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REVIEW Carbohydrate terminology and classification JH Cummings 1 and AM Stephen 2 1 Gut group, Division of Pathology and Neuroscience, Ninewells Hospital and Medical School, Dundee, UK and 2 Population 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 The dietary carbohydrates are a diverse group of substances with a range of chemical, physical and physiological proper- ties. While carbohydrates are principally substrates for energy metabolism, they can affect satiety, blood glucose and insulin, lipid metabolism and, through fermentation, exert a major control on colonic function, including bowel habit, transit, the metabolism and balance of the commensal flora and large bowel epithelial cell health. They may also be immunomodulatory and influence calcium absorption. These properties have implications for our overall health; contributing particularly to the control of body weight, diabetes and ageing, cardiovascular disease, bone mineral density, large bowel cancer, constipation and resistance to gut infection. Classification As for other macronutrients, the primary classification of dietary carbohydrates, as proposed at the Joint Food and Agriculture Organization (FAO)/World Health Organization (WHO) Expert Consultation on Carbohydrates in human nutrition convened in Rome in 1997 (FAO, 1998), is by molecular size, as determined by degree of polymerization (DP), the type of linkage (a or non-a) and character of individual monomers (Table 1). This classification is analo- gous 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 necessary for a coherent and enforceable approach to measurement and labelling forms the basis for terminology Correspondence: Professor JH Cummings, Division of Pathology and Neuroscience, Ninewells Hospital and Medical School, Dundee DD1 9SY, UK. E-mail: [email protected] European Journal of Clinical Nutrition (2007) 61 (Suppl 1), S5–S18 & 2007 Nature Publishing Group All rights reserved 0954-3007/07 $30.00 www.nature.com/ejcn
Transcript
  • 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 NutritionResearch, 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 andhealth benefits. As with other macronutrients, the primary classification of dietary carbohydrate is based on chemistry, that ischaracter of individual monomers, degree of polymerization (DP) and type of linkage (a or b), as agreed at the Food andAgriculture Organization/World Health Organization Expert Consultation in 1997. This divides carbohydrates into three maingroups, sugars (DP 12), oligosaccharides (short-chain carbohydrates) (DP 39) and polysaccharides (DPX10). Within thisclassification, 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 primarychemistry, they are modified by their physical properties. These include water solubility, hydration, gel formation, crystallinestate, association with other molecules such as protein, lipid and divalent cations and aggregation into complex structures in cellwalls and other specialized plant tissues. A classification based on chemistry is essential for a system of measurement, predicationof properties and estimation of intakes, but does not allow a simple translation into nutritional effects since each class ofcarbohydrate has overlapping physiological properties and effects on health. This dichotomy has led to the use of a number ofterms 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 andsuggests that some are more useful than others. A clearer understanding of what is meant by any particular word used todescribe carbohydrate is essential to progress in translating the growing knowledge of the physiological properties ofcarbohydrate into public health messages.

    European Journal of Clinical Nutrition (2007) 61 (Suppl 1), S5S18. doi:10.1038/sj.ejcn.1602936

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

    Introduction

    The dietary carbohydrates are a diverse group of substances

    with a range of chemical, physical and physiological proper-

    ties. While carbohydrates are principally substrates for

    energy metabolism, they can affect satiety, blood glucose

    and insulin, lipid metabolism and, through fermentation,

    exert a major control on colonic function, including bowel

    habit, transit, the metabolism and balance of the commensal

    flora and large bowel epithelial cell health. They may also be

    immunomodulatory and influence calcium absorption.

    These properties have implications for our overall health;

    contributing particularly to the control of body weight,

    diabetes and ageing, cardiovascular disease, bone mineral

    density, large bowel cancer, constipation and resistance to

    gut infection.

    Classification

    As for other macronutrients, the primary classification of

    dietary carbohydrates, as proposed at the Joint Food and

    Agriculture Organization (FAO)/World Health Organization

    (WHO) Expert Consultation on Carbohydrates in human

    nutrition convened in Rome in 1997 (FAO, 1998), is by

    molecular size, as determined by degree of polymerization

    (DP), the type of linkage (a or non-a) and character ofindividual monomers (Table 1). This classification is analo-

    gous 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

    necessary for a coherent and enforceable approach to

    measurement and labelling forms the basis for terminology

    Correspondence: Professor JH Cummings, Division of Pathology and

    Neuroscience, Ninewells Hospital and Medical School, Dundee DD1 9SY, UK.

    E-mail: [email protected]

    European Journal of Clinical Nutrition (2007) 61 (Suppl 1), S5S18& 2007 Nature Publishing Group All rights reserved 0954-3007/07 $30.00

    www.nature.com/ejcn

    title

  • and an understanding of the physiological and health effects

    of these macronutrients.

    A chemical approach divides carbohydrates into three

    main groups, sugars (DP12), oligosaccharides (short-chain

    carbohydrates) (DP39) and polysaccharides (DPX10).Sugars comprise (i) monosaccharides, (ii) disaccharides and

    (iii) polyols (sugar alcohols). Oligosaccharides are either (a)

    malto-oligosaccharides (a-glucans), principally occurringfrom the hydrolysis of starch and (b) non-a-glucan such asraffinose and stachyose (a galactosides), fructo- and galacto-oligosaccharides and other oligosaccharides. Polysaccharides

    may be divided into starch (a-1:4 and 1:6 glucans) and non-starch polysaccharides (NSPs), of which the major compo-

    nents are the polysaccharides of the plant cell wall such as

    cellulose, hemicellulose and pectin but also includes plant

    gums, mucilages and hydrocolloids. Some carbohydrates,

    like inulin, do not fit neatly into this scheme because they

    exist in nature in multiple molecular forms. Inulin, GFN,

    from plants may have from 2 to 200 fructose units and so

    crosses the boundary between oligosaccharides and poly-

    saccharides (Roberfroid, 2005).

    A variety of methodologies are available for the measure-

    ment of the carbohydrate content of food and the compo-

    nents are listed in Table 1 (Englyst et al., 2007).

    Terminology

    Total carbohydrate

    Although the individual components of dietary carbohy-

    drate are readily identifiable, there is some confusion as to

    what comprises total carbohydrate as reported in food tables.

    Two principal approaches to total carbohydrate are used,

    first, that derived by difference and second, the direct

    measurement of the individual components that are then

    combined to give a total. Calculating carbohydrate by

    difference has been used since the early 20th century and

    is still widely used around the world (Atwater and Woods,

    1986; United States Department of Agriculture, 2007). The

    moisture, protein, fat, ash and alcohol content of a food are

    determined, subtracted from the total weight of the food and

    the remainder, or difference, is considered to be carbohy-

    drate. There are, however, a number of problems with this

    approach in that the by difference figure includes non-

    carbohydrate components such as lignin, organic acids,

    tannins, waxes and some Maillard products. In addition to

    this error, it combines all the analytical errors from the other

    analyses. Also, a single global figure for carbohydrates in

    food is uninformative because it fails to identify the many

    types of carbohydrates and thus to allow some under-

    standing of the potential health benefits of those foods.

    Direct analysis of carbohydrate components and summa-

    tion to obtain a total carbohydrate value has been the basis

    of carbohydrate analysis in the UK since 1929, when the first

    values were published by McCance and Lawrence (1929).

    Those countries that use McCance and Widdowsons, The

    Composition of Foods (Food Standards Agency/Institute

    of Food Research, 2002) also express carbohydrate using

    this approach. The total figure obtained is for what McCance

    and Lawrence called available carbohydrate and therefore

    differs from carbohydrate by difference in that it does not

    contain the plant cell wall polysaccharides (fibre). In

    addition, it is not complicated by analytical difficulties with

    other food components. Dietary intake of total carbohydrate

    and its components using direct analysis enables examina-

    tion of geographic variations and changes in intake over

    time of individual carbohydrate types and their relationship

    with health outcomes. Total carbohydrate by direct measure-

    ment is preferable and simplified methods to do this should

    be developed.

    Figures obtained for carbohydrate by difference and

    carbohydrate analysed directly are not always the same,

    particularly for complex mixtures, and foods containing fibre

    or certain types of starch, like pasta (Stephen, 2006). This

    results in apparently different carbohydrate intakes for the

    same list of foods consumed, as shown in Table 2. Fifty-two

    dietary records from a study conducted in Canada, where

    carbohydrate by difference is used (Health Canada, 2005)

    were subsequently analysed in the UK using values based on

    McCance and Widdowsons 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

    by difference (Stephen, 2006). Comparison of carbohydrate

    intake among different countries should therefore be viewed

    with caution if the method of carbohydrate determination is

    not the same. Worldwide variations in carbohydrate intake

    assumed to be due to differences in types of foods consumed,

    are also, in part, due to methodology.

    Table 1 The major dietary carbohydrates

    Class (DPa) Subgroup Principal components

    Sugars (12) Monosaccharides Glucose, fructose, galactoseDisaccharides Sucrose, lactose, maltose,

    trehalosePolyols (sugaralcohols)

    Sorbitol, mannitol, lactitol,xylitol, erythritol, isomalt,maltitol

    Oligosaccharides(39) (short-chaincarbohydrates)

    Malto-oligosaccharides(a-glucans)

    Maltodextrins

    Non-a-glucanoligosaccharides

    Raffinose, stachyose, fructo andgalacto oligosaccharides,polydextrose, inulin

    Polysaccharides(X10)

    Starch(a-glucans)

    Amylose, amylopectin, modifiedstarches

    Non-starchpolysaccharides(NSPs)

    Cellulose, hemicellulose, pectin,arabinoxylans, b-glucan,glucomannans, plant gums andmucilages, hydrocolloids

    aDegree of polymerization or number of monomeric (single sugar) units.

    Based on Food and Agriculture Organization/World Health Organization

    Carbohydrates in Human Nutrition report (1998), and Cummings et al.

    (1997).

    Carbohydrate terminology and classificationJH Cummings and AM Stephen

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    European Journal of Clinical Nutrition

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  • Sugars

    The term sugars is conventionally used to describe the

    mono- and disaccharides in food.

    The three principal monosaccharides are glucose, fructose

    and galactose, which are the building blocks of naturally

    occurring di-, oligo- and polysaccharides. Free glucose and

    fructose occur in honey and cooked or dried fruit (invert

    sugar), in small amounts, and in larger amounts in fruit and

    berries where they are the main energy source (Holland et al.,

    1992). Corn syrup, a glucose syrup produced by the

    hydrolysis of cornstarch, and high fructose corn syrup,

    containing glucose and fructose, are increasingly used by the

    food industry in many countries. Fructose is the sweetest of

    all the food carbohydrates. Sugars are used as a sweetener to

    improve the palatability of many foods and beverages, and

    are also used for food preservation and in jams and jellies.

    Sugars confer functional characteristics to foods, like visco-

    sity, texture, body and browning capacity. They increase

    dough yield in baked goods, influence starch and protein

    breakdown, and control moisture thus preventing drying out

    (Institute of Medicine, 2001).

    The polyols, such as sorbitol are alcohols of glucose and

    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.

    Sorbitol is used as a replacement for sucrose in the diet of

    people with diabetes.

    The principal disaccharides are sucrose (a-Glc(1-2)b-Fru)and lactose (b-Gal(1-4)Glc). Sucrose is found very widely infruits, berries and vegetables, and can be extracted from

    sugar cane or beet. Lactose is the main sugar in milk. Of the

    less abundant disaccharides, maltose, derived from starch,

    occurs in sprouted wheat and barley. Trehalose (a-Glc(1-4)a-Glc) is found in yeast, fungi (mushrooms) and in smallamounts in bread and honey. It is used by the food industry

    as a replacement for sucrose where less sweet taste is desired

    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

    more specifically, mainly to highlight their origin and

    identify them for labelling purposes, for example total

    sugars, added sugar, free sugars (WHO, 2003), refined sugars

    (Nordic Council, 2004), discretionary sugar (New Zealand

    Nutrition Foundation, 2004) and intrinsic sugars, milk

    sugars and non-milk extrinsic sugars (Department of Health,

    1989).

    Total sugars

    For labelling purposes, the category of total sugars has been

    proposed. This includes all sugars from whatever source in a

    food, and is defined as all monosaccharides and disaccha-

    rides other than polyols (European Communities, 1990).

    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,

    measure and label sugars.

    Free sugars

    Traditionally free sugars referred to any sugars in a food that

    were free and not bound (Holland et al., 1992), and included

    all mono- and disaccharides present in a food, including

    lactose (Southgate, 1978). This term was also used analyti-

    cally to describe when the carbohydrate in a food was

    hydrolysed and components detected by chromatography or

    colorimetric methods (Southgate, 1978). In recent years, the

    use of the term free sugars has changed, to refer to all

    monosaccharides and disaccharides added to foods by the

    manufacturer, cook and consumer, plus sugars naturally

    present in honey, syrups and fruit juices and was the

    preferred term for the WHO/FAO Expert Consultation on

    Diet, Nutrition and the Prevention of Chronic Diseases

    (WHO, 2003). This new meaning of the term reflects the

    same sources as those captured in the term non-milk

    extrinsic sugars outlined below. However, it is entirely

    different from the traditional use of the term by the analyst,

    which is a potential source of confusion.

    Added sugars

    In the United States, added sugars is a commonly used term

    and comprises sugars and syrups that are added to foods

    during processing or preparation (Institute of Medicine,

    2001). In the new United States Department of Agriculture

    food composition tables, added sugars are defined as those

    sugars added to foods and beverages during processing or

    home preparation (Pehrsson et al., 2005). This would include

    sugars listed in the ingredient list on a food product,

    including honey, molasses, fruit juice concentrate, brown

    sugar, corn sweetener, sucrose, lactose, glucose, high-fructose

    corn syrup and malt syrup.

    Extrinsic and intrinsic sugars

    These terms had their origin in a United Kingdom (UK)

    Department of Health Committee report in 1989 (Department

    Table 2 Energy and macronutrient intakes for 52 weighed recordsanalysed using Canadian and UK food tables

    Energy(kcal)

    Protein(g) (%)

    Fat(g) (%)

    CHO(g) (%)

    Analysis using Canadian nutrient file

    Mean of 52 records 2265 95.9 (16.9) 81.4 (31.5) 294.2 (52.9)

    Analysis using The composition of foodsMean of 52 records 1992* 89.8 (17.9) 74.5 (32.7) 252.4* (48.5)*

    *Po0.001.From Stephen, 2006.

    Carbohydrate terminology and classificationJH Cummings and AM Stephen

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    European Journal of Clinical Nutrition

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  • of Health, 1989), which examined the role of sugars in the

    diet. The terms were developed to distinguish sugar as

    naturally integrated into the cellular structure of a food

    (intrinsic) from those that are free in the food or added to it

    (extrinsic). These were defined in the report as:

    Intrinsic sugars. Sugars forming an integral part of certain

    unprocessed foodstuffs, that is enclosed in the cell, the most

    important being whole fruits and vegetables (containing

    mainly fructose, glucose and sucrose). Intrinsic sugars are

    therefore naturally occurring and are always accompanied by

    other nutrients.

    Extrinsic sugars. Sugars not located within the cellular

    structure of a food. Extrinsic sugars are mainly found in fruit

    juice and are those added to processed foods. Lactose in milk

    is extrinsic in that it is not found within the cellular

    structure of food and has important nutritional benefits, so

    the term non-milk extrinsic sugars was introduced to

    indicate the group of sugars, other than intrinsic and milk

    sugars, that should be restricted in the diet.

    Non-milk extrinsic sugars. All extrinsic sugars, which are

    not from milk, that is excluding lactose. This includes fruit

    juices and honey and those sugars added to foods as a

    sweetener in cooking or at the table, as in hot drinks and

    breakfast cereal, or during processing. This terminology has

    remained popular among nutritionists in the UK, and is used

    in dietary surveys and other reports where intakes are

    described (Gibson, 2000; Kelly et al., 2005). However, it is

    not well understood by the public and is not used in public

    communications about sugars.

    Dividing sugars into intrinsic and extrinsic creates pro-

    blems for the analyst and, therefore, for food labelling.

    While ingredient lists can be used to identify the source of

    sugars in foods, analytically it is not readily possible to

    distinguish their origin in a processed food.

    Other terms in use include sugars, sugar, discretionary

    sugar, refined sugars, refined sugar, natural sugar and

    total available sugars (Stephen and Thane, 2007). Some of

    these appear to equate to sucrose only, and within the EU

    sucrose may be designated as sugars on food labels

    (European Communities, 2000). Many of the terms are used

    in publications about intakes, often with little reference to

    what components they include. This has the result of

    making intake comparisons very difficult and points to the

    need for a uniform terminology. There is little justification

    for most of these terms apart from total sugars and their

    subdivision into mono- and disaccharides. The relation of

    sugars to health is determined more by the food matrix

    in which they are contained and more thought should be

    given to characterizing this because it also affects the other

    nutrients in the food, and these many alternative terms do

    not really describe a property of sugars per se.

    Oligosaccharides, short-chain carbohydrates

    Oligosaccharides are compounds in which monosaccharide

    units are joined by glycosidic linkages. Their DP has been

    variously defined as including anything from 2 to 19

    monosaccharide units (http://www.britannica.com/eb/

    article-9057022/oligosaccharide; British Nutrition Foundation,

    1990; Food and Drug Administration, 1993). However, the

    disaccharides (DP2) are thought of as sugars by nutritionists

    (Roberfroid et al., 1993; Asp, 1995; Cummings and Englyst,

    1995; Southgate, 1995), although a disaccharide composed

    of two fructose residues, for example inulobiose, is consid-

    ered a fructan (Roberfroid, 2005).

    The dividing line between oligo- and polysaccharides is

    also arbitrary since there is a continuum of molecular size

    from simple sugars to complex polymers of DP 100 000 or

    more in food. Most authorities recommend a DP of 10 as

    the dividing point between oligo- and polysaccharides (IUB

    IUPAC and Joint Commission on Biochemical Nomencla-

    ture, 1982), although in the most recent International Union

    of Pure and Applied ChemistryInternational Union of

    Biochemistry Nomenclature Recommendation the issue is

    not really addressed and a polysaccharide is just considered

    to be a macromolecule consisting of a large number of

    monosaccharide (glycose) residues joined to each other by

    glycosidic linkages (IUPACIUB Joint Commission on

    Biochemical Nomenclature, 1996).

    In practice, precipitation from aqueous solutions with

    80%v/v ethanol is the step used in many carbohydrate

    analysis procedures to separate these two groups (Southgate,

    1991; Prosky et al., 1992; Englyst et al., 1994). However, some

    branched-chain carbohydrates of DP between 10 and 100

    remain in solution in 80% v/v ethanol so there is no clear

    and absolute division. Furthermore, carbohydrates such as

    inulin and polydextrose contain mixtures of polymers of

    different chain lengths that cross the oligosaccharide/poly-

    saccharide boundary. In categorizing oligosaccharides found

    normally in the diet, alcohol precipitation would seem to be

    the most practical way of delineating them from polysac-

    charides. For novel oligosaccharides, such as that are now

    being developed by the food industry as ingredients, the

    average DP for that particular substance, as determined by

    the manufacturer, should provide the basis on which to put

    it into the appropriate carbohydrate class. In the light of the

    lack of clarity surrounding the definition of oligosaccharides,

    the Paris carbohydrate group suggested calling this group

    short-chain carbohydrates (Cummings et al., 1997).

    Food oligosaccharides fall into two groups: (i) maltodex-

    trins, which are mostly derived from starch and include

    maltotriose and a-limit dextrins that have both a14 anda16 bonds and an average DP8. Maltodextrins are widelyused in the food industry as sweeteners, fat substitutes and to

    modify the texture of food products. They are digested and

    absorbed like other a-glucans and (ii) oligosaccharides thatare not a-glucans. These oligosaccharides include raffinose(a-Gal(1-6)a-Glc(1-2)b-Fru), stachyose ((Gal)2 1:6 Glu 1:2Fru) and verbascose ((Gal)3 1:6 Glu 1:2 Fru). They are in

    effect, sucrose joined to varying numbers of galactose

    molecules and are found in a variety of plant seeds, for

    example peas, beans and lentils. Also important in this group

    Carbohydrate terminology and classificationJH Cummings and AM Stephen

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  • are inulin and fructo oligosaccharides (a-Glc(1-2)b-Fru(2-1)b-Fru(N) or b-Fru(2-1)b-Fru(N)). They are fructans and are thestorage carbohydrates in artichokes and chicory with small

    amounts of low molecular weight found in wheat, rye,

    asparagus and members of the onion, leek and garlic family.

    They can be produced industrially. The chemical bonds

    linking these oligosaccharides are not a-1,4 or 1,6 glucansand, therefore, they are not susceptible to pancreatic or

    brush border enzyme breakdown (Oku et al., 1984; Hidaka

    et al., 1986; Cummings et al., 2001). They have become

    known as non-digestible oligosaccharides (Roberfroid et al.,

    1993). Some of them, mainly the fructans and galactans,

    have unique properties in the gut and are known as

    prebiotics (see later).

    Milk oligosaccharides

    Milk, especially human milk, contains oligosaccharides that

    are predominantly galactose containing, although great

    diversity of structure is found (Kunz et al., 2000). Almost

    all carry lactose at their reducing end and are elongated by

    addition of N-acetylglucosamine-linked b13 or b16 to agalactose residue, followed by further galactose with b13 orb14 bonds. Other monomers include L-fucose and sialicacid. The principal oligosaccharide in milk is lacto-N-

    tetraose. Total oligosaccharides in human milk are in the

    range 5.08.0 g/l, but only trace amounts are present in cows

    milk (Ward et al., 2006).

    The oligosaccharides of breast milk have long been

    credited with being the principal growth factor for bifido-

    bacteria in the infant gut and thus primarily responsible for

    these bacteria dominating the microbiota found in breast-fed

    babies. In this context, milk oligosaccharides are acting as

    prebiotics. Bifidobacteria can grow on milk oligosaccharides

    as their sole carbon source while lactobacilli may not be able

    to do so (Ward et al., 2006). The similarities between milk

    oligosaccharide structure and epithelial cell surface carbohy-

    drates in the gut suggest that milk oligosaccharides may act

    as soluble receptors for gut pathogens and thus form an

    essential part of colonization resistance. They may also be

    immunomodulatory.

    Starch and modified starch

    Starch, the principal carbohydrate in most diets, is the

    storage carbohydrate of plants such as cereals, root vegeta-

    bles and legumes and consists of only glucose molecules. It

    occurs in a partially crystalline form in granules and

    comprises two polymers: amylose (DPB103) and amylopec-tin (DPB104105). Most common cereal starches contain1530% amylose, which is a non-branching helical chain of

    glucose residues linked by a-1,4 glucosidic bonds. Amylo-pectin is a high-molecular-weight, highly branched polymer

    containing both a-1,4 and a-1,6 linkages. Some starches frommaize, rice, sorghum and barley contain largely amylopectin

    and are known as waxy. The crystalline form of the amylose

    and amylopectin in the starch granules confers on them

    distinct X-ray diffraction patterns, A, B and C. The A type is

    characteristic of cereals (rice, wheat and maize), the B type of

    potato, banana and high amylose starches while the C type is

    intermediate between A and B and found in legumes. In their

    native (raw) form, the B starches are resistant to digestion by

    pancreatic amylase. The crystalline structure is lost when

    starch is heated in water (gelatinization), thus permitting

    digestion to take place. Recrystallization (retrogradation)

    takes place to a variable extent after cooking and is in the B

    form (Galliard, 1987; Hoover and Sosulski, 1991).

    Modified starch

    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

    wide range of amylose to amylopectin ratios (Kennedy and

    Burlingame, 2003). Techniques are rapidly emerging,

    enabling starches to be produced for specific purposes by

    genetically modifying the crop used for their production

    (Regina et al., 2006). High amylose cornstarch and high

    amylopectin (waxy) cornstarch have been available for some

    time, and display quite different functional as well as

    nutritional properties. High amylose starches require higher

    temperatures for gelatinization and are more prone to

    retrograde and to form amyloselipid complexes. Such

    properties can be utilized in the formation of foods with

    high-resistant starch (RS) content.

    Starches can also be modified chemically to impart func-

    tional properties needed to produce certain qualities in

    foodstuffs such as a decrease in viscosity and to improve gel

    stability, mouth feel, appearance and texture, and resistance to

    heat treatment. Various processes are used to modify starch,

    the two most important being substitution and crosslinking.

    Substitution involves etherification or esterification of a

    relatively small number of hydroxyl groups on the glucose

    units of amylose and amylopectin. This reduces retrograda-

    tion, which is part of the process of staling of bread, for

    example. Substitution also lowers gelatinization temperature,

    provides freezethaw stability and increases viscosity. Cross-

    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

    granule. Crosslinking increases gelatinization temperature,

    improves acid and heat stability, inhibits gel formation and

    controls viscosity during processing. Altering the chemical

    nature of starch can lead to it becoming resistant to digestion.

    NSPs

    NSPs are the non-a-glucan polysaccharides of the diet(Table 1). They are essentially macromolecules consisting

    of a large number of monosaccharides (glycose) residues

    joined to each other by glycosidic linkages (IUB-IUPAC and

    Joint Commission on Biochemical Nomenclature, 1982) and

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  • are principally found in the plant cell wall. The term NSP was

    first proposed at a meeting sponsored by the European

    Economic Community Committee on Medical Research in

    Cambridge in December 1978. The meeting was convened to

    discuss the results of the analysis of nine foods for dietary

    fibre by a number of different methods in use in laboratories

    around the world. The proposal was made because An

    accurate chemical identification of polysaccharides in the

    diet is the first priorityy (James and Theander, 1981). Atthe meeting, the first NSP values, measured as the sum of

    constituent sugars, were presented for a selection of the

    test samples (James and Theander, 1981). NSPs are the most

    diverse of all the carbohydrate groups and comprise a

    mixture of many molecular forms, of which cellulose, a

    straight chain b14-linked glucan (DP 103106) is the mostwidely distributed. Because of its linear, unbranched nature,

    cellulose molecules are able to pack closely together in a

    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

    between 10 and 30% of the NSP in foods (Holland et al.,

    1988, 1991a, 1992).

    In contrast, the hemicelluloses are a large group of

    polysaccharide hetero polymers, which contain a mixture

    of hexose (6C) and pentose (5C) sugars, often in highly

    branched chains. Mostly, they comprise a backbone of xylose

    sugars with branches of arabinose, mannose, galactose and

    glucose and have a DP of 150200. Typical of the hemi-

    celluloses are the arabinoxylans found in cereals. About half

    of hemicelluloses contain uronic acids, which are carboxy-

    lated derivatives of glucose and galactose. They are impor-

    tant in determining the properties of hemicelluloses,

    behaving as carboxylic acids and are able to form salts with

    metal ions such as calcium and zinc.

    Common to all cell walls is, pectin, which is primarily a

    14b-D galacturonic acid polymer, although 1025% othersugars such as rhamnose, galactose and arabinose, may also

    be present as side chains. Between 3 and 11% of the uronic

    acids have methyl substitutions, which improve the gel-

    forming properties of pectin, as used in jam making. Some

    residues are acetylated. Calcium and magnesium complexes

    with uronic acids are characteristic of pectins.

    Chemically related to the cell wall NSP, but not strictly cell

    wall components, are the plant gums and mucilages. Plant

    gums are sticky exudates that form at the sites of injuries to

    plants. Many are highly branched complex uronic acid

    containing polymers, such as Gum Arabic, named after the

    Arabian port from which it was originally exported to Europe.

    It comes from the Acacia tree and is one of the better known

    plant gums, being sold commercially as an adhesive and used

    in the food industry as a thickener and to retard sugar

    crystallization. Other plant gums include karaya (sterculia),

    guar, locust bean gum, xanthan and tragacanth, all of which

    are licensed food additives (Saltmarsh, 2000).

    Plant mucilages are botanically distinct in that they are

    usually mixed with the endosperm of storage carbohydrates

    of seeds. Their role is to retain water and prevent desiccation.

    They are neutral polysaccharides like the hemicelluloses, of

    which guar gum, from the cluster bean (Cyamopsis tetra-

    gonolobus), and carob gums are similar 14b-D galactoman-nans with 16a-galactose single-unit side chains. Again, theyare widely used in the food and pharmaceutical industries as

    thickeners and stabilizers in mayonnaise, soups and tooth-

    pastes.

    The algal polysaccharides, which include carageenan, agar

    and alginate, are all NSP extracted from seaweeds or algae.

    They replace cellulose in the cell wall and have gel-forming

    properties. Carageenan and agar, are highly sulphated and

    the ability of carageenan to react with milk protein has led to

    its use in dairy products and chocolate.

    Up-to-date values for the NSP content of foods are

    published (Food Standards Agency/Institute of Food

    Research, 2002).

    Terminology based on physiology

    In classifying dietary carbohydrate by its chemistry, the

    principal challenge is to reconcile the various chemical

    divisions with those that reflect physiology and health. A

    classification based purely on chemistry does not allow a

    simple translation into nutritional benefits since each of

    the major chemical classes of carbohydrate has a variety of

    overlapping physiological effects (Table 3). Terminology

    based on physiological properties helps to focus on the

    potential health benefits of carbohydrate, and identify foods

    that are likely to be part of a healthy diet. But, as can be seen

    from Table 4, each physiological or health benefit of

    carbohydrate is attributable to several subgroups from the

    main classification (Table 1). Moreover, this approach is

    always open to the possibility of extensive revision, as new

    physiological properties of dietary carbohydrates become

    known. For example, the concept of prebiosis has added a

    new dimension to understanding of how carbohydrates

    behave in both the small and large intestines.

    The physiology of carbohydrate can vary among indivi-

    duals and populations. The classic example is lactose, which

    is poorly hydrolysed by the small bowel mucosa of all adults

    except Caucasians, most of whom retain the ability to digest

    lactose into adult life. Additionally, within any simple

    chemical group of carbohydrate, for example polyols, wide

    variation in absorption may occur, ranging from almost

    complete absorption of erythritol, to complete lack of

    absorption of lactitol (Livesey, 2003). Similarly, starch may

    have a variety of fates in the gut depending on granule

    structure, whether raw or cooked and subsequent processing,

    for example freezing (Stephen et al., 1983; Englyst et al.,

    1992; Silvester et al., 1995). Furthermore, terminology based

    on physiological properties alone provides the analyst with

    an impossible target.

    This dichotomy has led to the introduction of a number of

    terms to describe various fractions and subfractions of

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  • carbohydrate and these are listed in Table 5. However, the

    problems are by no means insurmountable in reconciling

    these different objectives for classification. With a sound

    chemical identification for all the carbohydrates, it is then

    possible to group them according to their health and

    physiological effects.

    Prebiotics

    A prebiotic is a non-digestible food ingredient that benefi-

    cially affects the host by selectively stimulating the growth

    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).

    As a group, prebiotics are thus defined by a single

    physiological parameter, although this is by no means itself

    clearly established (Macfarlane et al., 2006). Analytically

    they cross the boundaries between disaccharides and

    polysaccharides (DPX10) (van Loo et al., 1995). It is likelyin the future that a wider spectrum from the point of DP and

    molecular form of carbohydrates will be shown to be

    prebiotic. Prebiotic carbohydrates have unexpected proper-

    ties in the gut in that they alter the balance of the gut

    microflora towards what is considered to be a more healthy

    one (Macfarlane et al., 2006). They have been shown to

    increase calcium absorption and bone mineral density in

    adolescents. (Elia and Cummings, 2007; prebiotics are dealt

    with in more detail in the accompanying paper on

    Physiology).

    Resistant starch

    RS is the sum of starch and products of starch digestion (such

    as maltose, maltotriose and a-limit dextrins) that are notabsorbed in the small bowel (Englyst et al., 1992; Champ

    et al., 2003). All unmodified starch, if solubilized, can be

    hydrolysed by pancreatic a-amylase. However, the rate andextent to which starch is broken down is altered by a number

    of physical and chemical properties. This has led to a

    classification of RS that is now widely used (Englyst and

    Cummings, 1987).

    RS can be fractionated into four types:

    RS I: physically inaccessible starch mostly present inwhole grains

    Table 3 Principal physiological properties of dietary carbohydrates

    Provideenergy

    Increasesatiety

    Glycaemica Cholesterollowering

    Increase calciumabsorption

    Source ofSCFAb

    Alter balanceof microflora(prebiotic)

    Increase stooloutput

    Immunomodulatory

    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

    Glycaemica Glucose, fructose, galactose, sucrose, lactose,maltose, trehalose, maltodextrins, starch

    Non-glycaemic Polyols, oligosaccharides (non-a-glucan), resistantand modified starches, NSP

    Increase stooloutput

    Polyols (except erythritol), some starches, NSP,lactose (in some populations), fructose (if taken inlarge amounts)

    No effect on stoolweight

    Glucose, galactose, sucrose, maltose, trehalose,maltodextrins, oligosaccharides, most starches

    NSP, non-starch polysaccharide.aDefined as in Table 2.

    Table 5 Preferred terminology of dietary carbohydrates

    Chemical Physiological/botanical

    Useful MonosaccharidesDisaccharidesPolyolsTotal sugarsShort-chaincarbohydratesOligosaccharidesPolysaccharidesStarchNon-starchpolysaccharidesTotal carbohydrate

    PrebioticResistant starchDietary fibrea

    Glycaemic

    Lessuseful

    SugarsSugarFree sugarsRefined sugarsAdded sugarsExtrinsic and intrinsicsugars

    Non-digestible oligosaccharidesSoluble and insoluble fibreAvailable and unavailablecarbohydrateComplex carbohydrate

    aIntrinsic plant cell wall polysaccharides.

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  • RS II: RS granules (Type B) RS III: retrograded starch (after food processing) RS IV: modified starches.

    The observation that the rate and extent of starch

    digestion can vary has been one of the most important

    developments in our understanding of carbohydrates in the

    past 30 years. There are implications of this for the glycaemic

    response to foods, for fermentation in the large bowel and

    for conditions such as diabetes and obesity. Methods have

    been devised to measure these starch fractions in the

    laboratory (Champ et al., 2003).

    Dietary fibre

    The term fibre, or dietary fibre, has many different meanings

    in the nutrition world. It is not a precise reference to a

    chemical component, or components, of the diet, but is

    essentially a physiological concept as embodied in the

    original definition by Trowell, the proportion of food which

    is derived from the cellular walls of plants which is digested

    very poorly in human beings (Trowell, 1972).

    The dietary fibre hypothesis was one of the most compel-

    ling in nutrition and public health in the latter half of the

    twentieth century. It provided the stimulus to a great deal of

    research, for example epidemiological, physiological, analy-

    tical and technical. It has been the catalyst for progress in

    our understanding of the cause of a number of common

    diseases, especially those of the large bowel and has given

    governments and the food industry valuable targets for

    healthy eating. However, in the 30 years since Trowell,

    Walker, Burkitt and others first proposed the fibre hypo-

    thesis, nutritional science has progressed, especially our

    understanding of dietary carbohydrates and with this the

    apparently unique role of fibre, essentially the plant cell wall,

    in many physiological processes and in disease prevention

    (Cummings et al., 2004).

    Were it not for the perceived public perception that fibre is

    good for you, and therefore the need to provide a value for

    fibre on food labels, the term would be best consigned to the

    history books. However, various national and international

    bodies continue to struggle with the definition and the latest

    versions of their deliberations on fibre are given in Table 6.

    Common to these definitions is the concept of non-

    digestibility in the small intestine.

    Non-digestibility needs to be defined. If it is carbohydrate

    that passes across the ileo-caecal valve, then to define it

    requires complex physiological studies in humans. More-

    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

    affected by the cooking of food, storage, chewing, ripeness

    and the presence of other foods (Englyst and Cummings,

    1986; Champ et al., 2003). It will include many dietary

    components, for example lactose in some populations, some

    polyols, some starches (RS) and NSP. There is no enforceable

    method that can be used to measure this physiological

    fraction of the diet.

    As can be seen in the accompanying paper on the

    physiology of carbohydrates (Elia and Cummings, 2007),

    digestibility has an entirely different context when it is used

    in the description of energy metabolism. Here it is defined as

    the proportion of combustible energy that is absorbed over

    the entire length of the gastrointestinal tract. It would be

    useful to have these different concepts of digestion aligned.

    If there is a desire to use the word fibre, then it should

    always be qualified by a statement itemizing those carbohy-

    drates and other substances intended for inclusion, by

    which is meant carbohydrates identified in the chemical

    classification table (Table 1).

    At a meeting of the authors of the scientific update papers,

    and other experts, convened by WHO/FAO and held in

    Geneva on 1718 July 2006, the definition of dietary fibre

    was discussed, including the one suggested by the US

    Table 6 Some currently proposed definitions/descriptions of dietary fibre

    Dietary fibre consists of nondigestible carbohydrates and lignin that are intrinsic and intact in plantsFunctional fibre consists of isolated, nondigestible carbohydrates that have beneficial physiological effects in humansTotal 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 smallintestine. 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 amixture. 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 componentsthat are associated with the dietary fibre polysaccharides and may influence their physiological properties should be included as well European FoodStandards 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 arepredominantly 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 withcomplete 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).

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  • National Academy of Sciences in 2001 and that currently

    proposed by Codex (http://www.ccnfsdu.de/fileadmin/user_

    upload/PDF/ReportCCNFSDU2005.pdf) (Table 6).

    The experts agreed that the definition of dietary fibre

    should be more clearly linked to health and, after discussion,

    the following definition was proposed.

    Dietary fibre consists of intrinsic plant cell wall poly-

    saccharides.

    The established epidemiological support for the health

    benefits of dietary fibre is based on diets that contain fruits,

    vegetables and whole-grain foods, for which the intrinsic

    plant cell wall polysaccharides are a good marker. Although

    isolated or extracted fibre preparations have been shown to

    have physiological effects experimentally, these cannot be

    translated into health benefits directly because the epide-

    miological evidence points to fruits, vegetables and whole-

    grain foods as beneficial, and in a normal diet, these

    polysaccharides are part of the plant cell wall complex and

    do not exist individually.

    Soluble and insoluble dietary fibre

    These terms arose out of the early chemistry of NSPs, which

    showed that the fractional extraction of NSP could be

    controlled by changing the pH of solutions. They proved

    very useful in the initial understanding of the properties of

    dietary fibre, allowing a simple division into those which

    principally had effects on glucose and lipid absorption from

    the small intestine (soluble) and those which were slowly

    and incompletely fermented and had more pronounced

    effects on bowel habit (insoluble). However, the separation of

    soluble and insoluble fractions is very pH dependent, making

    the link with specific physiological properties less certain.

    Much insoluble fibre is completely fermented and not all

    soluble fibre has effects on glucose and lipid absorption. Many

    of the early studies were done with isolated gums or extracts

    of cell walls, whereas these various forms of fibre exist

    together mostly in intact cell walls of plants.

    Nevertheless, certain fibre-rich foods effect glycaemic

    control and lipid levels and have been widely used in the

    management of diabetes particularly the legumes and pulses

    rather than high bran products (Kiehm et al., 1976; Simpson

    et al., 1979, 1981; Rivellese et al., 1980; Mann, 1984;

    Chandalia et al., 2000; Giacco et al., 2000; Mann et al.,

    2004). Work on the variability in glycaemic response of

    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,

    concerned with glycaemic responses to carbohydrate-

    containing foods (Foster-Powell et al., 2002).

    Available and unavailable carbohydrate

    A major step forward conceptually in our understanding of

    carbohydrates was made by McCance and Lawrence (1929)

    with the division of dietary carbohydrate into available and

    unavailable. In an attempt to prepare food tables for diabetic

    diets, they realized that not all carbohydrates could be

    utilized and metabolized, that is provide the body with

    carbohydrates for metabolism. Available carbohydrate was

    defined as starch and soluble sugars and unavailable as

    mainly hemicellulose and fibre (cellulose). This concept

    proved useful, not the least because it drew attention to the

    fact that some carbohydrate is not digested and absorbed in

    the small intestine but rather reaches the large bowel where

    it is fermented or even excreted in faeces.

    An FAO technical workshop in Rome in 2002 on Food

    energymethods of analysis and conversion factors (FAO,

    2003) defined available carbohydrate as that fraction of

    carbohydrate that can be digested by human enzymes, is

    absorbed and enters into intermediary metabolism. (It does

    not include dietary fibre, which can be a source of energy

    only after fermentation).

    It is somewhat misleading to talk of carbohydrate as

    unavailable because carbohydrate that reaches the colon is

    able to provide the body with energy through fermentation

    and absorption of short-chain fatty acids. There are many

    properties of carbohydrate of which site of digestion is only

    one. An alternative to the terms available and unavailable

    today would be to describe carbohydrates either as glycaemic

    (that is providing carbohydrate for metabolism) or non-

    glycaemic, which is closer to the original concept of

    McCance and Lawrence. However, the FAO Technical work-

    shop on Food Energy in its recommendations said, Available

    carbohydrate is a useful concept in energy evaluation and

    should be retained. This recommendation is at odds with the

    view of the expert consultation in 1997 on carbohydrates,

    which endorsed the use of the term glycaemic carbohydrate

    to mean providing carbohydrate for metabolism. The group

    expressed concerns that glycaemic carbohydrate might be

    confused or even equated with the concept of glycaemic

    index, which is an index that describes the relative blood

    glucose response to different available carbohydrates. The

    term available seems to convey adequately the concept of

    providing carbohydrate for metabolism, while avoiding this

    confusion. Furthermore, in the discussion of the energy

    value of carbohydrate, the terms available and unavailable

    are extensively used (Elia and Cummings, 2007). On balance,

    however, we would recommend glycaemic as a more precise

    and measurable fraction.

    Glycaemic carbohydrate

    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

    does or does not directly provide carbohydrate as an

    energy source following the process of digestion and

    absorption in the small intestine. Carbohydrate, which

    provides glucose for metabolism is referred to as glycaemic

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  • carbohydrate, whereas carbohydrates that pass to the

    large intestine prior to being metabolized, is referred to

    as non-glycaemic carbohydrate. Most mono- and di-

    saccharides, some oligosaccharides (maltodextrins) and

    rapidly digested starches may be classified as glycaemic

    carbohydrate. Slowly digested starches are also considered

    to be glycaemic carbohydrate though glucose is less

    rapidly generated. The remaining oligosaccharides, NSPs

    and RS are considered to be non-glycaemic carbohydrates.

    Most carbohydrate-containing unprocessed foods contain

    both glycaemic and non-glycaemic carbohydrate. The extent

    to which carbohydrate in foods raises blood glucose

    concentration compared with an equivalent amount of

    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

    affect the glycaemic response to carbohydrate, including the

    intrinsic properties of the food and also extrinsic factors such

    as the composition of the meal, the overall diet and

    biological variations of the host.

    Complex carbohydrates

    This term was first used in the McGovern report, Dietary

    Goals for the United States in 1977 (Select Committee on

    Nutrition and Human Needs, 1977). It was coined largely to

    distinguish sugars from other carbohydrates and in the

    report denotes fruit, vegetables and whole-grains. The term

    has never been formally defined and has since come to be

    used to describe either starch alone, or the combination of all

    polysaccharides (British Nutrition Foundation, 1990). It was

    used to encourage consumption of what are considered to be

    healthy foods such as whole-grain cereals, etc., but becomes

    meaningless when used to describe fruits and vegetables,

    which are low in starch. As a substitute term for starch it

    would seem to have little merit and, in principle, it is better

    to discuss carbohydrate components by using their common

    chemical names.

    Physical effects of carbohydrates

    Aside from their chemistry, the physiological properties of

    carbohydrates are also affected by the physical state of the

    food. In this context, there may be a unique role for NSP in

    the control of carbohydrate metabolism. The early studies of

    viscosity on glucose responses pointed to the physical

    properties of NSP as being important (Jenkins et al., 1978).

    In a different context, the classic study of Haber et al. (1977)

    with apples shows clearly that where carbohydrate, in this

    case mainly glucose and fructose, is entrapped intracellularly

    in plant foods, its release in the gut is slowed and blood

    glucose moderated and insulin responses lowered. A unique

    property of NSP, therefore, is that it forms the plant cell wall

    and thus a physical structure to foods. Numerous studies

    have now shown that the physical structure of starchy foods

    influences the glycaemic response.

    The physical structure of a food has, therefore, a role to

    play in the regulation of carbohydrate metabolism. The use

    of viscous-soluble NSP isolates in this context will probably

    be seen as a stepping stone to understanding fibre but not

    the ultimate goal. From a nutritional and analytical view

    points, the intrinsic polysaccharides of the plant cell wall,

    known as dietary fibre or NSP, should be viewed as a single

    entity that uniquely provides physical structure to foods.

    There is however a major problem in characterizing and

    measuring the key physical attributes of a food that

    contributes to modifying its effects.

    Whole grain

    The essence of the dietary recommendations in many

    countries is to eat a diet high in whole grains, fruits and

    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

    intake goals. However, the term whole grain has several

    meanings from whole of the grain through to physically

    intact structures. A precise definition is clearly needed for

    labelling purposes.

    Whole grain comprises whole wheat, whole-wheat flour,

    wheat flakes, bulgar wheat, whole and rolled oats, oatmeal,

    oat flakes, brown rice, whole rye and rye flour, whole barley

    and popcorn. Cornmeal is not included as it is generally

    dehulled, de-branned and de-germed. Sweet corn has been

    included in some analyses (Harnack et al., 2003), but is not

    included in analyses from the UK, where it is considered a

    vegetable (Henderson et al., 2002; Thane et al., 2005, 2007).

    Foods containing added bran, but not including endosperm

    or germ, are included in some analyses (Jacobs et al., 2001)

    but not in others, but are not whole grains and should be

    excluded. Similarly, foods which are largely whole grain, but

    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

    they may be consumed by a considerable proportion of the

    population and are indicated as whole wheat on the label of

    some products but not others.

    There are also problems with the definition of a whole

    grain food. For labelling purposes, the Food and Drug

    Administration (1999) in the United States has defined a

    whole grain food as a product containing 451% wholegrain by weight per reference amount customarily consumed

    per day (Seal, 2006), and this standard has been used in

    some surveys to assess intake (Lang et al., 2003; Jensen et al.,

    2004). However, many foods contain less whole grain than

    this, but can still make a substantial contribution to total

    whole-grain intake (Thane et al., 2005, 2007).

    In studies by Jacobs et al. (1998) in the United States,

    breakfast cereals were considered to be whole grain if the

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  • product contained X25% whole grain or bran y. In amore complete analysis of the United Kingdom, foods with

    whole-grain contents of 10% or more were used, rather than

    the cutoffs of 25 or 51%. In the UK National Diet and

    Nutrition Surveys, it was found that for young people aged

    418 years, intake of whole grains was underestimated by

    28% if only those products with 451% whole grains wereincluded and underestimated by 15% if only those with

    whole-grain content greater than 25% were included. More

    recently for adults, the 51% cutoff would have under-

    estimated intake by 18% for the 198687 Dietary Survey of

    British Adults (Gregory et al., 1990), and 27% in the NDNS

    survey of adults in 200001 (Henderson et al., 2002),

    indicating not only the underestimation but that the

    manner of consuming whole grains may also be changing,

    with more foods with lower amounts now being consumed.

    It is a considerable amount of work to determine whole-grain

    content down to the 10% level, but this would include foods

    like porridge, which when cooked is 90% water but is

    consumed in substantial quantities in parts of the world

    (Thane et al., 2007), and which may have important health

    benefits.

    In his editorial comment on the 1998 Jacobs paper,

    Willett (1998) remarks The physical form of whole grains

    can vary from intact kernels (for which we should probably

    reserve the term whole grain) to finely milled flour (whole

    grain flour). This distinction between intact whole grains or

    physically disrupted, although present in the food in its

    entirety, is important. Grain structure affects the glycaemic

    response to food (Foster-Powell et al., 2002) and high intakes

    of whole-grain foods protect against the development of type

    II diabetes (Venn and Mann, 2004) and cardiovascular

    disease (Seal, 2006), yet we know little about the physical

    form of grains in these studies.

    It is also worth noting that the type of grain contributing

    to whole grains may vary from country to country. For the

    UK, about 90% of the whole-grain intake is wheat (Thane

    et al., 2005), while in the United States, a larger proportion is

    likely to be from oats, given the popularity of whole-grain

    oat cereals. With the different physical and physiological

    properties of these two grains, such differences need to be

    taken into account when interpreting health impacts of

    whole-grain consumption.

    Conclusions

    (1) Dietary carbohydrates should be classified according to

    their chemical form, as recommended at the 1997 FAO/

    WHO Expert Consultation.

    (2) The physiological and health effects of carbohydrates are

    dependent not only on their primary chemical form but

    also on their physical properties, which include water

    solubility, gel formation, crystallization state, association

    with other molecules and aggregation into the complex

    structures of the plant cell wall.

    (3) Total carbohydrate in food should be determined by

    direct measurement rather than by difference.

    (4) Many terms exist to describe sugars in the diet. The most

    useful are total sugars and their division into mono- and

    disaccharides. The use of other terms creates difficulties

    for the analyst, confusion for the consumer and suggests

    properties of foods that are not related to sugars

    themselves, but to the food matrix.

    (5) Because neither chemical nor physical description of

    carbohydrates directly reflects their physiological pro-

    perties and health benefits, a number of terms to

    describe carbohydrates, based on their physiology, have

    been created. Of these prebiotic, glycaemic, RS and

    dietary fibre are useful.

    (6) Dietary fibre should be defined to reflect the health

    benefits of a diet rich in fruits, vegetables and whole

    grains and not the variable physiological properties or

    health effects of the various carbohydrate types. The

    definition proposed by the group was intrinsic plant cell

    wall polysaccharides.

    (7) The effects of foods containing different types of fibre on

    glycaemic control and lipid levels should be investigated

    further to determine the exact properties needed for

    their effects. The distinction between soluble and

    insoluble forms of fibre is inappropriate since the

    separation is pH dependent and does not reflect the

    physiological properties of whole foods in the gut.

    (8) The term whole grains should be defined more clearly

    and the role of intact versus milled grains established.

    The whole-grain concept, along with fresh fruits and

    vegetables is central to a healthy diet message.

    Acknowledgements

    The authors thank Professor Ingvar Bosaeus, Dr Barbara

    Burlingame, Professor Jim Mann, Professor Timothy Key,

    Professor Carolyn Summerbell, Dr Bernard Venn and Dr

    Martin Wiseman for the valuable comments they provided

    on the earlier manuscript.

    Conflict of interest

    During the preparation and peer review of this paper in 2006,

    the authors and peer reviewers declared the following

    interests.

    Authors

    Professor John H Cummings: Chairman, Biotherapeutics

    Committee, Danone; Member, Working Group on Foods

    with Health Benefits, Danone; funding for research work at

    the University of Dundee, ORAFTI (2004).

    Dr Alison M Stephen: Contract with World Sugar Research

    Organization on trends in intakes of sugars and sources in

    the diet (contract is with MRC-Human Nutrition Resource);

    contracts with Cereal Partners UK on whole-grain intakes in

    the UK and relationship to adiposity (contract was with

    Carbohydrate terminology and classificationJH Cummings and AM Stephen

    S15

    European Journal of Clinical Nutrition

    title

    title

    title

    title

    title

  • MRC-Human Nutrition Resource); Adviser to Audrey Eyton

    on scientific content on book F2 Diet; Scientific Advisory

    Panel of Canadian Sugar Institute (not for profit but funded

    by sugar industry) (19952002).

    Peer-reviewers

    Professor Ingvar Bosaeus: none declared.

    Dr Barbara Burlingame: none declared.

    Professor Jim Mann: none declared.

    Professor Timothy Key: none declared.

    Professor Carolyn Summerbell: none declared.

    Dr Bernard Venn: none declared.

    Dr Martin Wiseman: none declared.

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    Carbohydrate terminology and classificationIntroductionClassificationTerminologyTotal carbohydrateSugarsTotal sugarsFree sugarsAdded sugarsExtrinsic and intrinsic sugarsIntrinsic sugarsExtrinsic sugarsNon-milk extrinsic sugars

    Oligosaccharides, short-chain carbohydratesMilk oligosaccharidesStarch and modified starchModified starch

    NSPsTerminology based on physiologyPrebioticsResistant starchDietary fibre

    Soluble and insoluble dietary fibreAvailable and unavailable carbohydrateGlycaemic carbohydrateComplex carbohydratesPhysical effects of carbohydratesWhole grainConclusionsTable 1 The major dietary carbohydratesTable 2 Energy and macronutrient intakes for 52 weighed records analysed using Canadian and UK food tablesTable 3 Principal physiological properties of dietary carbohydratesTable 4 Physiological/health groupings of dietary carbohydrateTable 5 Preferred terminology of dietary carbohydratesTable 6 Some currently proposed definitions/descriptions of dietary fibreAcknowledgementsReferences


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