Carbohydrate Terminology and Classification

REVIEW Carbohydrate terminology and classification

JH Cummings1 and AM Stephen2

1Gut group, Division of Pathology and Neuroscience, Ninewells Hospital and Medical School, Dundee, UK and 2Population Nutrition Research, MRC Human Nutrition Research, Elsie Widdowson Laboratory, Cambridge, UK

Dietary carbohydrates are a group of chemically defined substances with a range of physical and physiological properties and health benefits. As with other macronutrients, the primary classification of dietary carbohydrate is based on chemistry, that is character of individual monomers, degree of polymerization (DP) and type of linkage (a or b), as agreed at the Food and Agriculture Organization/World Health Organization Expert Consultation in 1997. This divides carbohydrates into three main groups, sugars (DP 1–2), oligosaccharides (short-chain carbohydrates) (DP 3–9) and polysaccharides (DPX10). Within this classification, a number of terms are used such as mono- and disaccharides, polyols, oligosaccharides, starch, modified starch, non-starch polysaccharides, total carbohydrate, sugars, etc. While effects of carbohydrates are ultimately related to their primary chemistry, they are modified by their physical properties. These include water solubility, hydration, gel formation, crystalline state, association with other molecules such as protein, lipid and divalent cations and aggregation into complex structures in cell walls and other specialized plant tissues. A classification based on chemistry is essential for a system of measurement, predication of properties and estimation of intakes, but does not allow a simple translation into nutritional effects since each class of carbohydrate has overlapping physiological properties and effects on health. This dichotomy has led to the use of a number of terms to describe carbohydrate in foods, for example intrinsic and extrinsic sugars, prebiotic, resistant starch, dietary fibre, available and unavailable carbohydrate, complex carbohydrate, glycaemic and whole grain. This paper reviews these terms and suggests that some are more useful than others. A clearer understanding of what is meant by any particular word used to describe carbohydrate is essential to progress in translating the growing knowledge of the physiological properties of carbohydrate into public health messages. European Journal of Clinical Nutrition (2007) 61 (Suppl 1), S5–S18. doi:10.1038/sj.ejcn.1602936

Keywords: carbohydrate; sugars; oligosaccharides; starch; dietary fibre; classification

Introduction density, large bowel cancer, constipation and resistance to gut infection. The dietary carbohydrates are a diverse group of substances with a range of chemical, physical and physiological properties. While carbohydrates are principally substrates for energy metabolism, they can affect satiety, blood glucose Classification and insulin, lipid metabolism and, through fermentation, exert a major control on colonic function, including bowel As for other macronutrients, the primary classification of habit, transit, the metabolism and balance of the commensal dietary carbohydrates, as proposed at the Joint Food and flora and large bowel epithelial cell health. They may also be Agriculture Organization (FAO)/World Health Organization immunomodulatory and influence calcium absorption. (WHO) Expert Consultation on Carbohydrates in human These properties have implications for our overall health; nutrition convened in Rome in 1997 (FAO, 1998), is by contributing particularly to the control of body weight, molecular size, as determined by degree of polymerization a a diabetes and ageing, cardiovascular disease, bone mineral (DP), the type of linkage ( or non- ) and character of individual monomers (Table 1). This classification is analogous to that used for dietary fat, which is based on carbon chain length, number and position of double bonds and their configuration as cis or trans. A chemical approach is Correspondence: Professor JH Cummings, Division of Pathology and Neuroscience, Ninewells Hospital and Medical School, Dundee DD1 9SY, UK. necessary for a coherent and enforceable approach to E-mail: [email protected] measurement and labelling forms the basis for terminology Carbohydrate terminology and classification JH Cummings and AM Stephen S6 Table 1 The major dietary carbohydrates Two principal approaches to total carbohydrate are used, first, that derived ‘by difference’ and second, the direct Class (DPa) Subgroup Principal components measurement of the individual components that are then Sugars (1–2) Monosaccharides Glucose, fructose, galactose combined to give a total. Calculating carbohydrate ‘by Disaccharides Sucrose, lactose, maltose, difference’ has been used since the early 20th century and trehalose is still widely used around the world (Atwater and Woods, Polyols (sugar Sorbitol, mannitol, lactitol, 1986; United States Department of Agriculture, 2007). The alcohols) xylitol, erythritol, isomalt, maltitol moisture, protein, fat, ash and alcohol content of a food are Oligosaccharides Malto- Maltodextrins determined, subtracted from the total weight of the food and (3–9) (short-chain oligosaccharides the remainder, or ‘difference’, is considered to be carbohy- carbohydrates) (a-glucans) drate. There are, however, a number of problems with this Non-a-glucan Raffinose, stachyose, fructo and oligosaccharides galacto oligosaccharides, approach in that the ‘by difference’ figure includes non- polydextrose, inulin carbohydrate components such as lignin, organic acids, Polysaccharides Starch Amylose, amylopectin, modified tannins, waxes and some Maillard products. In addition to X ( 10) (a-glucans) starches this error, it combines all the analytical errors from the other Non-starch Cellulose, hemicellulose, pectin, polysaccharides arabinoxylans, b-glucan, analyses. Also, a single global figure for carbohydrates in (NSPs) glucomannans, plant gums and food is uninformative because it fails to identify the many mucilages, hydrocolloids types of carbohydrates and thus to allow some understanding of the potential health benefits of those foods. aDegree of polymerization or number of monomeric (single sugar) units. Based on Food and Agriculture Organization/World Health Organization Direct analysis of carbohydrate components and summa- ‘Carbohydrates in Human Nutrition’ report (1998), and Cummings et al. tion to obtain a total carbohydrate value has been the basis (1997). of carbohydrate analysis in the UK since 1929, when the first values were published by McCance and Lawrence (1929). and an understanding of the physiological and health effects Those countries that use McCance and Widdowson’s, The of these macronutrients. Composition of Foods (Food Standards Agency/Institute A chemical approach divides carbohydrates into three of Food Research, 2002) also express carbohydrate using main groups, sugars (DP1–2), oligosaccharides (short-chain this approach. The total figure obtained is for what McCance carbohydrates) (DP3–9) and polysaccharides (DPX10). and Lawrence called ‘available carbohydrate’ and therefore Sugars comprise (i) monosaccharides, (ii) disaccharides and differs from carbohydrate by difference in that it does not (iii) polyols (sugar alcohols). Oligosaccharides are either (a) contain the plant cell wall polysaccharides (fibre). In malto-oligosaccharides (a-glucans), principally occurring addition, it is not complicated by analytical difficulties with from the hydrolysis of starch and (b) non-a-glucan such as other food components. Dietary intake of total carbohydrate raffinose and stachyose (a galactosides), fructo- and galacto- and its components using direct analysis enables examina- oligosaccharides and other oligosaccharides. Polysaccharides tion of geographic variations and changes in intake over may be divided into starch (a-1:4 and 1:6 glucans) and non- time of individual carbohydrate types and their relationship starch polysaccharides (NSPs), of which the major compo- with health outcomes. Total carbohydrate by direct measure- nents are the polysaccharides of the plant cell wall such as ment is preferable and simplified methods to do this should cellulose, hemicellulose and pectin but also includes plant be developed. gums, mucilages and hydrocolloids. Some carbohydrates, Figures obtained for carbohydrate by difference and like inulin, do not fit neatly into this scheme because they carbohydrate analysed directly are not always the same,

exist in nature in multiple molecular forms. Inulin, GFN, particularly for complex mixtures, and foods containing fibre from plants may have from 2 to 200 fructose units and so or certain types of starch, like pasta (Stephen, 2006). This crosses the boundary between oligosaccharides and poly- results in apparently different carbohydrate intakes for the saccharides (Roberfroid, 2005). same list of foods consumed, as shown in Table 2. Fifty-two A variety of methodologies are available for the measure- dietary records from a study conducted in Canada, where ment of the carbohydrate content of food and the compo- carbohydrate by difference is used (Health Canada, 2005) nents are listed in Table 1 (Englyst et al., 2007). were subsequently analysed in the UK using values based on McCance and Widdowson’s The Composition of Foods (Hol- land et al., 1991b, 1992). In this study, energy intake was 12% higher and carbohydrate intake 14% higher when measured Terminology ‘by difference’ (Stephen, 2006). Comparison of carbohydrate intake among different countries should therefore be viewed Total carbohydrate with caution if the method of carbohydrate determination is Although the individual components of dietary carbohy- not the same. Worldwide variations in carbohydrate intake drate are readily identifiable, there is some confusion as to assumed to be due to differences in types of foods consumed, what comprises total carbohydrate as reported in food tables. are also, in part, due to methodology.

European Journal of Clinical Nutrition Carbohydrate terminology and classification JH Cummings and AM Stephen S7 Table 2 Energy and macronutrient intakes for 52 weighed records sugars, added sugar, free sugars (WHO, 2003), refined sugars analysed using Canadian and UK food tables (Nordic Council, 2004), discretionary sugar (New Zealand Energy Protein Fat CHO Nutrition Foundation, 2004) and intrinsic sugars, milk (kcal) (g) (%) (g) (%) (g) (%) sugars and non-milk extrinsic sugars (Department of Health, 1989). Analysis using Canadian nutrient file Mean of 52 records 2265 95.9 (16.9) 81.4 (31.5) 294.2 (52.9) Total sugars Analysis using ‘The composition of foods’ For labelling purposes, the category of total sugars has been Mean of 52 records 1992* 89.8 (17.9) 74.5 (32.7) 252.4* (48.5)* proposed. This includes all sugars from whatever source in a food, and is defined as ‘all monosaccharides and disaccharides other than polyols’ (European Communities, 1990). *Po0.001. From Stephen, 2006. This term is now accepted by the European Union, Australia and New Zealand and may well be adopted by other countries. It is probably the most useful way to describe, Sugars measure and label sugars. The term ‘sugars’ is conventionally used to describe the mono- and disaccharides in food. The three principal monosaccharides are glucose, fructose Free sugars and galactose, which are the building blocks of naturally Traditionally ‘free sugars’ referred to any sugars in a food that occurring di-, oligo- and polysaccharides. Free glucose and were free and not bound (Holland et al., 1992), and included fructose occur in honey and cooked or dried fruit (invert all mono- and disaccharides present in a food, including sugar), in small amounts, and in larger amounts in fruit and lactose (Southgate, 1978). This term was also used analyti- berries where they are the main energy source (Holland et al., cally to describe when the carbohydrate in a food was 1992). Corn syrup, a glucose syrup produced by the hydrolysed and components detected by chromatography or hydrolysis of cornstarch, and high fructose corn syrup, colorimetric methods (Southgate, 1978). In recent years, the containing glucose and fructose, are increasingly used by the use of the term ‘free sugars’ has changed, to refer to all food industry in many countries. Fructose is the sweetest of ‘monosaccharides and disaccharides added to foods by the all the food carbohydrates. Sugars are used as a sweetener to manufacturer, cook and consumer, plus sugars naturally improve the palatability of many foods and beverages, and present in honey, syrups and fruit juices’ and was the are also used for food preservation and in jams and jellies. preferred term for the WHO/FAO Expert Consultation on Sugars confer functional characteristics to foods, like visco- ‘Diet, Nutrition and the Prevention of Chronic Diseases’ sity, texture, body and browning capacity. They increase (WHO, 2003). This new meaning of the term reflects the dough yield in baked goods, influence starch and protein same sources as those captured in the term ‘non-milk breakdown, and control moisture thus preventing drying out extrinsic sugars’ outlined below. However, it is entirely (Institute of Medicine, 2001). different from the traditional use of the term by the analyst, The polyols, such as sorbitol are alcohols of glucose and which is a potential source of confusion. other sugars. They are found naturally in some fruits and are made commercially by using aldose reductase to convert the aldehyde group of the glucose molecule to the alcohol. Added sugars Sorbitol is used as a replacement for sucrose in the diet of In the United States, ‘added sugars’ is a commonly used term people with diabetes. and comprises sugars and syrups that are added to foods The principal disaccharides are sucrose (a-Glc(1-2)b-Fru) during processing or preparation (Institute of Medicine, and lactose (b-Gal(1-4)Glc). Sucrose is found very widely in 2001). In the new United States Department of Agriculture fruits, berries and vegetables, and can be extracted from food composition tables, added sugars are defined as those sugar cane or beet. Lactose is the main sugar in milk. Of the sugars added to foods and beverages during processing or less abundant disaccharides, maltose, derived from starch, home preparation (Pehrsson et al., 2005). This would include occurs in sprouted wheat and barley. Trehalose (a-Glc(1-4) sugars listed in the ingredient list on a food product, a-Glc) is found in yeast, fungi (mushrooms) and in small including honey, molasses, fruit juice concentrate, brown amounts in bread and honey. It is used by the food industry sugar, corn sweetener, sucrose, lactose, glucose, high-fructose as a replacement for sucrose where less sweet taste is desired corn syrup and malt syrup. but with similar technological properties. Because of the perceived negative impact of sugars on health, a number of terms have been used to categorize them Extrinsic and intrinsic sugars more specifically, mainly to highlight their origin and These terms had their origin in a United Kingdom (UK) identify them for labelling purposes, for example total Department of Health Committee report in 1989 (Department

European Journal of Clinical Nutrition Carbohydrate terminology and classification JH Cummings and AM Stephen S8 of Health, 1989), which examined the role of sugars in the variously defined as including anything from 2 to 19 diet. The terms were developed ‘to distinguish sugar as monosaccharide units (http://www.britannica.com/eb/ naturally integrated into the cellular structure of a food article-9057022/oligosaccharide; British Nutrition Foundation, (intrinsic) from those that are free in the food or added to it 1990; Food and Drug Administration, 1993). However, the (extrinsic)’. These were defined in the report as: disaccharides (DP2) are thought of as sugars by nutritionists Intrinsic sugars. Sugars forming an integral part of certain (Roberfroid et al., 1993; Asp, 1995; Cummings and Englyst, unprocessed foodstuffs, that is enclosed in the cell, the most 1995; Southgate, 1995), although a disaccharide composed important being whole fruits and vegetables (containing of two fructose residues, for example inulobiose, is consid- mainly fructose, glucose and sucrose). Intrinsic sugars are ered a fructan (Roberfroid, 2005). therefore naturally occurring and are always accompanied by The dividing line between oligo- and polysaccharides is other nutrients. also arbitrary since there is a continuum of molecular size Extrinsic sugars. Sugars not located within the cellular from simple sugars to complex polymers of DP 100 000 or structure of a food. Extrinsic sugars are mainly found in fruit more in food. Most authorities recommend a DP of 10 as juice and are those added to processed foods. Lactose in milk the dividing point between oligo- and polysaccharides (IUB– is extrinsic in that it is not found within the cellular IUPAC and Joint Commission on Biochemical Nomencla- structure of food and has important nutritional benefits, so ture, 1982), although in the most recent International Union the term non-milk extrinsic sugars was introduced to of Pure and Applied Chemistry–International Union of indicate the group of sugars, other than intrinsic and milk Biochemistry Nomenclature Recommendation the issue is sugars, that should be restricted in the diet. not really addressed and a polysaccharide is just considered Non-milk extrinsic sugars. All extrinsic sugars, which are to be ‘a macromolecule consisting of a large number of not from milk, that is excluding lactose. This includes fruit monosaccharide (glycose) residues joined to each other by juices and honey and those sugars added to foods as a glycosidic linkages’ (IUPAC–IUB Joint Commission on sweetener in cooking or at the table, as in hot drinks and Biochemical Nomenclature, 1996). breakfast cereal, or during processing. This terminology has In practice, precipitation from aqueous solutions with remained popular among nutritionists in the UK, and is used 80%v/v ethanol is the step used in many carbohydrate in dietary surveys and other reports where intakes are analysis procedures to separate these two groups (Southgate, described (Gibson, 2000; Kelly et al., 2005). However, it is 1991; Prosky et al., 1992; Englyst et al., 1994). However, some not well understood by the public and is not used in public branched-chain carbohydrates of DP between 10 and 100 communications about sugars. remain in solution in 80% v/v ethanol so there is no clear Dividing sugars into intrinsic and extrinsic creates pro- and absolute division. Furthermore, carbohydrates such as blems for the analyst and, therefore, for food labelling. inulin and polydextrose contain mixtures of polymers of While ingredient lists can be used to identify the source of different chain lengths that cross the oligosaccharide/poly- sugars in foods, analytically it is not readily possible to saccharide boundary. In categorizing oligosaccharides found distinguish their origin in a processed food. normally in the diet, alcohol precipitation would seem to be Other terms in use include ‘sugars’, ‘sugar’, ‘discretionary the most practical way of delineating them from polysac- sugar’, ‘refined sugars’, ‘refined sugar’, ‘natural sugar’ and charides. For novel oligosaccharides, such as that are now ‘total available sugars’ (Stephen and Thane, 2007). Some of being developed by the food industry as ingredients, the these appear to equate to sucrose only, and within the EU average DP for that particular substance, as determined by ‘sucrose’ may be designated as ‘sugars’ on food labels the manufacturer, should provide the basis on which to put (European Communities, 2000). Many of the terms are used it into the appropriate carbohydrate class. In the light of the in publications about intakes, often with little reference to lack of clarity surrounding the definition of oligosaccharides, what components they include. This has the result of the Paris carbohydrate group suggested calling this group making intake comparisons very difficult and points to the ‘short-chain carbohydrates’ (Cummings et al., 1997). need for a uniform terminology. There is little justification Food oligosaccharides fall into two groups: (i) maltodex- for most of these terms apart from total sugars and their trins, which are mostly derived from starch and include subdivision into mono- and disaccharides. The relation of maltotriose and a-limit dextrins that have both a1–4 and sugars to health is determined more by the food matrix a1–6 bonds and an average DP8. Maltodextrins are widely in which they are contained and more thought should be used in the food industry as sweeteners, fat substitutes and to given to characterizing this because it also affects the other modify the texture of food products. They are digested and nutrients in the food, and these many alternative terms do absorbed like other a-glucans and (ii) oligosaccharides that not really describe a property of sugars per se. are not a-glucans. These oligosaccharides include raffinose

(a-Gal(1-6)a-Glc(1-2)b-Fru), stachyose ((Gal)2 1:6 Glu 1:2 Fru) and verbascose ((Gal)3 1:6 Glu 1:2 Fru). They are in Oligosaccharides, short-chain carbohydrates effect, sucrose joined to varying numbers of galactose ‘Oligosaccharides are compounds in which monosaccharide molecules and are found in a variety of plant seeds, for units are joined by glycosidic linkages’. Their DP has been example peas, beans and lentils. Also important in this group

European Journal of Clinical Nutrition Carbohydrate terminology and classification JH Cummings and AM Stephen S9 are inulin and fructo oligosaccharides (a-Glc(1-2)b-Fru(2-1) and amylopectin in the starch granules confers on them - b-Fru(N) or b-Fru(2 1)b-Fru(N)). They are fructans and are the distinct X-ray diffraction patterns, A, B and C. The A type is storage carbohydrates in artichokes and chicory with small characteristic of cereals (rice, wheat and maize), the B type of amounts of low molecular weight found in wheat, rye, potato, banana and high amylose starches while the C type is asparagus and members of the onion, leek and garlic family. intermediate between A and B and found in legumes. In their They can be produced industrially. The chemical bonds native (raw) form, the B starches are resistant to digestion by linking these oligosaccharides are not a-1,4 or 1,6 glucans pancreatic amylase. The crystalline structure is lost when and, therefore, they are not susceptible to pancreatic or starch is heated in water (gelatinization), thus permitting brush border enzyme breakdown (Oku et al., 1984; Hidaka digestion to take place. Recrystallization (retrogradation) et al., 1986; Cummings et al., 2001). They have become takes place to a variable extent after cooking and is in the B known as ‘non-digestible oligosaccharides’ (Roberfroid et al., form (Galliard, 1987; Hoover and Sosulski, 1991). 1993). Some of them, mainly the fructans and galactans, have unique properties in the gut and are known as Modified starch prebiotics (see later). The proportions of amylose and amylopectin in a starchy food are variable and can be altered by plant breeding. Different cultivars of common species such as rice, have a Milk oligosaccharides wide range of amylose to amylopectin ratios (Kennedy and Milk, especially human milk, contains oligosaccharides that Burlingame, 2003). Techniques are rapidly emerging, are predominantly galactose containing, although great enabling starches to be produced for specific purposes by diversity of structure is found (Kunz et al., 2000). Almost genetically modifying the crop used for their production all carry lactose at their reducing end and are elongated by (Regina et al., 2006). High amylose cornstarch and high addition of N-acetylglucosamine-linked b1–3 or b1–6 to a amylopectin (waxy) cornstarch have been available for some galactose residue, followed by further galactose with b1–3 or time, and display quite different functional as well as b1–4 bonds. Other monomers include L-fucose and sialic nutritional properties. High amylose starches require higher acid. The principal oligosaccharide in milk is lacto-N- temperatures for gelatinization and are more prone to tetraose. Total oligosaccharides in human milk are in the retrograde and to form amylose–lipid complexes. Such range 5.0–8.0 g/l, but only trace amounts are present in cow’s properties can be utilized in the formation of foods with milk (Ward et al., 2006). high-resistant starch (RS) content. The oligosaccharides of breast milk have long been Starches can also be modified chemically to impart func- credited with being the principal growth factor for bifido- tional properties needed to produce certain qualities in bacteria in the infant gut and thus primarily responsible for foodstuffs such as a decrease in viscosity and to improve gel these bacteria dominating the microbiota found in breast-fed stability, mouth feel, appearance and texture, and resistance to babies. In this context, milk oligosaccharides are acting as heat treatment. Various processes are used to modify starch, prebiotics. Bifidobacteria can grow on milk oligosaccharides the two most important being substitution and crosslinking. as their sole carbon source while lactobacilli may not be able Substitution involves etherification or esterification of a to do so (Ward et al., 2006). The similarities between milk relatively small number of hydroxyl groups on the glucose oligosaccharide structure and epithelial cell surface carbohy- units of amylose and amylopectin. This reduces retrograda- drates in the gut suggest that milk oligosaccharides may act tion, which is part of the process of staling of bread, for as soluble receptors for gut pathogens and thus form an example. Substitution also lowers gelatinization temperature, essential part of colonization resistance. They may also be provides freeze–thaw stability and increases viscosity. Cross- immunomodulatory. linking involves the introduction of a limited number of linkages between the chains of amylose and amylopectin. The process reinforces hydrogen bonding, which occurs within the Starch and modified starch granule. Crosslinking increases gelatinization temperature, Starch, the principal carbohydrate in most diets, is the improves acid and heat stability, inhibits gel formation and storage carbohydrate of plants such as cereals, root vegeta- controls viscosity during processing. Altering the chemical bles and legumes and consists of only glucose molecules. It nature of starch can lead to it becoming resistant to digestion. occurs in a partially crystalline form in granules and comprises two polymers: amylose (DPB103) and amylopectin (DPB104–105). Most common cereal starches contain NSPs 15–30% amylose, which is a non-branching helical chain of glucose residues linked by a-1,4 glucosidic bonds. Amylo- NSPs are the non-a-glucan polysaccharides of the diet pectin is a high-molecular-weight, highly branched polymer (Table 1). They are essentially ‘macromolecules consisting containing both a-1,4 and a-1,6 linkages. Some starches from of a large number of monosaccharides (glycose) residues maize, rice, sorghum and barley contain largely amylopectin joined to each other by glycosidic linkages’ (IUB-IUPAC and and are known as ‘waxy’. The crystalline form of the amylose Joint Commission on Biochemical Nomenclature, 1982) and

European Journal of Clinical Nutrition Carbohydrate terminology and classification JH Cummings and AM Stephen S10 are principally found in the plant cell wall. The term NSP was of seeds. Their role is to retain water and prevent desiccation. first proposed at a meeting sponsored by the European They are neutral polysaccharides like the hemicelluloses, of Economic Community Committee on Medical Research in which guar gum, from the cluster bean (Cyamopsis tetra- Cambridge in December 1978. The meeting was convened to gonolobus), and carob gums are similar 1–4b-D galactoman- discuss the results of the analysis of nine foods for ‘dietary nans with 1–6a-galactose single-unit side chains. Again, they fibre’ by a number of different methods in use in laboratories are widely used in the food and pharmaceutical industries as around the world. The proposal was made because ‘An thickeners and stabilizers in mayonnaise, soups and tooth- accurate chemical identification of polysaccharides in the pastes. diet is the first priorityy’ (James and Theander, 1981). At The algal polysaccharides, which include carageenan, agar the meeting, the first NSP values, measured as the sum of and alginate, are all NSP extracted from seaweeds or algae. constituent sugars, were presented for a selection of the They replace cellulose in the cell wall and have gel-forming test samples (James and Theander, 1981). NSPs are the most properties. Carageenan and agar, are highly sulphated and diverse of all the carbohydrate groups and comprise a the ability of carageenan to react with milk protein has led to mixture of many molecular forms, of which cellulose, a its use in dairy products and chocolate. straight chain b1–4-linked glucan (DP 103–106) is the most Up-to-date values for the NSP content of foods are widely distributed. Because of its linear, unbranched nature, published (Food Standards Agency/Institute of Food cellulose molecules are able to pack closely together in a Research, 2002). three-dimensional latticework forming microfibrils. These form the basis of cellulose fibres, which are woven into the plant cell wall and give it structure. Cellulose comprises Terminology based on physiology between 10 and 30% of the NSP in foods (Holland et al., 1988, 1991a, 1992). In classifying dietary carbohydrate by its chemistry, the In contrast, the hemicelluloses are a large group of principal challenge is to reconcile the various chemical polysaccharide hetero polymers, which contain a mixture divisions with those that reflect physiology and health. A of hexose (6C) and pentose (5C) sugars, often in highly classification based purely on chemistry does not allow a branched chains. Mostly, they comprise a backbone of xylose simple translation into nutritional benefits since each of sugars with branches of arabinose, mannose, galactose and the major chemical classes of carbohydrate has a variety of glucose and have a DP of 150–200. Typical of the hemi- overlapping physiological effects (Table 3). Terminology celluloses are the arabinoxylans found in cereals. About half based on physiological properties helps to focus on the of hemicelluloses contain uronic acids, which are carboxy- potential health benefits of carbohydrate, and identify foods lated derivatives of glucose and galactose. They are impor- that are likely to be part of a healthy diet. But, as can be seen tant in determining the properties of hemicelluloses, from Table 4, each physiological or health benefit of behaving as carboxylic acids and are able to form salts with carbohydrate is attributable to several subgroups from the metal ions such as calcium and zinc. main classification (Table 1). Moreover, this approach is Common to all cell walls is, pectin, which is primarily a always open to the possibility of extensive revision, as new 1–4b-D galacturonic acid polymer, although 10–25% other physiological properties of dietary carbohydrates become sugars such as rhamnose, galactose and arabinose, may also known. For example, the concept of prebiosis has added a be present as side chains. Between 3 and 11% of the uronic new dimension to understanding of how carbohydrates acids have methyl substitutions, which improve the gel- behave in both the small and large intestines. forming properties of pectin, as used in jam making. Some The physiology of carbohydrate can vary among indivi- residues are acetylated. Calcium and magnesium complexes duals and populations. The classic example is lactose, which with uronic acids are characteristic of pectins. is poorly hydrolysed by the small bowel mucosa of all adults Chemically related to the cell wall NSP, but not strictly cell except Caucasians, most of whom retain the ability to digest wall components, are the plant gums and mucilages. Plant lactose into adult life. Additionally, within any simple gums are sticky exudates that form at the sites of injuries to chemical group of carbohydrate, for example polyols, wide plants. Many are highly branched complex uronic acid variation in absorption may occur, ranging from almost containing polymers, such as Gum Arabic, named after the complete absorption of erythritol, to complete lack of Arabian port from which it was originally exported to Europe. absorption of lactitol (Livesey, 2003). Similarly, starch may It comes from the Acacia tree and is one of the better known have a variety of fates in the gut depending on granule plant gums, being sold commercially as an adhesive and used structure, whether raw or cooked and subsequent processing, in the food industry as a thickener and to retard sugar for example freezing (Stephen et al., 1983; Englyst et al., crystallization. Other plant gums include karaya (sterculia), 1992; Silvester et al., 1995). Furthermore, terminology based guar, locust bean gum, xanthan and tragacanth, all of which on physiological properties alone provides the analyst with are licensed food additives (Saltmarsh, 2000). an impossible target. Plant mucilages are botanically distinct in that they are This dichotomy has led to the introduction of a number of usually mixed with the endosperm of storage carbohydrates terms to describe various fractions and subfractions of

European Journal of Clinical Nutrition Carbohydrate terminology and classification JH Cummings and AM Stephen S11 Table 3 Principal physiological properties of dietary carbohydrates

Provide Increase Glycaemica Cholesterol Increase calcium Source of Alter balance Increase stool Immunomodulatory energy satiety lowering absorption SCFAb of microflora output (prebiotic)

Monosaccharides || Disaccharides || | Polyols ||c | Maltodextrins || Oligosaccharides ||||| (non-a-glucan) Starch || |d |d NSP || |e || aProvides carbohydrate for metabolism (FAO, 1998). bShort chain fatty acids. cExcept erythritol. dResistant starch. eSome forms of non-starch polysaccharide (NSP) only.

Table 4 Physiological/health groupings of dietary carbohydrate Table 5 Preferred terminology of dietary carbohydrates

Glycaemica Glucose, fructose, galactose, sucrose, lactose, Chemical Physiological/botanical maltose, trehalose, maltodextrins, starch Non-glycaemic Polyols, oligosaccharides (non-a-glucan), resistant Useful Monosaccharides Prebiotic and modified starches, NSP Disaccharides Resistant starch Increase stool Polyols (except erythritol), some starches, NSP, Polyols Dietary fibrea output lactose (in some populations), fructose (if taken in Total sugars Glycaemic large amounts) Short-chain No effect on stool Glucose, galactose, sucrose, maltose, trehalose, carbohydrates weight maltodextrins, oligosaccharides, most starches Oligosaccharides Polysaccharides NSP, non-starch polysaccharide. Starch a Defined as in Table 2. Non-starch polysaccharides Total carbohydrate carbohydrate and these are listed in Table 5. However, the Less Sugars Non-digestible oligosaccharides useful Sugar Soluble and insoluble fibre problems are by no means insurmountable in reconciling Free sugars Available and unavailable these different objectives for classification. With a sound Refined sugars carbohydrate chemical identification for all the carbohydrates, it is then Added sugars Complex carbohydrate possible to group them according to their health and Extrinsic and intrinsic sugars physiological effects. aIntrinsic plant cell wall polysaccharides.

Prebiotics adolescents. (Elia and Cummings, 2007; prebiotics are dealt ‘A prebiotic is a non-digestible food ingredient that benefi- with in more detail in the accompanying paper on cially affects the host by selectively stimulating the growth Physiology). and/or activity of one of a limited number of bacteria in the colon, and thus improves host health’ (Gibson and Roberfroid, 1995; Gibson et al., 2004). Resistant starch As a group, prebiotics are thus defined by a single RS is the sum of starch and products of starch digestion (such physiological parameter, although this is by no means itself as maltose, maltotriose and a-limit dextrins) that are not clearly established (Macfarlane et al., 2006). Analytically absorbed in the small bowel (Englyst et al., 1992; Champ they cross the boundaries between disaccharides and et al., 2003). All unmodified starch, if solubilized, can be polysaccharides (DPX10) (van Loo et al., 1995). It is likely hydrolysed by pancreatic a-amylase. However, the rate and in the future that a wider spectrum from the point of DP and extent to which starch is broken down is altered by a number molecular form of carbohydrates will be shown to be of physical and chemical properties. This has led to a prebiotic. Prebiotic carbohydrates have unexpected proper- classification of RS that is now widely used (Englyst and ties in the gut in that they alter the balance of the gut Cummings, 1987). microflora towards what is considered to be a more healthy RS can be fractionated into four types: one (Macfarlane et al., 2006). They have been shown to RS I: physically inaccessible starch mostly present in increase calcium absorption and bone mineral density in whole grains

European Journal of Clinical Nutrition Carbohydrate terminology and classification JH Cummings and AM Stephen S12 Table 6 Some currently proposed definitions/descriptions of dietary fibre

Dietary fibre consists of nondigestible carbohydrates and lignin that are intrinsic and intact in plants Functional fibre consists of isolated, nondigestible carbohydrates that have beneficial physiological effects in humans Total fibre is the sum of Dietary fibre and Added fibre (Institute of Medicine, 2001). ‘Dietary fibre means carbohydrate polymers with a degree of polymerization (DP) not lower than 3 which are neither digested nor absorbed in the small intestine. A degree of polymerization not lower than 3 is intended to exclude mono- and disaccharides. It is not intended to reflect the average DP of a mixture. Dietary fibre consists of one or more of: K Edible carbohydrate polymers naturally occurring in the food as consumed; K carbohydrate polymers, which have been obtained from food raw material by physical, enzymatic or chemical means, K synthetic carbohydrate polymers.’ http://www.ccfnsdu.de/fileadmin/user_upload/PDF/ReportCCFNSDU2005.pdf ‘Dietary fibre should be defined to include all non-digestible carbohydrates (NDC). Lignin and other non-digestible but quantitatively minor components that are associated with the dietary fibre polysaccharides and may influence their physiological properties should be included as well’ European Food Standards Agency Draft Paper on Carbohydrates and Dietary Fibre (Becker and Asp, 2006). ‘Dietary fibres are the endogenous components of plant material in the diet which are resistant to digestion by enzymes produced by humans. They are predominantly non-starch polysaccharides and lignin and may include, in addition, associated substances’ (Health and Welfare Canada, 1985). ‘Dietary fibre is the edible parts of plants or analogous carbohydrates that are resistant to digestion and absorption in the human small intestine with complete or partial fermentation in the large intestine. Dietary fibre includes polysaccharides, oligosaccharides, lignin, and associated plant substances. Dietary fibres promote beneficial physiological effects including laxation, and/or blood cholesterol attenuation, and/or blood glucose attenuation’ (American Association of Cereal Chemists, 2001).

RS II: RS granules (Type B) Were it not for the perceived public perception that fibre is RS III: retrograded starch (after food processing) good for you, and therefore the need to provide a value for RS IV: modified starches. fibre on food labels, the term would be best consigned to the history books. However, various national and international The observation that the rate and extent of starch bodies continue to struggle with the definition and the latest digestion can vary has been one of the most important versions of their deliberations on fibre are given in Table 6. developments in our understanding of carbohydrates in the Common to these definitions is the concept of non- past 30 years. There are implications of this for the glycaemic digestibility in the small intestine. response to foods, for fermentation in the large bowel and Non-digestibility needs to be defined. If it is carbohydrate for conditions such as diabetes and obesity. Methods have that passes across the ileo-caecal valve, then to define it been devised to measure these starch fractions in the requires complex physiological studies in humans. More- laboratory (Champ et al., 2003). over, it will vary widely from person to person (Stephen et al., 1983; Englyst et al., 1992; Silvester et al., 1995; Molis et al., 1996; Ellegard et al., 1997; Langkilde et al., 2002) and be Dietary fibre affected by the cooking of food, storage, chewing, ripeness The term fibre, or dietary fibre, has many different meanings and the presence of other foods (Englyst and Cummings, in the nutrition world. It is not a precise reference to a 1986; Champ et al., 2003). It will include many dietary chemical component, or components, of the diet, but is components, for example lactose in some populations, some essentially a physiological concept as embodied in the polyols, some starches (RS) and NSP. There is no enforceable original definition by Trowell, ‘the proportion of food which method that can be used to measure this physiological is derived from the cellular walls of plants which is digested fraction of the diet. very poorly in human beings’ (Trowell, 1972). As can be seen in the accompanying paper on the The dietary fibre hypothesis was one of the most compel- physiology of carbohydrates (Elia and Cummings, 2007), ling in nutrition and public health in the latter half of the digestibility has an entirely different context when it is used twentieth century. It provided the stimulus to a great deal of in the description of energy metabolism. Here it is defined as research, for example epidemiological, physiological, analy- ‘the proportion of combustible energy that is absorbed over tical and technical. It has been the catalyst for progress in the entire length of the gastrointestinal tract’. It would be our understanding of the cause of a number of common useful to have these different concepts of digestion aligned. diseases, especially those of the large bowel and has given If there is a desire to use the word ‘fibre’, then it should governments and the food industry valuable targets for always be ‘qualified by a statement itemizing those carbohy- healthy eating. However, in the 30 years since Trowell, drates and other substances intended for inclusion’, by Walker, Burkitt and others first proposed the fibre hypo- which is meant carbohydrates identified in the chemical thesis, nutritional science has progressed, especially our classification table (Table 1). understanding of dietary carbohydrates and with this the At a meeting of the authors of the scientific update papers, apparently unique role of fibre, essentially the plant cell wall, and other experts, convened by WHO/FAO and held in in many physiological processes and in disease prevention Geneva on 17–18 July 2006, the definition of dietary fibre (Cummings et al., 2004). was discussed, including the one suggested by the US

European Journal of Clinical Nutrition Carbohydrate terminology and classification JH Cummings and AM Stephen S13 National Academy of Sciences in 2001 and that currently with the division of dietary carbohydrate into available and proposed by Codex (http://www.ccnfsdu.de/fileadmin/user_ unavailable. In an attempt to prepare food tables for diabetic upload/PDF/ReportCCNFSDU2005.pdf) (Table 6). diets, they realized that not all carbohydrates could be The experts agreed that the definition of dietary fibre ‘utilized and metabolized’, that is provide the body with should be more clearly linked to health and, after discussion, ‘carbohydrates for metabolism’. Available carbohydrate was the following definition was proposed. defined as ‘starch and soluble sugars’ and unavailable as ‘Dietary fibre consists of intrinsic plant cell wall poly- ‘mainly hemicellulose and fibre (cellulose)’. This concept saccharides’. proved useful, not the least because it drew attention to the The established epidemiological support for the health fact that some carbohydrate is not digested and absorbed in benefits of dietary fibre is based on diets that contain fruits, the small intestine but rather reaches the large bowel where vegetables and whole-grain foods, for which the intrinsic it is fermented or even excreted in faeces. plant cell wall polysaccharides are a good marker. Although An FAO technical workshop in Rome in 2002 on ‘Food isolated or extracted fibre preparations have been shown to energy—methods of analysis and conversion factors’ (FAO, have physiological effects experimentally, these cannot be 2003) defined available carbohydrate as ‘that fraction of translated into health benefits directly because the epide- carbohydrate that can be digested by human enzymes, is miological evidence points to fruits, vegetables and whole- absorbed and enters into intermediary metabolism’. (It does grain foods as beneficial, and in a normal diet, these not include dietary fibre, which can be a source of energy polysaccharides are part of the plant cell wall complex and only after fermentation). do not exist individually. It is somewhat misleading to talk of carbohydrate as ‘unavailable’ because carbohydrate that reaches the colon is Soluble and insoluble dietary fibre able to provide the body with energy through fermentation and absorption of short-chain fatty acids. There are many These terms arose out of the early chemistry of NSPs, which properties of carbohydrate of which site of digestion is only showed that the fractional extraction of NSP could be one. An alternative to the terms ‘available’ and ‘unavailable’ controlled by changing the pH of solutions. They proved today would be to describe carbohydrates either as glycaemic very useful in the initial understanding of the properties of (that is providing carbohydrate for metabolism) or non- dietary fibre, allowing a simple division into those which glycaemic, which is closer to the original concept of principally had effects on glucose and lipid absorption from McCance and Lawrence. However, the FAO Technical work- the small intestine (soluble) and those which were slowly shop on Food Energy in its recommendations said, ‘Available and incompletely fermented and had more pronounced carbohydrate is a useful concept in energy evaluation and effects on bowel habit (insoluble). However, the separation of should be retained. This recommendation is at odds with the soluble and insoluble fractions is very pH dependent, making view of the expert consultation in 1997 on carbohydrates, the link with specific physiological properties less certain. which endorsed the use of the term ‘glycaemic carbohydrate’ Much insoluble fibre is completely fermented and not all to mean ‘providing carbohydrate for metabolism’. The group soluble fibre has effects on glucose and lipid absorption. Many expressed concerns that ‘glycaemic carbohydrate’ might be of the early studies were done with isolated gums or extracts confused or even equated with the concept of ‘glycaemic of cell walls, whereas these various forms of fibre exist index’, which is an index that describes the relative blood together mostly in intact cell walls of plants. glucose response to different ‘available carbohydrates’. The Nevertheless, certain fibre-rich foods effect glycaemic term ‘available’ seems to convey adequately the concept of control and lipid levels and have been widely used in the ‘providing carbohydrate for metabolism’, while avoiding this management of diabetes particularly the legumes and pulses confusion’. Furthermore, in the discussion of the energy rather than high bran products (Kiehm et al., 1976; Simpson value of carbohydrate, the terms ‘available’ and ‘unavailable’ et al., 1979, 1981; Rivellese et al., 1980; Mann, 1984; are extensively used (Elia and Cummings, 2007). On balance, Chandalia et al., 2000; Giacco et al., 2000; Mann et al., however, we would recommend ‘glycaemic’ as a more precise 2004). Work on the variability in glycaemic response of and measurable fraction. different types of foods has led to the concept of the glycaemic index (Crapo et al., 1977; Jenkins et al., 1981) and a new area of nutritional science has been developed, Glycaemic carbohydrate concerned with glycaemic responses to carbohydrate- containing foods (Foster-Powell et al., 2002). A more recently developed distinction with regard to human health, although arising out of the original McCance and Lawrence concept, is whether or not the carbohydrate source Available and unavailable carbohydrate does or does not directly provide carbohydrate as an energy source following the process of digestion and A major step forward conceptually in our understanding of absorption in the small intestine. Carbohydrate, which carbohydrates was made by McCance and Lawrence (1929) provides glucose for metabolism is referred to as ‘glycaemic

European Journal of Clinical Nutrition Carbohydrate terminology and classification JH Cummings and AM Stephen S14 carbohydrate’, whereas carbohydrates that pass to the have now shown that the physical structure of starchy foods large intestine prior to being metabolized, is referred to influences the glycaemic response. as ‘non-glycaemic carbohydrate’. Most mono- and di- The physical structure of a food has, therefore, a role to saccharides, some oligosaccharides (maltodextrins) and play in the regulation of carbohydrate metabolism. The use rapidly digested starches may be classified as glycaemic of viscous-soluble NSP isolates in this context will probably carbohydrate. Slowly digested starches are also considered be seen as a stepping stone to understanding fibre but not to be glycaemic carbohydrate though glucose is less the ultimate goal. From a nutritional and analytical view rapidly generated. The remaining oligosaccharides, NSPs points, the intrinsic polysaccharides of the plant cell wall, and RS are considered to be non-glycaemic carbohydrates. known as dietary fibre or NSP, should be viewed as a single Most carbohydrate-containing unprocessed foods contain entity that uniquely provides physical structure to foods. both glycaemic and non-glycaemic carbohydrate. The extent There is however a major problem in characterizing and to which carbohydrate in foods raises blood glucose measuring the key physical attributes of a food that concentration compared with an equivalent amount of contributes to modifying its effects. reference carbohydrate has also been used as a means of classifying dietary carbohydrate and is known as the glycaemic index (Venn and Green, 2007). Many factors Whole grain affect the glycaemic response to carbohydrate, including the intrinsic properties of the food and also extrinsic factors such The essence of the dietary recommendations in many as the composition of the meal, the overall diet and countries is to eat a diet high in whole grains, fruits and biological variations of the host. vegetables and this is embodied in the WHO/FAO report on ‘Diet, Nutrition and the Prevention of Chronic Diseases’ (WHO, 2003) in the description of population nutrient Complex carbohydrates intake goals. However, the term ‘whole grain’ has several meanings from ‘whole of the grain’ through to physically This term was first used in the McGovern report, ‘Dietary intact structures. A precise definition is clearly needed for Goals for the United States’ in 1977 (Select Committee on labelling purposes. Nutrition and Human Needs, 1977). It was coined largely to Whole grain comprises whole wheat, whole-wheat flour, distinguish sugars from other carbohydrates and in the wheat flakes, bulgar wheat, whole and rolled oats, oatmeal, report denotes ‘fruit, vegetables and whole-grains’. The term oat flakes, brown rice, whole rye and rye flour, whole barley has never been formally defined and has since come to be and popcorn. Cornmeal is not included as it is generally used to describe either starch alone, or the combination of all dehulled, de-branned and de-germed. Sweet corn has been polysaccharides (British Nutrition Foundation, 1990). It was included in some analyses (Harnack et al., 2003), but is not used to encourage consumption of what are considered to be included in analyses from the UK, where it is considered a healthy foods such as whole-grain cereals, etc., but becomes vegetable (Henderson et al., 2002; Thane et al., 2005, 2007). meaningless when used to describe fruits and vegetables, Foods containing added bran, but not including endosperm which are low in starch. As a substitute term for starch it or germ, are included in some analyses (Jacobs et al., 2001) would seem to have little merit and, in principle, it is better but not in others, but are not whole grains and should be to discuss carbohydrate components by using their common excluded. Similarly, foods which are largely whole grain, but chemical names. not entirely, such as puffed wheat, where the puffing and toasting causes some of the outer layers to drop off are not truly whole grain. Such foods are difficult to consider, since Physical effects of carbohydrates they may be consumed by a considerable proportion of the population and are indicated as whole wheat on the label of Aside from their chemistry, the physiological properties of some products but not others. carbohydrates are also affected by the physical state of the There are also problems with the definition of a whole food. In this context, there may be a unique role for NSP in grain food. For labelling purposes, the Food and Drug the control of carbohydrate metabolism. The early studies of Administration (1999) in the United States has defined a viscosity on glucose responses pointed to the physical whole grain food as ‘a product containing 451% whole properties of NSP as being important (Jenkins et al., 1978). grain by weight per reference amount customarily consumed In a different context, the classic study of Haber et al. (1977) per day’ (Seal, 2006), and this standard has been used in with apples shows clearly that where carbohydrate, in this some surveys to assess intake (Lang et al., 2003; Jensen et al., case mainly glucose and fructose, is entrapped intracellularly 2004). However, many foods contain less whole grain than in plant foods, its release in the gut is slowed and blood this, but can still make a substantial contribution to total glucose moderated and insulin responses lowered. A unique whole-grain intake (Thane et al., 2005, 2007). property of NSP, therefore, is that it forms the plant cell wall In studies by Jacobs et al. (1998) in the United States, and thus a physical structure to foods. Numerous studies breakfast cereals were ‘considered to be whole grain if the

European Journal of Clinical Nutrition Carbohydrate terminology and classification JH Cummings and AM Stephen S15 product contained X25% whole grain or bran y’. In a (3) Total carbohydrate in food should be determined by more complete analysis of the United Kingdom, foods with direct measurement rather than ‘by difference’. whole-grain contents of 10% or more were used, rather than (4) Many terms exist to describe sugars in the diet. The most the cutoffs of 25 or 51%. In the UK National Diet and useful are total sugars and their division into mono- and Nutrition Surveys, it was found that for young people aged disaccharides. The use of other terms creates difficulties 4–18 years, intake of whole grains was underestimated by for the analyst, confusion for the consumer and suggests 28% if only those products with 451% whole grains were properties of foods that are not related to sugars included and underestimated by 15% if only those with themselves, but to the food matrix. whole-grain content greater than 25% were included. More (5) Because neither chemical nor physical description of recently for adults, the 51% cutoff would have under- carbohydrates directly reflects their physiological pro- estimated intake by 18% for the 1986–87 Dietary Survey of perties and health benefits, a number of terms to British Adults (Gregory et al., 1990), and 27% in the NDNS describe carbohydrates, based on their physiology, have survey of adults in 2000–01 (Henderson et al., 2002), been created. Of these prebiotic, glycaemic, RS and indicating not only the underestimation but that the dietary fibre are useful. manner of consuming whole grains may also be changing, (6) Dietary fibre should be defined to reflect the health with more foods with lower amounts now being consumed. benefits of a diet rich in fruits, vegetables and whole It is a considerable amount of work to determine whole-grain grains and not the variable physiological properties or content down to the 10% level, but this would include foods health effects of the various carbohydrate types. The like porridge, which when cooked is 90% water but is definition proposed by the group was ‘intrinsic plant cell consumed in substantial quantities in parts of the world wall polysaccharides’. (Thane et al., 2007), and which may have important health (7) The effects of foods containing different types of fibre on benefits. glycaemic control and lipid levels should be investigated In his editorial comment on the 1998 Jacobs’ paper, further to determine the exact properties needed for Willett (1998) remarks ‘The physical form of whole grains their effects. The distinction between soluble and can vary from intact kernels (for which we should probably insoluble forms of fibre is inappropriate since the reserve the term whole grain) to finely milled flour (whole separation is pH dependent and does not reflect the grain flour)’. This distinction between intact whole grains or physiological properties of whole foods in the gut. physically disrupted, although present in the food in its (8) The term whole grains should be defined more clearly entirety, is important. Grain structure affects the glycaemic and the role of intact versus milled grains established. response to food (Foster-Powell et al., 2002) and high intakes The whole-grain concept, along with fresh fruits and of whole-grain foods protect against the development of type vegetables is central to a healthy diet message. II diabetes (Venn and Mann, 2004) and cardiovascular disease (Seal, 2006), yet we know little about the physical form of grains in these studies. Acknowledgements It is also worth noting that the type of grain contributing to whole grains may vary from country to country. For the The authors thank Professor Ingvar Bosaeus, Dr Barbara UK, about 90% of the whole-grain intake is wheat (Thane Burlingame, Professor Jim Mann, Professor Timothy Key, et al., 2005), while in the United States, a larger proportion is Professor Carolyn Summerbell, Dr Bernard Venn and Dr likely to be from oats, given the popularity of whole-grain Martin Wiseman for the valuable comments they provided oat cereals. With the different physical and physiological on the earlier manuscript. properties of these two grains, such differences need to be taken into account when interpreting health impacts of Conflict of interest whole-grain consumption. During the preparation and peer review of this paper in 2006, the authors and peer reviewers declared the following interests. Conclusions Authors (1) Dietary carbohydrates should be classified according to Professor John H Cummings: Chairman, Biotherapeutics their chemical form, as recommended at the 1997 FAO/ Committee, Danone; Member, Working Group on Foods WHO Expert Consultation. with Health Benefits, Danone; funding for research work at (2) The physiological and health effects of carbohydrates are the University of Dundee, ORAFTI (2004). dependent not only on their primary chemical form but Dr Alison M Stephen: Contract with World Sugar Research also on their physical properties, which include water Organization on trends in intakes of sugars and sources in solubility, gel formation, crystallization state, association the diet (contract is with MRC-Human Nutrition Resource); with other molecules and aggregation into the complex contracts with Cereal Partners UK on whole-grain intakes in structures of the plant cell wall. the UK and relationship to adiposity (contract was with

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