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5

Digestion and Metabolism of Carbohydrates


John Mathers and Thomas MS Wolever

Key messages
• Carbohydrates are the single most abundant and economic methane in the large bowel. Absorbed SCFAs are metabolized in
sources of food energy in the human diet, constituting 40–80% colonic epithelial, hepatic, and muscle cells.
of total energy intake in different populations. • For optimum function of the nervous system and other cells,
• Carbohydrates are classified according to their degree of poly- blood glucose concentrations are tightly controlled by a group of
merization into sugars, oligosaccharides, and polysaccharides – hormones (insulin in the absorptive phase; glucagon, epine-
the last consisting of starches with different degrees of resistance phrine, and cortisol in the postabsorptive phase), utilizing
to digestion – and dietary fibers or nonstarch polysaccharides. several possible metabolic pathways for glucose anabolism and
• Glycemic carbohydrates are digested (hydrolyzed by enzymes) to catabolism.
sugars (monosaccharides) in the small bowel and absorbed and • Intakes of optimum amounts of different types of carbohydrates
metabolized. are associated with good health through effects on energy
• Nonglycemic carbohydrates are fermented in varying degrees to balance, digestive functions, blood glucose control, and other risk
short-chain fatty acids (SCFAs), carbon dioxide, hydrogen, and factors for several chronic diseases.

5.1 Introduction: carbohydrates in foods monosaccharide composition and the type of linkage
between sugar residues. Examples of food carbohy-
Carbohydrates are one of the four major classes of drates and an overview of their digestive fates are
biomolecules and play several important roles in all given in Table 5.1.
life forms, including: From birth, carbohydrate provides a large part of
the energy in human diets, with approximately 40%
● sources of metabolic fuels and energy stores
of the energy in mature breast milk being supplied as
● structural components of cell walls in plants and of
lactose. After weaning, carbohydrates are the largest
the exoskeleton of arthropods
source (40–80%) of the energy in many human diets,
● parts of RNA and DNA in which ribose and
with most of this derived from plant material except
deoxyribose, respectively, are linked by N-glycosidic
when milk or milk products containing lactose are
bonds to purine and pyrimidine bases
consumed. The carbohydrate contents of some vege-
● integral features of many proteins and lipids
table dishes are summarized in Table 5.2.
(glycoproteins and glycolipids), especially in cell
membranes where they are essential for cell–cell
recognition and molecular targeting. 5.2 Digestive fate of dietary
carbohydrates
Carbohydrates are very diverse molecules that can
be classified by their molecular size (degree of poly- As with other food components, the digestive fate of
merization or DP) into sugars (DP 1–2), oligosac- particular carbohydrates depends on their inherent
charides (DP 3–9), and polysaccharides (DP > 9). The chemical nature and on the supramolecular struc-
physicochemical properties of carbohydrates and tures within foods of which they are a part. To be
their fates within the body are also influenced by their absorbed from the gut, carbohydrates must be broken

© 2009 J Mathers and TMS Wolever.


Digestion and Metabolism of Carbohydrates 75

Table 5.1 Classes of food carbohydrates and their likely fates in the human gut

Class DP Example Site of digestion Absorbed molecules

Monosaccharides 1 Glucose Small bowel Glucose


1 Fructose Small bowela Fructose
2 Sucrose Small bowel Glucose + fructose
2 Lactoseb Small bowel Glucose + galactose
Oligosaccharides 3 Raffinose Large bowel SCFA
3–9 Inulin Large bowel SCFA
Polysaccharides >9 Starches Predominantly small bowelc Glucose
>9 Nonstarch polysaccharides Large bowel SCFA

a
Except where very large doses are consumed in a single meal.
b
Except in lactose-intolerant subjects, in whom lactose flows to the large bowel.
c
Some starch escapes small bowel digestion (resistant starch). In all these cases, the carbohydrate entering the large bowel becomes a substrate
for bacterial fermentation to short-chain fatty acids (SCFAs).
DP, degree of polymerization.

down to their constituent monosaccharide units, and protein-1 (SGLT1), a process that is powered by Na+/
a battery of hydrolytic enzymes capable of splitting K+-ATPase on the basolateral membrane (Figure 5.1).
the bonds between sugar residues is secreted within In contrast, fructose is absorbed by facilitated trans-
the mouth, from the pancreas, and on the apical port via the membrane-spanning GLUT5 protein. A
membrane of enterocytes. While these carbohydrases member of the same family of transporter proteins,
ensure that about 95% of the carbohydrate in most GLUT2, is the facilitated transporter on the basolat-
human diets is digested and absorbed within the eral membrane which shuttles all three monosaccha-
small intestine, there is considerable variation in rides from the enterocyte towards the blood vessels
bioavailability between different carbohydrate classes linking with the portal vein for delivery to the liver.
and between different foods. Carbohydrates that are The capacity of the human intestine for transport
digested to sugars and absorbed as such in the small of glucose, galactose, and fructose is enormous – esti-
bowel are called “glycemic” carbohydrates. mated to be about 10 kg per day – so that this does
not limit absorption in healthy individuals. Carbohy-
Hydrolysis in the mouth and small bowel drate malabsorption is usually caused by an inherited
The major carbohydrase secreted by the salivary or acquired defect in the brush border oligosacchari-
glands and by the acinar cells of the pancreas is the dases. More than 75% of human adults are lactose
endoglycosidase α-amylase, which hydrolyzes (digests) intolerant because of a loss (possibly genetically
internal α-1,4-linkages in amylose and amylopectin determined) of lactase activity after weaning (primary
molecules to yield maltose, maltotriose, and dextrins. lactose intolerance). In such individuals, ingestion of
These oligosaccharides, together with the food disac- more than very small amounts of lactose leads to the
charides sucrose and lactose, are hydrolyzed by spe- passage of the sugar to the large bowel, where it is
cific oligosaccharidases expressed on the apical fermented to produce short-chain fatty acids (SCFAs)
membrane of the epithelial cells that populate the and gases as end-products. The appearance of hydro-
small intestinal villi. Sucrase–isomaltase is a glycopro- gen in the breath after ingestion of lactose is the basis
tein anchored via its amino-terminal domain in the for diagnosis of malabsorption of this carbohydrate.
apical membrane that hydrolyzes all of the sucrose Diseases of the intestinal tract, such as protein-energy
and most of the maltose and isomaltose. The resulting malnutrition, intestinal infections, and celiac disease,
monomeric sugars are then available for transport which reduce expression of lactase on the enterocyte
into the enterocytes. apical membrane, can result in secondary lactase
insufficiency. Sucrase–isomaltase activity, which rises
Absorption and malabsorption in rapidly from the pylorus towards the jejunum and
the small bowel then declines, is inducible by sucrose feeding. About
Glucose and galactose are transported across the 10% of Greenland Eskimos and 0.2% of North Amer-
apical membrane by the sodium–glucose transport icans have sucrase–isomaltase deficiency. A missense
76 Introduction to Human Nutrition

Glucose

Cellulose
and

1.0
0.8
1.1
1.1
0.1
0.2
0.8
Fructose galactose Na
Gut
lumen
NSPs

3.2
1.2
3.6
4.5
0.9
1.4
2.4
Oligosaccharides

Apical
membrane
1.7

0.8
1.4

0.4
Tr

Tr
0

Tight
Lactose

junction
1.7

1.8
Tr

Tr
0
0

0
Maltose


Fructose Glucose Na
Basolateral and
0.1

0.1
Tr
0

0
0

membrane galactose
Sucrose

ADP
K⫹

1.9
0.1
1.6
1.0
0.1
0.9
0.6

Pi
Galactose

ATP
0
0
0
0
0
0
0
Fructose

Glucose and
Fructose K⫹ Na⫹
1.7
0.1
1.4
0.1
0.2
0.6
0.4

Blood galactose
Glucose

1.9
0.1
1.3

0.2
0.6
0.5

GLUT5 GLUT2
Tr

NSPs, nonstarch polysaccharides (Englyst method; Englyst et al. 1999); Tr, trace.

Na⫹/K⫹-ATPase
Total sugars

SGLT1
Data from Holland et al. (1992). Reproduced with permission from HMSO.
Table 5.2 Carbohydrate composition (g/100 g) of some vegetable dishes

Figure 5.1 Sugar transporters on enterocytes, showing the transport


5.5
2.2
4.3
1.2
2.3
2.2
1.4

of glucose and galactose across the apical membrane.


Starch

0.4

7.9
10.4

18.7
16.4
23.0
14.0

mutation in SGLT1 is responsible for the very rare


Carbohydrate

glucose–galactose malabsorption syndrome, but such


individuals absorb fructose well. In up to 60% of
7.6
12.6
13.1
21.3
18.7
25.2
15.8

adults, the capacity for facilitated diffusion of fructose


appears to be limited, resulting in symptoms of
Water

“intestinal distress” when challenged by consumption


77.7
73.4
72.6
52.7
49.1
51.0
71.7

of 50 g fructose.
Flan, cheese and mushroom

Shepherd’s pie, vegetable

5.3 Glycemic carbohydrates


Pizza, cheese and tomato
Chili, beans and lentils
Cannelloni, spinach

The rate of uptake of glucose (and other sugars) from


Curry, chickpea

the gut is determined by the rate of hydrolysis of oli-


Bhaji, okra

gosaccharides and polysaccharides that are suscepti-


ble to pancreatic and brush border enzymes. In addi-
Dish

tion to the primary structure of the polymers, many


Digestion and Metabolism of Carbohydrates 77

factors intrinsic to the ingested foods and to the con- complete oxidation of glucose to carbon dioxide and
sumer influence these rates, including: water occurs under aerobic conditions through the
reactions of the glycolytic pathway (in the cell’s cyto-
● food factors
plasm), the Krebs cycle, and oxidative phosphoryla-
● particle size
tion (in the mitochondrion). The overall reaction can
● macrostructure and microstructure of food,
be summarized stoichiometrically as:
especially whether cell walls are intact
● amylose–amylopectin ratio of starches C6H12O6 + 6O2 → 6CO2 + 6H2O
● lipid content of food
Approximately 40% of the free energy (ΔG) released
● presence (or otherwise) of enzyme inhibitors
by this transformation is captured by the production
● consumer factors
of ATP (38 moles of ATP per mole of glucose oxi-
● degree of comminution in the mouth
dized), which is used for a wide variety of purposes,
● rate of gastric emptying
including powering muscle contraction, transporting
● small bowel transit time.
substances across membranes against a concentration
All three main sugars absorbed from the gut gradient, and synthesis of cell macromolecules. The
(glucose, galactose, and fructose) are transported via remainder of the free energy is released as heat.
the portal vein to the liver (glucose concentrations in When the demand for oxygen exceeds supply, as in
the portal vein after a meal can rise to almost 10 mM), muscle during intense exercise, anaerobic glycolysis
but only glucose appears in significant concentrations produces lactic acid as a major end-product. The rela-
in the peripheral circulation. Most of the galactose tive lack of oxygen means that oxidative phosphoryla-
and fructose is removed during first pass through the tion cannot keep up with the supply of reduced
liver via specific receptors on hepatocytes, so that the dinucleotides and, for glycolysis to proceed, NADH
blood concentration of these sugars rarely exceeds must be recycled back to NAD+. This is achieved by
1 mM. Within the hepatocytes, galactose is converted the reaction:
to galactose-1-phosphate by the enzyme galactoki-
Pyruvate + NADH + H+ → Lactate + NAD+
nase and then to glucose-1-phosphate in three further
steps. Fructose is also phosphorylated in hepatocytes which is catalyzed by the enzyme lactate dehydro-
(by fructokinase) to fructose-1-phosphate, which is genase. Anaerobic glycolysis provides some or all of
subsequently split by aldolase B to yield one molecule the ATP needs for some cells and tissues; for example,
of each of the glycolytic intermediates dihydroxyace- erythrocytes, white blood cells, lymphocytes, the
tone phosphate and glyceraldehyde. Although the kidney medulla, and eye tissues. The lactate released
liver removes some glucose, using the bidirectional from tissues undergoing anaerobic glycolysis is taken
transporter GLUT2, most is transported in the periph- up by other tissues that have a high number of mito-
eral circulation for utilization by muscle, adipose, and chondria per cell, such as heart muscle, in which the
other tissues. lactate is converted back to pyruvate and then enters
the Krebs cycle via acetyl coenzyme A.
Metabolic utilization of carbohydrate In hepatic and muscle cells some glucose is con-
Peripheral tissues utilize glucose and the above-men- verted to glycogen in the glycogenesis pathway. Gly-
tioned intermediates from fructose and galactose via cogen is a readily mobilized storage form of glucose
glycolysis and the citric acid or Krebs cycle pathways. residues linked with α-1,4-glycosidic bonds into a
Glycolysis, a sequence of reactions in which glucose large, branched polymer. Glycogen is a reservoir of
is converted to pyruvate, with concomitant produc- glucose for strenuous muscle activity and its synthesis
tion of ATP, is the prelude to the citric acid cycle and and degradation are important for the regulation of
electron transport chain, which together release the blood glucose concentrations.
energy contained in glucose. Under aerobic condi-
tions pyruvate enters mitochondria, where it is com- Regulation of blood glucose concentration
pletely oxidized to carbon dioxide and water. If the The exocrine pancreas (and other tissues) is primed
supply of oxygen is limited, as in actively contracting to expect a rise in blood glucose concentration by
muscle, pyruvate is converted to lactate. Therefore, peptide hormones such as gastric inhibitory peptide
78 Introduction to Human Nutrition

(GIP) that are secreted from enteroendocrine cells tions in T1DM requires the exogenous supply of
within the mucosa of the small bowel. As the glucose insulin by injection. Implanted insulin minipumps or
concentration in blood rises above 5 mM after a meal, pancreatic β-cells may offer alternative forms of treat-
these peptide hormones amplify the response of the ment in the future. Symptoms of type 1 diabetes
β-cells of the endocrine pancreas, resulting in the dis- include the presence of glucose in urine, passage of
charge of the hormone insulin from secretory gran- large volumes of urine, body weight loss, and, in
ules which fuse with the cell membrane. Insulin has extreme cases, ketosis (excess production of acetone,
several effects on metabolism, including facilitating acetoacetate, and β-hydroxybutyrate). Although there
the transport, by GLUT4, of glucose into adipocytes is good evidence of genetic predisposition to T2DM,
and muscle cells. expression of the disease is due mainly to lifestyle
In healthy people, blood glucose concentration (excess energy intakes and low physical activity),
(glycemia) is homeostatically controlled within a resulting in obesity, especially when the extra fat is
fairly narrow range. It seldom falls below about 5 mM, accumulated on the trunk. The early stages of T2DM
even after a prolonged fast, and returns to this value are characterized by insulin insensitivity/resistance,
within a couple of hours of a meal. In the absence of i.e., failure of the tissues to produce a normal response
uptake from the gut (the postabsorptive state), about to insulin release that can be seen as relatively wide
8 g glucose per hour is provided for those tissues with swings in blood glucose concentrations following a
an obligatory demand for glucose – namely, the brain, carbohydrate-containing meal. Raised blood glucose
red blood cells, mammary gland, and testis – by concentration sustained for several years is believed
breakdown of stores of glycogen in the liver and to be fundamental to the spectrum of complications,
muscle and by gluconeogenesis. The brain of an adult including macrovascular (atherosclerosis) and micro-
has a glucose requirement of about 120 g/day. The vascular diseases and problems with the kidneys
amount readily available in glycogen approximates (nephropathy), nerves (neuropathy), and eyes (reti-
190 g. In long periods of fasting and starvation glucose nopathy and cataract) experienced by diabetics.
must be formed from noncarbohydrate sources by a
process known as gluconeogenesis. Gluconeogenesis Dietary management of blood
occurs in the liver (responsible for about 90% of glucose concentration
gluconeogenesis) and kidney and is the synthesis of Glycemic index
glucose from a range of substrates including pyruvate, As an aid to the dietary management of blood glucose
lactate, glycerol, and amino acids. Amino acids are concentrations in diabetics, Jenkins and colleagues
derived by catabolism of the body’s proteins. All (1981) introduced the concept of the glycemic index
amino acids, with the exceptions of lysine and leucine, (GI), which provides a means of comparing quanti-
are glucogenic. Triacylglycerols (from adipose tissue) tatively the blood glucose responses (determined
are catabolized to release glycerol. These gluconeo- directly by in vivo experiments) following ingestion
genic processes are triggered by a fall in blood glucose of equivalent amounts of digestible carbohydrate
concentration below about 5 mM and are signaled to from different foods. When a range of carbohydrate-
the tissues by the secretion of glucagon and the glu- containing foods was ranked according to their GI
cocorticoid hormones. values, there was a strong linear relationship with the
rapidly available glucose (RAG) from similar foods
Diabetes and its consequences determined in vitro as the sum of free glucose, glucose
Diabetes may be diagnosed as an exaggerated response from sucrose, and glucose released from starches over
in blood glucose concentration following ingestion of a 20 minute period of hydrolysis with a battery of
a fixed amount of glucose (glucose tolerance test). enzymes under strictly controlled conditions (Englyst
The most common forms of diabetes are type 1 dia- method; Englyst et al. 1999). This offers the possibil-
betes (T1DM) and type 2 diabetes (T2DM). T1DM ity of assaying foods in vitro for their RAG content,
results from the autoimmune destruction of the β- which will be quicker and cheaper than the current
cells of the endocrine pancreas (possibly following approach based on GI measurements in vivo.
viral exposure), the consequence of which is insulin Studies with glucose and starches enriched with
insufficiency. Control of blood glucose concentra- the stable isotope carbon-13 have demonstrated that
Digestion and Metabolism of Carbohydrates 79

glucose absorption from the gut following a meal con- 0.08


tinues for several hours after blood concentrations

Breath 13CO2 enrichment


(atoms percent excess)
have returned to fasting levels. In this later postpran-
0.06
dial period, insulin secretion is sufficient to ensure
that the rate of glucose absorption is matched by the
rate of glucose removal from the circulation. 13C- 0.04
Labeled substrates are being used increasingly to
investigate the kinetics of digestion, absorption, and [13C]-fructose-labeled meal
0.02
metabolic disposal of glucose and other sugars from a [13C]-glucose-labeled meal
range of foods. When continued over several years,
high rates of glucose absorption and the subsequent
challenge to the capacity of the pancreatic β-cells to 0 100 200 300 400
secrete insulin may be the primary determinants of Time after consumption of test meals (min)
insulin resistance and eventual pancreatic failure that Figure 5.2 Enrichment of breath 13CO2 following ingestion of high-
contribute strongly to the etiology of diabetes and sucrose test meals labeled with [13C]-fructose and [13C]-glucose.
cardiovascular disease. Such kinetic studies are likely (Redrawn from Daly et al., 2000, with permission of the American
Society for Nutrition.)
to be helpful in identifying foods with slower rates of
intestinal hydrolysis – information that can be used in
public health advice or in counseling of individuals. metabolism” to the body. They called these carbohy-
drates “unavailable.” This was a very useful concept
Fructose because it drew attention to the fact that some carbo-
When glucose and fructose are available simultane- hydrate is not digested and absorbed in the small
ously after a meal containing sucrose, how does the intestine, but rather reaches the large bowel where it
body select which fuel to use first for oxidative is fermented. However, it is now realized that it is
purposes? This question has been resolved by experi- misleading to talk of carbohydrate as unavailable
ments in which volunteers consumed, on two sepa- because some indigestible carbohydrate can provide
rate occasions, high-sucrose test meals which were the body with energy through fermentation in the
identical except that one or other of the constituent colon. Thus, “unavailable carbohydrates” are not
monomeric sugars was 13C-labeled in each meal. The really unavailable. For this reason, it has been sug-
volunteers blew into tubes at intervals after the meals gested by the Food and Agriculture Organization
to provide breath samples for measurement of enrich- (FAO 1998) of the United Nations and World Health
ment of expired carbon dioxide with 13C. The results Organization that the term “nonglycemic carbohy-
showed that, after the high sucrose meal, fructose was drates” is more appropriate.
oxidized much more rapidly and extensively than was
glucose (Figure 5.2). Nature of carbohydrates that enter
This rapid oxidation of fructose may be explained the colon
by the fact that, because it is phosphorylated in hepa- Carbohydrates that enter the colon can be classified
tocytes, it bypasses 6-phosphofructokinase, one of the either physiologically or chemically. Neither of these
key regulatory enzymes in glycolysis. classifications is entirely satisfactory because it is dif-
ficult to measure the physiologically indigestible car-
5.4 Nonglycemic carbohydrates bohydrate and this varies in different people. Further,
the chemical structure of carbohydrates does not
Carbohydrates that are not absorbed in the small always predict their physiological behavior.
intestine enter the large bowel, where they are par-
tially or completely broken down by bacteria in the Physiological classification of
colon by a process called fermentation. McCance and carbohydrates entering the colon
Lawrence in 1929 were the first to classify carbohy- Carbohydrates enter the colon because (1) monosac-
drates as “available” and “unavailable.” They realized charide transporters do not exist in the intestinal
that not all carbohydrates provide “carbohydrates for mucosa or do not function at a high enough rate; (2)
80 Introduction to Human Nutrition

the enzymes needed to digest the carbohydrates are Finally, there are many reasons why carbohydrates
not present in the small intestine; (3) the enzymes are may not be digested rapidly enough to be completely
present but cannot gain access to the carbohydrates; absorbed. Some forms of retrograded or resistant
or (4) the enzymes do not digest the carbohydrates starch, or foods with a large particle size, are digested
rapidly enough for them to be completely absorbed. so slowly that the time spent in the small intestine is
In addition, a small amount of carbohydrate entering not long enough for their complete digestion. Diges-
the colon consists of carbohydrate residues occurring tion of these carbohydrates can be altered by factors
on mucopolysaccharides (mucus) secreted by the that affect transit time. The presence of osmotically
small and large intestinal mucosal cells. active and unabsorbed molecules (such as unabsorbed
Some carbohydrates are always nonglycemic sugars) will draw water into the intestine and speed
because the human species lacks the enzymes neces- the rate of transit. Substances that increase bulk, such
sary for their digestion. However, a significant pro- as wheat bran, will have similar effects. Transit rate is
portion (perhaps up to half ) of all carbohydrates that slowed in old age and in the presence of viscous fibers.
escape digestion in the small intestine have a chemical Drugs may increase or decrease the rate of transit.
structure which is such that they could potentially be Certain disorders can also affect transit time, such as
digested or absorbed in the small intestine, but they gastroparesis, a complication of type I diabetes.
are variably absorbed for various reasons, examples
of which are given below. Chemical classification of carbohydrates
First, some monosaccharides and sugar alcohols entering the colon
are only partially absorbed because of low affinity for The chemical classification of carbohydrates entering
intestinal transporters. Xylose is taken up by the the colon is as follows:
glucose transporter, but is only partly absorbed
because of a low affinity. Fructose is poorly absorbed ● Monosaccharides: all except for glucose, fructose,
on its own, but readily absorbed in the presence of and galactose are partly or completely unabsorbed.
glucose. The surface area of the small intestine avail- Fructose in the absence of a source of glucose
able for absorption is reduced by diseases that cause (mono-, di-, or polysaccharide) is partly
atrophy of the intestinal mucosa, such as tropical unabsorbed.
sprue or celiac disease, or surgical resection of a ● Sugar alcohols: all are partly or completely
portion of the intestine (e.g., for Crohn’s disease). An unabsorbed.
increased rate of intestinal transit (e.g., high osmotic ● Disaccharides: all except for maltose, sucrose, and
load in the small intestinal lumen from undigested lactose are unabsorbed. Lactose is completely or
sugars) reduces the time available for absorption to partly unabsorbed in individuals with low intestinal
occur. lactase activity.
Second, some individuals have a low or absent ● Oligosaccharides: all are unabsorbed except for
intestinal lactase activity; thus, lactose is partly or maltodextins.
completely nonabsorbed in these individuals. The ● Polysaccharides: all nonstarch polysaccharides are
availability of pancreatic amylase may be reduced in unabsorbed.
cystic fibrosis or in individuals whose pancreatic ● Resistant starch.
mass has been destroyed by, for example, recurrent
pancreatitis. Amount of carbohydrate entering
Third, although starch (amylopectin or amylose) is the colon
potentially digested in the small intestine, if it is It is difficult to measure the amount of carbohydrate
trapped inside intact cell walls or other plant cell entering the human colon. However, it has been esti-
structures, intestinal enzymes may not be able to gain mated that at least 30 g of carbohydrate is required to
access to it, and therefore it remains undigested. The support the growth of the bacterial population in the
digestibility of the carbohydrates in banana depends colon of an individual on a typical Western diet pro-
on the degree of ripeness. The starch in green banana ducing about 100 g stool per day. About half of that
is very indigestible, but, as the banana ripens, the amount will come from nonstarch polysaccharide
starch is converted to digestible sugars. (NSP, also known as dietary fiber), 1–2 g from indi-
Digestion and Metabolism of Carbohydrates 81

gestible oligosaccharides, and probably about 1–2 g colon could be sampled. Another method was to
from intestinal mucopolysaccharides. These compo- study people who have had their colons removed sur-
nents add up to only 18–20 g. Where does the other gically and in whom the end of the ileum was sutured
10–12 g come from? It is believed to come from starch, to a stoma in the body wall. In this way, the material
because experiments in humans show that about 5– leaving their small intestine could be collected quan-
15% of the starch in foods enters the colon. Typical titatively in a bag attached to their abdomen. With
Western diets contain about 120–150 g starch per day, these methods, the amount of carbohydrate leaving
and, if 8% of this enters the colon, this will provide the small intestine can be measured directly. These
the additional 10–12 g carbohydrate. The amount of methods confirmed that a substantial amount of
carbohydrate entering the colon, however, can be starch enters the colon.
increased several-fold, up to 100 g/day or more, by The main forms of resistant starch (RS) are physi-
changes in diet such as increased intake of NSP, cally enclosed starch, for example within intact cell
non-digestible or partially digestible carbohydrates structures (known at RS1); raw starch granules (RS2);
(ingredients in functional foods), total starch, resis- and retrograded amylose (RS3). These kinds of starch
tant starch, or slowly digested, low-GI foods. can be identified chemically using methods developed
by Englyst and colleagues (Englyst et al. 1996).
Resistant starch
Resistant starch is starch that escapes digestion in the Dietary fiber
small intestine and enters the colon. However, there Major interest in dietary fiber began in the early 1970s
is controversy over the amounts of resistant starch in with the proposal by Burkitt and Trowell (1975) that
foods because there is no universally accepted method many Western diseases were due to a lack of fiber in
for measuring it (different methods yield different the diet. However, the definition of dietary fiber has
results). The amount of resistant starch measured been, and continues to be, a source of scientific con-
chemically is generally less than that observed to enter troversy. Indeed, two consecutive reports from the
the colon (or leave the small intestine) in experiments FAO (1997 and 1998) recommended that the term
in human volunteers. “dietary fiber” be phased out. Nevertheless, the term
In the 1970s and early 1980s it first became appar- appears to be here to stay because it is accepted by
ent that appreciable amounts of starch are not digested consumers, the food industry, and governments.
in the small bowel, from experiments showing that A definition and method of measuring fiber is
breath hydrogen increased after eating normal starchy important for scientific studies and for food-labeling
foods. The only source of hydrogen gas in the human purposes. The student must be aware that the defini-
body is as a product of the anaerobic fermentation of tions and methods of measuring fiber have changed
carbohydrates by colonic bacteria (see below). If a over time, and differ in different parts of the world.
person consumed a load of an absorbable sugar such Knowledge of what is meant by the term “fiber” and
as glucose, breath hydrogen did not go up. In contrast, what is included in the measurement is essential for
if lactulose (an unabsorbed disaccharide of fructose proper interpretation of the scientific literature (but
and galactose) was consumed, breath hydrogen often is not given in the methods section of papers
increased rapidly, and the area under the breath and reports).
hydrogen curve over an 8–12 hour period was directly Originally, Burkitt and Trowell (1975) defined fiber
proportional to the amount of lactulose consumed. If as the components of plant cell walls that are indigest-
subjects ate common starchy foods such as white ible in the human small intestine. Later, the definition
bread or potato, breath hydrogen levels increased to was expanded to include storage polysaccharides
an extent that suggested that 5–10% of the starch was within plant cells (e.g., the gums in some legumes).
fermented in the colon. Subsequently, other ways of Many different methods were developed to measure
measuring carbohydrate entering the colon were dietary fiber, but they measured different things. All
developed. In one technique, subjects swallowed a of the methods start with the drying and grinding of
tube that was passed through the stomach and along the food and extraction of the fat using an organic
to the end of the small intestine so that the material solvent. If the remaining material is treated with
leaving the small intestine and about to enter the strong acid, the chemical bonds in starch and many
82 Introduction to Human Nutrition

(but not all) polysaccharides will be broken down to artificial, that could be classified as “fiber” (e.g., poly-
release their component sugars. If these are filtered dextrose, sucrose polyester, styrofoam). Should these
away, the residue is “crude fiber.” For many years this be included in dietary fiber? In favor of this is the
was the way in which fiber was measured for food argument that some of these materials have physio-
tables. However, acid hydrolysis breaks down many logical properties associated with fiber, such as stool
carbohydrates that would not be digested in the small bulking, or effects on satiety or blood glucose and
intestine. So, in more modern methods, the food cholesterol. Against this is the feeling that dietary fiber
residue is digested with amylase to hydrolyze the should include only plant materials that are normally
starch to soluble sugars and oligosaccharides. The present in the diet. These are not easy issues and they
latter are removed by filtration or by centrifugation have not been resolved.
to leave a residue containing mainly dietary fiber, pro-
teins, and inorganic materials. Intakes of dietary fiber, oligosaccharides,
The two main methods used to determine dietary and other indigestible sugars
fiber are chemical and gravimetric. In the chemical Vegetarians tend to have higher fiber intakes than
method (used in the UK), the residue is subjected to omnivores. The typical intake of dietary fiber in North
acid hydrolysis and the resultant sugars are measured America and northern and central Europe is about
colorimetrically, by gas chromatography or by high- 15 g/day. In Scandinavia and Italy, fiber consumption
performance liquid chromatography. The sum of all is 20–30 g/day, whereas in African countries such as
these sugars constitutes the NSP. The chemical method Uganda, Kenya, Malawi, and Nigeria intakes may be
includes only carbohydrates in the NSP. In the gravi- as high as 50 g/day or more. Naturally occurring
metric method (used in the USA and elsewhere), the oligosaccharides are consumed in legumes, onions,
residue is dried and weighed, and the amounts of fennel, chicory, and similar foods. Intakes in Western
protein and mineral materials present are subtracted countries are probably up to 2–4 g/day. Fructo- and
(after separate analyses). The gravimetric method galactooligosaccharides are now being added to
includes the NSP, plus other noncarbohydrate com- certain “functional foods” in a number of countries,
ponents such as lignin and waxes. Recently, all coun- and intakes from such sources may increase substan-
tries in Europe have recognized the gravimetric tially (up to 10–20 g/day). Many kinds of indigestible
method as an approved method for measuring fiber or partially digested carbohydrates are entering the
in foods. food supply in dietetic, diabetic, or functional foods,
The main areas of disagreement now with respect including sugar alcohols (polyols, e.g., sorbitol, man-
to fiber are whether indigestible oligosaccharides and nitol, lactitol), polydextrose, resistant starch, hydroge-
sugars and nonplant compounds should be included nated starch, and other chemically modified starches
and whether the definition of fiber should include and carbohydrates. Thus, the total amount of carbo-
a physiological component. In Japan, fructooligo- hydrate entering the colon could become very sub-
saccharides (FOSs) are classified as dietary fiber for stantial for people using these foods. Individually,
food-labeling purposes. However, FOSs and similar these ingredients are generally recognized as safe, and
compounds, being soluble in water, are not included evidence from populations consuming 50 g and more
in the dietary fiber methods, because they are filtered NSP per day suggests that the colon has the capacity
out along with the sugars resulting from the starch to adapt to large increases in the load of carbohydrate.
hydrolysis. Specific methods exist for FOSs and related However, safe upper limits of intake are unknown and
compounds, and they could be included as fiber. the health implications of an increased supply of a
Certain animal-derived compounds, such as chitin wide range of carbohydrates to the colon are currently
and chitosan, derived from the shells of shrimp and based on inference rather than scientific data.
crabs, are indigestible, would be included in the gravi-
metric fiber analysis, and could be classified as fiber. Fermentation in the colon
Chitin has some physiological properties, such as The colon contains a complex ecosystem consisting of
cholesterol lowering, which are associated with dietary over 400 known species of bacteria that exist in a sym-
fiber. There are many other indigestible carbohydrate biotic relationship with the host. The bacteria obtain
and noncarbohydrate compounds, both natural and the substrates that they require for growth from the
Digestion and Metabolism of Carbohydrates 83

host, and return to the host the by-products of their The first step in fermentation is the breakdown of
metabolism. The major substrate that the bacteria polysaccharides, oligosaccharides, and disaccharides
receive from the host is carbohydrate, mostly in the to their monosaccharide subunits. This is achieved
form of polysaccharides. They obtain nitrogen from either by the secretion of hydrolytic enzymes by bac-
urea (which diffuses into the colon from the blood) teria into the colonic lumen or, more commonly, by
and undigested amino acids and proteins.Fermentation expression of such enzymes on the bacterial surface
is the process by which microorganisms break down so that the products of hydrolysis are taken up directly
monosaccharides and amino acids to derive energy for by the organism producing the enzyme. To degrade
their own metabolism. Fermentation reactions do not the NSP of dietary fiber, the bacteria may need to
involve respiratory chains that use molecular oxygen attach themselves to the surface of the remnants of
or nitrate as terminal electron acceptors. Most of the the plant cell walls or other particulate material.
fermentation in the human colon is anaerobic, i.e., it Once the monosaccharide is internalized, the
proceeds in the absence of a source of oxygen. Different majority of carbohydrate-fermenting species in the
bacteria use different substrates via different types colon use the glycolytic pathway to metabolize carbo-
of chemical reaction. However, as a summary of the hydrate to pyruvate. This pathway results in the
overall process, fermentation converts carbohydrates reduction of NAD+ to NADH. Fermentation reactions
to energy, plus various end-products, which include are controlled by the need to maintain redox balance
the gases carbon dioxide, hydrogen, and methane, and between reduced and oxidized forms of pyridine
the SCFAs acetic (C2), propionic (C3), and butyric nucleotides. The regeneration of NAD+ may be
(C4) acids. Acetate, propionate, and butyrate appear achieved in a number of different ways (Figure 5.4).
in colonic contents in approximate molar ratios of Electron sink products such as ethanol, lactate,
60:20:20, respectively. Most of the SCFAs produced are hydrogen, and succinate are produced by some
absorbed and provide energy for the body (Figure bacteria to regenerate oxidized pyridine nucleotides.
5.3). These fermentation intermediates are subsequently
The roles of SCFAs in metabolism are discussed fermented to SCFAs by other gut bacteria, and are
later in this chapter. Formic acid (C1) and minor important factors in maintaining species diversity in
amounts of longer chain SCFAs and branched-chain the ecosystem.
SCFAs may also be produced. In addition, lactic
and succinic acids and ethanol or methanol may be Fate of short-chain fatty acids
intermediate or end-products depending on the Colonic fermentation can be viewed as a way in which
conditions of the fermentation. For example, rapid the human host can recover part of the energy of
fermentation in an environment with a low pH results malabsorbed carbohydrates. The amount of energy
in the accumulation of lactic and succinic acids. recovered from fermentation depends on the fer-
mentability of the carbohydrate (which can range
from 0% to 100%) and the nature of the products of
Carbohydrate fermentation. On a typical Western diet, about 40–
50% of the energy in carbohydrate that enters the
colon is available to the human host as SCFAs. The
Pyruvate rest of the energy is unavailable to the host, being lost
as heat or unfermented carbohydrate or used to
CO2 produce gases or for bacterial growth (Figure 5.5).
60% Acetate
20% Propionate H2 SCFAs are almost completely absorbed and, while
20% Butyrate CH4 some butyrate is oxidized by colonocytes (the epithe-
lial cells lining the colon), most arrives at the liver via
the portal vein. Propionate and butyrate are removed
Absorbed
Feces
Breath in first pass through the liver, but increased concen-
and utilized Flatus trations of acetate can be observed in peripheral
Figure 5.3 Overview of carbohydrate fermentation in the human blood several hours after consumption of indigestible
colon. but fermentable carbohydrates. These absorbed
84 Introduction to Human Nutrition

Hexose
NAD+ H2 CO2

NADH2 H+ CH4
2 ATP

ATP

Lactate Pyruvate Succinate

NAD+ Biotin
NAD+ NADH2
NADH2
Biotin CO2
Ethanol Acetyl CoA

Propionate
Figure 5.4 Summary of biochemical
ATP pathways used by the anaerobic
ATP
bacteria in the colon. Acetyl CoA, acetyl
Acetate Butyrate coenzyme A.

Carbohydrate
entering the colon the ability of butyrate to induce differentiation and
(17.2kJ/g) apoptosis (programmed cell death) of colon cancer
cells. There is some support for the hypothesis that
propionate may help to reduce the risk of cardiovas-
cular disease by lowering blood cholesterol concen-
H2 and CH4 tration and/or by an effect on hemostasis, but the
(0.6kJ/g)
Colon
SCFA evidence so far is not conclusive.
(7.2kJ/g)
Heat
(0.6kJ/g)
5.5 Carbohydrates and dental caries
The resident bacteria in the mouth ferment carbohy-
drates to yield acidic end-products (mainly lactic acid
Unfermented Bacterial but also some formic, acetic, and propionic acids),
carbohydrate matter
(5.2kJ/g) (3.6kJ/g) which result in a drop in dental plaque pH. When the
pH falls below 5.5, the dental enamel dissolves in the
plaque fluid and repeated exposure to periods of very
low pH can lead to caries. Not all carbohydrates are
Feces equally cariogenic. The sugars found commonly in
(8.8kJ/g) human foods, e.g., sucrose, fructose, glucose, and
Figure 5.5 Quantitative fate of carbohydrate in the colon. SCFA, maltose, are all readily fermented by bacteria in the
short-chain fatty acid. mouth. Lactose, galactose, and starches are less cario-
genic, while sugar alcohols such as xylitol (used as a
SCFAs are readily oxidized and contribute modestly sweetener in some confectionery and chewing gums)
(up to 10%) to the body’s energy supply. are noncariogenic. Eating sugars with meals reduces
There is considerable interest in the possible effects the risk of caries, as does the consumption of cheese,
of individual SCFAs on the health of the colon and which provides phosphates to prevent demineraliza-
the whole body. The strongest evidence to date is for tion and to encourage demineralization of the enamel.
an anticancer effect of butyrate, which may be due to Fluoride ingestion in foods and drinking water or
Digestion and Metabolism of Carbohydrates 85

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