Perspective in Nutrition

The contribution of the large intestine to energy

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supplies in man1’2
NI McNeil, MD, MRCP

ABSTRACT Herbivores obtain a considerable proportion of energy requirements from

carbohydrate by the chain of anaerobic carbohydrate fermentation producing short-chain fatty
acids that are absorbed then metabolized. The evidence for this sequence occurring in the large
intestine of man is reviewed and estimated to produce 5 to 10% of human energy requirements.
Further small amounts of energy may come from large intestinal absorption of fat and the
bacterial breakdown products ofprotein. Am J Clin Nuir l984;39:338-342.

KEY WORDS Intestinal absorption, short-chain fatty acids, dietary fiber, large intestine

Introduction down and the subsequent absorption of the

products produced. Fermentation and the
The symbiosis between animals and their absorption of end products, the short-chain
intestinal microflora works to the benefit of fatty acids acetic, propionic, and butyric
both. The microflora is able to obtain only acid, have been well established for the
a fraction of the energy present in food by forestomach of ruminants where the many
fermentation and provides end products, complex steps have been carefully identified
principally short-chain fatty acids, that can
(1). Short-chain fatty acids provide 60 to
be absorbed by the host animal who is then
85% of metabohizable energy for sheep (2).
able to metabolize them fully. The impor-
The large intestine is also a site of fermen-
tance ofthis interrelationship is most appar-
tation in ruminants and is responsible for
ent in the ruminant, but is also well known
up to 13% of the animal’s total short-chain
for many other mammals, where the large
intestine is the site of bacterial metabolism. fatty acid production (3, 4). In nonruminant
In man, the energy provided by absorption herbivores, conditions in the large intestine
in the large intestine of short-chain fatty are similar to those found in the rumen and
acids and other nutrients has only recently it is known that a considerable proportion
been considered. of the energy supply is provided by short-
chain fatty acid production and absorption.
Role of short-chain fatty acids in animals For example, the cecum alone contributes
30 to 40% of energy requirements of the
In herbivorous animals simple sugars and
I From the Department ofMedicine, University Col-
starch as well as structural carbohydrates, lege London Medical School, Rayne Institute, London,
such as cellulose, are used as an energy England.
source by the animal. The small intestine is 2 Address reprint requests to: Dr NI McNeil, De-
the site ofdigestion and absorption of starch partment of Medicine, University College London
Medical School, Rayne Institute, University Street,
and mono- and disaccharides. The energy London WC1 E 6JJ, England.
contained in the structural carbohydrates of ReceivedMay2, 1983.
plants is made available by bacterial break- Accepted for publication August 23, 1983.

338 The American Journal ofClinical Nutrition 39: FEBRUARY 1984, pp 338-342. Printed in U.S.A.
© 1984 American Society for Clinical Nutrition
 HUMAN COLONIC CONTRIBUTION TO ENERGY 339

rabbit and pony (5, 6). The pig is frequently were not absorbed from the large intestine.
used as a model for the human. In this Absorption from a mixture of short-chain
omnivore, it has been shown that 0.7 to 0.8 fatty acids was measured using a dialysis bag
mol of short-chain fatty acid are absorbed method (1 5) and rapid absorption of ace-
daily yielding 10% of maintenance energy tate, propionate, and butyrate was found
requirements (7). (16, 17). The rates found in man, 6 to 12
tmol/cm2/h (1 5-18), were similar to those
Man--background found in the large intestine of the pig, 8 to

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10 tmol/cm2/h ( 19), pony, 8 tmol/cm2/h
However, in man it has been considered (20), and rumen epithehium 10.5 zmoh/cm2/
for many years that short-chain fatty acids h (2 1). Using a perfusion method, with pro-
are absorbed poorly if at all (8, 9) and the pionate as the principal short-chain fatty
carbohydrates remaining in the gut produce acid studied, Ruppin et al (22) confirmed
diarrhea because of their osmotic properties human large intestinal absorption of short-
and the net fluid secretion stimulated by chain fatty acids. In these studies short-chain
products of bacterial fermentation (10). The fatty acid absorption considerably exceeded
role of the large intestine as a potential en- sodium absorption, by 70 to 250%, from
ergy source in man has been discounted, all equimolar solutions (16, 22). The rate of
material passing the terminal ileum being absorption was linearly related to initial con-
considered as lost. Recently evidence has centration and no difference has been found
been accumulating suggesting a place for the between rates of absorption of acetate, pro-
human large intestine in energy conserva- pionate, or butyrate (22, 23). The mecha-
tion, the principal mechanism being the ab- nisms involved remain unclear but it seems
sorption of short-chain fatty acids produced likely that absorption of the ionized form
by anaerobic bacterial metabolism of car- related to sodium absorption as well as in-
bohydrate. dependent absorption of the unionized
moiety occurs with luminal accumulation of
Short-chain fatty acid production bicarbonate. Furthermore, short-chain fatty
Short-chain fatty acid concentrations rise acids may enhance sodium absorption (22).
during the passage of intestinal contents
through the large intestine from less than 4 Amount of carbohydrate fermented
mM in the terminal ileum (1 1) to 80 to 90
mM in fecal fluid (12, 1 3) where they con- The total amount ofshort-chain fatty acid
stitute the major anion component. Fecal produced each day in the large intestine is
loss amounts to 7 to 20 mmol daily in British unknown, but fecal output is likely to be
subjects ( 1 3). It is likely that short-chain only a small proportion. Substrates for an-
fatty acids are generated from carbohydrate aerobic degradation are dietary fiber and
by a series of pathways similar to those unabsorbed sugars and starch, as well as
found in the rumen (14) (Fig 1). Starch, mucus pohysaccharide. The quantity of pro-
cellulose, and hemicelluhose are degraded by tein entering the large intestine is likely to
extracelluhar bacterial enzymes to hexoses be small although deaminated carbon skel-
and pentoses whose further metabolism oc- etons of amino acids may be further metab-
curs inside bacteria. Subsequent metabolism ohized by the same processes as carbohy-
via glycolysis or the pentose phosphate path- drates. Dietary fiber intake in the United
way provides pyruvate which is rapidly Kingdom is on average 20 g daily (24). Half
changed to the end products of the short- to three-quarters of this is broken down in
chain fatty acids, hydrogen, carbon dioxide transit through the gastrointestinal tract
and, in some people, methane. (25), almost entirely in the large intestine.
The amount of sugar and starch passing the
Shod-chain fatty acid absorption in man terminal ileum is more difficult to deter-
mine. Six g/day ofsugar and starch has been
Man would be a unique member of the found in ileostomy effluent (26), but this is
animal kingdom if short-chain fatty acids likely to be an underestimate of normal ileal
340 McNEIL

ENTERS LARGE
Starch Cellulose Hemicellulose
INTESTI

NETABOLIZED BY
Hexose
I
Pentose
.
BACTERIA FOR Glycolysis Pentose pathway
BACTERIAL GROWTH
“Pyruvate’

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END PRODUCTS Acetate Hydnxjen
Propionate thane
Butyrate Carbon dioxide
.
FATE Absorbed by Fecal loss Lost in breath after
large intestine absorption
and metabolised
FIG 1 . Stages in the breakdown and assimilation ofcarbohydrate in the human large intestine.

loss because of intestinal adaptation. Ter- Energy obtained from the large intestine
minal ileal intubation for recovery of unab-
sorbed starch showed small intestinal mal- The fermentation of 50 to 60 g of carbo-
absorption of9.3 and 6% ofthe starch from hydrate daily will yield 500 to 600 mmol
single meals containing 20 or 60 g (27). short-chain fatty acids, with a total energy
Several indirect methods have been used to value of 600 to 750 Id. This represents ap-
proximately 75% ofthe original energy con-
estimate the amount of carbohydrate that
tent ofthe carbohydrate: the remaining 25%
enters the large intestine. Anderson et al (28)
is used by the microflora for growth or host
estimated that 10 to 20% of a meal of white
as gas (hydrogen and methane). As fecal
bread reached the right colon, basing the
output of short-chain fatty acids is only 7 to
calculation on quantitative breath hydrogen 20 mmol (12), almost all this must be ab-
production. sorbed contributing 6 to 9% of energy re-
A second indirect method of calculating quirements. Established ileostomists have
cohonic short-chain fatty acid production is been shown to weigh 4 kg less than age- and
based on the growth requirements of intes- height-matched controls (26) with similar
tinal bacteria. Approximately 0. 1 mol aden- energy intake (33); the loss of both the large
osine triphosphate (ATP) is needed to gen- intestine and the ability to conserve energy
erate I g (dry weight) of bacteria (29). Feces may be a major factor contributing to this
from people on a British diet contain, on difference. Malabsorption or diets high in
the average, 15 to 20 g bacteria (dry) (30) fiber are likely to increase the amount of
and so 1.5 to 2.0 mol ATP is needed to carbohydrate entering the colon. Although
replace the daily fecal output of bacteria in lactose mahabsorption 40 to 75% of a
(3 1 ). As 1 mol hexose yields 5 mol ATP lactose load passes the iheocecal valve, only
4 to 10% leaves in any form in the feces, the
when metabolized anaerobically, then 50 to
difference becoming available for metabo-
65 g hexose are required to produce 1.5 to 2
lism (34): similar events occur after jejuno-
mol AlP. Ofthis 50 to 65 g hexose 1 5 g will
ileal bypass (35). Dietary fiber intakes in
be dietary fiber, the rest will be 35 to 50 g Africa are up to seven times higher than in
sugars and starch that fail to be digested and the United Kingdom (36). The amount of
assimilated in the small intestine. This is 10 fiber and other carbohydrate in the stool is
to 15% of dietary sugar and starch (32). unknown, but it is likely that a substantial
Carbohydrate from mucus will contribute a proportion of the fiber will be metabolized
small part in addition. to short-chain fatty acids, and for these peo-
 HUMAN COLONIC CONTRIBUTION TO ENERGY 341

plc the energy made available is likely to be the sheep caecum. Aust J Agric Res 1969:20:491-
8.
proportionately higher.
4. Allo AA, Oh JH, Longhurst WM, Connolly GE.
The amount of protein and fat entering VFA production in the digestive systems of deer
the large intestine is unknown. Protein is and sheep. J Wildl Mgmt 1973;37:202-l I.
likely to be used by bacteria for growth or 5. Parker DS. The measurement of production rates
deaminated to a carbon skeleton and am- ofvolatile fatty acids in the caecum ofthe conscious
rabbit. Br J Nutr I 976:36:61-7.
monia, and to provide little or no absorbable
6. Glinsky MJ, Smith RM, Spires HP, Davies CL.
energy. Fat has a high calorific value and Measurement of volatile fatty acid production rates

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any fat absorbed will be proportionately in the cecum of the pony. J Anim Sci
more important. In normal subjects long- 1976;42: 1465-70.
chain fatty acids will be trapped in the lumen 7. Imoto 5, Namioka S. VFA production in the pig
large intestine. J Anim Sci 1978;47:467-78.
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may be absorbed by the colon: fat globules 1936; 10:717-27.
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38.
Conclusion 1 1. Newton CR, Bennett AN, Billings JA, Milton-
Thompson GJ. Ileal short chain fatty acid concen-
In conclusion, all that enters the large trations after a chemically defined diet. Arch Mal
intestine is not lost. Perhaps 10 to 15% of Appar Dig 1972;6l:37C(abstr).
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The organic anion component. Clin Sci
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