuzhat, Amer, and Haq, 2008) to improve textureand properties of cereal/legume based fermented product (idli)(Aachary & Prapulla, 2011); they are included in formulatedhealth drink (Fujikawa, Sasaki, and Ishizuka, 2006). Thus, XOSprovide a potential candidate as an ingredient for functionalfoods such as health drinks, biscuits, breads, health bars, jellies,jam, as well as a component of synbiotic preparations. Aspreviously mentioned, XOS show a range of health benefits atlower doses as compared to other oligosaccharides such as FOSand inulin,, thus can be included in special foods for babies andthe elderly. It can be further used as a supplement in case ofirritable bowel syndrome, to prevent diarrhea associated withantibiotics, or in cases of gut infection. However, it must benoted that, before being incorporated in food, there is a need toevaluate the interaction between food components and theoligosaccharides, effect of processing conditions on XOS stabilityand relationship between XOS concentrations and functionality.

As gut flora composition depends on genetic makeup, ageand disease state (Marathe, Shetty, Lanjekar, Ranade, andShouche, 2012) a detailed study with respect to utilization ofXOS by gut flora in individual with different ethnicity, race, age,sex, disease state (colon disease and cancer) of patients need tobe performed. In addition, studies directed towards understand-ing of dosage range of XOS in healthy individual as well as forindicated disease condition should be performed. Further in-vitroand in-vivo studies should be performed to ascertain the effect ofmixed XOS with different DP, xylose to arabinose ratio andattached substituents for their ability to produce SCFA, alter gut

health, as well as provide antioxidant and immunomodulatoryactivities. Few researchers have focused on elucidating themechanism of action of XOS and their fermentation products;however, the data is limited. More investigations directedtowards studying of changes occurring at cellular and genomelevel can be conducted to support the proposed health benefitsand non-toxicity of XOS. It may be worthwhile to evaluate XOSfor their synergistic effects on colon cancer treatment to reducechemotherapy side-effects.

7. Conclusion

Experimental evidences support the need for consumption ofxylan derived oligosaccharides instead of xylan itself. Gut andother health benefits of XOS as a prebiotics have beensupported by various lab studies and clinical trials. However,the elucidation of their mechanism of action, toxicity (pri-marily genotoxicity and mutagenicity) is still in nascent stageand needs further investigations. Structure function relation-ship studies need to be conducted to evaluate the influence ofsubstituents on biological activity of XOS. Moreover, physi-cochemical properties of XOS such as wide pH stability,thermal stability, sweetness allow for their use in various foodpreparations. Fermentability of XOS and substituted XOS maybe evaluated in presence of different commensal bacteria torealize their full potential as a synbiotic ingredient.

Overall further work is needed towards developing viable,economic technology for production, refining and purificationof XOS, as well as conducting detailed in-vitro and in-vivostudies to support the health benefits of these prebiotics andthus, develop marketable product.

r e f e r e n c e s

Aachary, A. A., & Prapulla, S. G. (2011). Xylooligosaccharides: apotential prebiotic used to improve batter fermentation andits effect on the quality attributes of idli, a cereal/legumebased indian traditional food. International Journal of FoodScience and Technology, 46, 1346–1355.

Akpinar, O., Gunay, K., Yilmaz, Y., Levent, O., & Bostanci, S. (2010).Enzymatic processing and antioxidant activity of agriculturalwaste autohydrolysis liquours. BioResources, 5(2), 699–711.

Al-Sheraji, S. H., Ismail, A., Manap, M. Y., Mustafa, S., Yusof, R. M.,& Hassan, F. A. (2013). Prebiotics as function foods: a review.Journal of Functional Foods, 5, 1542–1553.

Archer, S., Meng, S., Wu, J., Johnson, J., Tang, R., & Hodin, R. (1998).Butyrate inhibits colon carcinoma cell growth through twodistinct pathways. Surgery, 124, 248–253.

Apolinario, A. C., Damasceno, B. P., Beltrao, N. E., Pessoa, A.,Converti, A., & Alexsandro da Silva, J. (2014). Inulin-typefructans: a review on different aspects of biochemical andpharmaceutical technology. Carbohydrate Polymers, 101,368–378.

Barron, C., Surget, A., & Rouau, X. (2007). Relative amounts oftissues in mature wheat (Triticum aestivum L.) grain and theircarbohydrate and phenolic acid composition. Journal of CerealScience, 45, 88–96.

Bian, J., Peng, F., Peng, X. P., Peng, P., Xu, F., & Sun, R.-C. (2013).Structural features and antioxidant activity ofxylooligosaccharides enzymatically produced from sugarcanebagasse. Bioresource Technology, 127, 236–241.

B i o a c t i v e C a r b o h y d r a t e s a n d D i e t a r y F i b r e 5 ( 2 0 1 5 ) 1 9 – 3 0 27

Bone, E., Tamm, A., & Hill, M. (1976). The production of urinary

phenols by gut bacteria and their possible role in the

causation of large bowel cancer. The American Journal of ClinicalNutrition, 29, 1448–1454.

Bornet, F. R., Brouns, F., Tashiro, Y., & Duvillier, V. (2002).

Nutritional aspects of short-chain fructooligosaccharides:

natural occurrence, chemistry, physiology and health

implications. Digestive and Liver Disease, 32(2), S111–S120.Bouhnik, Y., Attar, A., Joly, F. A., Riottot, M., Dyard, F., & Flourie, B.

(2004). Lactulose ingestion increases faecal bifidobacterial

counts: a randomized double-blind study in healthy humans.

European Journal of Clinical Nutrition, 58, 462–466.Bouhnik, Y., Vahedi, K., Achour, L., Attar, A., Salfati, J., Pochart, P.,

et al. (1999). Short-chain fructooligosaccharide administration

dose-dependently increases fecel bifidobacteria in healthy

humans. Journal of Nutrition, 129(1), 113–116.Broekaert, W. F., Courtin, C. M., Verbeke, K., Van De Wiele, T.,

Verstraete, W., & Delcour, J. A. (2011). Prebiotic and other

health related effects of cereal derived arabinoxylans,

arabinoxylan-oligosaccharides, and xylooligosaccharides.

Critical Reviews in Food Science and Nutrition, 51, 178–194.Cadoche, L., & Lopez, G. D. (1989). Assessment of size reduction as

a preliminary step in the production of ethanol from

lignocellulosic wastes. Biological Wastes, 30, 153–157.Campbell, J. M., Fahey, G. C., & Wolf, B. W. (1997). Selected

indigestible oligosaccharides affects large bowel mass, cecal

and fecal short-chain fatty acids, pH and microflora in rats.

Journal of Nutrition, 127, 130–136.Canam, T., Town, J., Iroba, K., Tabil, L., & Dumonceausx, T. (2013).

Pretreatment of lignocellulosic biomass using

microorganisms: approaches, advantages, and limitations. In

Anuj K. Chandel, & Silvio Silverio da Silva (Eds.), Sustainabledegradation of lignocellulosic biomass – techniques, applications andcommercialisation (pp. 181–206)).

Cao, L., Liu, X., Qian, T., Sun, G., Guo, Y., Chang, F., et al. (2011).

Antitumour and immunomodulatory activity of

arabinoxylans: a major constituent of wheat bran. InternationalJournal of Biological Macromolecules, 48, 160–164.

Carvalho, A. F., Neto, P. d., Fernandes da Silva, D., & Pastore, G. M.

(2013). Xylo-oligosaccharides from lignocellulosic materials:

chemical structure, health benefits and production by chemical

and enzymatic hydrolysis. Food Research International, 51, 75–85.Chapla, D., Pandit, P., & Shah, A. (2012). Production of

xylooligosaccharides from corncob xylan by fungal xylanase and

their utilization by probiotics. Bioresource Technology, 115, 215–221.Chen, H. H., Chen, Y. K., Chang, H. C., & Lin, S. Y. (2012).

Immunomodulatory effects of xylooligosaccharides. FoodScience and Technology Research, 18, 195–199.

Childs, C. E., Roytio, H., Alhoniemi, E., Fekete, A. A., Forssten, S. D.,

Hudjec, N., Lim, Y. N., Steger, C. J., Yaqoob, P., Tuohy, K. M.,

Rastall, R. A., Ouwehand, A. C., & Gibson, G. R. (2014). Xylo-

oligosaccharides alone or in synbiotic combination with

Bifidobacterium animalis subsp. lactis induce bifidogenesis and

modulate markers of immune function in healthy adults: a

double-blind, placebo-controlled, randomised, factorial cross-

over study. British Journal of Nutrition, 111(11), 1945–1956.Chockchasawasdee, S., Athanasopoulos, V. I., Niranjan, K., &

Rastall, R. A. (2005). Synthesis of galacto-oligosaccharides

from lactose using β-galactosidase from Kluvyeromyces lactis:

studies on batch and continuous UF membrane-fitted

bioreactors. Biotechnology and Bioengineering, 89(4), 434–443.Chung, Y. C., Hsu, C. K., Ko, C. Y., & Chan, Y. C. (2007). Dietary

intake of xylooligosaccharides improves the intestinal

microbiota, fecal moisture and ph value in the elderly.

Nutrition Research, 27, 756–761.Conlon, M. A., Licht, T. R., Petersen, A., & Christophersen, C. T.

(2013). Xylo-oligosaccharides and inulin affect genotoxicity

and bacterial populations differently in a human colonic

simulator challenged with soy protein. Nutrients, 5, 3740–3756.Costabile, A., Kolida, S., Klinder, A., Gietl, E., Bauerlein, M.,

Frohberg, C., et al. (2010). A double-blind, placebo-controlled,

cross-over study to establish the bifidogenic effects of a very-

long-chain-inulin extracted from globe artichoke (Cynara

scolymus) in healthy human subjects. British Journal ofNutrition, 104, 1007–1017.

Courtin, C. M., Swennen, K., Verjans, P., & Delcour, J. A. (2009).

Heat and pH stability of prebiotic

arabinoxylooligosaccharides, xylooligosaccharides and

fructooligosaccharides. Food Chemistry, 112(4), 831–837.Crittenden, R., Karppinen, S., Ojanen, S., Tenkanen, M.,

Fagerstrom, R., Matto, J., Saarela, M., Mattila- Sandholm, T., &

Poutanen, K. (2002). In-vitro fermentation of cereal dietary fiber

carbohydrates by probiotic and intestinal bacteria. Journal ofthe Science of Food and Agriculture, 82(8), 781–789.

Cummings, J. H., Macfarlane, G. T., & Englyst, H. N. (2001).

Prebiotic digestion and fermentation. Amerian Journal of ClinicalNutrition, 73, 415S–420S.

Delzenne, N. M., & Cani, P. D. (2005). A place for dietary fibre in the

management of the metabolic syndrome. Current Opinion inClinical Nutrition and Metabolic Care, 8(6), 636–640.

Das, D., Maiti, S., Maiti, T. K., & Islam, S. S. (2013). A new arabinoxylan

from green leaves of Litsea glutinosa (Lauraeae): structural and

biological studies. Carbohydrate Polymers, 92, 1243–1248.Ebringerova, A. (2006). Structural diversity and application potential

of hemicelluloses. Macromolecular Symposia, 232(1), 1–12.Ebringerova, A., & Heinze, T. (2000). Xylan and xylan derivatives-

biopolymers with valuable properties. Macromolecular RapidCommunications, 21, 542–556.

Espinosa-Martos, I., & Ruperez, P. (2006). Soybean

oligosaccharides. Potential as new ingredients in functional

foods. Nutricion Hospitalaria, 21(1), 92–96.Falck, P., Precha- Atsawanan, S., Grey, C., Immerzeel, P., Stalbrand, H.,

Adlercreutz, P., & Karlsson, E. N. (2013). Xylooligosaccharides from

hardwood and cereal xylans produced by a thermostable

xylanase as carbon sources for Lactobacillus brevis and

Bifidobacterium adolescentis. Journal of Agricultural and Food Chemistry,61(30), 7333–7340.

Fujikawa, S., Sasaki, H., Ishizuka, T. Xylooligosaccharides

composition with high purity. US Patent Wo 2006112380 A1; 2006.Galisteo, M., Duarte, J., & Zarzuelo, A. (2008). Effects of dietary

fibers on disturbances clustered in the metabolic syndrome.

The Journal of Nutritional Biochemistry, 19(2), 71–84.Gibson, G. R., & Roberfroid, M. B. (1995). Dietary modulation of

human colonic microbiota: introducing the concept of

prebiotics. The Journal of Nutrition, 125(6), 1401–1412.Goulas, A. K., Fisher, D. A., Grimble, G. K., Grandison, A. S., &

Rastall, R. A. (2004). Synthesis of isomaltooligosaccharides

and oligodextrans by combined use of dextransucrase and

dextranase. Enzyme and Microbiology Technology, 35, 327–338.Grazek, W., Olejnik, A., & Sip, A. (2005). Probiotics, prebiotics and

antioxidants as functional foods. Acta Biochemica Polonica, 52,665–671.

Guio, F., Rodriguez, M. A., Almeciga-Diaz, C. J., & Sanchez, O. F. (2009).

Recent trends in fructooligosaccharides production. Recent Patentson Food, Nutrition and Agriculture, 1, 221–230.

Gullon, P., Moura, P., Esteves, M. P., Girio, F. M., Dominguez, H., &

Parajo, J. C. (2008). Assessment on the fermentability of

xylooligosaccharides from rice husk by probiotic bacteria.

Journal of Agricultural and Food Chemistry, 56(16), 7482–7487.Gupta, P. K., Agarwal, P., & Hegde, P. (2013). A review on

xylooligosaccharides. International Research Journal of Pharmacy,3(8), 71–74.

Hardy, G. (2000). Nutraceuticals and functional foods:

introduction and meaning. Nutrition, 16, 688–697.

B i o a c t i v e C a r b o h y d r a t e s a n d D i e t a r y F i b r e 5 ( 2 0 1 5 ) 1 9 – 3 028

Holloway, W. D., Tasman-Jones, C., & Bell, E. (1980). The

hemicellulose component of dietary fiber. The American Jorunalof Clinical Nutrition, 33, 260–263.

Holvoet, P., Jenny, N. S., Schreiner, P. J., Tracy, R. P., & Jacobs, D. R.

(2007). The relationship between oxidized LDL and other

cardiovascular risk factor and subclinical CVD in different

ethnic groups: the multi-ethnic study of atherosclerosis

(MESA). Atherosclerosis, 194, 245–252.Hromadkova, Z., Paulsen, B. S., Polovka, M., Kostalova, Z., &

Ebringerova, A. (2013). Structural features of two heteroxylan

polysaccharides fractions from wheat bran with anti-

complementary and anti- oxidant activites. CarbohydratePolymers, 93, 22–30.

Hsu, C. K., Liao, J. W., Chung, Y. C., Hsieh, C. P., & Chan, Y. C.

(2004). Xylooligosaccharides and Fructooligosaccharides affect

the intestinal microbiota and precancerous colonic lesion

development in rats. Journal of Nutrition, 134(6), 1523–1528.Iino, T., Nishijima, Y., Sawada, S., Sasaki, H., Harada, H., Suwa, Y.,

& Kiso, Y. (1997). Improvement of constipation by a small

amount of xylooligosaccharides ingestion in adult women.

Journal of Japanese Association of Dietary Fiber Research, 1, 19–24.Imaizumi, K., Nakatsu, Y., Sato, M., Sedarnawati, Y., & Sugano, M.

(1991). Effects of xylooligosaccharides on blood glucose, serum

and liver lipids and cecum short chain fatty acids in diabetic

rats. Agricultural and Biological Chemistry, 55, 199–205.Immerzeel, P., Falck, P., Galbe, M., Adlercreutz, P., Karlsson, E. N.,

& Stalbrand, H. (2014). Extraction of water-soluble xylan from

wheat bran and utilisation of enzymatically produced

xylooligosaccharides by lactobacillus, bifidobacterium and

weissella spp. LWT – Food Science and Technology, 56, 321–327.Jaskari, J., Kontula, P., Siitonen, A., Jousimies-Somer, H.,

Mattila-Sandholm, T., & Poutanen, K. (1998). Oat beta-glucan

and xylan hydrolysates as selective substrates for

Bifiodbacterium and Lactobacillus strains. Applied Microbiologyand Biotechnology, 49(2), 175–181.

Jenkins, D. J., Kendall, C. W., Augustin, L. S., Martini, M. C.,

Axelsen, M., Faulkner, D., et al. (2002). Effect of wheat bran on

glycemic control and risk factors for cardiovascular disease in

type 2 diabetes. Diabetes Care, 25, 1522–1528.Jensen, J. K., Johnson, N., & Wilkerson, C. G. (2013). Discovery of

diversity in xylan biosynthesis genes by transciptional

profiling of a heteroxylan containing mucilaginous tissue.

Frontiers in Plant Science, 4, 1–15.Kelly, G. (2009). Inulin-type prebiotics: a review (part 2)..

Alternative Medicine Review, 14(1), 36–55.Kiso, Y., Tateyama, I., Koji, H., Johno, I., Iino, T., Hirai, K., et al.

(2005). Effect of xylooligosaccharide intake on severe

constipation in pregnant women. Journal of Nutritional sciencevitaminology, 51, 445–448.

Knowles, S. E., Jarrett, I. G., Filsell, O. H., & Ballard, F. J. (1974).

Production and utilization of acetate in mammals. TheBiochemical Journal, 142(2), 401–411.

Kobayashi, H., & Fukuoka, A. (2013). Synthesis and utilisation of

sugar compounds derived from lignocellulosic biomass. GreenChemistry, 15, 1740–1763.

Lamsal, B. P. (2012). Production, health aspects and potential food

uses of dairy prebiotic galactooligosaccharides. Journal of theScience of Food and Agriculture, 92, 2020–2028.

Lee, C. C., Wang, H. F., & Lin, S. D. (2008). Effect of

isomaltooligosaccharide syrup on quality characteristics of

sponge cake. Cereal Chemistry, 85(4), 515–521.Loo, J. V., Cummings, J., Delzenne, N., Englyst, H., Franck, A.,

Hopkins, M., et al. (1999). Functional food properties of non-

digestible oligosaccharides: a consensus report from the

ENDO project (DGXII-AIRII-CT94-1095. British Journal ofNutrition, 81, 121–132.

Lu, Z. X., Walker, K. Z., Muir, J. G., & O’ Dea, K. (2004). Arabinoxylanfiber improves metabolic control in people with Type IIDiabetes. European Journal of Clinical Nutrition, 58(4), 621–628.

Macfarlane, S., Macfarlane, G. T., & Cummings, J. H. (2006). Reviewarticle: prebiotics in the gastrointestinal tract. AlimentaryPharmacology and Therapeutics, 24, 701–714.

Madhukumar, M. S., Chandrashekar, P. M., Venkatesh, Y. P., &Muralikrishna, G. (2011). Immunomodulatory activity of xylo-oligosaccharides from Bengalgram (Cicer arietinum L.) husk.Trends in Carbohydrate Research, 3(3), 44–50.

Madhukumar, M. S., & Muralikrishna, G. (2012). Fermentation ofXylo-oligosaccharides obtained from wheat bran and Bengalgram husk by lactic acid bacteria and bifidobacteria. Journal ofFood Science Technology, 49(6), 745–752.

Makelainen, H., Forssten, S., Saarinen, M., Stowell, J., Rautonen,N., & Ouwehand, A. C. (2010). Xylo-oligosaccharides enhancethe growth of Bifidobacteria and Bifidobacterium lactis in asimulated colon model. Beneficial Microbes, 1, 81–91.

Makelainen, H., Juntunen, M., & Hasselwander, O. (2009). Prebioticpotential of xylo-oligosaccharides. In D. Charalampopoulous,& R. A. Rastall (Eds.), Prebiotics and probiotics science andtechnology (pp. 245–258). New York: Springer.

Marathe, N., Shetty, S., Lanjekar, V., Ranade, D., & Shouche, Y.(2012). Changes in human gut flora with age: an indianfamilial study. BMC Microbiology, 12, 222–232.

Martinez, R., Torres, P., Meneses, M. A., Figueroa, J. G., Perez-Alvarez, J. A., & Viuda-Martos, M. (2012). Chemical,technological and in-vitro antioxidant properties of mango,guava, pineapple and passion fruit dietary fibre concentrate.Food Chemistry, 136, 1520–1536.

McVeagh, P., & Miller, J. B. (1997). Human milk oligosaccharides:only the breast. Journal of Paeditrics and Child Health, 33, 281–286.

Moura, P., Barata, R., Carvalheiro, F., Girio, F., Loureiro-Dias, M. C.,& Esteves, M. P. (2007). In vitro fermentation of xylo-oligosaccharides from corn cobs autohydrolysis byBifidobacterium and Lactobacillus strains. LWT – Food Science andTechnology, 40(6), 963–972.

Moure, A., Gullon, P., Dominguez, H., & Parajo, J. C. (2006).Advances in the manufacture, purification and applications ofxylooligosaccharides as food additives and nutraceuticals.Process Biochemistry, 41, 1913–1923.

Mussatto, S. I., & Mancilha, I. M. (2007). Non-digestibleoligosaccharides: a review. Carbohydrate Polymers, 68, 587–597.

Na, M. H., & Kim, W. K. (2007). Effects of xylooligosaccharidesintake on feceal bifidobacteria, lactic acid and lipidmetabolism in Korean young women. Korean Journal ofNutrition, 40, 154–161.

Nabarlatz, D., Montane, D., Kardosova, A., Bekesova, S., Hribalova, V.,& Ebringerova, A. (2007). Almond shell xylo-oligosaccharidesexhibiting immunostimulatory activity. Carbohydrate Research,342(8), 1122–1128.

Neyrinck, A. M., Van Hee, V. F., Piront, N., De Backer, F., Toussaint, O.,Cani, P. D., et al. (2012). Wheat-derived arabinoxylanoligosaccharides with prebiotic effects increase satietogenic gutpeptides and reduce metabolic endotoxemia in diet-inducedobese mice. Nutrition and Diabetes, 2, 1–9.

Nguyen, T.-A. D., Kin, K.-R., Han, S., Cho, H., Kin, J., Park, S., et al.(2010). Pretreatment of rice straw with ammonia and ionicliquid for lignocellulose conversion to fermentable sugars.Bioresources Technology, 101, 7432–7438.

Niness, K. R. (1999). Inulin and Oligofructose: what are they?.Journal of Nutrition, 129, S1402–S1406.

Ogawa, K., Takeuchi, M., & Nakamura, N. (2005). Immunologicaleffects of partially hydrolyzed arabinoxylan from corn husk inmice. Bioscience, Biotechnology, and Biochemistry, 69(1), 19–25.

Ohno, H., Hattori, M., Fukuda, S., Toh, H., Hase, K., Oshima, K., etal. (2011). Bifidobacteria can protect from enteropathogenicinfection through production of acetate. Nature, 469, 543–547.

B i o a c t i v e C a r b o h y d r a t e s a n d D i e t a r y F i b r e 5 ( 2 0 1 5 ) 1 9 – 3 0 29

Okazaki, M., Fujikawa, S., & Matsumoto, N. (1990). Effect ofxylooligosaccharide on the growth of bifidobacteria.Bifidobacterial Microflora, 9(2), 77–86.

O’Shea, N., Arendt, E. K., & Galaghar, E. (2012). Dietary Fibre andphytochemical characteristics of fruits and vegetablesbyproducts and their recent applications as novel ingredientsin food products. Innovative Food Science and EmergingTechnologies, 16, 1–10.

Otieno, D. O., & Ahring, B. K. (2012). The potential foroligosaccharide production from the hemicellulose fraction ofbiomass trhough pretreament process: Xylooligosaccharides(XOS), Arabinooligosaccharides (AXOS), andMannooligosaccharides (MOS). Carbohydrate Research, 360,84–92.

Ou, S. Y., Jackson, G. M., Jiao, X., Chen, J., Wu, J. Z., & Huang, X. S.(2007). Protection against oxidative stress in diabetic rats bywheat bran feruloyl oligosaccharides. Journal of Agriculture andFood Chemistry, 55, 3191–3195.

Parajo, J. C., Vazquez, M. J., & Alonso, J. L. (2000).Xylooligosaccharides: manufacture and application. Trends inFood Science and Technology, 11, 387–393.

Patel, A., Falck, P., Shah, N., Immerzeel, P., Adlercreutz, P.,Stalbrand, H., Prajapati, J. B., Holst, O., & Nordberg, K. E. (2013).Evidence for xylooligosaccharide utilization in Weissellastrains isolated from Indian fermented foods and vegetables.FEMS Microbiology Letters, 346(1), 20–28.

Pizzoferrato, L. (2003). Functional ingredients and functionalcomponents. Ingredient Aliment, 2, 26–30.

Prapulla, S. G., & Aachary, A. A. (2011). Xylooligosaccharides (XOS)as an emerging prebiotic: microbial synthesis, utilization,structure characterisation, bioactive properties andapplications. Comprehensive Reviews in Food Science and FoodSafety, 10, 2–16.

Prapulla, S. G., Gobinath, D., Madhu, A. N., Prashant, G., &Krishnapura, S. (2010). Beneficial effects of xylo-oligosaccharides and fructooligosaccharides in streptozocininduced diabetic rats. British Journal of Nutrition, 104, 40–47.

Ramadoss, G., & Muthukumar, K. (2014). Ultrasound assistedammonia pretreament of sugarcane bagasse for fermentablesugar production. Biochemical Engineering Journal, 83, 33–41.

Ramakrishna, B. S., Roberts-Thomson, I. C., Pannall, P. R., &Roediger, W. E. (1991). Impaired sulphation of phenol by thecolonic mucosa in quiescent and active ulcerative colitis. Gut,32, 46–49.

Renault, E., Barbat-Rogeon, A., Chaleix, V., Calliste, C. A., Colas, C., &Gloaguen, V. (2014). Partial structural characterisation andantioxidant activity of a phenolic-xylan from Castanea sativahardwood. International Journal of Biological Macromolecules, 70,373–380.

Roberfroid, M. (2007). Prebiotics:the concept revisited. The Journalof Nutrition Effects of Probiotics and Prebiotics, 137, 831S–837S.

Roberfroid, M. B., Gibson, G. R., Hoyles, L., McCartney, A. L.,Rastall, R., Rowland, I., et al. (2010). Prebiotics effects:metabolic and health benefits. British Journal of Nutrition, 104(2), S1–63.

Roberfroid, M., & Slavin, J. (2000). Nondigestible oligosaccharides.Critical Reviews in Food Science and Nutrition, 40, 461–480.

Roediger, W. E. (1982). Utilization of nutrients by isolatedepithelial-cells of the rat colon. Gastroenterology, 83, 424–429.

Roediger, W. E., & Moore, A. (1981). Effect of short chain fatty acidon sodium absorption in isolated human colon perfusedthrough the vascular bed. Digestive Diseases and Sciences, 26(2),100–106.

Samuelsen, A. B., Rieder, A., Grimmer, S., Michaelsen, T. E., &Knutsen, S. H. (2011). Immunomodulatory activity of dietaryfibers: arabinoxylan and mixed-linked beta-glucan isolatedform barley show modest activities in-vitro. InternationalJournal of Molecular Sciences, 12, 570–587.

Sanders, M. E. (2008). Probiotics: definition, sources, selection anduses. Clinical Infectious Diseases, 46, S58–61.

Scheller, H. V., & Ulvskov, P. (2010). Hemicelluloses. Annual Reviewof Plant Biology, 61, 263–289.

Schrezenmeir, J., & de Vrese, M. (2001). Probiotics, prebiotics andsymbiotics-approaching a definition. American Journal ofClinical Nutrition, 73, S61–S64.

Schley, P. D, & Field, C. J. (2002). The immune-enhancing effects ofdietary fibres and prebiotics. British Journal of Nutrition, 87(2),S221–S230.

Semee, M., Rehman, S., Nuzhat, H., Amer, J., & Haq, N. (2008).Xylooligosaccharide enriched yoghurt: physicochemical andsensory evaluation. Pakistan Journal of Nutrition, 7, 566–569.

Shahidi, F. (2009). Nutraceuticals and functional foods: wholeversus processed foods. Trends in Food Science and Technology,69, 146–149.

Shallom, D., & Shoham, Y. (2003). Microbial hemicellulase. CurrentOpinion in Microbiology, 6, 219–228.

Sharma, M., & Majumdar, P.K (2009). Occupational lifestylediseases: an emerging issue. Indian Journal of Occupational andEnvironmental Medicine, 13(3), 109–112.

Sheu, W. H.-H., Lee, I. T., Chen, W., & Chan, Y. C. (2008). Effects ofxylooligosaccharides in type 2 diabetes mellitus. Journal ofNutritional Science and Vitaminology, 54, 396–401.

Shi, L., Dong, Q., & Ding, K. (2014). Structure elucidation andimmunomodulatory activity in vitro of a xylan from roots ofCudrania tricuspidata. Food Chemistry, 152, 291–296.

Skutches, C. L., Holroyde, C. P., Myers, R. N., & Reichard, G. A. (1979).Plasma acetate turnover and oxidation. Journal of ClinicalInvestigation, 64(3), 708–713.

Slavin, J. (2013). Fiber and prebiotics: mechanisms and healthbenefits. Nutrients, 5(4), 1417–1435.

Staneva, G., Petkova, D., Hazarasova, R., Georgieva, R., Pankov, R.,Skrobanska, R., et al. (2013). Intake of xylooligosaccharidesalters the structural organisation of liver plasma membranebilayer. Food Biophysics, 9, 1–7.

Staton, C., Gardiner, G., Meehan, H., Collins, K., Fitzgerald, G.,Lynch, P. B., & Ross, R. P. (2001). Market potential for probiotics.The American Journal of Clinical Nutrition, 73(2), 476S–483S.

Sugawara, M., Suzuki, K., Endo, K., Kumemura, M., Takeuchi, M.,& Mitsuoka, T. (1990). Effects of the dietary supplementationof corn hemicellulose on fecal flora and bacterial enzyme-activities in human adults. Agricultural and Biological Chemistry,54, 1683–1688.

Suwa, Y, Koga, K, Fujikawa, S, Okazaki, M, Irie, T, Nakada, T.Bifidobacterium Bifidum proliferation promoting compositioncontaining xylooligosaccharide. US patent 5939309; 1999.

Suzuki, K., Kitamura, S., Kato, Y., & Itoh, T. (2000). Highlysubstituted glucuronoarabinoxylans (hsGAXs) and low-branched xylans shows a distinct localization patternin the tissues of zea mays L. Plant Cell Physiology, 41(8),948–959.

Swennen, K., Courtin, C. M., & Delcour, J. A. (2006). Non-digestibleoligosaccharides with prebiotic properties. Critical Reviews inFood Science and Nutrition, 46, 459–471.

Teitelbaum, J. E., & Walker, W. A. (2002). Nutritional impact of preand probiotics as protective gastrointestinal organisms.Annual Review in Nutrition, 22, 107–138.

Ten Bruggencate, S. J., Bovee-Oudenhoven, I. M., Lettink-Wissink, M. L.,Katan, M. B., & Van der Meer, R. (2006). Dietaryfructooligosaccharides affects intestinal barrier function in healthymen. Journal of Nutrition, 136(1), 70–74.

Tomomatsu, H. (1994). Health effects of oligosaccharides. FoodTechnology, 48, 61–65.

Topping, D. L., & Clifton, P. M. (2001). Short chain fatty acids andhuman colonic functions: roles of resistant starch andnonstarch polysaccharides. Physiological Reviews, 81,1031–1064.

B i o a c t i v e C a r b o h y d r a t e s a n d D i e t a r y F i b r e 5 ( 2 0 1 5 ) 1 9 – 3 030

Torsdottir, I., Alspten, M., Holm, G., Sandberg, A. S., & Tolli, J. (1991).

A small dose of soluble alginate fiber affects postprandial

glycemia and gastric emptying in humans with diabetes. Journalof Nutrition, 121, 795–799.

Van Craeyveld, V., Courtin, C. M., Swennen, K., Dornez, E.,

Van de Wiele, T., Marzorati, M., et al. (2008). Structurally

different wheat-derived Arabinoxylooligosaccahrides have

different prebiotic and fermentation properties in rats. TheJournal of Nutrition, 138, 2348–2355.

Van Dyk, J. S., Gama, R., Morrison, D., Swart, S., & Pletscheke, B. I.

(2013). Food processing waste: problems, current management

and prospects fro utilisation of the lignocellulose

commponents through enzymes synergistic degradation.

Renewabale and Sustainable Energy Reviews, 26, 521–531.Vankova, K., Onderkova, Z., Antosova, M., & Polakovic, M. (2008).

Design and economics of industrial production of

fructooligosaccharides. Chemical Papers, 62(4), 375–381.Vardakou, M., Palop, C. N., Gasson, M., Narbad, A., &

Christakopoulous, P. (2007). In vitro three-stage continuous

fermentation of wheat arabinoxylan fractions and induction

of hydrolase activity in gut microflora. International Journal ofBiological Macromolecules, 41, 584–589.

Vazquez, J. M., Alonso, J. L., Dominguez, H., Garrote, G., &

Parajo, J. C. (2003). Xylooligosaccharides: properties and

production technologies. Electronic Journal of Environmental,Agricultural and Food Chemistry, 2(1), 230–232.

Vazquez, M. J., Alonso, J. L., Dominguez, H., & Parajo, J. C. (2000).

Xylooligosaccharides: manufacture and application. Trends inFood Science and Technology, 11, 387–393.

Veenashri, B. R., & Muralikrishna, G. (2011). In vitro antioxidant

activity of xylo-oligosaccharides derived from cereal and

millet brans – a comparative study. Food Chemistry, 126,1475–1481.

Vieira, A. T., Teixeira, M. M., & Martins, F. S. (2013). The role of

probiotics and prebiotics in inducing gut immunity. Frontiers inImmunology, 4, 1–12.

Vitali, B., Ndagijimana, M., Maccaferri, S., Biagi, E., Guerzoni,

M. E., & Brigidi, P. (2012). An in vitro evaluation of the effects of

probiotics and prebiotics on the metabolic profile of human

micorbiota. Anaerobe, 18, 386–391.

Voragen, A. G., Kabel, M. A., Kortenoveven, L., & Schols, H. A. (2002).In vitro fermentability of differently substitued xylo-oligosaccharides. Journal of Agricultural and Food Chemistry, 50,6205–6210.

Voragen, A. G., Van Laere, K. M., Hartemink, R., Bosveld, M., &Schols, H. A. (2000). Fermentation of plant cell wall derivedpolysaccharides and their corresponding oligosaccharides byintestinal bacteria. Journal of Agriculture and Food Chemistry, 48,1644–1652.

Walton, G. E., Lu, C., Trogh, I., Arnaut, F., & Gibson, G. R. (2012). Arandomised, double-blind, placebo controlled cross-overstudy to determine the gastrointestinal effects ofconsumption of arabinoxylan-oligosaccharides enrichedbread in healthy volunteers. Nutritional Journal, 11, 1–11.

Wang, J., Sun, B., Cao, Y., Tian, Y., & Wang, C. (2009). Enzymaticpreparation of wheat bran xylooligosaccharides and theirstability during pasteurization and autoclave sterilization atlow pH. Carbohydrate Polymers, 77(4), 816–821.

Wang, J., Cao, Y., Wang, C., & Sun, B. (2011). Wheat branxylooligosaccharides improves blood lipid metabolism andantioxidant status in rat fed a high-fat diet. CarbohydratePolymers, 86, 1192–1197.

Wang, J., Sun, B., Cao, Y., & Wang, C. (2010). Wheat bran feruloyloligosaccharides enhances the antioxidant activity of ratplasma. Food Chemistry, 123, 472–476.

Yamani, L. N., Kristanti, A. N., & Puspaningsih, N. N. (2012). Thepreliminary study of antioxidant activity from xylo-oligosaccharide of corncob (Zea mays) hydrolysis productwith endo-β-xylanase enzyme. Indonesian Journal of Tropical andInfectious Disease, 3(2), 112–117.

Yin, D., Jing, Q., AlDajani, W.W., Duncan, S., Tschirner, U., Schilling, J.,et al. (2011). Improved pretreatment of lignocellulosic biomassusing enzymatically-generated peracetic acid. BioresourceTechnology, 102, 5183–5192.

Zha, Y., & Punt, P. J. (2013). Exometabolomics approaches instudying the application of lignocellulosic biomass asfermentation feedstock. Metabolites, 3, 119–143.

Zhou, S., Liu, X., Guo, Y., Wang, Q., Peng, D., & Cao, L. (2010).Comparison of the immunological activities of arabinoxylansfrom wheat bran with alkali and xylanase-aided extraction.Carbohydrate Polymers, 81, 784–789.