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International Journal of Food Sciences and Nutrition, December 2012; 63(8): 1001–1013

Wheat : its composition and benefits to health, aEuropean perspective

LEO STEVENSON1 ,FRANKIE PHILLIPS1 ,KATHRYN O’SULLIVAN2 ,&JENNY WALTON2

1 Food &Nutrition Research Group,Faculty of Education, Community &Leisure, Liverpool John Moores University, Liverpool, UK, and 2 Department of Nutrition and Scientific Affairs, Kellogg CompanyGBLtd, Manchester,UK

Abstract bran is aconcentrated source of insoluble fibre. Fibre intakes are generally lower than recommendations. This paper reviews the physiological effects of wheat bran and the health benefits it mayprovideinterms of the prevention of diseases such as colon and breast cancers, cardiovascular disease, obesity and gastrointestinal diseases.Inrecognition of the weight of evidence, the European Food Safety Authority has recently approved two health claims for wheat bran and gastrointestinal health.

Keywords: dietaryfibre, wheat bran, wheatgerm, , cancer,CVD,dietaryantioxidants,gastrointestinal health, health claims

Introduction Wheat, atype of grassplant,issecond only to as safety andevennutrientbioavailability (Topping the main human food crop.Commercially, Tr iticum 2007),there has been interest in the potential health aestivum vulgare and Tr iticum turgidumdurum (hard benefits of high fibre food products for several years. wheat, mainly used in products) are of most In terms of health, epidemiological(as well as importance(Macrae et al. 1993). The wheat or experimental) evidence is accumulating to show that ‘’, which is harvested for humannutrition, is fibre may reduce the risk of certain chronic diseases, in composed of anumberofdifferent tissues: the germ particular cardiovascular disease (CVD), metabolic (orembryo); the ,whichispackedwith syndrome, type 2diabetes andcertain cancers(Fung starchgrains to provide energy forgermination; the 2002; Koh-Banerjee et al. 2004; Sayhoun et al. 2006; thick cell-walledaleurone layer, encasing the endo- Seal2006; de Munter et al. 2007; Schatzkin et al. 2007; sperm;and the pericarp. The bran fractions consist of Mellen et al. 2009).Although it has been suggested that the pericarp, testa, and hyaline and layers. By it is the complex combination of components in the weight, the wheat caryopsis is composed of an outer wholegrain matrix that may work togethertoimpart branny (14–16% of the grain), the germor embryo (2–3%), and the central endosperm (mainly healthbenefits (Slavin 2003; Fardet 2010),othershave : 81–84%) (Pomeranz 1988). suggested the particular role of the bran component Conventional millingofwheat is based on (Jensen et al. 2004).Inseveral epidemiological studies, separating the endosperm(whichproduces white flour analysis of data obtained for whole grains and adjusted when milled)from the bran layersand embryo.The for intake of its constituents (namely bran, aleurone cells, along with the other bran layersand the germ andendosperm) showedanindependent embryo,are removed to formthe bran fraction. associationonlyfor thewheat brancomponent Although some processing is necessaryfor palatability, (Vitaglione et al. 2008).

Correspondence: Kathryn O’Sullivan, Department of Nutrition and Scientific Affairs, Kellogg CompanyGBLtd, Kellogg Building,Talbot Rd, Manchester M16 OPU,UK. Tel: þ 44 161 869200. E-mail: kathryn.O’[email protected]

ISSN 0963-7486 print/ISSN 1465-3478 online q 2012 Informa UK, Ltd. DOI:10.3109/09637486.2012.687366 1002 L. Stevenson et al.

Physiological effectsofwheat bran and wheat fermentation)with ahigh capacity are also germ often ignored. Both wheat variety and growing conditions can Nutritionally,bran fractions produced by milling are significantly alter the antioxidant profiles, concen- rich in fibre,minerals, B6, , folate trations andproperties of compounds such as phenolic andvitamin Eand some phytochemicals, in particular acids, carotenoids and tocopherols found in wheat such as phenolic compounds (Shewry brans (Zhouetal. 2004; Menga et al. 2010; Shewry 2009).However, bioavailability is affected by the food et al. 2010),althoughwheat bran fractions seem to matrix as well as processing conditions. Bran is used consistentlyretain theirradical scavenging and in the production of brown and wholemeal flours, chelating capacities. Additionalwork has shown that henceretainingsomeofthe valuable nutritional it is the aleurone layer (wheat bran fraction) that components that are depletedwhen these fractions consistently hasthe highest antioxidant capacity are furtherremoved in the refinement of white flour. amongwheat fractions andthatferulic acidin The physiological effects of wheat brancan be split particular (a derivative of the phenolic acid cinnamic intonutritional effects (fromthe present), acid)accounts for up to 60% of this antioxidant mechanical effects (mainlyonthe gastrointestinal capacity (Mateo Anson et al. 2008; Vaher et al. 2010). tract,due to the fibre content) and antioxidant effects It has been suggested that the antioxidant phyto- (arising from thephytonutrientspresent such as chemicals found in wheat bran fractions may modulate phenolic acid and ). Table Ilists the cellularoxidative status andprevent biologically major bioactivecompounds foundinwholegrain important molecules such as DNA, and wheat, wheat bran and germfractions. membranelipids from oxidative damage, andthat Studies have reportedthat the majority of bene- this consequently plays arole in reducing the risk ficialantioxidant phytochemicals (including phenolic of chronic diseases such as CVD and cancer (Zhou acid and alkylresorcinols) in wholewheatgrainare et al. 2004). present in the germ/bran fractions. In wholegrain The phenolic antioxidants present in wheat bran wheat flour, the bran/germfractions contained83% havebeen shown to inhibit LDLoxidation, possibly by of total phenolic content(Adom et al. 2005).Con- binding with apolipoprotein-B (Yuetal. 2005; Liyana- sequently,the bran fraction has higher antioxidant Pathiranaand Shahidi 2007). Alkylresorcinols, activity than other milled fractions (Liyana-Pathirana another antioxidant found in wheat bran, has been andShahidi 2007). showntoinhibit platelet binding to fibrinogen, Although theantioxidant capacity of cereal stimulate thromboxane production and inhibit trigly- fractions, such as wheatbran, is wellreported, ceride formation, suggesting apotential role for Perez-Jimenez andSaura-Calixto (2005) suggest that phenolic compounds found in the branfractions in the antioxidant capacity maybeunderestimated in the CVD (Ross et al. 2004). literature, since the laboratoryextraction methods More recent work has also shown that wheat bran used do not always allow for acomplete release of phenolic compounds, such as feruloyl oligosacchar- antioxidant compounds, and non-extractable poly- ides, protect against free radical-induced oxidative phenols (which may be released in the gut after colonic damage in human erythrocytes (Wang 2009).

Table I. Average content (g/100 gfood) of bioactivecompoundsinwholegrain wheat and wheat bran and germfractions.

Bioactivecompound Wholegrain wheat Wheat bran Wheat germ a -Linoleic acid (18:3n –3)–*0.16 0.53 Sulphur compounds0.5 0.7 1.2 Total free glutathione 0.007 0.038 0.27 Fibre (as AOAC)13.2 44.6 17.7 Lignins 1.9 5.6 1.5 Oligosaccharides 1.9 3.7 10.1 Phytic acid 0.9 4.2 1.8 Minerals and trace elements 1.12 3.39 2.51 Bvitamins 0.0091 0.0303 0.0123 (tocopherolsand ) 0.0047 0.0095 0.0271 Carotenoids 0.00034 0.00072 –* Polyphenols 0.15 1.10 . 0.37 Phenolic acids 0.11 1.07 . 0.07 Flavonoids 0.037 0.028 0.300 Lignans 0.0004 0.0050 0.0005 Alkylresorcinol0.07 0.27 –* Phytosterols 0.08 0.16 0.43

Note: From Fardet (2010); *Nodata found. Wheat bran 1003

Arabinoxylan is an important source of antioxidant in wholegrain fractions (such as ferulicacid,mag- phenolic compounds, includingalkylresorcinols and nesium, ,copper, , policosanol and phenolic acids (including ). Whendelivered melatonin)havealso beensuggested to have arole in to the colon complexed with arabinoxylan, these promoting mental health(Fardet 2010). phenolic compounds maybereleased by fermentation to havepotentially beneficial effects (Vitaglione et al. Phytic acidand wheat bran 2008).Alkylresorcinols can be incorporated intocell membranes and play arole in vivo,inmembrane The bioavailability of minerals in wheat branisunder function. debate because of the presence of the ‘anti–’ Ferulic acid likemost of the phenolic compounds in phytic acid. wholegrain wheat fractions exists in bound form Phytic acid is anaturally occurring organic com- (approximately 76%), usually bound to arabinoxylans pound present in , usually as myoinositol andother indigestible polysaccharides(Liu2007; hexaphosphate. It is concentrated in the external Mateo Anson et al. 2009).Although processing (such coversinthe pericarpand aleurone layer of the grain as as thermal treatments and fermentation) mayimprove well as, at lower levels, in the germ(Cheryan 1980); the release of ferulic acid andotherbound phenolics, 90% of the phytic acid in grainisinthe aleurone layer some authorsquestionthe availability of such with 10% in the embryo (Dost andTokul 2005). phenolics for absorption in the gastrointestinal tract Consequently,the amount of phytic acid is greatly (MateoAnson et al.2009).Otherssuggest the determined by the fractions removed during milling: importanceofbound phytochemicals, andthat unlike white flour has almost no phytate. Wheat contains phytochemicalsfrom and (whichare around 1.13% phytate (dryweight) (Cheryan 1980) or mainly in free or soluble conjugate forms and readily 3% expressed as grossproduct(Pointillart and available in the upper gastrointestinal tract) theymay Gueguen1992). haveamore site-specific effect in the colon, suggesting Phytic acid content ranges from 200 to 400 mg/100 g that wheat bran may impartgreater health benefits in refined flour and 600–1000 mg/100 ginwhole flour when consumed as partofawiderdiet(Liu 2007). (Febles et al. 2002).Inwheat bran, it ranges from 3116 Although most of the phenolics in wheat branare to 5839 mg/100 gdry weight (Bilgicli andIbanoglu bound to cell wall materials that are difficult to digest, 2007).Anaverage 2–3tablespoon serving of comm- theymay reach the colon in tact, where they undergo ercial wheat bran is estimated to contain 200–300 mg colonicdigestion by microflora andconsequently may of phytic acid. Thereisalack of data on average daily exerttheir potentialhealthbenefits locally. For intakes of phytic acid. In Spain, where daily example, gastrointestinal esterase can release ferulic consumptioniscalculated at 151 g/day,phytic acid acid (a potent antioxidant) from bran (Andreasen et al. intakefrom bread is estimated at 159 mg/day (if white 2001). Saura-Calixto(2011) points outthatthe bread was consumed) to 350 mg/day (wholewheat presence of bound antioxidants, such as polyphenols bread) (Garcia-Estepa et al. 1999).Onthe basis of a andcarotenoids, in dietaryfibre may significantly similar calculation, phytic acid intake is estimated at affectthe physiological properties and health effectof 96 g/day (if is consumed) to 211 mg/day dietary fibre,and thatperhaps dietaryfibre and (wholemeal bread). antioxidants should be approachedjointly in nutrition Most of the minerals in wheat kernels are presentas andhealth studies because of their common fate in complexes with phytic acid.Maturewheat grain has the gut. high activity,hydrolysing phytates andmaking Other biologically important components in whole- the minerals nutritionally available (Brinch-Pedersen grain fractions include sulphur containing amino acids et al. 2002).However, the presence of phytate has (methionine andcystine). These two amino acids are been consideredasananti-nutrient in humans because found in higher levels in the wheat bran (0.6%) of its effect on the bioavailability of iron, , (Fardet 2010). Both methionine and cysteineare zinc and calcium.Whilethe mechanism is not entirely precursorsofglutathione (an intracellular antioxidant) understood, it is suggestedthat phytic acid binds andcontribute to the control of cell oxidative status strongly with these mineralcations to formphytate– (Metayer et al.2008).Lignans,also found in wheat complexes,changing their solubility,func- bran, havebeen shown to have anti-tumour properties tionality absorption and digestibility (Rickard and in mice and humancells that maybemediated by Thompson 1997). Consequently,the complex cannot cytostatic and apoptotic mechanisms(Qu et al. 2005). be absorbedoreasily hydrolysedbythe human body Wheat bran and wheat germfractions also contain and so there is an adverseeffectonbioavailabilityof almost allofthe B-groupvitamins: thiamine, minerals (Harland and Harland1980). riboflavin, niacin, pantothenic acid, pyridoxine, biotin Humanstudies haveshown thatthe absorption of andfolates,withwheat bran andwheat germ calcium, iron, magnesium andzinc is significantly fractions containing about30.3 mg and12.3 mg B lowerindiets high in phytic acid (Kies1985; /100 grespectively.They are also asourceof Sandstrom and Lonnerdal 1989; Heaney et al. 1991; vitamin Eand the carotenoids. Other bioactives found Larsson et al. 1996; Sandberg et al. 1999). 1004 L. Stevenson et al.

Historical studies have shown adecreased absorp- (e.g. from bran) have been shown to be unavailable tion of calciumafter phytic acid was added to white (Fly andCzarnecki-Maulden 1996).Atmoderate bread (Harris1955). More recently, studies have levels (providing 2–4% of totaldietaryfibre), the shown that wheat bran, when digested with milk (e.g. authors concluded that iron from wheat bran is readily as ), reduces the absorbability of the available.However, some human studies have shown calcium in milk (Weaver et al. 1991),possibly through adecrease in iron retention when fed wheat bran physical entrapment, adsorption or ionic binding. (Cook et al. 1983; Hallberg et al. 1987),while others Weaver et al. (1996) showed, in arandomized cross- like Dintzis et al. (1985) showed no change. Indeed, over study of healthy women, that with comparable according to Gibson et al. (2006), phytic acid begins to calcium load,fractionalcalcium absorptionwas lose its inhibitory effectoniron at ratios of , 1.0:1.0 significantly lower when the diet was supplemented (phytate:iron), but the effectisstill present as low with 16 g/day wheat bran; the impact of wheat bran on as 0.2:1.0. calcium availability continued even at calciumloads as There is apotential public health nutritionproblem high as 75 mmol, suggestingthat the ability of wheat of iron and zinc deficiencyfor populations whose diets brantobind calciumisnot saturated at doses higher are mainly cereal andlegume-based, or those whose than those provided by most meals. Consequently,it diets are marginal in essential minerals (Raboy 2001). has been suggested that high intakes of insoluble fibre Vegetarians, whose intakes of phytate are typically maycontribute to osteoporosis. Whether this is of higherthan those of omnivores, appear to be most physiological significance in termsofbonehealth has affected by phytate-containing foods as despite having been explored further. Short-term(4weeks) and similar intakes of,e.g., iron and zinc as omnivores the longer-term(2years) studieshavedemonstrated that bioavailability may be compromised (Agte et al. 1999). wheat braninthe diethad no significant effecton Nevertheless,most studies of vegetarians indicate that boneturnover markersinyoung and older women iron andzinc status is adequate, and it appearsthat (Zitterman et al. 1999; Chen et al. 2004).Therefore, theremay be some degree of physiological adaption of despite the negative effects of wheat bran on calcium the gastrointestinal tract to increase absorption of trace bioavailability,there is insufficient evidence to suggest elements and so overcome the presence of phytic acid that it has any detrimental effectonbone metabolism, (Gibson 1994). causing accelerated bone loss. The degree to whichphytic acid can influence Zinc absorption follows adose-dependent response nutritional status, however, is dependant on anumber with phytate (Navertetal. 1985).Hunt et al. (2008) of food andhost-related factors: the amountdigested showed that diets higher in phytic acid may necessitate in the gut, the content of phytate andminerals in the greater intakes of zinc, and suggested that humans food and the nutritional status (replete or deficient in a only minimally adapt to increase zinc absorption from nutrient), and the overall diet of the individual can all diets high in phytic acid with aphytate:zinc ratio haveanimpactonmineralbioavailability(McKevith . 15–20. However, if the diet is low in phyticacid, 2004). absorption of zinc is up-regulated when zinc intakes Processing significantly affects the bioavailability of are habitually low.Currently,USand Canadian diets minerals in the presence of phytates; germination, haveatypicalphytate: zinc ratio of 2, which would fermentation and baking,leading to phytate hydroly- make the current zinc intakes of 7.1 mg (women) and sis, havebeen shown to have abeneficial impacton 9.0 mg (men) adequate. Meeting current US rec- mineral bioavailability (Watzke 1998). ommendations on increasing wholegrain consumption Animalstudies haveshown that othercomponents would lead to aphytate: zinc ratio of 8, which Hunt of fibre,inulinand oligofructose, act as potent et al.(2008) calculate to equate to azinc intakeof enhancersofmineralbioavailabilityinplant-derived 9.2 mg and 13.4 mg for women andmen respectively. foodsand human studies, havepartially confirmed There are currently no data available on the UK these findings (Coudray et al. 1997; Vanden Heuvel dietary phytate: zinc ratio, but assuming it is similar to et al.1999; Vitali et al.2008). Furthermore, the US ratio, current UK intakes of zinc (7.8 mg and preliminaryhuman studies havealso shown that 10.1 mg for women andmen respectively; meeting the carotenoids (lycopene,lutein andzeaxanthin) RNI of 7.0 and9.5); it could be anticipated that increased iron absorption from awheat-based break- increasing consumptionofwhole grains (and, conse- fast by 8.4–14.4% (Garcia-Casal 2006), but this used quently,ahigherwheat bran intake) could have a white wheat flour, likelytobelow in phytate. negative impactonzinc status in UK adults: RNIs may However, the presence of phytic acid does not only need to be adjusted accordingly. implynutritionalproblems. In contrast to the reported There is no consensus on the effect of wheat bran on anti-nutrient properties of phytic acid,studies have iron bioavailability.Animalstudies have shown that shown apotentially beneficial role for the compound. iron from wheat branforms amonoferricphytate, In particular, phytic acid is reported to lead to delayed which is highly available,possibly because it remains post-prandial absorption (Yoon et al. 1983),decrease soluble at intestinalpHand hydrolyses to aid in plasma cholesterol and triglycerides (Katayama absorption, whereas other iron–phytate complexes 1995),inhibition of hypercalcuria and renal stone Wheat bran 1005 development (Grases et al.1998, 2000) and anti- 6.1 milliontonnes. Totalhuman andindustrial carcinogenic effects(Thomsonand Zhang1991; consumptionofwheat for the same year was estimated Huang et al. 1997),the latter being purported to be at 6.836 million tonnes (FAO 2010), implying wheat owing to antioxidant action. The antioxidant functions consumptionofnearly110 kg per capita. Data for of phytic acid are thought to result mainly from its iron consumptionofwheat bran perse are not currently andcopperchelating properties, althoughmechan- available;however, bran for human consumptionis isms are not yet fully understood (Minihane and produced by flour millersratherthanother wheat Rimbach 2002). users. It is estimated that it accounts for approximately 10% of their total outputofco-products (i.e. products otherthan flour); this wouldamountto112,000 Dietaryfibre and wheat bran tonnesin2008/2009(Alex Waugh, NABIM, personal communication).Wheat is consumed in Europe Thefibrecontent of thewholewheatgrain ranges from typically as bread, pasta, breakfast cereals andbiscuits, 11.6%to12.7% dryweight(Carson andEdwards cakesand pastries. Withinformation takenfrom 2009). Most of thefibrethatisinthe outerlayers of the manufacturer’swebites, Table IV shows sources of grain (pericarp andseedcoat) is typicallycalledwheat wheat bran in the diet. bran.Itisone of therichest sourcesoffibre, 46% is non- starch polysaccharide (NSP). ThemainNSPspresent arearabinoxylan, celluloseand beta-glucanthatare Dietaryfibre and wheat bran intakes respectively 70%, 24%and 6% of theNSP of thebran The European-recommended dietaryfibre intake is (Maesand Delcour2002).The concentrationofsoluble 25 g/day based on the AOAC method. In the UK, fibre fibre in wheatissignificantlylessthaninother cereals, recommendations basedonNSP are set at 18 g/day. e.g. andoats, 3–11%and 3–7%respectively, Forchildren, this varies andthe general rule for health compared with less than 1% in wheat(dryweight) care professionals is age of child plus 5g.Average (Wood1997).The amount andtypeoffibreinwheat, dietaryfibre intakes in Europe range from 10 to andspecifically in wheatbran, is showninTable II. 20 g/day in young children andfrom 16 to 29 g/day in adults (European Food Safety Authority [EFSA] 2010). These recommendations cover totalfibre Wheat consumption in the diet intakeand there is currently no established guidelines Cereals are staplefoodsinwestern countries, and that differentiate between fibre type and source. typically contribute about50% of dietaryfibre intake Fibre intakes are ascertainedthrough dietarysurvey (Lambo et al. 2005). The recommendation that cereals eitherafull dietaryrecall including portion sizes,diet formthe basis of the diet is well recognized in the diariesorfoodfrequency questionnaires. These majority of countries with dietaryguidelines including methods are often time-consuming andwhendealing most EU memberstates,the USAand Canada. with alarge datasettake agreat deal of time, effort, TableIII shows the cereal andcereal product attention to detail andconsistencyofmethodology. consumptionbyadults in Franceand also the The DINE questionnaire (Roe et al. 1994) was %contribution to average intakes of energy andfibre developed to be administered andscored in under (AFSSA 2009).Similar data for UK adults (Hoare et al. 10 minutes by primarycare staff without specialized 2004) show that cereal products contribute 37% of nutritional knowledge. The questionnaire gives an fibre intake and 28% of total kcal intake, while in outputoflow,medium or high for fatand fibre intakes. Belgium it is estimated that average consumption is This validated questionnaire is in wide use and is 186.5 g/day,with cereal and cereal products contribut- currently being modified to provide amore numeric ing 22.3% to total energy and 34% to fibre intakes value for fibre intake basedonmore modernAOAC (De Vriese et al. 2005). fibre values. Wheat is the most heavily consumedgrain in the The majority of data from cohortand epidemiolo- world. Forexample, in the UK wheat consumptionis gical studiesusedtodemonstrate thepotential more than 10 times as muchasrice(which is mostly healthbenefits of wholegrain consumptionhavebeen consumed as ), andoats(419,000 tonnesin derived from dietaryassessment methods that were 2008/2009), or (305,000 tonnes).Usage of not originally designed to quantify wholegrain intakes wheat for flour and starch milling in 2008/2009 was –the majority relied on semi-quantitativefood frequencyquestionnaires using alimited range of Table II. Fibre concentration in wheat and wheat bran. wholegrain foodswith varying descriptions of whole- Total fibre Insoluble fibre Soluble fibre grain foods (Seal 2006). (g/100 g) (g/100 g) (g/100 g)

Wheat grain 11.6–17.0 10.2–14.7 1.4–2.3 Wheat bran and health benefits Wheat bran 36.5–52.4 35.0–48.4 1.5–4.0 Studies haveshown that wheat branmay havea Note: From Vitaglioneetal. (2008). beneficialeffectonthe prevention of diseases, 1006 L. Stevenson et al.

Table III. Cereal products consumptionand %contribution to energy and fibre intakes by French adults.

Consumption (g/person/day)

Age (years) Males Females Total %contribution to energy %contribution to fibre

Bread and rusk 18–34104.1 70.3 83.8 14.7 20.8 35–54149.7 89.8 117.0 55–79163.5 101.7 136.1 Breakfast cereals 18–346.7 7.9 7.4 0.9 1.7 35–543.5 4.7 4.1 55–794.1 3.2 3.7 18–3464.7 39.2 49.3 2.0 3.5 35–5447.5 28.5 37.1 55–7935.8 22.8 30.1 Rice and hard wheat/ 18–3433.9 21.7 26.5 1.4 0.9 35–5432.9 24.1 28.1 55–7922.1 16.7 19.7 Other cereals 18–340.3 0.7 0.6 0.1 0.2 35–540.7 0.8 0.7 55–790.3 0.4 0.3 Pastry/bakeryproducts 18–3420.6 14.3 16.8 2.1 1.5 35–5413.6 11.5 12.4 55–798.6 6.0 7.4 Sweet and savourybiscuits/bars 18–3415.3 14.5 14.8 2.0 1.6 35–548.8 8.1 8.4 55–795.7 4.7 5.3 Cakes 18–3442.2 35.6 38.2 6.0 4.0 35–5441.8 38.6 40.0 55–7932.0 37.1 34.2

Note: From AFSSA (2009). including some cancers(in particularcolorectal by 40%, by eating more fibre-rich foods. Similarly,the cancer), CVD, obesityand some gastrointestinal World Cancer Research Fund’sreportoncancer and diseases, including diverticular disease, constipation diet, physical activity and weight suggestedthat foods andirritable bowel syndrome (IBS)(Fardet 2010). containing fibre decrease risk of colorectal cancer (WCRF/AICR 2007). The Familial Adenomatous Polyposis Trial (De Wheat bran and cancer Cosseetal. 1989) is arandomizedcontrolled trial that Bowel cancer is amajor cause of mortality in the UK. investigated the effects of wheat bran fibre, with or The European Prospective Investigation into Cancer without supplements of ascorbicacid and alpha- andNutrition(EPIC)(Binghametal. 2003) tocopherol, on development of rectal adenomas in recommendedthatpeopleeatinglow fibre diets patients with familial adenomatous polyposis (pre- couldsignificantly reduce risk of colorectal cancer, cursortocolorectal cancer). After 4yearsoffollow-up,

Table IV.Sources of wheat bran in the diet.

Product Fibre per 100 gAOACStandard portion size (g) Fibre per portion (g)

Bran shreds breakfast cereal 27 40 10.8 Bran flakes breakfast cereal; 15 30 4.5 Shredded wheat breakfast cereal 11.8 45 5.3 Extruded pillos breakfast cereal 9.9 45 4.5 Whole wheat biscuits breakfast cereal 10 37.5 3.8 Wholemeal bread 7362.5 Granarybread 5.3 36 1.9 Brownbread 5361.8 Sliced white bread 2.5 36 0.9 Dried wholemeal pasta (uncooked weight)9 44 4.0 Dried wholemeal pasta (uncooked weight)9 87 7.8 Dried wholemeal pasta (uncooked weight)9 130 11.7 Dried white pasta (uncooked weight) 2.8 75 2.1 White pasta (cookedweight) 1.2 180 2.2 Wheat (dryweight) 5603.0

Note: Compiled from Manufacturer’swebsites 2011. Wheat bran 1007 there was some evidence of decreased numberof from colon cancers. Rat model studies haveshown that polyps and therefore reduced risk of cancer where maystimulate, ratherthan inhibit colonic patients consumed at least 50% of their prescribed epithelial cell proliferation (Lupton andKurtz 1993). fibre. The authorsconcluded that the effect of SCFAs on In another randomized control trial of patients colonocytes is different in normal cellsfrom trans- following colonicpolypremoval surgery, Alberts et al. formedcells. Butyrateseems to inhibit growth of (1996) found that adiet supplemented with wheat transferredcells while enhancing proliferationin bran cereal (13.5 g/day) reduced faecal bileacid normal human and rat mucosa. concentration. Bile acids are consideredtoplay a An animal model study (Zoran et al. 1997) showed role in colorectal cancer risk. However, later follow- that although oat bran produces more butyric acid in up studies, after 3years(Albertsetal. 1997),failed the colon, wheat bran is more protective against colon to show any significant effectofthe high wheat bran carcinogenesis, reducing incidence of tumours. In a diet on the development of colorectal adenomas. study involving patientswith ahistory of colon cancer The Australian PolypPrevention Project (Maclen- fed 13.5 gofwheat bran fibre for 2months, Alberts nanetal. 1995) reportedthatalow fatwheat bran et al.(1990) concluded that wheat bran fibre supplemented diet(25 gwheat bran/day) reduced the supplementationcan inhibit DNAsynthesis and incidence of large colorectal adenomas,suggesting epithelial cell proliferation within rectal mucosa crypts that wheat bran, alongside alow- diet, inhibitsthe of patients at high risk for colon cancer. development of malignantadenomas. These studies Finally,studieshaveshownthat phyticacidmay support, to someextent, that awheat bran sup- blockPI-3 kinase activation, which acceleratesapop- plementeddiet may be protective against colorectal tosis andmay be protectiveagainst colorectal cancer and polyps. cancer development (Huang et al. 1997). Other data Furthermore, animal studies have demonstrated a suggest that some of the phytochemicalcompounds significant protective effectofwheat branoncolon in wheat bran,including beta-sitosterol, mayalso carcinogenesis in rats fed ahigh-fat western-style diet have abeneficialeffect on colon cancer (Waliszewski (Alabaster et al. 1996).Wheat bran, in addition to et al. 1997) (50:50),led to enhanced protection and Colon cancer maynot be the only cancer linkedto synergistic effects may inhibit different phases of the fibre.Apotentially protective effectoffibre has also carcinogenicprocess, with wheat bran phytic acid been observedinbreastcancer research. Cade et al. inhibiting earlier stages and psyllium inhibiting later (2007) suggest that in pre-menopausal women total stages(Alabaster et al. 1993). fibre is protective against breastcancer,inparticular Theprotectivemechanismsofwheat bran, fibre from cereals andpossibly fruit. Their work that especially in terms of colon cancer,fall into three involvedanalysis of alarge cohort of adult women categories (Lupton and Turner 1999). The first is the found that in pre-menopausal, but not post-meno- established effect on dilutionofpotential carcinogens pausal, womenastatistically significant inverse andpromotersofcarcinogens –amore bulkystool relationship was found between total fibre intake and reduces access to the cells lining the colon. Second, it risk of breast cancer. The top quintile of fibre intake is well established that wheat bran accelerates transit of was associated with ahazard ratio of 0.48 [95% faecal material through the colon, such that rapid confidence interval(CI)0.24–0.96] compared with transit reduces accessofthe colonicepithelial cells to the lowestquintile. Pre-menopausally,fibre from faecal constituents. However, notall fibre has the same cerealswas inversely associatedwith risk of breast ability to dilute contents of the lumen, or the same cancer and fibre from fruit had aborderline inverse potential to accelerate colonictransit. Animal models relationship.Mechanisms of effectare postulative, but haveshown that wheat bran is the bestdiluterand has plausible mechanisms could be the role in fibre and the shortest transit time comparedwith pectin, guar weight management and the potential for fibre to bind gum,oat bran and cellulose (Gazzaniga and Lupton with estrogens (Goldin et al. 1986; Rose et al. 1991; 1987; Lupton and Meacher1988). Stoll 1996). The third is the effectoffermentation of wheat bran to ShortChainFatty Acids(SCFA) (including butyric Wheat bran and CVD acid)throughout the colon. Studies have found that SCFAs may modulate carcinogenesis through their The cardiovascular benefits from wholegrains are only effects on proliferation, differentiation and apoptosis supported where the wholegrain contains significant of colonocytes,aswell as stimulation of the immune amounts of fibre or bran. In adouble-blind placebo- system (Topping and Clifton 2001; Schley and Field controlled crossover study of wholegrain cereal and 2002). wheatbran, Costabileetal. (2008) reported a Clausen et al. (1991)haveshown that wheat bran significant reduction in total serum cholesterol. After doublesthe productionofSCFAs and in vitro consuming awheat bran-based breakfast cereal for fermentation, resulted in reduced productionof 3weeks, containing approximately 13.5 goffibre, butyrate in subjects with colonic adenomas or suffering serum cholesterolwas reduced from5.576 to 1008 L. Stevenson et al.

4.385 mmol/l in those participants with the highest the effectofwheat bran on GLP-1 secretion, and quintileofserum cholesterol.Furthermore,no found no effect on bodyweight, adipose tissue mass, reduction was found in beneficial HDL-C, suggesting glucose or insulin resistance. However, this study did beneficial effects on CVD risk. demonstrate an impactofwheat branoninflam- In across-sectional analysis of US adolescents, mation, including decreased inflammatorycytokines. Carlson et al. (2011) found that increasing dietaryfibre was associated with lower risk of metabolic syndrome. Wheat bran and digestive health In aprospective cohortstudy of 42,850males, Jensen et al. (2004) examined the effectofaddedbraninthe In termsofdigestive health, wheat bran can offer diet, in addition to wholegrain intakes, on risk of several beneficial effects. Wheat bran has an effect on coronaryheartdisease (CHD). However, while the faecal bulking,delays gastric emptying and accelerates type of bran was notidentified, the authorsreported small bowel transit (McIntyre et al. 1997). Generally, that it was predominantly wheat and oat bran. The faecal bulking has beenlinked with anumberof relative risk of CHD in menwith the highest intake of potentially beneficial effects as summarized in Table V. added bran was 0.70 (95% CI: 0.60–0.82) compared Faecal bulk is aresult of multiple interactions with men who had no addedbran. He et al. (2010) between the food, the host andthe gut ecosystem recently reported on the mortality and CVD-specific (Eastwood 1993).The bulking effects of fibre are mortality of 7822 women with type 2diabetes from the greatestwith cereal fibre, especially products high in Nurses HealthStudy.Compared with those women insoluble NSP such as wheat bran(Topping 2007) with the lowest intake of bran, womenwith the highest Wheat bran is so effective at faecal bulking thatitisthe intake haveall-cause mortality relative risk of 0.72 reference against whichotherfoods are measured for (95%CI: 0.56–0.92) and relative risk for CVD- their faecal bulking efficiency (Monro 2002). specific mortality was 0.65 (95% CI: 0.43–0.99). The mechanismbywhich wheat bran increases stool weight has been studied by Chen et al. (1998), who showed that a30g/day supplementwas associated with Wheat bran and obesity amean wetstool weight increase of 52.4 g/day.Wheat Evidence from epidemiological studies suggests an branwas shown to increase faecal concentrations of inverse relationship between intake of dietaryfibre and sugars(glucose, arabinose and xylose)and mass of weight gain and obesity,while fibre consumption is plant material more than oat bran, althoughoat bran associated with increased satiety anddecreased energy had agreater effectonincreasing bacterial mass. With intake (Freeland et al. 2009).Ithas also been proposed wheat bran, the increase in stool weight was largely a that dietary fibre increases faecal energy loss result of undigested plantfibre(50–60%)but (Astrup et al. 2010). Viscous fibre is thought to exert increased bacteria contributed12–17% of the the greatesteffectonappetite regulation, but studies increase. These studies reportednoincrease in the using wheat bran havealso reported areduction in proportion of in the stool, which supports other food intake following atestmeal with wheat bran, but reports (Cummings 1993). it is not clear whether this effectislong-lasting in terms Both the European Food Safety Authority and the of management of obesity (Freeland et al. 2009). UK Scientific AdvisoryCommittee conclude that the The effectofwheat bran on postprandial appetite- mean increase in daily faecal weight is approximately regulating hormones is less well studied, althougha 5g per 1g wheat branconsumedcompared to other recentanimal study (Neyrinck et al. 2008) investigated fibressuchasfruit and vegetables (4.1 g/g), gums

Table V. Effects of faecal bulking.

Property/effect Consequenteffect

Bulkiness Bulk transfer Bulk transfer Toxin removed, colonic exposure reduced,decreased transit time Replenishmentofsubstrates for fermentation –decreased colon cancer risk Decreased transit time Less putrefaction to harmful products –decreased colon cancer risk Less time for dehydration and stool hardening Increased water load Diluted colon contents, stool softening Pressure distribution –decreased risk of diverticulitis and haemorrhoids ReplenishmentProvides substrate for bacterial growth. Butyrate produced by fermentation protects against colorectal cancer. Shortchain fatty acid productiondecreases solubility of carcinogenic bile acids Binding Decreased toxin /carcinogen activity Pressure distribution Reduces risk of diverticulitis and haemorrhoids by reducingpressure points Distension Stimulates defaecation, preventing stagnation Defaecation DigestiveComfortand continued flow,sense of well-being

Note: From Monro (2002). Wheat bran 1009 including psyllium (4 g/g),soya products (2.5 g/g) and means,such as increasing intake. Prebiotics pectinleast of all (1.2 g/g) (SACN 2008). are definedasnon-digestible food ingredients that Transittime is also affected by wheat bran. Payler beneficially affect host health by selectively stimulating et al. (1975) showed that adding 20 g/day of wheat the growth and/or activity of one or alimitednumber branreduced transit time from 2.75 to 2.0 days, and of bacteria in the colon (Gibson and Roberfroid 1995). the authorsalso confirmed thatwhile bran accelerates It is not the prebioticitself that brings aboutchange, slow transit time, it may also slow down fast transit but its effect on the gut microflora (Wangetal. 2009). time (that is less than 1day). The likely mechanism for There is agrowing body of evidence to supportthe the increase in transit time is the high content of beneficial health effects of prebiotics on bowel health cellulose and hemicelluloses in wheat bran, which and risk of colon cancer andCVD (Costabile et al. softenand expandthe stool. 2008).Prebiotic components of dietary fibre in wheat Insoluble fibre (the maincomponent of wheat bran) bran(including beta-glucans) maybefermentedby is notreadily brokendownbygastrointestinal colonicmicroflora to form SCFA,resulting in microflora and it increases faecal bulk,shortening physiological changes to the coloniccontents, affecting colonictransit time. Soluble fibre dissolves in water to bulking,water retention capacity andviscosity.Butyric formgel and maybedigested by the colonic microflora, acid is one suchSCFAthat has been recognized as a increasing bacterial numbersand thus increasing bulk. fuelfor colonocytes andalso contributes to faecal pH, influencing colonic function Costabile et al. (2008) found amore modest change Wheat bran and IBS in gutmicroflora after consuming awheat brancereal, Increasing fibre intake hasbeen suggested as an initial compared with awholegrain cereal.Markersofcolonic treatment forIBS,although thereare conflicting data metabolic output (including ferulic acid and SCFAs) on itseffectiveness.Conversely, wheatisoften associated also increased. with increasedsymptomsand reducing, butnot necessarilyexcluding, wheatintakemay be beneficialin Wheat bran and health claims within the IBSmanagement(NICE 2008). Nevertheless,Bijkerk European Union et al. (2003, 2009) reported that most GPsrecommend an increase in fibre forpatients with IBS, advisingthe TheEFSAhas been taskedtopreapprove any additionofinsoluble fibre in theformofbran. Amore nutrition and health claim for market in the EU.In recentrandomizedcontrolledtrial showedthatwhile this relatively early stage of the legislation, the EFSA soluble fibre (psyllium)was effective at reducing is working through alist of over 40,000 so-called symptomsofIBS,wheat bran (20g/day)was not, ‘generally accepted claims’. Eightypercent of these especiallyatthe onset of treatment (Bijkerketal. 2009). claimshavebeen rejectedonseveral grounds from Ameta-analysis of the effect of wheat bran on stool insufficient characterization of the food to causeand weight and transit time (Muller-Lissner 1988) showed effectrelationship not being established. In October that wheat branincreased stool weight anddecreased 2010, the EFSA panel passed opinion on two claims transit time in healthy controls and patients with IBS pertaining to the benefits of wheat bran. The two andchronic constipation. The NICE (2008) guideline approved claims are as follows: consensus on IBS states that wheat branshouldnot be recommended for peoplewith IBS as it is ineffective in Increase in faecal bulk the management of symptoms,and may even increase The claimed effectis‘intestinal health: faecal symptoms for some people–an increase in fibre, if bulking’. The targetpopulation is assumed to be neededshouldbeinthe formofsoluble fibre. the general population. The panel considersthat Other gut conditions, however, maybehelped by an increase in faecal bulk might be abeneficial wheat bran. Painteretal. (1972) showed that there was physiological effect. In weighing the evidence, the marked relief from symptoms of diverticular disease panel took into account that the majority of the with ahigh residue, low sugar diet, including 12–14g humanintervention studies showed aconsistent of rawunprocessed wheatbranper day(range: effectofwheat bran fibre on faecal bulk and that 3–45g). More recently, aCochrane review of evidence no threshold dose for the effectcan be established. has found that adding more wheat and branfibre to the Alinear dose dependent relationship was demon- diet was effective at alleviating constipation during strated in several studies. pregnancy, increasing frequency of defaecation, and is The claimed effects are ‘guthealth’ and‘intestinal preferable to taking stimulant , which may transit time, intestinal health’.The target popu- haveundesired side effects (Jewell andYoung 2001). lation is assumed to be the general population. In thecontext of theclarifications providedby Member States, the panel assumes that the claimed Wheat bran as aprebiotic effectreferstoareduction in intestinal transit time. Colonic microflora has aprofound effectonhealth. The panel considers that areduction in intestinal The gut flora components can be modified by dietary transit time withinthe normal range might be a 1010 L. Stevenson et al.

beneficial physiological effect. In weighing the Alberts DS, Einspahr J, Ritenbaugh C. 1997. The effect of wheat evidence, the panel took into account that the bran fibre and calcium supplementation on rectal mucosal studies provided consistentlyindicated that wheat proliferation rates in patients with resected adenomatous polyps. Cancer Epidemiol BiomarkersPrev 6:161–169. branfibre consumedatanamountofatleast Alberts DS, Ritenbaugh C, StoryJA. 1996. Randomised double 10 g/day decreased intestinal transit time. blinded placebo controlled study of the effect of wheat bran fibre and calcium on faecal bile acids in patients with respected Wheat bran is easy to characterize and the evidence for adenomatous colon polyps.JNatl Cancer Inst 88:81–92. theeffect on stool weight andtransit time is Andreasen MF,Kroon PA,Williamson G, Garcia-Conesa MT. unequivocal. The conditions of use for the claim, i.e. 2001. 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