Caballero B. (ed.) Encyclopaedia of Food Science, Food Technology and Nutrition. Ten-Volume Set

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Food Stability) to about 0.8, and the product resists

microbial growth because of the prevailing high os-

motic pressure. Jams and preserves owe their stability

at ambient temperature to this effect. The long shelf-

life of intermediate-moisture foods (e.g., fruitcake)

depends on the same principle. Glucose is not useful

in this respect, because of its relatively low solubility.

Conversely, invert sugar causes a considerable reduc-

tion in water activity as in honey, for example

¼0.75). ‘Set honey’ is saturated with respect to

glucose, which remains suspended as very small crys-

tals in a viscous, almost solid, medium. Unlike sugars,

polysaccharides do not cause any significant lowering

of water activity, because they have a large molecular

weight and because they are used at a very low con-

centration (normally < 5%).

0007 Apart from sugar–sugar and sugar–water inter-

actions as discussed above, sugars may interact chem-

ically and form more extensive bonding (covalent

bonds) with themselves and other molecules (below).

However, certain sugars (like glucose) are also valu-

able in food systems because of their inherent reduc-

ing properties. These interactions may stabilize ionic

groups in solutions and facilitate their absorption

when ingested (e.g., maintenance of the ferrous form

of iron and conversion from the ferric form).

Polysaccharides

0008 Polysaccharides are macromolecules, many of which

can adopt organized structures in foods. Most are

polyhydric alcohols, acids and/or esters, which,

depending on the monomeric sugar composition, are

likely to interact with themselves, other polysacchar-

ides, or other molecules. Polysaccharides may be

insoluble in water, dissolve, and form true solutions,

colloidal dispersions, and/or gels. In mixed poly-

saccharide systems, the polymers may intersperse

and form a number of interactive states. These inter-

actions may be described as:

0009 Additive, where the measured property is the sum

of the property of the individual polymers.

0010 Complementary, where polymer one provides a

characteristic that polymer two (or more) lacks.

0011 Synergistic, where the effect of the combined

polymer population is greater than the additive

effect.

0012 Antagonistic with respect to a ternary system,

where there is phase separation as a consequence

of solvent incompatibility. The phase separation

process (coacervation) results in one phase

being rich in one of the two solutes and the

other phase being rich in the other solute. This

process is utilized in, for example, encapsulation

of flavors.

When polysaccharides are added to foods to stabilize

structural form, they are described as ‘stabilizers’

(See Stabilizers: Types and Function; Applications)

or ‘gums’ (See Gums: Properties of Individual

Gums). Stabilization reflects thickening rather than

emulsification in the true sense, although stabilizers

are used in foods to prevent separation of emulsions

and sedimentation of suspended solids. In many prod-

ucts (e.g., instant soups), they impart a desirable

‘mouth feel.’ Some act as gelling agents, which again

impart desirable physical properties. With the excep-

tion of gelatine (a protein), all stabilizers are polysac-

charides whose main function is to increase the

viscosity of aqueous systems. Most of the polysac-

charides listed in Table 1 are used as stabilizers in a

wide range of manufactured foods. Nonmodified

(native) starch is exceptional, because it is primarily

a very important nutrient (together with sugars, it

provides about 50% of food energy in the UK),

which also happens to be a good stabilizer and texture

modifier. According to Stokes’ law, the velocity of

sedimentation of particles is inversely proportional

to the viscosity of the medium in which the particles

are suspended.

0013Polysaccharides consist of chains of varying length,

which generally occur as random coils in dilute

aqueous systems. The chains can be branched or

linear. They are surrounded by a cloud of water mol-

ecules, and this gives rise to internal friction and

hence viscosity. They behave as imaginary spheres

whose ‘effective volume’ or ‘hydrodynamic volume’

is related to the ‘radius of gyration’ of the polysac-

charide chain. Branched polysaccharides have a lower

viscosity than their linear counterparts of the same

molecular weight because their hydrodynamic

volume is smaller. Polysaccharides give rise to a sub-

stantial increase in viscosity, even at a very low con-

centration (< 1%). As the concentration increases, the

random coils begin to overlap and a considerable

increase in viscosity is observed as the chains interact

with each other. Many polysaccharides, but not all,

give rise to gels at a higher concentration (1–4%). The

gel-forming properties of polysaccharides may be due

to weak Van der Waals interactions, ionic inter-

actions, hydrogen bonding, or helix formation. As a

consequence, junction zones are established, which

stabilize the three-dimensional structure that leads

to self-supporting gels.

0014With the exception of starch, polysaccharides are

not digested by the endogenous enzymes of the

human digestive tract and are considered as dietary

fiber. Nutritionally speaking, however, there may be a

drawback, in so far as charged polysaccharides may

bind minerals (cations) and make them less available

to the human body.

876 CARBOHYDRATES/Interactions with Other Food Components

Homopolysaccharides

0015 Homopolysaccharides (homoglycans) consist of a

single type of monomer. Cellulose and starch are the

best-known examples. However, they have very dif-

ferent properties. Cellulose (See Cereals: Contribu-

tion to the Diet) consists of b-(1 !4)-linked glucose

units arranged in a ribbon-type conformation in a

zigzag pattern. Parallel chains fit closely to each

other and associate with multiple hydrogen bonds to

give rise to long fibers, which are totally insoluble in

water and relatively inert. Although subject to some

swelling in water, cellulose is completely unaffected

by boiling in water. Natural cellulose (cellulose I) has

considerable crystallinity (60–80%), as revealed by

X-ray diffraction. Starch consists of two components,

viz. amylose (essentially linear) and amylopectin

(branched).

0016The a-(1 !4)-linked glucose molecules in amylose

allow considerable conformational freedom. In

freshly prepared dilute solution, amylose is in the

form of a random coil. On standing at ambient tem-

perature, it ‘retrogrades’ (see below), i.e., the random

coils form double helical associations, which are

tbl0001 Table 1 Polysaccharides used in foods

Polysaccharide Origin Monomeric sugars E-number

Starch Cereals, tubers, roots a-(1! 4)-

D-Glucose [amylose] and a-(1 !6)-

D-glucose branches [amylopectin]

Cellulose Cell walls, wood, cotton b-(1 !4)-

D-Glucose E 460

Tree exudates

Gum acacia (Arabic) Acacia senegal b-(1 !3)-

D-Galactose backbone with L-rhamnose,

D-glucuronic acid, D-galactose, L-arabinose side-

chains

E 414

Gum karaya (sterculia) Sterculia urens

D-galacturonic acid, D-galactose, L-rhamnose,

D-glucuronic acid in three-dimensional

arrangement

E 416

Gum tragacanth Astragalus gummifer a-(1 !4)-

D-Galacturonic acid backbone with

D-galactose -b-(1 !2)-D-xylose, L-fucose-

b-(1 !2)-

D-xylose and D-xylose-b-(1 !3) side-

chains

E 413

Seed gums

Locust bean (carob) gum Ceratonia siliqua b-(1 !4)-

D-Mannose with a-(1 !6)-D-galactose

side-chains (Man:Gal ¼4:1)

E 410

Guar gum Cyamopsis tetragonoloba b-(1 !4)-

D-Mannose with a-(1 !6)-D-galactose

side-chains (Man:Gal ¼2:1)

E 412

Algal products

Agar Gelidium spp. b-

D-Galactose and 3,6-anhydro-D-galactose. Low

esterification with sulfate groups

E 406

Alginic acid Ascophyllum nodosum, Laminaria

hyperborea, Macrocystis pyrifera

b-(1 !4)-Mannuronic acid chains and a-(1 !4)-

guluronic acid chains, with alternating

mannuronic–guluronic acid chains

E 400

Carrageenan Gigartina stallata, Chondrus crispus, etc. Galactose-sulfate, galactose disulfate and

anhydogalactose chains; occurs in different

forms: t-, k-, l-, m- and n-carrageenan

E 407

Fruit products

Pectin Apple pomace, citrus peal a-(1 !4)-Galacturonic acid, largely esterified with

methanol; some rhamnose and xylose may be

present

E 440

Microbial products

Curdlan Alcaligenes faecalis var. myxogenes b-(1 !3)-

D-Glucose

Gellan Pseudomonas elodea b-(1 !4)-

D-Glucose-b-(1 !4)-glucuronic acid-

b-(1 !4)-glucose-a-rhamnose-tetrameric repeat

unit

E 418

Xanthan Xanthomonas campestris a-(1 !4)-glucose backbone with mannose–

glucuronic acid–mannose side-chains with

terminal carboxyl groups

E 415

Root polysaccharides

Inulin Helianthus tuberosus

(Jerusalem artichoke) and

Cichorium intybus (chicory root)

b-(1 !2)-

D-Fructose

Konjac Amorphophallus konjac b-(1 !4)-

D-Mannose, b-(1 !4)-D-glucose E 425

CARBOHYDRATES/Interactions with Other Food Components 877

insoluble and sediment as a white precipitate. At a

high concentration, free settling is prevented, and

gels are formed as the randomly oriented chains

approach each other at several junction zones.

Double helices are formed at the junctions, which

do not extend the full length of the molecule.

The net result is a three-dimensional structure,

whose rigidity depends on the concentration of

amylose and hence the number of junction zones

per unit volume. Amylose gels are translucent to

almost opaque, owing to light scattering. Double

helices of retrograded amylose are dissociated at a

temperature of about 160



0017 Amylopectin consists of a-(1 !4)-linked glucose

units (95%) and a-(1 !6)-linked branched points

(5%) and is fairly soluble in water. The outer chains

of amylopectin, consisting of about 15–25 glucose

units, because of their close proximity readily form

short double helices during starch biosynthesis and

within food systems upon storage. Amylopectin is

fairly stable in solution and forms soft gels at a high

concentration. Waxy maize starch consists almost

entirely of amylopectin and gives clear or slightly

translucent weak gels.

0018 When native starches (See Starch: Structure, Prop-

erties, and Determination; Sources and Processing;

Functional Properties) are heated in excess water,

the double helices progressively dissociate, water is

imbibed, and the granules swell. This process of

gelatinization is characteristic of the botanical origin.

Typically, it occurs at around 65



C and is irrevers-

ible, forming a solution, a colloid, or a gel, depending

on the origin of starch and its concentration. Once

gelatinized, double helices may reform in food

systems (below).

0019 Fructans are polymers of fructose linked by b-

(1 !2) bonds. The best-known example is inulin

with 3–60 fructose units per chain. This forms clear

viscous solutions in water. Inulin is not digested by

the endogenous enzymes of the human digestive

system. It is considered as dietary fiber and is used in

some functional foods (See Functional Foods).

0020 Curdlan is a microbial homopolysaccharide that

is insoluble in water at ambient temperature.

It forms a gel > 54



C with an almost constant

strength between 60–80



C and increases up to, and

beyond, 100



C. It is an approved food additive in

the USA.

Heteropolysaccharides

0021 Heteropolysaccharides (heteroglycans) consist of

more than one type of monomeric sugar. Indeed, the

majority of polysaccharides used as food additives are

heteropolysaccharides (Table 1).

Single Polymer Systems

0022Heteropolysaccharides can associate in a number of

ways in food and nonfood systems forming solutions,

colloids, gels, and sometimes associated helices. The

physical properties are critical in terms of texturiza-

tion in food systems and must be optimized for a

given application. These structures are dependent on

the nature of the polysaccharide and its concentra-

tion; agar, for example, can form relatively strong gels

at the level of 1%, whereas starch concentrations of

> 4% are required for gelling. Some, like carrageenan

[b-(1 !4)-linked galactose and galactose sulfate

residues], form hydrogen-bonded ‘junction zones’

between two polymer chains that stabilize the gels.

In agar [also b-(1 !4)-linked galactose and galactose

sulfate residues] and carrageenan, the polysaccharide

chains form double helices, which associate further

to form more complex junction structures. Pectin

forms strong gels (e.g., jam-making) by a different

mechanism. In pectin, the highly esterified polymers

(methylated polygalacturonic acid) are heated in acid

solution (pH about 3.5) in the presence of a high

proportion (> 50%) of sucrose. The low pH sup-

presses ionization of the nonesterified galacturonic

acid units, whereas the high degree of methylation

favors the formation of junction zones by hydropho-

bic interactions. The sucrose further competes for

water allowing junction zones to form without separ-

ation from water. However, when the gel is mechan-

ically disturbed (broken), liquid is released as a result

of shrinkage (syneresis).

0023Alkali metal salts of alginates are soluble in water,

although the free acids are insoluble. These polymers

are composed of mannuronic (M) and guluronic (G)

acids. Three major arrangements of the sugars occur,

namely linear regions consisting of M or G (M

and

are known as periodically arranged monosacchar-

ides) interspersed with regions of alternating M and G

(MG

, aperiodic segments). In the presence of divalent

cations (especially calcium), the carboxylic groups of

adjacent chains are linked to form the so-called ‘egg-

box’ structure. The final three-dimensional structures

give exceptionally rigid and stable gels. Addition of

sodium phosphate or of sodium ethylenediamine-

tetraacetate destroys the gel structure by removing

calcium ions.

Mixed Polymer Systems – Synergistic and

Nonsynergistic Interactions

0024It is known that the viscosity of binary mixtures

of some polysaccharides can be higher than the

viscosity of the individual components measured at

the same concentration. This synergistic interaction

is particularly pronounced in mixtures of guar

878 CARBOHYDRATES/Interactions with Other Food Components

(galactomannan) and xanthan gums. This interaction

can be interpreted by the Flory and Huggins theory.

0025 Three types of polymeric interactive behavior have

been identified and characterized:

0026 Incompatibility, where there is phase separation.

0027 Compatibility, where a uniform homogeneous

phase is created.

0028 Polymer associations, where solid coacervates or

gels are formed. Most mixed polymer systems are

incompatible (especially above solution concen-

trations of 1–2%). If one of the polymers is

charged, miscibility is promoted, but if both

species are charged, immiscibility results.

In terms of strength of interactions, agarose–galacto-

mannan and k-carrageenan–galactomannan inter-

actions are reduced as the galactose content of

the galactomannan increases. This is because linear

mannan regions form tight associations with double

helices (below) of the other polymers. All these inter-

actions can be very important in polysaccharide

blends used in food systems.

Electrostatic Interactions

0029 Polysaccharides carrying acidic groups have a strong

tendency to bind cations. Neutral polysaccharides

do not bind cations, whereas polycarboxylates like

demethylated pectin, alginic acid, and xanthan read-

ily bind divalent cations. Similarly, sulfated polysac-

charides like k-carrageenan also bind cations. Certain

polysaccharides contain primary amine groups (like

chitin and chitosan) and form associations with

transition metals.

0030 Polysaccharide–cation interactions lead to two

transitions: sol–gel and phase separation. Where

sol–gel transitions occur, viscous solutions are present

below the transition concentration and above the

transition temperature. Above the sol–gel transition

concentration and below the sol–gel transition tem-

perature, gels exist that exhibit viscoelasticity. High

cation concentrations generally lead to phase sep-

aration in the form of precipitation of the poly-

saccharide.

0031 There is a real nutritional concern (although there

is some controversy regarding its significance) that

minerals may be lost from the human body owing to

polysaccharide–mineral interactions. Acidic condi-

tions in the stomach will tend to discharge the min-

erals and make them potentially more easily absorbed

lower in the intestine. In the almost neutral pH of the

small intestine where the minerals would primarily

be absorbed, however, re-association of cations with

charged polymers will occur. The stability of these

associations in this region of the gastrointestinal

tract is uncertain as well as the restrictions imposed

upon absorption. Additionally, the polysaccharides

may be fermented in the large intestine, releasing the

minerals for absorption in this region (assuming that

there is little or no competition from the microflora,

which will also tend to absorb the minerals).

Helical Structures

0032Polysaccharides can, as discussed above, assume a

helical conformation. The helices may be single (one

chain) where stabilization is achieved by the presence

of a guest molecule (ligand) in the lumen of the helix.

These structures are commonly referred to as ‘inclu-

sion complexes.’ Starch polymers (amylose and amy-

lopectin) are highly effective in forming inclusion

complexes; especially amylose with its long linear a-

(1 !4) bonded chains. The formation of a blue color

when iodine solution is added to starch is a familiar

example, and it has been shown to be due to the

formation of a helical complex. The starch–iodine

reaction is used as a quantitative tool for the deter-

mination of amylose by colorimetry where a blue

color is generated with a l

max

at 635 nm. This color

is a function of the chain length. Amylopectin, with

its shorter unit chain, gives rise to a red color with

iodine and absorbs light in the region 570–580 nm.

0033Starch (particularly amylose) can also form inclu-

sion complexes with organic guest molecules. Free

fatty acids and their alkali metal salts, acyl monogly-

cerides of fatty acids, fatty alcohols, and surfactants

containing linear acyl groups give rise to amylose–

lipid complexes that are insoluble in water at pH < 7.

These interactions occur during food processing and

are common in extruded foods. Acyl monoglycerides

are added to instant mash potato granules to prevent

stickiness, and acetylated tartaric acid esters of acyl

monoglycerides are added to bread to retard staling.

Sodium and potassium salts of fatty acids are permit-

ted additives in Dutch type rusks. Complexes are also

possible with many other guest molecules, including

flavoring agents, aldehydes, ketones, alcohols, vita-

mins, and dyes. However, many of these so-called

‘complexes’ have not been structurally characterized

as being true inclusion complexes rather than uniden-

tified associations.

0034It should be emphasized that amylose in solution

occurs as a random coil, and not as a preformed helix.

It assumes a helical conformation (left-handed helix)

only in the presence of a hydrophobic guest (e.g.,

palmitic acid), because the interior of the helix is

essentially hydrophobic with an affinity for the

hydrocarbon chain of the ligand. Inclusion complexes

(V-type helices) containing 6, 7, or 8 glucose residues

per helical turn can be formed, depending on the

CARBOHYDRATES/Interactions with Other Food Components 879

cross-sectional dimensions of the guest molecule. Ad-

jacent helical turns (pitch 0.8 nm) are held together by

hydrogen bonding, which is the main stabilizing force

of the complexes. It has been shown that a stoichio-

metric relationship exists between the amylose and

the guest molecules when the helix is completely

saturated with the ligand. For instance, lauric acid

(1.73 nm chain length, C12:0) is completely sur-

rounded by 2.16 helical turns corresponding to

about 13 anhydroglucose residues. Arachidic acid

(2.74 nm chain length, C20:0) is surrounded by 3.42

helical turns corresponding to 20.5 anhydroglucose

units. The long complexed helices fold upon them-

selves to form three-dimensional structures, which

give characteristic X-ray diffraction patterns (amy-

lose V-pattern), owing to the ordered packing of the

helices. Complexes are also characterized by their

distinct dissociation temperatures, which are mainly

functions of the chain length of the ligand and the

temperature at which the complexes are formed. The

dissociation energy of the complexes is a measure of

the energy required to disrupt intrahelical hydrogen

bonds. Thermal properties of complexes are studied

by differential scanning calorimetry.

0035 Apart from single helices, which form around guest

molecules, double helices may be formed from poly-

saccharide chains. Furthermore, these double helices

may form ordered (registered) arrays and conse-

quently generate crystalline regions (see below), as

found in native starch granules. Double helices are

stabilized by interchain hydrogen bonding and in this

form are essentially insoluble.

Crystallinity and Retrogradation

0036 Although helices or similar structures of polysacchar-

ides may be formed from solutions/food systems,

these structures need not necessarily be crystalline.

For crystallinity to be present (as determined by

X-ray diffraction, for example), the helical structures

must be associated in ordered/registered structures.

The ordered structures have unit cell repeats, which

create characteristic diffraction patterns. Many poly-

saccharides associate to form true crystalline struc-

tures, although these are often ‘contrived’ by making

specific derivatives of the polymers.

0037 In food systems, polysaccharides would generally

find it difficult to crystallize, because of interference

from other molecular species. However, starch poly-

mers (especially amylose) do crystallize relatively

quickly in/from solutions and in highly hydrated

systems like baked goods (bread, cakes, etc.). The

consequence in terms of product texture is apparent

to anyone who has eaten stale bread. This contains

appreciable quantities of recrystallized or retrograded

starch, which, being a form of ‘resistant starch’ (See

Starch: Resistant Starch), imparts an unpleasant tex-

ture and potentially restricts amylase hydrolysis. In

some products, there is a relatively high resistant

starch content owing to retrogradation, and this is

sometimes promoted as a positive dietary feature.

Probably, the best-known example is corn flakes.

Formation of Covalent Bonds

0038Some carbohydrate interactions with other carbo-

hydrates or other types of molecules incorporate

true covalent bonding, as described below.

Caramelization

0039The process of caramelization (See Caramel: Proper-

ties and Analysis; Methods of Manufacture; Carbo-

hydrates: Classification and Properties) involves the

formation of brown-colored and odorous products

from melted sugars. Many confectionery products

incorporate steps that cause caramelization (e.g.,

toffee-making), although commercially available

caramel is also added to products to impart a desir-

able color (e.g., colas and whisky). Hexoses are con-

verted by heat to dicarbonyl compounds via an

enediol intermediate. Loss of water leads to 5-hydro-

xymethylfurfural and related chemical species, which

are very reactive. Pentoses give furfural. Maltol and

isomaltol are also produced, both of which have a

characteristic odor.

Nonenzymic (Maillard) Browning

0040Nonenzymic browning, as the name indicates, does

not depend on the action of enzymes. The NH

groups of amino acids (especially the e-amino group

of lysine) in alkaline or neutral pH react with the

aldehyde groups of sugars to form brown pigments.

The N-substituted 1-amino-1-deoxy-ketoses (Ama-

dori compounds) lead to the formation of a range of

dicarbonyl compounds. These compounds may react

further with amino acids (Strecker degradation) to

form pyrazines, for example. Polymerization of the

products of the amino acid sugar reactions causes the

formation of very complex polymers (melanoidins),

which impart color to foods. Flavor compounds are

also generated as a consequence of these processes.

Hence, in food systems, these browning reactions

generate products with desirable sensory characteris-

tics. However, there is a loss of nutritional quality as

the amino acid availability progressively declines.

This can be particularly undesirable in low-protein

diets, where amino acids (especially essential) are

made unavailable. The Maillard reaction can be min-

imized by lowering the pH, avoiding high tempera-

tures and long storage times, and maintaining a low

880 CARBOHYDRATES/Interactions with Other Food Components

water activity. The reaction is inhibited by SO

busulfite salts and can be avoided in some foods by

the use of nonreducing sugars.

Other Interactions

0041 Sucrose is readily hydrolyzed to glucose and fructose

(invert sugar) either by acids or by the enzyme

b-fructosidase (invertase). In soft drinks containing

acid (e.g., citric or phosphoric), gradual inversion of

sucrose takes place, even at ambient temperature.

See also: Caramel: Properties and Analysis; Methods of

Manufacture; Carbohydrates: Classification and

Properties; Cereals: Contribution to the Diet; Functional

Foods; Gums: Properties of Individual Gums;

Stabilizers: Types and Function; Applications; Starch:

Structure, Properties, and Determination; Sources and

Processing; Functional Properties; Resistant Starch;

Sweets and Candies: Sugar Confectionery; Water

Activity: Principles and Measurement; Effect on Food

Stability

Further Reading

Axelos MAV (1998) Polysaccharide–metal interactions. In:

Walter RH (ed.) Polysaccharide Association Structures

in Food. New York: Marcel Dekker.

Belitz H D and Grosch W (1999) Food Chemistry, 2nd edn.

Berlin: Springer.

Ikan R (ed.) (1996) The Maillard Reaction. Consequences

for the Chemical and Life Sciences. Chichester, UK:

Wiley.

Karkalas J and Raphaelides S (1986) Quantitative aspects

of amylose–lipid interactions. Carbohydrate Research

157: 215–234.

Karkalas J, Ma S, Morrison WR and Pethrick RA (1994)

Some factors determining the thermal properties of amy-

lose inclusion complexes with fatty acids. Carbohydrate

Research 268: 233–247.

O’Brien J, Nursten HE, Crabbe MJC and Ames JM (eds)

(1998) The Maillard Reaction in Foods and Medicine.

Cambridge: Royal Society of Chemistry.

Tomasik P and Schilling CH (1998a) Complexes of starch

with inorganic guests. In: Horton D (ed.) Advances in

Carbohydrate Chemistry and Biochemistry. San Diego,

CA: Academic Press.

Tomasik P and Schilling CH (1998b) Complexes of starch

with organic guests. In: Horton D (ed.) Advances in

Carbohydrate Chemistry and Biochemistry. San Diego,

CA: Academic Press.

Walter RH (1998) Origin of polysaccharide supramolecular

assemblies. In: Walter R H (ed.) Polysaccharide Associ-

ation Structures in Food. New York: Marcel Dekker.

Williams PA and Phillips GO (1995) Interactions in mixed

polysaccharide systems. In: Stephen AM (ed.) Food

Polysaccharides and Their Applications. New York:

Marcel Dekker.

Digestion, Absorption, and

Metabolism

D H Alpers, Washington University School of Medicine,

Washington, USA

Introduction

0001The assimilation of dietary carbohydrate into the

body is a complex process involving secretion

(salivary glands, stomach, and pancreas), hydrolysis

(stomach, small intestine, and colon), and absorption

(small intestine and colon; Figure 1). Abnormalities in

each of these organs or processes can lead to

diminished assimilation of carbohydrates.

Digestion

Dietary Carbohydrates

0002Western diets contain on average 200–300 g of carbo-

hydrates day

1

, accounting for 40–50% of total food

sources of energy but only 22% of total daily calories.

The sources of this carbohydrate include complex

polymers (e.g., starch), and simple sugars, including

the disaccharides lactose and sucrose, and the mono-

saccharides glucose and fructose. Nearly all of these

carbohydrates, except for lactose in milk and some

muscle glycogen, are found in plants. Dietary fiber is

the term used to describe polymeric substances

(nearly all carbohydrate) that are not digested and

absorbed in the small intestine. In addition to dietary

Salivary

glands

α-Amylase secretion

Pancreas

α-Amylase secretion

Food

Starch type

Disaccharide type

Food processing

CHO load

Fat, protein content

Stomach

Emptying rate

Colon

Fermentation

SCFA absorption

Small bowel

Transit time

Disaccharidase activity

Monosaccharide absorption

Transcellular

Paracellular?

fig0001Figure 1 Factors affecting carbohydrate (CHO) assimilation.

SCFA, short chain fatty acid. Reproduced from Carbohydrates:

Digestion, Absorption and Metabolism. Encyclopaedia of Food

Science and Nutrition, Macrae R, Robinson RK and Sadler MJ

(eds), 1993, Academic Press.

CARBOHYDRATES/Digestion, Absorption, and Metabolism 881

fiber, plants contain oligosaccharides (3–8 sugars)

mainly as a-galactosides in legumes (e.g., raffinose,

stachyose) and as fructans (e.g., fructooligosacchar-

ides) found in onions and other vegetables. Some of

the undigested fiber and oligosaccharides (or disac-

charides) can be hydrolyzed by colonic bacteria and

their products absorbed.

0003 Starch is the major storage form of polysaccharides

in plants, along with cellulose (a b1–4 linked

glucopolymer), hemicelluloses (e.g., galactans, arabi-

nans), pectins, and gums. Starch is composed of

polymers of glucose joined in straight-chain a1–4

linkages without (amylose) or with a1–6 branched

chains (amylopectin). Even the starch is not com-

pletely digested, and some of the dietary fiber re-

presents ‘resistant starch.’ Although the assay of

‘resistant starch’ is not well standardized, its presence

is probably proportional to the amount of dietary

fiber. The plant content of starch depends upon

the type, part, and age of the plant. The efficiency

of digestion of plant starch is inconsistent, as

plant starches are enclosed in granules that are in-

completely and variably disrupted during cooking or

processing. Thus, actual dietary starch content may

vary significantly from that contained in published

tables.

0004 The percentage of carbohydrate ingested as simple

sugars has been increasing in recent decades. Sucrose

is found in most fruits and vegetables and (in purified

form) as table sugar and a sweetener for many

foods. Sucrose accounts for about 40 g day

1

(30%

of carbohydrate intake, 9% of calories), two-thirds in

the form of sweetener. Lactose is the major sugar in

milk and processed foods, and can account for as

much as 10% of total carbohydrate calories in non-

lactase-deficient persons. Glucose and fructose are

also found in fruits and vegetables, but most fructose

is ingested as the sweetener, high-fructose corn syrup.

Estimated intake for glucose is 20 g day

1

, but may

be as high as 150 g day

1

for fructose. The sugar

alcohol d-glucitol (sorbitol), found in many fruits,

especially prunes, pears, plums, and cherries, is

slowly absorbed. It may cause diarrhea when it is

added to foods as a noncaloric sweetener, if consumed

in excessive amounts. Another sugar alcohol, xylitol,

is tolerated somewhat more effectively by the

digestive tract.

0005 Starches and disaccharides are digested by secreted

and by mucosal enzymes, respectively, in the mouth,

stomach, and small intestine. The resistant portion of

starch, undigested or malabsorbed disaccharides and

monosaccharides, and the dietary fiber components

are digested by bacteria in the lumen of the nonrumi-

nant colon. In the ruminant this digestion occurs in

the forestomach.

Salivary and Gastric Digestion

0006Salivary amylase is probably important in initiating

starch digestion, depending upon the time spent

chewing. Human salivary amylase is 94% identical

with pancreatic amylase, but is inactivated in the acid

pH of the gastric lumen. Starch supplements are

better tolerated in breast-fed than bottle-fed infants,

because of the presence of human milk amylase. In

humans before 1 year of age, a-amylase activity in the

duodenum is fairly low, due to delay in development

of full secretory capacity. Presence of starch or its

hydrolytic products can protect the enzyme from

acid denaturation, and in this way some salivary or

milk amylase reaches the more neutral pH of the

duodenal lumen.

0007Gastric juice contains no other carbohydrases than

a-amylase. Acid nonenzymic hydrolysis of some

carbohydrates can occur, presumably in the stomach,

although the extent of this process in vivo is probably

small. The rate of gastric emptying is inversely related

to caloric load, limiting the delivery of undigested

food to the duodenum so as not to exceed hydrolytic

capacity.

Pancreatic Digestion

0008Although lipid and protein substrates are hydrolyzed

by more than one gastric and pancreatic enzyme,

duodenal fluid contains only a-amylase, derived

largely from pancreatic secretion. Starch hydrolysis

begins with random cleavage of internal a1–4 glucose

bonds, proceeding to smaller fragments until only

small linear glucopolymers (2–8 residues) or small

a-limit dextrins (containing a1–6 branch chains) are

left. These compounds require brush border disac-

charidases for digestion.

0009There are many factors that affect the completeness

of starch digestion in addition to the physical form

and processing of the starch in foods. Meal compos-

ition may affect variation in transit time from meal to

meal, and intestinal transit time is slowed by nutrient-

triggered inhibitory feedback. This feedback is initi-

ated in part by lipids, and mediated by peptide YY.

Starch feeding can increase amylase secretion in

animals and in newborn humans. Fat and protein

may also increase the secretion of pancreatic amylase

via release of cholecystokinin. These nutrients also

delay gastric emptying, preventing too rapid delivery

of starch into the duodenum. Amylase activity can

be inhibited by proteins found in certain plants,

although their role in normal assimilation of carbo-

hydrates is unclear.

0010The release of glucose from maltose, resulting from

starch digestion, elicits a rise in blood glucose. The

amount of this rise (glycemic response) varies

882 CARBOHYDRATES/Digestion, Absorption, and Metabolism

depending upon the form and processing of the food

starch, the presence of other nutrients in the meal,

and the degree of secretion of the fat-responsive

gastric-inhibitory polypeptide (GIP) that mediates

the enhancement of the glucose-stimulated insulin

release. Because of the variety of factors affecting

the glycemic response to food carbohydrates, it is

not surprising that this response is variable and

often unpredictable.

Intestinal (Brush Border) Digestion

0011 All the hydrolytic products of starch digestion, as well

as ingested disaccharides, are hydrolyzed by the brush

border carbohydrases, sucrase-isomaltase, lactase,

maltase-glucoamylase, and trehalase (Table 1).

These enzymes are all a-hydrolases, except for lac-

tase, which cleaves b-bonds. The result of this diges-

tion is monosaccharides that can be absorbed across

the apical membrane of the enterocyte by specific

transporters. These proteins are ectoenzymes present

either as heterodimers (sucrase) or as single subunits

(lactase, maltase, trehalase). They are synthesized as

single peptide chains and modified by glycosylation

with or without subsequent cleavage.

0012 Only monosaccharides can be absorbed readily

from the human intestine. Disaccharide absorption

is very low, but does increase slightly relative to

monosaccharides in conditions such as celiac sprue

that produce mucosal damage. The disaccharidase

activity is rate-limiting for absorption of glucose and

galactose from lactose, and of glucose from hydroly-

sis of glucose oligomers when a-amylase activity is

scarce (e.g., in the newborn child). The distribution of

disaccharidases along the length of the gut is designed

for efficient digestion, as digestion is nearly complete

by mid-jejunum, and the enzyme content peaks in the

jejunum. Expression along the vertical axis of the villi

is also appropriate for hydrolysis of luminal contents.

The enzymes are transcribed maximally in the lower

and mid-villus, decreasing to the villus tip, and the

enzyme content follows this pattern. Lactase mRNA

in adults is more restricted to the lower villus, in

contrast to its appearance in all villus cells before

birth, but the protein persists in all villus enterocytes.

The lower levels of enzymes near the villus tip may be

related to their release from the membrane by pancre-

atic proteases.

0013The products of amylase digestion (maltotriose,

maltose, and a-limit dextrins) cannot be absorbed

without further digestion. Two of the disacchari-

dases, maltase-glucoamylase and sucrase-isomaltase,

act sequentially to complete the hydrolysis of starch

begun by a-amylase. Maltase-glucoamylase has max-

imal activity against linear polymers of 5–9 glucose

residues, and cleaves all maltotriose, and a small

amount of maltose and a-limit dextrins. Sucrase-

isomaltase hydrolyzes most of the a-limit dextrins

and maltose, providing the monosaccharides that

can be efficiently absorbed.

0014Sucrase-isomaltase is anchored to the membrane by

a transmembrane N-terminal fragment, and cleavage

into sucrase and isomaltase subunits is mediated by

trypsin on the external surface of the enterocyte.

Sucrase-isomaltase is expressed in the colon from

12–28 weeks of gestation, but disappears at birth,

along with the villus/crypt structure seen in small intes-

tine. At birth in humans there is high sucrase activity in

the small intestine that persists into adulthood. In

rodents born with immature intestines, sucrase is

hardly detectable at birth, and rises to adult levels

after weaning. In rats, the high fasting levels of

sucrase-isomaltase decline after eating, because of

tbl0001 Table 1 Human carbohydrases used in dietary carbohydrate digestion

Enzymes Size of protein (kDa) Substrate specificity Bonds cleaved Products

Proprotein Mature

CHO þCHO

Amylase

Salivary

55 Glu

n>6

Glca1,4Glc Maltose, maltotriose,

a-limit dextrins

Pancreatic

Sucrase-isomaltase 155 210

130

þ Sucrose, a-limit dextrins Glca1,2Fru Glucose, fructose

245

145

Glca1,4Glc

Lactase-phlorizin hydrolase 210 215

160

Lactose, cellobiose, b-glycosides Glcb1,4Gal Glucose, galactose

225

145

Glcb1,4Glc hydrophobic aglycons

Maltase-glucoamylase 255 285

335

Glc

n¼ 2–9

Glca1,4Glc Glucose

Glca1,6Glc

Trehalase 65.5

?75

trehalose Glca1,Glc Glucose

Not synthesized as proproteins;

high mannose form;

fully glycosylated form;

intracellular cleavage form delivered to brush border (human) or

cleaved at brush border surface (rat);

final active form after surface cleavage by pancreatic trypsin;

predicted size (from cDNA) of rabbit enzyme;

mature form is linked by glycosylphosphatidylinositol, not by transmembrane segment as for other disaccharidases.

CARBOHYDRATES/Digestion, Absorption, and Metabolism 883

rapid enzyme turnover mediated by pancreatic prote-

ases. Starvation decreases sucrase activity, and refeed-

ing restores it. Sucrose and fructose more than starch

induce sucrase and maltase activities. Sucrase defi-

ciency in humans results from a number of different

defects in glycosylation, intracellular transport, and

possibly in altered catalytic activity.

0015 The digestion and absorption of lactose, the major

carbohydrate in milk, are often variable, and are

related to lactase-phlorizin hydrolase levels that are

rate-limiting for absorption, as well as the rate of

gastric emptying, small intestinal transit rate, and

the degree of colonic digestion and salvage. Lactase

is anchored by a COOH-terminal sequence and then

undergoes SH-sensitive intramolecular folding in the

endoplasmic reticulum. Prior to arrival at the apical

membrane, the 225-kDa lactase precursor undergoes

cleavage to a 160-kDa intermediate form. On the

apical cell surface final cleavage to the 145-kDa

active enzyme occurs by the action of trypsin. Unlike

the human, the rat lactase undergoes a several-step

cleavage on the apical surface. Lactase activity is high

at birth in most mammals, and declines in the human

during childhood or adolescence, reaching levels

about 5–10% those at birth. Initiation of this process

is ‘hard-wired,’ but can be modified by hormones and

nutrients, at least in animals. The age at which the fall

in activity occurs varies according to the genetic back-

ground of the individual. Inherited lactase deficiency

in humans involves transcriptional and posttranscrip-

tional mechanisms. The phenotype in many Cauca-

sians for persistence of lactase is inherited as an

autosomal recessive trait. In all other mammals, lac-

tase activity falls after weaning. Lactose feeding in

humans does not increase lactase activity, and the

absence of dietary lactose, in diets used for patients

with galactosemia, does not cause a fall in activity.

Lactase activity falls during malnutrition in children,

but not in adults. A variety of infectious and inflam-

matory processes decrease lactase activity more than

that of other disaccharidases. Activity may be slow to

recover after an acute infectious process, and remains

low in chronic inflammatory conditions, such as

Crohn’s disease and human immunodeficiency virus

(HIV-1) infection. Table 2 summarizes the factors

altering carbohydrase activity.

0016Maltase-glucoamylase accounts for about 2% of

the brush border protein, and cleaves small glucose

polymers and a-limit dextrins produced by a-amylase

activity. Unlike sucrase and maltase in humans, the

protein is inserted into the brush border membrane

without any intra- or extracellular cleavage. In the pig

and rat surface cleavage by pancreatic enzymes

occurs. As all forms are enzymatically active; the

significance of these structural differences is un-

known. Also, unlike sucrase and lactase there is rela-

tively little change in maltase levels at the time of

birth, either in human or animal intestines.

Colonic (Bacterial) Digestion

0017Up to 70 g of carbohydrate (including the compon-

ents of dietary fiber and other dietary carbohydrates

that escape small bowel digestion) may reach the

colon each day in humans. This carbohydrate is fer-

mented by colonic bacteria to short-chain fatty acids

(largely acetate, propionate, and butyrate), hydrogen

gas, and methane. The overall fermentation reaction

can be estimated thus:

34.5 C

! 48 CH

COOH þ CH

COOH

þ 5CH

(CH

)

COOH þ 23.75 CH

þ 34.25 CO

þ 10.5 H

In ruminants these fatty acids are produced in the

forestomach, and in other mammals in the cecum

and colon. Butyrate and caproate can be released by

tbl0002 Table 2 Factors affecting carbohydrase activity

Enzyme Factor Enzyme content Mechanism

a-Amylase Starch feeding ""d mRNA content

Hydrolytic products " Degradation inhibited

Prenatal development ""d mRNA content

Disaccharidase Hydrolytic products No change Active site

Pancreatic enzymes # Shortened t/2

Pancreatic insufficiency " Prolonged t/2

Sucrase-isomaltase Single-meal feeding #"d mRNA content

Sucrose or fructose feeding ""d mRNA content

Prenatal development ""d mRNA content

Diabetes mellitus " Multifactorial

Lactase-phlorizin hydrolase Postnatal development ##d mRNA

Infection and inflammation ##d translation

Malnutrition (children) # Multifactorial #d mRNA

t/2, half life.

884 CARBOHYDRATES/Digestion, Absorption, and Metabolism

gastric lipase action on milk triacylglycerols, and may

be nutritionally important in infants. The carbohy-

drate moieties of mucins and other glycoproteins are

also used to support bacterial growth. Thus, endogen-

ous carbohydrates are important in perpetuating co-

lonic bacterial cultures, which in turn are responsible

for salvaging much of the nutrient value of undigested

dietary carbohydrate.

Absorption and Metabolism

General Characteristics of the Mucosal Barrier

0018 The only carbohydrates absorbed to any extent

across the intestinal mucosa are monosaccharides.

The mechanism for absorption involves the use

of either Na

-coupled or non-Na

transporters

(Table 3). The GLUT transporters mediate a facili-

tated diffusion process, whereas SGLT1-associated

transport is an active process, involving the Na

-ATPase located in the basolateral membrane of

the enterocyte. This protein uses adenosine triphos-

phate (ATP) to maintain a low intracellular Na

con-

centration, providing a chemical gradient for Na

(and coupled glucose) from the lumen to the cell.

The delivery of the solute to the cell surface is a

function of the efficiency of stirring of the luminal

contents. Although the thickness of this unstirred

water layer in humans has been thought to be large,

in the dog, where stirring can be vigorously con-

ducted, the unstirred water layer is only 40 mm. Me-

tabolism of disaccharides proceeds in two steps, with

surface digestion by disaccharidases preceding ab-

sorption of the sugar. Thus, the delay in traversing

this barrier should be brief, and the rate-limiting step

for absorption is most likely due to the apical sugar

transporters.

0019 Water absorption is coupled with that of the mono-

saccharide and Na

. The mechanism whereby this

occurs is not well defined. In some epithelial cells,

such as renal collecting ducts, there are specialized

water transporters called aquaporins. Expression of

these proteins in the intestinal mucosa is either non-

existent or sufficiently low to be functionally insig-

nificant. A unique hypothesis suggests that SGLT is

able to account for the water absorption, as about

260 water molecules are cotransported in vitro for

every 2 Na

and every one sugar molecule. This

capacity should be large enough to account for

about 5 l of waterday

1

for a human ingesting a

diet of average carbohydrate content. This hypothesis

has yet to be tested in vivo in humans.

0020Another hypothesis suggested from data in small

rodents that water movement in the intestine is para-

cellular, via the tight junctions. This route might also

account for absorption of ions and other solutes for

which there are no specific apical transporters. More-

over, the tight junctions are subject to regulation of

their cross-sectional area, and could serve as a size-

selective filter mechanism. Calculations have sug-

gested that the rates of glucose absorption in humans

(> 200 mmol h

1

) exceed by an estimated 2–10-fold

the predicted capacity for active sugar absorption.

However, l-glucose, a driver for paracellular move-

ment potentially equivalent to d-glucose, does not

produce significant water absorption in either dog

or rat intestines. Thus, there are insufficient data to

suggest that paracellular movement of sugar or its

coupled water is important in mammals.

Glucose and Galactose Absorption

0021Active hexose transport is driven by an electrogenic

sodium gradient. The stoichiometry for Na

-coupled

glucose transport is 2:1. In intact brush border ves-

icles, both high- and low-affinity glucose uptake has

been found, depending on the species. The low-

affinity uptake would be suitable for the high intra-

luminal postprandial concentrations. These ‘systems’

vary independently depending on the developmental

or fed status of the animal form which the membranes

were made.

0022Despite these data suggesting more than one active

hexose transport system in intestinal brush border

membranes, only one Na

-coupled transporter has

tbl0003 Table 3 Major cellular monosaccharide transporters

Tr a n s p o r t e r N a

-coupled Organ expression Transport function

GLUT1 No Many tissues, especially RBC, blood–brain barrier Glucose, across blood–tissue barriers

GLUT2 No Liver, kidney, small bowel, pancreatic b-cells Low-affinity, across basolateral membranes

GLUT3 No Many tissues, especially brain Glucose across basolateral membranes

GLUT4 No Skeletal and cardiac muscle, adipose tissue Insulin-dependent uptake

GLUT5 No Small bowel, kidney, testis, adipose tissue, muscle Fructose>>glucose across apical>>basolateral

membranes

SGLT1 Yes Intestine, kidney High-affinity glu > gal, apical transport

SGLT2 Yes Kidney Low-affinity glu > gal apical transport

RBC, red blood cells.

CARBOHYDRATES/Digestion, Absorption, and Metabolism 885