British Journal of Nutrition (2005), 93, Suppl. 1, S125–S138 DOI: 10.

1079/BJN20041355
q The Authors 2005

Application of inulin-type fructans in animal feed and pet food

J. M. A. J. Verdonk1*, S. B. Shim2, P. van Leeuwen1 and M. W. A. Verstegen2

1
Animal Sciences Group, Wageningen UR, PO Box 65, 8200 AB Lelystad, The Netherlands
2
Animal Nutrition Group, Department of Animal Science, Wageningen University, Wageningen UR, PO Box 338, 6700 AH Wageningen,
The Netherlands

The inulin-type fructans are non-digestible oligosaccharides that are fermented in the gastrointestinal tract of farm animals and pets. This review focuses on
the various effects of inulin-type fructans in pigs, poultry, calves and companion animals. Effects of the inulin-type fructans on gut microflora, digestion and
availability of nutrients, gut morphology, fermentation characteristics and animal performance are discussed. Inulin-type fructans can support animal per-
formance and health by affecting nutrient digestion, gut microflora and gut morphology, although results vary depending on composition of the basal diet,
inclusion level, type of fructan, adaptation period and experimental hygienic conditions.

Inulin-type fructans: Feed and pet food: Performance and health

For several decades, antibiotics and chemotherapeutics and availability of nutrients; gut microflora and morphology; immu-
in prophylactic doses have been used in animal feed to improve nity and health; and performance in farm animals and pets.
animal welfare and to obtain economic benefits in terms of
improved animal performance and reduced medication costs.
Application of inulin-type fructans in diets for pigs (Table 1)
However, there are increasing concerns about the risk of develop-
ing cross-resistance and multiple-antibiotic resistance in patho- Weaning is a stressful event for pigs. Under commercial con-
genic bacteria both in man and livestock, linked to the ditions, weaning piglets often face nutritional, social and psycho-
therapeutic and subtherapeutic uses of antibiotics in livestock logical stress. As a result, abrupt weaning is typically accompanied
and pets. by low feed intake. Weaning also causes morphological and histo-
The European Union has banned all in-feed use of antibiotics logical changes of the small intestine of pigs resulting in mal-
from 2006 and the use of antibiotics in feed is being considered digestion and malabsorption. When feed intake increases,
for elimination (or intense regulation) in other parts of the enterotoxaemic bacteria may proliferate causing diarrhoea. Diar-
world. This perspective has stimulated nutritionists and feed rhoea frequently occurs after the weaning transition (Nabuurs,
manufacturers to search for new, safer alternatives. The primary 1991). Supplementing inulin-type fructans to weaning diets may
alternatives studied include acidification of the feed by organic be a practical strategy to reduce weaning-related transition of
acids, feeding probiotic organisms and feeding prebiotic intestinal microflora by supporting beneficial bacteria such as
compounds. bifidobacteria and lactobacilli and thereby decreasing intestinal
In the 1980s, the possible potential effects of prebiotics in pathogens like Escherichia coli.
animal feeds was already recognised. Since then, the interest Patterson & Burkholder (2003) and Flickinger et al. (2003a,b)
in the use of prebiotics in animal feed and pet food has resulted summarised several experiments in which different types of fruc-
in extensive research activity. Mul & Perry (1994; farm and pet tans and other prebiotics were supplied in solid feed, formula or
animals), Houdijk (1998; swine), Iji & Tivey (1998, 1999; poul- drinking-water to pigs alone or in combination with a probiotic.
try), Flickinger & Fahey (2002; pets, poultry, swine and rabbits) The effects of inulin-type fructans were categorised by the
and Patterson & Burkholder (2003; swine) have documented the effect on performance; availability, digestion and retention of
use of prebiotics in diets for farm animals and pets. nutrients; gut microflora; host defence; and gut integrity. Reported
The non-digestible inulin-type fructans are found widely in effects on performance of pigs varied from little to no effect
many vegetable feed and food ingredients and are perhaps the (Farnworth et al. 1992; Howard et al. 1993; Olsen & Maribo,
best studied and documented prebiotics in domesticated animals 1999), and from mixed (Houdijk et al. 1998) to stimulating
(Flickinger et al. 2003a). effects (Russell et al. 1996; Shim & Choi, 1997; Estrada et al.
The aim of this review is to provide an overview of recent 2001; He et al. 2002; SB Shim, IH Williams and MWA Verste-
developments on the use and application of inulin-type fructans in gan, unpublished results). Supplementation of inulin-type
livestock feed and pet food including effects on intake, digestion fructans to the diet or drinking-water resulted in fewer cases of

Abbreviations: DGGE, denaturing gradient gel electrophoresis; OF, oligofructose.

* Corresponding author: Dr J. M. A. J. Verdonk, fax þ31 320 237 320, email [email protected]
 S126
Table 1. Effect of inulin-type fructans in pigs

Reference* Design Type of fructan† and dosage Observations†,‡

I Weanling pigs fed during 28 d OF 3 g/kg OF supplementation " FI and " ADG
II Weanling pigs fed during 28 d OF 2·5 g/kg OF supplementation " FI and " ADG
III 135 weaned (28-d-old) pigs fed for 4 weeks Control (corn, barley, SBM, whey, fat) Lignosol was replaced by inulin (JAF) and OF. FI, ADG$ , VFA
Inulin 15 g/kg levels, bacterial counts in distal colonic digesta$ . Pigs fed inulin
OF 15 g/kg and OF had non-significant " number total anaerobes
and bifidobacteria. The manure samples had different colours
depending on the diet. The average panel smell score of the
manure $ [1·5 (control), 2·4 (inulin) and 2·1 (OF)]
IV 20 weaned pigs (36 h postpartum) fed nutritionally OF 0, 3 g/l Number of caecal bifidobacteria and total anaerobic flora; number
complete liquid diets for 15 d of proximal colonic bifidobacteria and total anaerobic flora, caecal
pH and SCFA concentrations $
Cell density and number of labelled cells in caecal epithelial
mucosa "
CD, leading edge, labelled cells, proliferation zone, labelling
index and cell density in proximal colonic eptithelial mucosa "
CD, leading edge, cell density, labelled cells, proliferation zone
and labelling index in distal colonic epithelial mucosa " by OF
supplementation
V 16 weaned pigs (7-d-old) fed a non-medicated milk OF 0, 3 g/d Within 36 h, 6 of 8 pigs developed symptoms of anorexia, pyr-
replacer and orally challenged with Escherichia coli exia, dehydration and diarrhoea; 7 of 8 OF pigs showed no vis-
ible symptoms. OF supplementation tended to " bifidobacteria
compared to control. In OF pigs E. coli # (numerically), clostridial
populations $
VI 20 weaned pigs (8·8 kg) fed a corn –soya diet during 20 d OF 0, 0·75 g/d, 1·5 g/d, 1·5 g/d þ carbadox þ Cu ADG " linearly (P, 0·25) as OF addition increased. N digestion
and retention " . The level of odour metabolites (concentration and
excretion in the faeces) #
J. M. A. J. Verdonk et al.

VII 96 weaned pigs fed solid diets during 4 weeks 2 £ 2 factorial design: OF 0, 1 g/d; carbadox (Ab) 0, 50 mg/kg Growth performance " by OF supplementation
VIII 8 male cannulated pigs (85 kg BWG) individually housed Inulin 60 g/kg Apparent ileal and faecal absorption and retention of Ca and P
in metabolic cages # ; apparent faecal Zn absorption " by inulin addition
IX 16 male cannulated pigs (90 kg BWG) individually Inulin 60 g/kg Ileal and faecal N excretion as well as N retention $ by inulin
housed in metabolic cages supplementation
X 96 weaned (18-d-old) pigs fed solid feed during 4 weeks 2 £ 2 factorial design: OF 0, 1 g/kg; SDAP 0, 35 g/kg Pig performance $ by inclusion of OF. The diet did not affect
CD in the small intestine. VH " by both SDAP and OF. VH:CD
ratio " by OF
XI Weaned (39-d-old) pigs fed solid feed during 29 d OF 50 g/kg FI " and ADG " by OF supplementation
XII 20 castrated male ileal cannulated (38-d-old, 10·4 kg) Control (cornstarch, glucose, casein) OF yielded " propionate than TOS in ileal chyme. pH and vol-
weaned pigs were fed solid feed OF 10, 40 g/kg atile fatty acid pool of ileal chyme were influenced by type and
TOS 10, 40 g/kg level of dietary non-digestible oligosaccharide. The OF diets
yielded " caecal anaerobes, " faecal pH, " protein-derived
SCFA and less butyric acid than the control diet
XIII 65 castrated male (9-week-old, 15·6 kg) pigs fed solid Control (corn/dextrose based diet) OF was not detected in faeces. OF and TOS supplementation
feed during 42 d OF 7·5, 15 g/kg resulted in significantly lower DM intake and ADG compared to
TOS 10, 20 g/kg the control pigs in weeks 1–3. During weeks 1– 6 mean growth
performance was not affected. Faecal pH was not affected, but
faecal DM content was lower for OF/TOS pigs compared to con-
trol pigs
Table 1. Continued

Reference* Design Type of fructan† and dosage Observations†,‡

XIV 41 weaned (21-d-old) cross-bred standard farm pigs were Oral electrolyte solutions (OES) Supplementation with OF resulted in accelerated recovery of
housed individually in metabolic cages and challenged orally with OES þ OF (9·5 g/d) bacteria perceived as beneficial while potentially slowing the
cholera toxin recovery of pathogenic forms. OF did not cause an obvious
reduction in the duration of diarrhoea and the associated loss of
water
XV Expt 1: 25 (57-d-old, 16 kg) pigs were fed solid feed as a slurry Control (corn/dextrose based diet) Apparent faecal and apparent ileal nutrient digestion (DM, ash,
OF 7·5, 15 g/kg CP, EE) $ by supplementation of OF and TOS
TOS 10, 20 g/kg
Expt 2: 20 (38-d-old, 10·4 kg) ileal-cannulated pigs were fed solid OF- and TOS-fed pigs produced dose dependently less faeces
feed than the control pigs. The apparent faecal digestion of the non-
starch neutral detergent soluble carbohydrates (including non-
digestible oligosaccharides) was " by OF and TOS supplemen-
tation. N and mineral balances were not affected
OF was nearly completely degraded pre-caecally
XVI 90 weaned (36-d-old, 7 kg) pigs during 20 d Control OF þ probiotic resulted in " count of total anaerobes, aerobes,
Probiotic lactobacilli and bifidobacteria as well as decreased clostridia,
OF (3 g/d) þ probiotic enterobacteriaceae and E. coli counts in faecal samples. Present
study indicates a synergistic effect of probiotic (Lactobacillus
paracasei) and OF on faecal microflora
XVII 2 experiments with 175 group fed pigs during 4 weeks CON: basal diet Average daily gains were not significantly affected by diet. Over-
AB: virginiamycin 0·5 g/kg all AB, OF and COM " ADG by 16, 9 and 6 %, respectively,
OF: 50 g/kg compared to CON in the clean nursery trial. In the dirty nursery
BP: beet pulp 100 g/kg trial, OF " feed efficiency (14 %) but reduced FI (24 %). OF was
COM: OF 25 g/kg, BP 50 g/kg associated with lower (trend) E. coli concentrations in ileal con-
tents and " bifidobactera in proximal colon samples
OF tended to reduce the E. coli concentrations and " bifidobac-
terial and total anaerobic bacteria concentrations in the distal
Prebiotics in feed and pet food

colon of pigs
XVIII Expt 1: in vitro adhesion assay Expt 1: inulin 0·1, 1, 5 % to incubation solution Inulin partially inhibited adhesion of F4acþ coliform to villous
brush border (52 % inhibition by 5 % inulin)
Expt 2: 20 BT-seronegative, weaned pigs (28-d-old) Expt 2: inulin 0, 50 g/kg Inulin supplementation to the diet did not affect the primary
immune response to BT immunisation. The secondary immune
response after a boost at day 21 in the inulin pigs was numeri-
cally "
XIX In vitro inoculation of intestinal tissue (jejunal and ileal sections) Expt 1 incubation solution: inulin 25 g/kg; GOS 25 g/kg; MOS Inulin (25 g/kg) resulted in non-significant decrease in association
from 30 pigs 25 g/kg of salmonella in ileal tissue and in association of E. coli in jejunal
tissue
Expt 2 dietary inclusion: inulin 40 g/kg; GOS 40 g/kg The numbers of E. coli in jejunal tissue and a numerical reduction
of Salmonella spp. in ileal tissue # in inulin pigs
XX Expt 1: 40 weaned pigs (18-d-old, 6 kg) were fed solid feed for Control diet The treatment with OF and B. longum improved ADG and FE,
21 d Control diet þ OF (5 g/kg), oral dose of Bifidobacterium reduced the number of faecal total anaerobes and clostridia and
longum at days 1 and 3 " the number of bifidobacteria only from day 0 to 7
Control diet (C)
Expt 2: 80 weaned pigs (18-d-old) were fed a solid diet in a 2 £ 2 C þ OF (5 g/kg) ADG and IGF-1 # by OF supplementation, while ADG and
factorial design C þ 1 £ 107 cfu B. longum/g IGF-1 " by administration of B. longum
C þ OF (5 g/kg) þ 1 £ 107 cfu B. longum/g
S127
 S128
Table 1. Continued

Reference* Design Type of fructan† and dosage Observations†,‡

XXI 180 weaned (17-d-old) pigs during 4 weeks in 3 phases (week 1, Basal diet (BD, control) ADG and FE " by supplementation of inulin in water or feed
week 2, weeks 3 and 4) BD þ inulin in water (132 g/l) compared to the control. Pig performance $ by inulin in both
BD þ inulin in feed (5, 2, 1 g/kg) water and feed compared to inulin in water or feed only
BD þ inulin in water and feed
BD þ antibiotic in feed
XXII 90 piglets (1-d-old) were fed 10 d after birth and 10 d after wean- C ¼ powdered milk Supplementation of OF in combination with L. paracasei did not
ing (36 d of age) with powdered milk L ¼ 2 g/d C þ L. paracasei 1 £ 109 cfu/g stimulate the immune system of newborn piglets compared to C
F ¼ 2 g/d C þ L. paracasei 1 £ 109 cfu/g; þ OF (3 g/d) or L
After weaning, OF in combination with L. paracasei resulted in
highest numbers for almost all measured immune parameters
(total count of several types of white blood cells, phagocytic
activity of leucocytes and neutrophils
XXIII 36 weaned pigs (25–28-d-old) from 9 litters fed Control (maize starch, fishmeal, dextrose) Piglets fed with SBP or SBP þ OF showed a " bacterial diversity
SBP 10 g/kg (Shannon index of diversity of DGGE bands) and a more rapid
SBP 5 g/kg þ OF 2·5 g/kg stabilisation of the bacterial community in faecal samples col-
lected per rectum compared to control pigs
Amplicons related to Ruminococcus-like species were found in
all DGGE fingerprints derived from SBP and SBP þ OF pigs but
not in pigs on the control diet
XXIV In vitro gas production Inulin 0, 25 g/kg Hourly rate of gas production of the inulin diet was " to 5 ml/g
diet compared to , 2 ml/g diet for the control diet. Inulin in vitro
fermentation comprised a period of less than 10 h while the fer-
mentation of other feed components continued until about 25 h
XXV In vitro gas production Inulin (chicory, Jerusalem artichoke) 0·2 g added to 0·5 g Except for antibiotic, the fermentation with added carbohydrates
J. M. A. J. Verdonk et al.

chyme compared with other carbohydrates and antibiotic (vir- resulted in " total gas production and a faster maximum rate of
giniamycin) gas production. Addition of all tested carbohydrates except xylan
resulted in shorter time at which half of the asymptotic gas had
been reached. The amount of ammonia decreased for all added
carbohydrates and was nearly the same for the antibiotic com-
pared to chyme only. The branched-chain ratio was significantly
lower for all additives compared with chyme whereas the anti-
biotic led to a significant higher value
XXVI 12 castrated male ileal-cannulated pigs (20 kg) fed ad libitum Control (barley –SBM diet) Protein and mineral utilisation $ by inulin and GOS supplemen-
GOS tation. The intestinal fermentation (ammonia and VFA concen-
Inulin 20 g/kg tration) was significantly changed. Inulin degradation reached
45 % at the end of the small intestine and 100 % in the faeces

* Reference: I, Nakamura (1986); II, Fukuyasu & Oshida (1986); III, Farnworth et al. (1992); IV, Howard et al. (1993); V, Bunce et al. (1995b); VI, Bunce et al. (1995c); VII, Russell et al. (1996); VIII, Vanhoof & De Schrijver (1996a); IX, Vanhoof & De
Schrijver (1996b); X, Spencer et al. (1997); XI, Shim & Choi (1997); XII, Houdijk et al. (1997); XIII, Houdijk et al. (1998); XIV, Oli et al. (1998); XV, Houdijk et al. (1999); XVI, Nemcová et al. (1999); XVII, Klein Gebbink et al. (2001); XVIII, Rossi et al.
(2001); XIX, Naughton et al. (2001); XX, Estrada et al. (2001); XXI, He et al. (2002); XXII, Herich et al. (2002); XXIII, Konstantinov et al. (2003); XXIV, van Leeuwen et al. (2003); XXV, Bauer et al. (2003); XXVI, De Schrijver & De Vos (2003).
† Abbreviations: BWG, body weight gain; BT, bovine thyroglobulin; OF, oligofructose; SMB, soyabean meal; TOS, trans-galactooligosaccharides; SBP, sugarbeet pulp; GOS, galactooligosaccharides; FI, feed intake, ADG, average daily gain; JAF, Jerusa-
lem artichoke flour, VFA, volatile fatty acids; CD, crypt depth; VH, villous height; SDAP, spray-dried animal plasma; CP, crude protein; EE, (diethyl) ether extract; FE, feed efficiency; IGF-1, insulin-like growth factor-1; DGGE, denaturing gradient gel
electrophoresis.
‡ ", increased; #, decreased; $, no change.
 Prebiotics in feed and pet food S129

diarrhoea, reduced mortality and decreased number of pigs shed- Application of inulin-type fructans in diets for poultry
ding the pathogen (Bunce et al. 1995b; Oli et al. 1998) compared (Table 2)
to controls.
There is scarce information on the effect of inulin and oligo- At hatching, the gastrointestinal tract of broilers is sterile. Immedi-
fructose (OF) on nutrient digestion, availability and retention. ately, bacteria originating from the mother, the environment or the
Studies by Vanhoof & De Schrijver (1996b), Houdijk et al. diet will colonise in the gastrointestinal tract. In case of mother con-
(1999) and De Schrijver & De Vos (2003) showed that OF and tacts, a diverse microbial population will enter the gastrointestinal
inulin supplementation does not affect protein digestion and nitro- tract. As a result, after the first colonisation, bacterial species
gen retention. Mineral absorption and retention was not affected coming later in time will have greater difficulty colonising (coloni-
by inulin or OF except for Zn (Vanhoof & De Schrijver, sation resistance) than the initial population. Because of the strict
1996a; Houdijk et al. 1999; De Schrijver & De Vos, 2003) and separation of generations in broiler chickens, any bacteria from
Fe (De Schrijver & De Vos, 2003). the environment might colonise (e.g. attach to intestinal binding
A number of studies have attempted to investigate the effect of sites or multiply faster than being removed via chyme passage)
inulin-type fructans on intestinal and faecal microbial populations the intestinal tract. Those feed components that are resistant to
and in vitro gut tissue association. Some studies in pigs evaluating enzymatic degradation, such as inulin-type fructans, serve as a sub-
(a limited number of) bacterial populations showed that sup- strate for bacterial activity in the intestinal lumen. The interaction
plementation had little effect on size and activity of microbial between host nutrition and the intestinal microbiota has been clearly
populations (Farnworth et al. 1992; Houdijk et al. 1997). Some illustrated using germ-free animals. Langhout (1998) clearly
studies found enhanced intestinal bifidobacteria populations showed the importance of controlling the activity of the intestinal
(Howard et al. 1993; Klein Gebbink et al. 2001). Others reported microbiota to support gut integrity and to avoid (i) bacterial over-
modulation of the intestinal flora (Nemcová et al. 1999) and growth, (ii) reduced nutrient digestibility and (iii) reduced pro-
speeding up of recovery of the normal intestinal microflora fol- duction performance.
lowing acute diarrhoea (Oli et al. 1998). Konstantinov et al. Feeding inulin-type fructans may be a practical strategy for
(2003) studied the changes in time of the predominant faecal bac- controlling pathogenic bacteria in chickens. Flickinger & Fahey
terial community in weaning pigs that were fed diets containing (2002) and Flickinger et al. (2003a) summarised several exper-
inulin-type fructans and/or sugarbeet pulp using denaturing gradi- iments in which different types of fructans were fed to broilers
ent gel electrophoresis (DGGE) analysis, which is used to alone or in combination with a probiotic to evaluate the effect
describe the microbial diversity in complex ecosystems including on colonisation of pathogens (i.e. Salmonella spp. and Campylo-
the mammalian intestinal tract. Piglets fed diets containing sugar- bacter jejuni) in caeca (Bailey et al. 1991; Oyarzabal & Conner,
beet pulp (10 g/kg) or inulin-type fructans þ sugarbeet pulp 1996; Chambers et al. 1997; Fukata et al. 1999) and on pre-
(2·5 þ 5 g/kg) showed a higher bacterial diversity and a more chilled poultry carcasses. Researchers concluded that supplemen-
rapid stabilisation of the bacterial community compared with tation of inulin-type fructans in combination with competitive
that of the animals fed the control diet (maize starch). exclusion flora may reduce colonisation by the pathogenic
Recently, some experiments have also demonstrated that bacteria.
inulin-type fructans affect in vitro fermentation kinetics when In recent experiments with broilers, we (Verdonk & van Leeu-
used as a substrate (Houdijk, 1998; Bauer et al. 2003; van Leeu- wen, 2004) evaluated the effect of supplementation of inulin-type
wen et al. 2003) or affects the inoculum when included in the diet fructans on the colonisation and shedding of pathogens. The first
(Houdijk, 1998). broiler study evaluated the effect of the inclusion of 20 g OF and
Only a few studies describe the effect of inulin-type fructans on inulin/kg feed on the colonisation and shedding of Salmonella
the host defence system and gut integrity. Herich et al. (2002) typhimurium and C. jejuni in broilers. The broilers were fed one
demonstrated that the combination of OF and probiotics given of four dietary treatments and challenged in the crop on days
to pigs before and after birth increased the number of CD4þ 10 and 11 of age with a low or high dose of S. typhimurium
T-lymphocytes compared to the control diet. and a single dose of C. jejuni. The birds were housed in three-
Inulin reduced the in vitro association of E. coli to jejunal organ tier battery cages. Feed intake and body weight were measured
tissue and of Salmonella spp. (non-significant) to ileal tissue (Naugh- at ages 9, 14, 21 and 35 d. During dissection of birds on days
ton et al. 2001). Rossi et al. (2001) showed that inulin reduced the in 14, 21 and 35, digesta samples of the crop and caeca were
vitro adhesion of a pathogenic coliform to intestinal porcine mucosa. taken and the colonisation was determined. On days 18 and
Results also suggested a systemic specific immunomodulatory effect 28, salmonella shedding via the excreta was measured.
of inulin in immunisation against bovine thyroglobulin. The second study evaluated the effect of inulin at four inclusion
Howard et al. (1993) concluded that OF improved the morpho- levels in a basal diet on the occurrence of lesions due to Eimeria
logical and the cellular kinetics of the epithelial mucosa in the acervulina and Clostridium perfringens. The broilers were housed
large intestine. Spencer et al. (1997) investigated the effect of in floor pens and given an E. acervulina challenge orally at day
supplementation of spray-dried animal plasma and inulin-type 10 of age, followed by an oral inoculation of Cl. perfringens on
fructans on the morphology of the small intestine in weaned days 14, 15 and 16. Intestinal lesions for coccidiosis and necrotic
pigs. Inulin-type fructans did not affect crypt depth but did enteritis in the duodenum and jejunum on days 15 – 17 and 22 were
increase the villous height and villous height:crypt depth ratio. scored visually.
Shim et al. (SB Shim, IH Williams and MWA Verstegen, The supplementation of inulin-type fructans in the diet stimu-
unpublished results) found that OF supplementation (2·5 and lated the performance of young broiler chickens, but did not
30 g/kg) for 3 weeks post-weaning (numerically) increased villous clearly affect the colonisation and shedding of S. typhimurium
height but not crypt depth in the small intestine of pigs compared and C. jejuni or the occurrence of lesions due to E. acervulina
to the control. Brush border enzyme activity was not affected. and Cl. perfringens.
 S130
Table 2. Effect of inulin-type fructans in poultry

Reference* Design Type of fructan† and dosage Observations†,‡

I 2800, 1-d-old male broilers fed for 46 d Commercial diet Final body weights numerically " and FE " by OF (results are not men-
OF in feed (2·5, 5·0 g/kg) tioned in the abstract but are referred to in Flickinger et al. 2003a,b)
BMD
II 2400, 1-d-old male broilers fed for 47 d Control Supplementation of OF at the inclusion level of 3·75 resulted in heavier
OF 3·75, 7·5 g/kg birds and improved carcass yield (hot carcass weight, percentage breast
Antibiotic (virginiamycin) 0·011 g/kg meat) at 47 d compared to control and antibiotic groups
III Broilers Control ADG, FE and carcass quality $ by OF supplementation
OF 3·75 g/kg
IV 10 pens with salmonella-negative day-old Cornish broiler chicks Control Salmonella score $ by supplementation of carbohydrates
Inulin crude Salmonella counts at 6 weeks in broilers fed crude inulin " compared to
Inulin refined all other broiler groups. Infections # in broilers fed refined inulin than in
Lactulose control broilers. The decline of salmonella infection in broilers fed refined
Lactosucrose inulin ceased after the dietary additive was discontinued at 5 weeks of
age. Caecal pH and density # by inulin
V 880 Ross broiler chicks in 16 pens, challenged at day 2 Control: buffered peptone water Treatments were provided in drinking-water at 6 weeks of age after feed
after hatching with Salmonella typhimurium by spraying OF þ microbial mixture with drawl. Caeca from treated birds weighed more than from control
birds. No difference in salmonella colonisation occurred between the trea-
ted and control group
VI 84, 1-d-old Hubbard £ Hubbard male broilers were housed Control (C) ADG, FE or concentrations of total aerobic bacteria, coliforms, lactoba-
in battery pens and fed a corn –soyabean diet with sprayed C þ 100 g kestoses (OF), sugars/kg cilli, total anaerobes or clostridia $ by supplementation of kestoses.
kestose/sugars for 28 d C þ 80 g sugars/kg Caecal bifidobacterial populations " 24-fold in kestose-treated birds
VII Expt 1 and 2: two trials with 60, 1-d-old birds (White Leghorn Hy-Line) Control Did not effect caecal salmonella colonisation or translocation in birds
J. M. A. J. Verdonk et al.

challenged orally with Salmonella enteritidis at day 7 (expt 1) or 21 CE challenged at 7 d $ by OF supplementation. In birds challenged at day
(expt 2) OF (1 g/kg) 21 the mean numbers of S. enteritidis in caecal contents on days 1 and 7
CE þ OF (1 g/kg) post-infection # by OF supplementation or OF þ CE
Expt 3 and 4: a total of 20, 1-d-old birds Control The major bacterial population of the caecal microflora $ by OF sup-
CE plementation
OF (1 g/kg)
CE þ OF (1 g/kg)
VIII 24 ISA Brown laying hens (20 weeks old) housed individually Wheat based Gut viscosity and egg production $ by dietary treatment
Oat based
Millrun based
Rice hull based
Wheat þ OF (2 g/kg)
Wheat þ MOS (2 g/kg)
IX 312, 1-d-old male Cobb broiler chicks in 26 pens during 35 d Control Supplementation of glucose, OF or MOS tended to result in heavier birds
OF with better FE until day 35
Glucose
MOS
Table 2. Continued

Reference* Design Type of fructan† and dosage Observations†,‡

X 98, 1-d-old male and female Ross broiler chicks in 12 pens Control corn – soya Faecal microbial counts of total aerobe, lactobacilli, salmonella and cam-
Inulin 10 g/kg pylobacter at 2, 4 and 6 week of age $ by the dietary treatment. Total
OF 10 g/kg faecal aerobes and Escherichia coli at week 4 # by OF compared to the
control
Lactobacilli counts in the gizzard and small intestine " in female OF
birds. Total campylobacter counts in the large intestine # in inulin and
OF birds
Faecal ammonia content and pH during weeks 1–4 # in OF birds but
not in inulin birds
XI 98, 1-d-old male and female Ross broiler chicks in 12 pens Control corn – soya ADG, carcass weight, FE and gut length in female birds " but in male
Inulin 10 g/kg birds $ by OF and inulin supplementation
OF 10 g/kg
XII Expt 1: 864, 1-d-old male Ross 308 birds were fed during 35 d and orally OF 20 g/kg Performance of young broiler chickens "
challenged with salmonella and campylobacter Inulin 20 g/kg Colonisation and sheding of salmonella and campylobacter $
High-molecular-inulin 20 g/kg
Expt 2: 704, 1-d-old male Ross 308 birds were housed in 32 floor pens Inulin Performance of young broiler chickens "
and orally challenged with Eimeria acervulina and Clostridium perfringens Occurrence of lesions due to E. acervulina and Cl. perfringens $

* Reference: I, Ammerman et al. (1988); II, Ammerman et al. (1989); III, Waldroup et al. (1993); IV, Chambers et al. (1997); V, Oyarzabal & Conner (1996); VI, Patterson et al. (1997); VII, Fukata et al. (1999); VIII, Hartini et al. (2003); IX, Ao & Choct
Prebiotics in feed and pet food

(2003); X, Yusrizal & Chen (2003a); XI, Yusrizal & Chen (2003b); XII, Verdonk & van Leeuwen (2004).
† Abbreviations: OF, oligofructose; BMD, bacitracin methylene disalicylate; CE, competitive exclusion; MOS, mannan oligosaccharides; FE, feed efficiency; ADG, average daily gain.
‡ " , increased; # , decreased; $ , no change.
S131
S132 J. M. A. J. Verdonk et al.

Yusrizal & Chen (2003a) reported that supplementation of OF glucose, lactate, triacylglycerols and insulin in blood in prerumi-
and inulin (10 g/kg) to a corn– soya diet did not affect the faecal nant calves as in animals and human subjects with diabetes
microbial counts of total aerobe, lactobacilli, salmonella and cam- mellitus.
pylobacter in broilers at 2, 4 and 6 weeks of age. OF resulted in Webb et al. (1992) observed greater weight gains in Holstein
significant reductions in total faecal aerobes and E. coli at week bull calves (3 – 5 d old) by adding a combination of inulin-type
4 compared to the control. It also increased the lactobacilli fructans (3·75 g/kg), sodium diacetate (10 g/kg) and decoquinate
counts in the gizzard and small intestine of female broilers. (50 mg/kg) into the milk replacer and starter grain compared
Inulin or OF supplementation reduced total campylobacter with supplementing the milk replacer with sodium diacetate and
counts in the large intestine. OF but not inulin resulted in reduced decoquinate alone. Unfortunately, the effects on rumen and gut
faecal ammonia content and pH during weeks 1 through 4. The microflora were not studied.
same authors (Yusrizal & Chen, 2003b) reported that supplemen- Donovan et al. (2002) reported that supplementation of a blend
tation of OF and inulin improved body weight gain, carcass of inulin-type fructans, allicin and gut-active microbes to the milk
weight, feed conversion efficiency and gut length in female replacer had similar effects to those of the antibiotics-supplemen-
birds but not in male birds. Also, Ao & Choct (2003) reported tation fed to Holstein male and female calves.
that birds given drinking-water supplemented with OF (0·05 %) Compared with diets for other species, dietary proteins and
were heavier and had more efficient feed conversion at day carbohydrates for veal calves are usually highly digestible. This
35 compared to the control birds. Recently, Hartini et al. (2003) was to a large extent related to the soluble/dispersible nature of
concluded that supplementation of inulin-type fructans (2 g/kg) the proteins used in veal calf diets. Commercial milk replacers
to a wheat-based diet did not affect the feed intake nor egg pro- were initially made based primarily on skimmed milk powder
duction in ISA Brown laying hens. and animal fat. During the last decade, replacement of milk pro-
teins and lactose by vegetable proteins and carbohydrates has
become an important issue both in practice and research (Verdonk
Application of inulin-type fructans in diets for (preruminant)
et al. 2002). Increasingly, part of the dietary lactose is being
calves (Table 3)
replaced by starch and by soya oligosaccharides. Up to 15 %
The common practice of early weaning of preruminant calves for starch can be added to veal calves’ diets, with only a minor
veal production, followed by long distance transport and regroup- decrease in starch digestibility. At higher levels (15– 25 %), the
ing of animals from different origins, may cause a challenge to decrease in starch digestibility is more pronounced (van Weerden
the natural defence system resulting in dysbacteriosis and diges- et al. 1967; van der Honing et al. 1974) and this causes increased
tive disorders. In many fattening systems, starter treatments fermentation in the large gut. Visual characteristics and pH of the
with antibiotics have become common practice. Mul & Perry faeces were affected by the quantity of starch fermented in the
(1994) mentioned a large-scale use of inulin-type fructans result- hindgut. We have demonstrated (Verdonk et al. 1998) that repla-
ing in similar fattening results compared to the in-feed antibiotics. cement of lactose (65 g/kg) by soluble or insoluble soya carbo-
Verdonk & van Leeuwen (2004) have evaluated the effect of hydrates resulted in significantly decreased apparent ileal
inclusion of inulin-type fructans in the milk replacer on health digestibility of DM, crude ash and N-free extract. Inclusion of
and production performance of preruminant calves during the the soya carbohydrates in the diet also tended to increase the
first 3 weeks after arrival at the fattening farm. Four groups of endogenous flow of N at the terminal ileum. It was suggested
eight calves, housed individually in wooden boxes with a slatted that this increase might be caused by fermentation in the small
floor, were fed the basal calf milk replacer supplemented with intestine increasing the flow of bacterial N to the large gut.
20 g of dextrose, OF, inulin or dextrose supplemented with anti- Inulin-type fructans may play a role in creating and maintaining
biotics/kg. Individual body weight of the calves was determined a desired, stable microflora in the rumen (supplementation to
at 7 d intervals and feed intake was measured per calf per feeding. solid feed), and the small and large gut (supplementation to milk
The faecal consistency scores were conducted daily. The compo- replacer) of (preruminant) calves.
sition of the microflora in rectal samples was determined by
DGGE and nucleotide sequence analysis of rDNA. During the
Application of inulin-type fructans in pet foods (Table 4)
3-week experimental period, the OF and the antibiotics groups
resulted in higher (P, 0·05) body weight gain compared to the Several reasons that justify the addition of OF and inulin in pet
dextrose group. The faeces consistency over the observed foods are as follows (Flickinger et al. 2003a):
period was best (P. 0·05) in the OF group and worse in the dex-
. manipulating the composition of the intestinal flora,
trose group. The DGGE gels revealed that the faecal flora in
. stimulating gut integrity,
young milk-fed calves in fattening farms is very unstable. The
. affecting nitrogen metabolism, and
dietary treatment did not affect the pattern or the shift in pattern
. reducing offensive faecal odour.
of the bands in the gels of the faecal samples. Analysis of ileal
contents and faeces showed that some 70 % of the dietary Furthermore, it was indicated that the geriatric pet population is
inulin-type fructans reached the caecum but that no fructans more prone to intestinal irregularities and has diminished diges-
were recovered in the faeces. tive microbial balance when compared to younger animals. In
Kaufhold et al. (2000) supplemented 10-week-old calves their review, Flickinger et al. (2003a) summarise the results of
(average body weight 117 kg) with 0 or 10 g OF/d (with the studies indicating an effect of supplementation of inulin-type
morning meal). Feed intake was similar between groups but fructans on the intestinal microflora, epithelial cell proliferation,
weight gain tended to be higher for the OF-supplemented faecal characteristics and nutrient digestibilities.
group. They concluded that OF had basically similar effects Recently, Hesta et al. (2001) studied the effect of supplemen-
on the metabolic and endocrine traits such as concentration of tation of OF (30, 60, 90 g/kg) and inulin (30, 60 g/kg) to a com-
Table 3. Effect of inulin-type fructans in calves

Reference* Design Type of fructan† and dosage Observations†,‡

I 40 male Holstein (3–5-d-old) fed milk replacer OF 0, 3·75 g/kg in MR and 0, 8·8 g/kg in CS In winter time, ADG " by adding a combination of OF, sodium diace-
(MR) and calf starter (CS) during a 10-week tate and decoquinate compared with controls. OF source NR
period
II Veal calves in practice OF þ probiotic (5/2·5 g/kg 0– 6 week/7 –26 week) Authors mention unpublished results in practice (Italy, Netherlands)
showing similar fattening results comparing a feeding regime using
OF compared to antibiotics
III 21 calves fed milk replacer and calf starter 0, 3, 7 g OF/d Plate counts in faecal samples for bifidobacteria " (P¼ 0·02) by OF
supplementation to the milk replacer. Counts for Escherichia coli,
clostridia and the total anaerobes were numerically changed
IV 14 Simmental £ Red Holstein calves (10 weeks GrC ¼ no supplementation ADG tended to be higher for GrF. The postprandial increase of glu-
old) fed whole milk plus milk replacer during a GrF ¼ 10 g OF/d cose concentrations was significantly smaller, of lactate tended to be
3-week period smaller, whereas maximal insulin concentrations reached were sig-
nificantly higher in OF calves
V 45 male and female Holstein calves (new- MRA ¼ antibiotics in milk replacer Total weight gain, feacal scores and serum proteins during 5-week
Prebiotics in feed and pet food

born) fed milk replacer and calf starter MRE ¼ OF þ allicin þ probiotics experimental period was not different between groups. OF source
NR
VI 32 male black and white (1-week-old) calves Dextrose (DEX), OF (20 g/kg) ADG " for OF and ANT calves compared to DEX, faecal score
fed milk replacer for 3 weeks Inulin (20 g/kg) numerically better for inulin compared to DEX
Dextrose þ antibiotics (ANT): 20 g/kg Composition of faecal microflora $ and highly variable

* Reference: I, Webb et al. (1992); II, Mul & Perry (1994); III, Bunce et al. (1995a); IV, Kaufhold et al. (2000); V, Donovan et al. (2002); VI, Verdonk & van Leeuwen (2004).
† Abbreviations: OF, oligofructose; ADG, average daily gain; NR, not reported.
‡ " , increased; #, decreased; $, no change.
S133
 S134
Table 4. Effect of inulin-type fructans in pets

Reference* Design Type of fructan† and dosage Observations†,‡

I 16 IgA-deficient 15- to 20-month-old German Shepherd OF 10 g/kg Number of aerobic bacteria in digesta from the duodenum/proximal part
dogs with intestinal bacterial overgrowth were fed a chicken of jejunum and in the duodenal mucosa # by supplementation with OF
based kibble diet for 50 d
II In vitro fermentation using cat faecal inoculum. Cats were OF OF together with some fermentable fibre sources resulted in highest OM
fed a diet with or without supplemental fibre (beet pulp) disappearance and acetate, propionate and total SCFA production
III In vitro fermentation using dog faecal inoculum OF OF had greatest OM disappearance (P, 0·05; . 80 %), greatest propio-
nate and intermediate total SCFA production
IV 8 castrated 1- to 1·4-year-old young adult male beagles Control (C) Total-tract digestibility of CP # by OF, but digestibility of DM, OM and
were fed minced meat, flaked maize based diet for 42 d C þ OF 40 g/kg þ SBF 10 g/kg EE $ . Postprandial plasma concentrations of insulin and cholesterol $
C þ OF 80 g/kg þ SBF 20 g/kg
V 8 beagle dogs (2 intact males and 6 neutered females), 5 Control (C) Inulin increased wet faecal output and water consumption compared to
years old, were fed minced one of four meat, flaked maize C þ inulin 70 g/kg DM C. Supplementation of inulin decreased digestibility of OM, CP and EE.
based diet in a 4 £ 4 latin square design for 20 weeks C þ SBF 70 g/kg DM Inulin showed no metabolic effects
C þ guar gum 70 g/kg DM
VI 6 male and 6 female healthy specific pathogen-free cats OF 7·5 g/kg Wide quantitative and qualitative variation in the duodenal flora was
were fed a dry diet for 32 weeks observed over time. Duodenal flora $ by OF
VII 6 male and 6 female healthy specific pathogen-free cats OF 7·5 g/kg Supplementation with OF resulted in alteration of faecal flora of cats.
were fed a dry diet for 32 weeks Total bacterial counts, aerobic and anaerobic counts were not affected
by diet. Mean counts of Lactobacilli and Bacteroides spp. " and Escher-
ichia coli and Clostridium perfringens # by OF
VIII 10 adult beagle dogs of both sexes were fed a chicken (by) Cellulose 36 g/kg Small intestinal dimensions " and in vitro carrier-mediated glucose
product brewers rice based diet for 6 weeks Beet pulp þ OF (42 þ 10 g/kg) uptake " by fermentable beet pulp and OF
IX Expt 1: 8 healthy adult cats, basal diet containing 26·5 g/kg OF 0, 30, 60 and 90 g/kg Supplementation with 60 and 90 g OF/kg significantly affected faecal
J. M. A. J. Verdonk et al.

crude fibre characteristics

Expt 2: 8 healthy adult cats, same basal diet, faeces OF 30 g/kg OF and inulin resulted in lower apparent faecal protein digestibility
collection Inulin 0, 30, 60 g/kg
X 7 adult mixed breed female dogs in a 4 £ 7 incomplete latin Crude inulin, 5 g/kg Ileal, large intestinal and total-tract DM and N digestibility $ , minor
square design effects on bacterial growth in the large intestine and VFA proportions in
the small intestine
XI In vitro OF, 4 inulin products Total production of SCFA " for OF and the inulin products OF, DP¼3–5;
inulin HP, DP ¼ 9; inulin IQ DP¼9; inulin, DP.12; OF, DP¼2–8 com-
pared to beet pulp, MOS and soya fibre or cellulose
XII 5 healthy dogs in a cross-over trial OF 10 g/kg OF (DP¼ 3– 20) ingestion changed faecal microflora, apparent Mg and
Ca absorption " . Faecal pH and the route of N excretion $ . Diet used
in the present study contained rice, corn and beet pulp and probably
was rich in non-digestible fermentable carbohydrates
XIII Expt 1: 20 healthy female and male dogs OF, Lactobacillus acidophilus (LAC) In expt 1, Cl. perfringens # (P¼0·08) and faecal butyrate (P¼ 0·06) and
lactate (P, 0·05) concentrations " by OF
Expt 2: 20 healthy female and male dogs OF þ LAC 6·7 g/kg (or 2 g OF/d), 1 £ 109 cfu, 6·7 g/kg In expt 2, FI and faecal DM output tended # OF had lowest faecal
OF þ 1 £ 109 cfu concentrations of hydrogen sulfide, methanethiol and dimethyl sulfide.
LAC was more affective when fed in combination with OF
Table 4. Continued

Reference* Design Type of fructan† and dosage Observations†,‡

XIV and 4 adult female dogs surgically fitted with ileal cannulas OF, MOS, OF þ MOS 5, 5, 10 g/kg (or 2 g OF/d) Ileal IgA concentrations " in OF þ MOS dogs, faecal microbial
XV populations $ by OF
Faecal total indole and phenol concentrations # by OF and OF þ MOS.
The dose of 2 g OF/d was maybe not high enough to affect the microbial
population in the distal colon or faeces
XVI Expt 1: 16 adult male beagles (12 kg, 3 years old) OF 0, 3, 6, 9 g/kg (or 0, 0·6, 1·2, 1·8 g OF/d) Total-tract digestibility of DM (P, 0·05), OM (P, 0·05), lipid (P, 0·01)
and CP (P, 0·07) #
Stool quality $
Faecal ammonia and urinary ammonia concentration numerically # by
45 %
Faecal concentrations of propionate (P, 0·05), butyrate (P¼ 0·15) and
total SCFA (P¼ 0·07) " in OF supplemented dogs
Expt 2: 4 adult female dogs (20 kg, 3 years old), OF 0, 2, 4, 6 g/kg (or 1, 2, 3 g OF/d) Faecal odour components and total anaerobe concentration $ . Total
surgically fitted with ileal cannulas aerobe concentration tended #
Ileal nutrient digestibility numerically " with increasing OF. Faecal con-
centrations of SCFA, BCFA, ammonia, phenols and indoles $ . Faecal
total aerobes " and Cl. perfringens #
Prebiotics in feed and pet food

XVII 7 ileal-cannulated adult female dogs, 7 £ 7 latin square OF 0, 3, 6, 9 g/kg Nutrient intake and ileal digestibility $
Inulin 0, 3, 6, 9 g/kg Total-tract digestibility of DM, OM and CP #
Faecal ammonia and SCFA (P, 0·10) concentrations "
Faecal total phenols #
Individual and total amines (only by OF) # by supplementation of OF
and inulin

* Reference: I, Willard et al. (1994); II, Sunvold et al. (1995a); III, Sunvold et al. (1995b); IV, Diez et al. (1997); V, Diez et al. (1998); VI, Sparkes et al. (1998a); VII, Sparkes et al. (1998b); VIII, Buddington et al. (1999); IX, Hesta et al. (2001); X, Strickling
et al. (2000); XI, Vickers et al. (2001); XII Beynen et al. (2002); XIII, Swanson et al. (2002a); XIV, Swanson et al. (2002c); XV, Swanson et al. (2002b); XVI, Flickinger et al. (2003b); XVII, Propst et al. (2003).
† Abbreviations: OF, oligofructose; SBF, soyabean fibre; MOS, mannan oligosaccharides; OM, organic matter; CP, crude protein; EE, (diethyl) ether extract; VFA, volatile fatty acids; DP, degree of polymerisation; BCFA, branched-chain fatty acids.
‡ ", increased; # , decreased; $ , no change.
S135
S136 J. M. A. J. Verdonk et al.

mercial diet in cats. Supplementation of 60 and 90 g/kg OF in the References

diet significantly affected faecal characteristics. Both OF (30 g/
kg) and inulin (30, 60 g/kg) resulted in lower apparent faecal pro- Ammerman E, Quarles C & Twining PV Jr (1988) Effect of dietary
tein digestibility. These results contradict Diez et al. (1997), who fructo-oligosaccharides on feed efficiency in floor pen-reared male
reported that 40 or 80 g diet OF/kg did not reduce total-tract broilers. Poult Sci 67, Suppl., 1.
Ammerman E, Quarles C & Twining PV Jr (1989) Evaluation of fructoo-
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(Strickling et al. 2000; Beynen et al. 2002; Grieshop et al. In vitro studies on the impact of carbohydrate-rich ingredients on
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