Carbohydrate terminology and classification

Abstract

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 (α or β), 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 (DP10). 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.

Introduction

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 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 (α or non-α) 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 necessary for a coherent and enforceable approach to measurement and labelling forms the basis for terminology and an understanding of the physiological and health effects of these macronutrients.

Table 1 The major dietary carbohydrates

A chemical approach divides carbohydrates into three main groups, sugars (DP1–2), oligosaccharides (short-chain carbohydrates) (DP3–9) and polysaccharides (DP10). Sugars comprise (i) monosaccharides, (ii) disaccharides and (iii) polyols (sugar alcohols). Oligosaccharides are either (a) malto-oligosaccharides (α-glucans), principally occurring from the hydrolysis of starch and (b) non-α-glucan such as raffinose and stachyose (α galactosides), fructo- and galacto-oligosaccharides and other oligosaccharides. Polysaccharides may be divided into starch (α-1:4 and 1:6 glucans) and non-starch polysaccharides (NSPs), of which the major components 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 polysaccharides (Roberfroid, 2005).

A variety of methodologies are available for the measurement of the carbohydrate content of food and the components are listed in Table 1 (Englyst et al., 2007).

Terminology

Total carbohydrate

Although the individual components of dietary carbohydrate 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 carbohydrate. 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 understanding of the potential health benefits of those foods.

Direct analysis of carbohydrate components and summation 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 Widdowson's, 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 examination of geographic variations and changes in intake over time of individual carbohydrate types and their relationship with health outcomes. Total carbohydrate by direct measurement 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 Widdowson's The Composition of Foods (Holland 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 2 Energy and macronutrient intakes for 52 weighed records analysed using Canadian and UK food tables

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 viscosity, 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 (α-Glc(1 → 2)β-Fru) and lactose (β-Gal(1 → 4)Glc). Sucrose is found very widely in fruits, 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 (α-Glc(1 → 4)α-Glc) is found in yeast, fungi (mushrooms) and in small amounts 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 disaccharides 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 analytically 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 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 problems 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 considered 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 Nomenclature, 1982), although in the most recent International Union of Pure and Applied Chemistry–International 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’ (IUPAC–IUB 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/polysaccharide boundary. In categorizing oligosaccharides found normally in the diet, alcohol precipitation would seem to be the most practical way of delineating them from polysaccharides. 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) maltodextrins, which are mostly derived from starch and include maltotriose and α-limit dextrins that have both α1–4 and α1–6 bonds and an average DP8. Maltodextrins are widely used in the food industry as sweeteners, fat substitutes and to modify the texture of food products. They are digested and absorbed like other α-glucans and (ii) oligosaccharides that are not α-glucans. These oligosaccharides include raffinose (α-Gal(1 → 6)α-Glc(1 → 2)β-Fru), stachyose ((Gal)2 1:6 Glu 1:2 Fru) 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 are inulin and fructo oligosaccharides (α-Glc(1 → 2)β-Fru(2 → 1)β-Fru(N) or β-Fru(2 → 1)β-Fru(N)). They are fructans and are the storage 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 α-1,4 or 1,6 glucans and, 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 β1–3 or β1–6 to a galactose residue, followed by further galactose with β1–3 or β1–4 bonds. Other monomers include L-fucose and sialic acid. The principal oligosaccharide in milk is lacto-N-tetraose. Total oligosaccharides in human milk are in the range 5.0–8.0 g/l, but only trace amounts are present in cow's milk (Ward et al., 2006).

The oligosaccharides of breast milk have long been credited with being the principal growth factor for bifidobacteria 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 carbohydrates 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 vegetables and legumes and consists of only glucose molecules. It occurs in a partially crystalline form in granules and comprises two polymers: amylose (DP103) and amylopectin (DP104–105). Most common cereal starches contain 15–30% amylose, which is a non-branching helical chain of glucose residues linked by α-1,4 glucosidic bonds. Amylopectin is a high-molecular-weight, highly branched polymer containing both α-1,4 and α-1,6 linkages. Some starches from maize, 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 amylose–lipid 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 functional 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 retrogradation, which is part of the process of staling of bread, for example. Substitution also lowers gelatinization temperature, provides freeze–thaw stability and increases viscosity. Crosslinking 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-α-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 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 priority…’ (James and Theander, 1981). At the 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 β1–4-linked glucan (DP 103–106) is the most widely 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 150–200. Typical of the hemicelluloses are the arabinoxylans found in cereals. About half of hemicelluloses contain uronic acids, which are carboxylated derivatives of glucose and galactose. They are important 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 1–4β-D galacturonic acid polymer, although 10–25% other sugars 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 tetragonolobus), and carob gums are similar 1–4β-D galactomannans with 1–6α-galactose single-unit side chains. Again, they are widely used in the food and pharmaceutical industries as thickeners and stabilizers in mayonnaise, soups and toothpastes.

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.

Table 3 Principal physiological properties of dietary carbohydrates
Table 4 Physiological/health groupings of dietary carbohydrate

The physiology of carbohydrate can vary among individuals 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 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.

Table 5 Preferred terminology of dietary carbohydrates

Prebiotics

‘A prebiotic is a non-digestible food ingredient that beneficially 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 (DP10) (van Loo et al., 1995). It is likely in 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 properties 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 α-limit dextrins) that are not absorbed in the small bowel (Englyst et al., 1992; Champ et al., 2003). All unmodified starch, if solubilized, can be hydrolysed by pancreatic α-amylase. However, the rate and extent 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 in whole grains

  • 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 compelling 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, analytical 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 hypothesis, 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.

Table 6 Some currently proposed definitions/descriptions of dietary fibre

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. Moreover, 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 carbohydrates 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 17–18 July 2006, the definition of dietary fibre was discussed, including the one suggested by the US 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 polysaccharides’.

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 epidemiological 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 energy—methods 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 workshop 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 carbohydrate’, whereas carbohydrates that pass to the large intestine prior to being metabolized, is referred to as ‘non-glycaemic carbohydrate’. Most mono- and disaccharides, 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 >51% whole grain 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 product contained 25% whole grain or bran …’. In a more 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 4–18 years, intake of whole grains was underestimated by 28% if only those products with >51% whole grains were included 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 underestimated intake by 18% for the 1986–87 Dietary Survey of British Adults (Gregory et al., 1990), and 27% in the NDNS survey of adults in 2000–01 (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. 1)

    Dietary carbohydrates should be classified according to their chemical form, as recommended at the 1997 FAO/WHO Expert Consultation.

  2. 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. 3)

    Total carbohydrate in food should be determined by direct measurement rather than ‘by difference’.

  4. 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. 5)

    Because neither chemical nor physical description of carbohydrates directly reflects their physiological properties 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. 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. 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. 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.

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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.

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Correspondence to J H Cummings.

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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 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) (1995–2002).

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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Cummings, J., Stephen, A. Carbohydrate terminology and classification. Eur J Clin Nutr 61, S5–S18 (2007). https://doi.org/10.1038/sj.ejcn.1602936

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Keywords

  • carbohydrate
  • sugars
  • oligosaccharides
  • starch
  • dietary fibre
  • classification

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