Bertha

A. Lewis,2

Ph.D.

ABSTRACT

Selected

rides

are

discussed.

size,

solubihity

proteins.

The

J. Clin.

Nutr.

and

These viscosity,

relationship 31: S82-S85,

characteristics

of dietary

properties, and between

which

TheAmerican

Journal

could

interactions

fiber

and

alter

gastrointestinal

with

structure

and

small

associated

nondigestible

pohysaccha-

function,

organic

compounds.

the physiochemical

properties

include cations,

is indicated.

particle salts,

and Am.

1978.

Although dietary fiber refers specifically to the insoluble linear and therefore fibrous carbohydrate polymers associated with plant cell walls, in considering physiological responses one should consider all nondigestible polysaccharides. All polysaccharides escaping digestion will play some role in the gastrointestinal tract if only to influence the course of fermentation in the lower tract (I). The structure and physicochemical characteristics of the polysaccharides will determine the role these polymers play. Of importance are solution viscosity of soluble polysaccharides, surface area and particle size of insoluble polysaccharides, ease and degree of hydration, crystahhinity, density, ion-exchange character, and interactions with other compounds. Even within families of structurally similar polymers, small differences in chemical structure greatly alter these physicochemical properties. The number of distinct polysaccharides in foods (present naturally or as additives) far exceeds the available knowledge about them. Far more is known about the polysaccharides of wood and animal forages than about those in vegetables and fruits of human diets. Associated with cellulose in the plant cell wall are the hemicelluloses-a heterogeneous group that includes arabinans, arabinoxyhans, xylans, gahactans, mannans, glucomannans, and xyloglucans. Closely associated with these in many plant tissues are the pectic substances, some of which are not clearly differentiated from the hemicelluhoses because of merging chemical structures and

S82

of

of Clinical

physical properties. Unique to the pectic substances are the (1 4)-a-D-galacturonans occurring as such or as heteropolymers composed of other sugars as well. Also present in plants, particularly in seeds or fruit, are storage polysaccharides such as the gahactomannans of legumes and oat gum of oat seeds. Since the human gastrointestinal tract possesses amylases, a-ghucosidases, and $-galactosidases as the only recognized digestive carbohydrases, it is apparent that the polysaccharides referred to above (soluble and insoluble) will continue through the intestinal tract until the microbial population utilizes them for energy. -*

Physical

properties:

particle

size

Rate of passage of digesta through the gastrointestinal tract appears to be influenced by particle size (unpublished observations), but the mechanism is not clear. Understanding of this phenomenon is further clouded by experimental variables. Excessive grinding of fiber causes some hydrolysis of polysaccharides and may promote dehignification as well (1, 2). Both factors will alter the ease and degree of hydration as well as total waterholding capacity (1, 3). Fractionation of the fiber into its components may also occur, leaving the different particle size fibers cornpositionally nonidentical (4). Nevertheless, From University, 2 Associate

Nutrition

the

Division

of Nutritional

Ithaca, New Professor,

31: OCTOBER

1978,

York 14853. Nutritional

pp.

S82-S85.

Sciences,

Cornell

Sciences.

Printed

in U.S.A.

Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S82/4656126 by East Carolina University user on 16 January 2019

Physical and biological properties structural and other nondigestible carbohydrates1

PHYSICAL

AND

BIOLOGICAL

PROPERTIES

Structure-solubility

NONDIGESTIBLE

CARBOHYDRATES

S83

molecular weight (D.P. ca. 20), the molecule with a single glucose side chain (II) is soluble while the linear polymer (III) retrogrades out of solution. GIc

relationships

.,

6

Structural features that disrupt chose packing and alignment of molecular chains decrease crystalhinity and promote water solubihity of polysaccharides. Cellulose is one of the most insoluble of all carbohydrate polymers. It achieves this distinction because of the equatorial configuration of the hydroxyl groups and glycosidic bonds, which gives the cellulose chain a flat ribbon-like conformation. This conformation permits the chain to fold back and forth upon itself, developing maximum hydrogen-bonding within chains and between molecular chains in the cellulose microfibril. The cumulative effect of the multiple hydrogen-bonding prevents internal hydration and swelling of the microfibrils except with strongly alkaline reagents. If on the other hand the cellulose is swelled in strong alkali, and methyl, ethyl, carboxymethyl or other small groups are introduced into the molecule in place of the hydroxyhic proton, the resulting cellulose ether readily hydrates and over an intermediate range of substitution becomes water soluble. Thus ethyl cellulose with a degree of substitution (D.S.) of 0.2 to 0.9 is readily soluble in alkali, ethyl cellulose with D.S. 1.4 to 1.5 is water soluble, and ethyl cellulose with D.S. 2.0 to 3.0 becomes soluble in organic solvents. This leads to the generalization that linear polysaccharides are insoluble whereas branching confers sohubihity. Thus the highly branched plant exudate gums such as acacia gum are highly soluble whereas linear hernicelluloses such as xylan are insoluble. Even a single unit branch confers sohubihity on the gahactomannans (I) of guar or locust bean. Gal

.1. -Man-(l

-.

In the laminaran closely related (1

6 4)-Man-(l

-*

-p

4)-Man-

family, a mixture of 3)-$-D-ghucans of low

GIc

l-(-i3 Ghc

I-j-i’,3Glc

l-f-’3 Glc

1.fm3

GIc

II GIc

I-(-.3 Ghc III

l-j-3

Glc

Molecular structure also affects solution viscosity. Highly branched polysaccharides give low viscosity solutions even at high molecular weight whereas the more linear polymers such as the gahactomannans hydrate slowly to give extremely viscous solutions. This highly viscous solution is also typical of oat gum (IV), which acquires its solubihity by virtue of the irregular conformation arising from the alternating sequence of (1 3) and (1 4)-/9-D-glucose units occurring either singularly or in blocks. -*

-+

-‘4Glc

l-fi3Ghc

l-j-*,,,[4Ghc

l-J-im3Glc-n

=

1 -3, ml

IV

Total water-holding capacity of fiber is related to the polysaccharide content of the plant and to cation-exchange capacity (3). Since chemical structure, crystalhinity, and particle size affect hydration and total waterholding capacity, meaningful comparisons of different fiber sources are difficult. Small alterations in chemical structure or crystallinity induced by grinding, cooking, food processing, or limited enzymic digestion in the gastrointestinal tract may drastically alter the hydration, sohubility, or viscosity potential of the polysaccharides. Interactions Inclusion

with

other

compounds

complexes

High-fiber diets are thought to bind and prevent absorption of certain nutrients, and certain nondigestible polysaccharides lower serum cholesterol possibly by binding cholesterol and bile salts. The mechanism of binding is not known. If the binding is nonspecific, the surface area of the fiber is probably the most important factor; however, structure-

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the dry bulk volume of coarse fiber is greater than that of fine fiber (I), which may be the most important factor in passage of digesta. In addition to size, particle shape and density may be important in flow rates.

OF

S84

LEWIS

-

-*

-

-*

-

-*

Proteins Soluble polysaccharides, by virtue of their strong affinity for water, compete with proteins for available water (7). This competition for solvent is shown by dextran solutions that depress the solubihity of such proteins as serum albumins, ‘y-globulin, and fibrinogen. The reduced solubility may have some effect on the rate of digestion of proteins but would probably have little other consequence. A second interaction is a structure-specific physical association which drastically alters

the physicochemical and biological properties of proteins. The concanavahin A interaction with branched a-glucans and z-mannans is typical ofthis type (8). Displaying the general characterjstics of an antigen-antibody interaction, this interaction is characterized by 1) strict structural requirements for both the carbohydrate and the protein; 2) competitive inhibition by the monomer sugar; 3) a reversible reaction; 4) aggregation and insohubilization ofthe polysaccharide-protein complex; and 5) dissolution of the complex at high carbohydrate concentrations. Certain nondigestible polysaccharides may interact with the intestinal mucosa or with the cell surfaces of colon bacteria and in this way affect either digestion and absorption of nutrients or microbial growth. It seems unlikely, however, that ingested lectins could escape denaturation or proteolytic digestion and protect against colon cancer as has been postulated (9). Metal

ions

A number of hemicelluhoses, pectins (galacturonans), and other polysaccharides such as the alginic acids show ion-exchange capacity as a consequence of the presence of the uronic acids D-glucuronic, D-galacturonic, and D-mannuronic acids, respectively. These weakly ionized carboxyhic acids readily form salts when titrated with bases. In addition, pohysaccharides such as the carrageenans are also weakly acidic by virtue of their sulfuric acid monoester content. Likewise, some glycolipids are acidic. The plant sulfohipid is a strongly acidic sulfonic acid derivative of glucose. Present knowledge confines these acidic glycolipids to certain leafy materials, and their content in the diet may not be significant. The ion-exchange capacity of the acidic pohysaccharides varies greatly, ranging from the high capacity of those homopohymers containing uronic acids only to the lower exchange capacity of the acidic hemicelluloses composed mainly of neutral sugars with a relatively small proportion of uronic acids. Ion-exchange capacities have been determined for a number of fiber sources and appear to be affected by cooking (3). The in vivo significance of these ion-exchange hemicehluloses is not known. Polysaccharides displaying anion-ex-

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specific interactions are also known. The most widely studied of these is the interaction between starch amylose and iodine. Iodine, fatty acids, monoglycerides, and many other organic compounds will occupy the cavity of the amylose helix, which can expand or contract to give the proper fit (5). Six to seven glucose units occupy one turn of the helix giving spacial dimensions similar to the cavity of ct-cyclodextrin, a cyclic ohigomer of six glucose units. -Cyclodextrin and any linear (1 4)-ct-D-glucan having a D.P. of at least six will form inclusion complexes. The characteristics of inclusion complexes of this type include 1) the concept of dimensional fit; 2) a saturation limit defined by the length of the helix (D.P. of the polymer); 3) a reversible complex stabilized by weak physical forces; and 4) modification of the physical properties of the polymer. Although relatively unstudied, other hydrophihic helical polymers also give inclusion complexes; thus, polyvinylalcohol gives a colored complex with iodine in the same manner as amylose. Although starch is rapidly digested in the body precluding inclusion complexing, the possibility remains that other linear pohysaccharides may possess the structural requirements for inclusion complexation. Rees and Scott (6) predicted on theoretical grounds that (1 3)-f3-D-glucans, -gahactans, -mannans, and -xylans, (1 4)-$-D-galactans, (1 4)-a-D-glucans, -mannans, -xylans, and -arabinans, (1 3)-a-D-arabinans and the (1 3; 1 4)-D-galactans (carrageenans) will possess helical structures. Singleor multiple-strand hehices have now been demonstrated for some of these polymers. Little investigation has been made into the possible binding of compounds to these polymers as inclusion complexes.

PHYSICAL TABLE 1 Carbohydrate-salt

AND

OF

NONDIGESTIBLE

CARBOHYDRATES

S85

(12) Salt

Calcium Potassium Sodium Calcium Potassium Potassium

chloride acetate chloride chloride acetate iodide

Ligand:salt

1:1 2:1 2:1 1:1 1:1, 2:1 2:1

change characteristics are almost unknown in plants and are probably of little significance. Amino sugars occur in relatively small quantities in plant tissues and usually appear as their N-acetylated derivatives. These amides are neutral and devoid of anion-exchange character unlike the nonacetylated amino sugar. Microbial cell walls may be as significant as fiber components in providing ion-exchange surfaces in the large intestine (10). The microbial cell wall contains several ionizable species in its macromolecular framework: acidic sugar derivatives (such as muramic acid), amino acids, and amino sugars. As in plant material, the various amino sugars may be present as the neutral N-acetate (or other amide) rather than with the free basic amino group. Beyond interaction of metal ions with acidic pohysaccharides, ample evidence in the literature documents interactions of metal ions with neutral polysaccharides. These interactions appear to be of several types from complexes with rather specific structural requirements (11) to incorporation of salts into the crystal lattice of sugars and pohysaccharides (12). The composition of some representative crystalline complexes is shown in Table 1. Many other crystalline adducts are known. In addition to the crystalline carbohydratesalt adducts shown in Table 1, ion-dipole interactions in aqueous and nonaqueous salt solutions can also be demonstrated by changes in optical rotation and viscosity and by infrared and nuclear magnetic resonance spectroscopy (II, 12). Electrophoresis of re-

sugars in acidic solutions of Ca, or Ba causes migration of the sugarcation complex toward the cathode (12). Gehation of water-soluble polysaccharides by metal ions is known (13). Divahent calcium ions cause alginic acid to gel, whereas the monovalent potassium ion gels the iota-fraction of carrageenan. Contrary to popular belief, the ion does not act as a cross-link of molecular chains but may promote conformation changes required for gel formation. References 1. VAN S0EST, P. J., AND J. B. ROBERTSON. Chemical and physical properties ofdietary fibre. Presented at Miles Symposium on Dietary Fibre. Halifax, Nova Scotia, June 1976. 2. HARKIN, J. M. Lignin. In: Chemistry and Biochemistry of Herbage, edited by G. W. Butler and R. W. Bailey. London: Academic Press, 1973, vol. 1, p. 352. 3. MCCONNELL, A. A., M. A. EASTWOOD AND W. D. MITCHELL.

Physical

characteristics

of

vegetable

foodstuffs Sci. Food

that could influence bowel function. J. Agric. 25: 1457, 1974. 4. HELLER, S. N., J. M. RIVERS AND L. R. HACKLER. Dietary fiber: The effect of particle size and pH on its measurement. J. Food Sci. 42: 436, 1977. 5. SENTI, F. R., AND S. R. ERLANDER. Carbohydrates. In: Non-stoichiometric Compounds, edited by L. Mandelcorn. New York: Academic Press, 1964, pp. 568-605. 6. REES, D. A., AND W. E. SCOTT. Polysacchanide conformation, part VI. J. Chem. Soc. (B) 469, 1971. 7. LAURENT, T. C. The interaction between polysaccharides and other macromolecules, part 5. Biochem. J. 89: 253, 1963. 8. So, L. L., AND I. J. GOLDSTEIN. Protein-carbohydrate interactions, part IV. J. Biol. Chem. 242: 1617, 1967. 9. FREED, D. L. J., AND F. H. Y. GREEN. Do dietary lectins protect against cohonic cancer? Lancet 2: 1261, 1975. 10. Fm, T. J., K. HUTTON, A. THOMPSON AND D. G. ARMSTRONG.

Binding

of magnesium

ions

by

isolated

cell walls of rumen bacteria and the possible relation to hypermagnesaemia. Proc. Nutr. Soc. 31: 100A, 1972. 11. ANGYAL, S. J., AND K. P. DAVIES. Comphexing of sugars with metal ions. Chem. Comm. 500, 1971. 12. RENDLEMAN, J. A., JR. Complexes of alkali metals and alkaline-earth metals with carbohydrates. Advan. Carbohyd. Chem. 21: 209, 1966. 13. REES, D. A. Structure, conformation and mechanism in

the

works.

formation Advan.

of

Carbohyd.

polysacchanide

gels

Chem.

24: 267,

and

1969.

net-

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Lactose Amylose

PROPERTIES

ducing complexes

Carbohydrate

D-Glucose

BIOLOGICAL