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Prebiotics may be considered as functional food ingredients. They are attracting considerable interest from pet owners, pet food manufacturers, livestock producers and feed manufacturers. The most common forms of prebiotics are nondigestible oligosaccharides (NDO), including inulin, oligofructose mannanoligosaccharides, gluco-oligosaccharides, and galacto-oligosaccharides. These NDO are nondigestible by enzymes present in the mammalian small intestine, but are fermented by bacteria present in the hindgut of nonruminants. Inulin and oligofructose are present in measurable quantities in feed ingredients like wheat, wheat by-products, barley, and peanut hulls. Consumption of prebiotic oligosaccharides elicits several purported health benefits. In companion animals, prebiotics have been shown to improve gut microbial ecology and enhance stool quality. In production livestock and poultry, prebiotics are employed to control pathogenic bacteria, reduce faecal odour, and enhance growth performance. Research to date indicates positive effects of prebiotics on health status and performance of companion animals, livestock, and poultry.
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Pet food and feed applications of inulin, oligofructose and other
oligosaccharides
E. A. Flickinger and G. C. Fahey Jr*
Department of Animal Sciences, University of Illinois, 132 Animal Sciences Laboratory, 1207 W. Gregory Drive,
Urbana, IL 61801, USA
Prebiotics may be considered as functional food ingredients. They are attracting considerable
interest from pet owners, pet food manufacturers, livestock producers and feed manufacturers.
The most common forms of prebiotics are nondigestible oligosaccharides (NDO), including
inulin, oligofructose mannanoligosaccharides, gluco-oligosaccharides, and galacto-oligosac-
charides. These NDO are nondigestible by enzymes present in the mammalian small intestine,
but are fermented by bacteria present in the hindgut of nonruminants. Inulin and oligofructose
are present in measurable quantities in feed ingredients like wheat, wheat by-products, barley,
and peanut hulls. Consumption of prebiotic oligosaccharides elicits several purported health
benefits. In companion animals, prebiotics have been shown to improve gut microbial ecology
and enhance stool quality. In production livestock and poultry, prebiotics are employed to con-
trol pathogenic bacteria, reduce faecal odour, and enhance growth performance. Research to
date indicates positive effects of prebiotics on health status and performance of companion ani-
mals, livestock, and poultry.
Prebiotics: Fructans: Animal nutrition
Introduction
There currently exists much interest in the use of prebiotics
for companion animals, livestock, and poultry as modu-
lators of colonic bacterial populations and fermentation
end-products. Prebiotics are nondigestible food ingredients
that positively affect the host by selectively stimulating the
activity of a limited number of beneficial colonic bacteria,
resulting in improved host health (Gibson & Roberfroid,
1995). Inulin and oligofructose are perhaps the most well
studied prebiotics (for a description of these products see
Roberfroid, 2002).
Concentrations of inulin and oligofructose in pet food
and feed ingredients
Hussein et al. (1998) selected twenty-five common ingredi-
ents and analysed them for oligofructose concentrations
(Table 1). In this study, the concentrations of three major
subcomponents of oligofructose (1-kestotriose, 1,1-kesto-
tetraose, and 1,1,1 kestopentaose) were assayed via anion
exchange HPLC. No oligofructose was detected in corn,
corn distiller’s solubles, hominy, milo, brown rice, white
rice, brewer’s rice, rice hulls, seaweed, or soybean meal.
On a dry matter basis, wheat co-products (bran, germ,
and middlings) contained the highest concentrations of
total oligofructose, followed by peanut hulls, alfalfa
meal, barley, and wheat. The remaining ingredients con-
tained very low concentrations (, 0·4 mg/g) of oligofruc-
tose. While this database provides information on a
number of commonly used pet food ingredients, additional
analysis of components of oligofructose with longer degree
of polymerization (DP) and inulin concentrations would be
desirable.
Van Loo et al. (1995) reported the concentrations of
inulin and oligofructose in common dietary ingredients
(Table 1). Their analyses quantified glucose and fructose
released by enzymatic hydrolysis of the food or plant
material and assayed oligofructose (DP up to ten) and
inulin contents with a DP of two to sixty (Quemener
et al. 1994). Values are reported on an ‘as-is’ basis
and indicate the range of concentrations determined due
to variation in sources of each food or plant material.
Garlic contained the highest concentration of oligofruc-
tose. Wheat and dried onion contained similar amounts
of oligofructose, while rye flour and barley contained
the lowest concentrations. The authors concluded that
inulin and oligofructose are present in significant
amounts in a wide variety of common foods and food
ingredients.
Note: For the definition of the terms inulin and oligofructose please refer to the introductory paper (p. S139) and its footnote.
* Corresponding author: Dr G. C. Fahey Jr. tel +1 217 333 2361, fax +1 217 244 3169, email g-fahey@uiuc.edu
Abbreviations: CE, competitive exclusion; MOS, mannanoligosaccharides; NDO, nondigestible oligosaccharides; TOS, transgalacto-oligosaccharides.
British Journal of Nutrition (2002), 87, Suppl. 2, S297–S300 DOI: 10.1079/BJN/2002552
q The Authors 2002
Applications of inulin and oligofructose in animal
nutrition
Perhaps the best-known nutritional effect of inulin and oli-
gofructose is their ability to modify the composition of the
intestinal microflora (e.g. increased numbers of bifidobac-
teria) and their metabolic activity in the large intestine
(Roberfroid et al. 1998; Van Loo et al. 1999). In general,
most gut bacteria can be divided into groups that exert det-
rimental effects (staphylococci, clostridia, and veillonella)
or those that benefit the host (bifidobacteria, lactobacilli,
and eubacteria). Detrimental influences include diarrhoea,
infection, and digesta putrefaction, as well as the absorp-
tion and metabolism of mutagenic and carcinogenic chemi-
cals (Rowland et al. 1985). Conversely, beneficial bacteria
bestow positive effects on the host and may inhibit the
growth of harmful bacteria, including E. coli, C. perfrin-
gens, salmonellae, listeria, campylobacter, and shigellas
(Gibson & Wang, 1994; Araya-Kojima et al. 1995).
Homma (1988) described bifidobacteria as a resistance
factor in humans based on defence against pathogens,
infections and reduction of serum cholesterol. Other bene-
ficial effects attributed to bacteria include stimulation of
immune function, increased mineral absorption, and syn-
thesis of vitamins (Gibson & Roberfroid, 1995). In addition
to their effects on gastrointestinal characteristics and sys-
temic metabolism, inulin and oligofructose have been pos-
tulated to enhance performance responses of poultry and
rabbits (Ammerman et al. 1988, 1989; Morisse et al.
1993). Finally, there are some microbial species that
exert both negative and positive effects (e.g. streptococci,
E. coli, and bacteroides) and, therefore, are considered neu-
tral (Gibson & Roberfroid, 1995).
Companion animal studies
Flickinger et al. (unpublished data) supplemented adult
female hounds with 0, 1, 2, or 3 g oligofructose (from
sucrose)/d in gelatin capsules. The basal diet consisted of
372 g/kg chicken protein, 196 g/kg corn, 195 g/kg brewer’s
rice, 130 g/kg oil, 40 g/kg beet pulp, 30 g/kg liquid digest,
10 g/kg dried brewer’s yeast, and 27 g/kg vitamin mineral
premix. Compared to the control, supplemental oligofruc-
tose (from sucrose) (3 g/d) tended (P, 0·10) to decrease
faecal concentrations of Clostridium perfringens (10·04 v.
9·67 log
10
CFU/g) and increased (P, 0·05) total aerobes
(8·52 v. 9·32 log
10
CFU/g). There were no differences
among treatments in total anaerobes, bifidobacteria or lac-
tobacilli. However, results from a second study by the
same group differed. Sixteen adult male beagles were fed
a corn-based diet with or without 3, 6 or 9 g/kg supplemen-
tal oligofructose (from sucrose) for 18 days. Dogs fed the
highest level of oligofructose tended (P, 0·10) to have
higher concentrations of bifidobacteria (9·80 v. 9·40 log
10
CFU/g) in their faeces when compared with the control
group. Differences in the results of these two studies may
be due to variability in basal diet formulations (meat- v.
corn- based diets) and in methods of administering oligo-
fructose (capsule v. incorporation into an extruded diet).
Also, the diet used in the second study contained some
wheat grain that contained fructans.
In a recent study from our laboratory, Swanson et al.
(unpublished data) fed ileally cannulated dogs a meat-
based premium diet supplemented either with 1 g/d oligo-
fructose (from sucrose), 1 g/d mannanoligosaccharides
(MOS), 1 g/d oligofructose (from sucrose) + 1 g MOS, or
1 g/d sucrose (control) administered via gelatin capsules.
Dogs were adapted to their respective diets for 10 days,
followed by a 4-day collection of ileal effluent and
faeces in a 4 £ 4 Latin square design. Although neither
oligofructose nor MOS altered faecal output, moisture
content, or score, MOS decreased (P, 0·05) faecal total
aerobes and tended ðP ¼ 0·13Þ to increase faecal concen-
trations of lactobacilli. Supplemental MOS also increased
(P, 0·05) serum lymphocyte concentrations and tended
(P¼0·14) to increase serum IgA concentrations.
Table 1. Inulin/oligofructose content of selected feeds, pet foods and food ingredients
Item
Oligofructose content* mg/g
(dry matter basis)
Inulin and oligofructose content†
mg/g (as-is basis)
Alfalfa meal 2·24
Barley 1·92 0·050·10
Beet pulp 0·05
Canola meal 0·04
Corn gluten feed 0·09
Corn gluten meal 0·34
Garlic 0·981·60
Oats 0·36
Oat groats 0·12
Onion, dried 0·110·75
Peanut hulls 2·40
Rice bran 0·14
Rye flour 0·050·10
Soybean hulls 0·12
Wheat 1·36 0·100·40
Wheat bran 4·00
Wheat germ 4·68
Wheat middlings 5·07
* Determined by Hussein et al. (1998) as sum of 1-kestotriose + 1,1-kestotetraose + 1,1,1-kestopentaose.
Determined by Van Loo et al. (1995) as sum of inulin and oligofructose with DP of 2 to 60.
E. A. Flickinger and G. C. Fahey JrS298
Supplemental oligofructose tended to decrease concen-
trations of three chemical indicators of faecal odour, trypt-
amine (P¼ 0·11), tyramine (P¼0·15), and indole (P, 0·10).
From these data, it appears that MOS may favourably alter
the composition of the colonic bacteria and elicit a sys-
temic immune response, while oligofructose may reduce
faecal odour. However, when combined, oligofructose
and MOS did not act synergistically.
Poultry, swine, and rabbit studies
Feeding fructans may be a practical strategy for controlling
pathogenic bacteria in chickens. Fukata et al. (1999) fed 1-
day-old chicks an antibiotic-free diet supplemented either
with probiotic bacteria (competitive exclusion; CE), 1 g/
kg dietary oligofructose (from sucrose), or probiotics +
1 g/kg oligofructose for 7 days. At 1 day after oral inocu-
lation with 10
8
CFU of Salmonella enteritidis, only
chicks fed CE had fewer (P, 0·05) S. enteritidis (log
10
CFU/g) organisms recovered in caecal digesta (2·35 v.
4·57, 4·05, and 2·76 for CE v. control, oligofructose, and
CE + oligofructose, respectively). In a second experiment,
1-day-old chicks were administered the same treatments,
but were adapted to diets for 21 days prior to inoculation
with S. enteritidis. Chicks receiving oligofructose or CE
+ oligofructose exhibited lower (P, 0·05) caecal concen-
trations of S. enteritidis at 1 day after inoculation (2·45
and 1·76 v. 4·31 and 4·04 for oligofructose, CE + oligofruc-
tose, control, and CE, respectively), suggesting that
addition of low levels of oligofructose to the diet of
chicks receiving a probiotic may reduce Salmonella
colonisation.
Two sources of dietary fructan were evaluated in a study
by Chambers et al. (1997). Chicks were fed diets sup-
plemented with either no carbohydrates (control), 80 g/kg
Jerusalem artichoke flour providing 50 g/kg inulin (JAF),
or 50 g/kg refined chicory inulin. Chicks were exposed to
Salmonella by being reared with seeder chicks gavaged
with 10
7
CFU of naladixic acid-resistant S. typhimurium.
At 6 weeks of age, the average Salmonella score of JAF-
fed chicks was higher (P, 0·05) than that of control-fed
chicks, while the score of chicory inulin-fed chicks was
lower (P, 0·05) than for other groups. Further research
needs to be done to elucidate the effects of different
sources of inulin and/or oligofructose on Salmonella colo-
nisation of broiler caeca.
In addition to their effects on gastrointestinal character-
istics, inulin and oligofructose have been postulated to
enhance performance responses of livestock. Houdijk
et al. (1998) investigated the effects of oligofructose and
transgalacto-oligosaccharides (TOS) in growing pigs.
Nine-week-old pigs were fed diets supplemented with
either 7·5 or 15 g/kg oligofructose or 10 or 20 g/kg TOS
for 6 weeks. The basal diet contained no additional
copper, antibiotics, or probiotics. In the first week, sup-
plemental oligosaccharides resulted in decreased
(P, 0·05) daily weight gain (control, 953 g; 7·5 g/kg oligo-
fructose, 860 g; 15 g/kg oligofructose, 750 g; 10 g/kg TOS,
765 g; and 20 g/kg TOS, 770 g) and feed conversion effi-
ciency (feed/gain; control, 1·16; 7·5 g/kg oligofructose,
1·23; 15 g/kg oligofructose, 1·35; 10 g/kg TOS, 1·40; and
20 g/kg TOS, 1·24). Dry matter intake was numerically
(P¼0·10) reduced in oligofructose and TOS treatment
groups (control, 1104 g; 7·5 g/kg oligofructose, 1061 g;
15 g/kg oligofructose, 982 g; 10 g/kg TOS, 1036 g; and
20 g/kg TOS, 957 g). During weeks 2 and 3, a similar nega-
tive trend occurred, but the differences were not signifi-
cant. In contrast, during weeks 4 6, oligofructose and
TOS supplementation resulted in numerically (P¼0·08)
increased daily weight gains (control, 861 g; 7·5 g/kg oligo-
fructose, 1056 g; 15 g/kg oligofructose, 981 g; 10 g/kg TOS,
964 g; and 20 g/kg TOS, 1032 g), numerically (P. 0·05)
greater feed consumption (control, 1655 g; 7·5 g/kg oligo-
fructose, 1852 g; 15 g/kg oligofructose, 1756 g; 10 g/kg
TOS, 1850 g; and 20 g/kg TOS, 1830 g) and numerically
(P¼0·08) enhanced feed conversion efficiency (feed/gain;
control, 1·91; 7·5 g/kg oligofructose, 1·73; 15 g/kg oligo-
fructose, 1·83; 10 g/kg TOS, 1·93; and 20 g/kg TOS,
1·78). Differences between the first and last 3-week periods
of this study may indicate that young pigs require an adap-
tation period to dietary oligosaccharides; initially, lower
performance can be offset with compensatory growth.
The initial depression in feed intake may coincide with
fluctuations in colonic microflora ecology, suggesting the
role of a non-specific immune response in the observed
anorexia.
Other investigators have not found similar effects in
swine. Farnworth et al. (1992) reported that 15 g/kg oligo-
fructose (from sucrose) or JAF in weanling pig diets did
not significantly affect daily feed intake, weight gain, or
feed efficiency. However, the authors speculated that the
lack of an effect was due to too low a concentration of diet-
ary oligofructose. Similarly, Olsen & Maribo (1999)
reported that 16·5 g/kg dietary inulin fed to weanling pig-
lets did not result in a significant difference in average
daily weight gain or feed efficiency. The lack of response
to supplemental inulin may have been caused by a high
fructan content of the basal diet due to wheat and barley
inclusion.
In rabbits experimentally infected with E. coli O103 and
fed either 0 or 2·5 g/kg dietary oligofructose, fewer
(P, 0·05) rabbits exhibited clinical signs of enteritis (diar-
rhoea) in the oligofructose group (14·8 %) as compared to
the control group (46·4 %) (Morisse et al. 1993). However,
mortality rate was not significantly different amongst the
treatments (17·9 and 22·2 % for control and oligofructose
treatments, respectively). Among surviving animals, oligo-
fructose-fed rabbits tended (P. 0·05) to have heavier body
weights (2454 v. 2359 g) and had numerically (P. 0·05)
higher average daily weight gains (33·5 v. 32·6 g/d) as com-
pared to the control. While oligofructose supplementation
reduced morbidity, it did not significantly improve mor-
tality or growth performance of rabbits.
Future research directions
Many issues remain unresolved concerning prebiotic oligo-
saccharides, including the establishment of accurate
relationships among the composition of the colonic micro-
flora, gastrointestinal tract health and clinical or per-
formance outcomes observed in the animal. Essential to
the determination of these relationships is an in-depth
Pet food and feed applications of prebiotics S299
understanding of the mechanisms that provide the basis for
any observed effect. Another unknown is whether fructans
can be used interchangeably. Optimal inulin and/or oligo-
fructose inclusion levels in diets have yet to be established
for most animal species. It is unknown whether combi-
nations of different oligosaccharides can elicit diverse
beneficial effects, exert a synergistic effect, or perhaps a
negative effect. Besides blending prebiotics, synbiotic
therapy (coupling probiotic bacteria with prebiotic sub-
strates) perhaps could have a greater impact on the intesti-
nal microflora by nourishing indigenous beneficial bacteria
and directly increasing numbers of favourable microbes.
Summary
A relatively small amount of research exists concerning
supplementation of fructans and other oligosaccharides in
the diets of companion animals, livestock, and poultry.
Studies to date indicate a generally positive effect of fruc-
tans on colonic microbial ecology, host health, and growth
performance. However, more research remains to be done
to determine the appropriate role of these oligosaccharides
in animal nutrition.
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... Indigestible oligosaccharides cannot be digested by enzymes in the small intestine of mammals, but can be fermented by bacteria in the hindgut of non-ruminants. Inulin, oligofructose, and oligogalactose can be added as prebiotics to pet food or feeds to reduce animal fecal odor and improve growth performance (Flickinger & Fahey, 2002). Dietary lactose and lactose intolerance are hot topics in the food and nutrition field today. ...
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... Salmonella spp. and Campylobacter jejuni) in caeca and on prechilled poultry carcasses [7,[9][10][11][12][13]. Researchers concluded that supplementation of inulintype fructans in combination with competitive exclusion flora may reduce colonisation by the pathogenic bacteria. ...
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