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The microbiota of the large intestine plays a fundamental role in maintaining the state of health of the gastrointestinal tract and the host. The use of specific dietary supplements such as prebiotics and synbiotics might positively influence the composition and metabolism of the intestinal microbial population. Several studies have been conducted on the use of prebiotics in dogs. Most studies have aimed to assess whether using prebiotics brings about an improvement in the canine intestinal ecosystem. Moreover, the effect of prebiotics on canine immune system has also been investigated. Among the prebiotics used in the studies present in the literature, short-chain fructooligosaccharides and oligofructose seem to be the most effective in modulating the canine intestinal ecosystem and improving intestinal absorption of minerals but with little or no effect on canine immune system. Conversely, mannanoligosaccharides may have a positive influence on the immune system of dogs. Some positive effects of prebiotics on canine intestinal microbiota might be enhanced when these are used in combination with one or more probiotic strains (synbiotic). Clinical effects of prebiotics have been investigated in humans and animal models but little evidence exists that prebiotics may be helpful in canine diseases. Finally, most studies on canine intestinal microbiota were conducted using traditional culture methods, so that more research remains to be done with modern molecular identification methods to investigate the effects of prebiotic substances. This paper presents an overview of the scientific literature dealing with the use of prebiotics and synbiotics in the canine species.
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[Ital J Anim Sci vol.13:2014] [page 169]
The utilisation of prebiotics
and synbiotics in dogs
Carlo Pinna, Giacomo Biagi
Dipartimento di Scienze Mediche
Veterinarie, Università di Bologna,
Ozzano dell’Emilia (BO), Italy
The microbiota of the large intestine plays a
fundamental role in maintaining the state of
health of the gastrointestinal tract and the host.
The use of specific dietary supplements such as
prebiotics and synbiotics might positively influ-
ence the composition and metabolism of the
intestinal microbial population. Several studies
have been conducted on the use of prebiotics in
dogs. Most studies have aimed to assess
whether using prebiotics brings about an
improvement in the canine intestinal ecosys-
tem. Moreover, the effect of prebiotics on
canine immune system has also been investi-
gated. Among the prebiotics used in the studies
present in the literature, short-chain fruc-
tooligosaccharides and oligofructose seem to be
the most effective in modulating the canine
intestinal ecosystem and improving intestinal
absorption of minerals but with little or no
effect on canine immune system. Conversely,
mannanoligosaccharides may have a positive
influence on the immune system of dogs. Some
positive effects of prebiotics on canine intestin-
al microbiota might be enhanced when these
are used in combination with one or more pro-
biotic strains (synbiotic). Clinical effects of pre-
biotics have been investigated in humans and
animal models but little evidence exists that
prebiotics may be helpful in canine diseases.
Finally, most studies on canine intestinal micro-
biota were conducted using traditional culture
methods, so that more research remains to be
done with modern molecular identification
methods to investigate the effects of prebiotic
substances. This paper presents an overview of
the scientific literature dealing with the use of
prebiotics and synbiotics in the canine species.
The gastrointestinal microbiota is a complex
ecosystem that influences gastrointestinal
functionality and the host’s health in general.
Prebiotics are non-digestible carbohydrates that
withstand digestion and reach the colon where
they stimulate growth and/or activity of benefi-
cial microbial species. Prebiotic substances
have been the object of several studies in dogs
as they may improve the composition of canine
intestinal microbiota, reducing the presence of
pathogens and toxins. Moreover, prebiotics may
result in enhanced immune function and could
be used in the treatment of specific diseases of
dogs such as infections by intestinal pathogens,
intestinal constipation and hepatic and renal
Recently, considerable interest has arisen
towards the use of fibre and prebiotic sub-
stances in the food intended for dogs. In fact,
though the dog is recognised as an animal
with a prevalently carnivorous diet, several
studies have demonstrated that by positively
modifying the intestinal microbiota, prebiotic
substances (mainly of vegetable origin) are
capable of exerting a large influence on the
trophic and health conditions of the digestive
system and, consequently, on the animal’s gen-
eral state of wellbeing. It is the purpose of this
review to present an overview of the scientific
literature dealing with the use of prebiotics
and synbiotics in the canine species.
The intestinal microbiota
of dogs
To date, studies on the characterisation of
canine intestinal microbiota are rather scarce
and little is known about which factors may
determine variations in terms of the number
and species of bacteria present. Like in all
mammals, a dog’s gastrointestinal tract is ster-
ile at birth, but with the passing of hours it
comes to be populated by numerous bacterial
species originating from the birth canal and
the surrounding environment, as well as from
maternal milk (Buddington, 2003). At the end
of the weaning period, with the transition to a
diversified diet, the resident microbial popula-
tion undergoes a considerable change in terms
of both species and number, also showing
enormous differences between one dog and
another (Schaible and Kaufmann, 2005).
Similarly to what had already been observed
by some authors in studies aimed at character-
ising human intestinal microbiota (Langendijk
et al., 1995; Harmsen et al., 2000), Greetham et
al. (2002) and more recently Hooda et al.
(2012) highlighted the scant reliability of tra-
ditional culture methods for isolating and
identifying dog intestinal microbiota.
Thanks to more recent studies making use of
molecular identification methods (Suchodolski
et al., 2009; Middelbos et al., 2010; Handl et al.,
2011; Suchodolski, 2011; Swanson et al., 2011;
Beloshapka et al., 2013), hundreds of phylo-
types have been identified in the intestine of
the dog. The phyla Firmicutes, Bacteroidetes,
Proteobacteria, Fusobacteria and Actino -
bacteria account for over 99% of the bacterial
species harboured in the intestine of dogs.
However, the phyla Spirochaetes, Tenericutes,
Verruco-microbia, Cyanobacteria and
Chloroflexi have also been identified. In the
study by Beloshapka et al. (2013), predominant
bacterial families in adult beagles fed raw
meat-based diets included Fusobacteriaceae,
Clostridiaceae, and Bacteroidaceae and pre-
dominant genera included Fusobacterium,
Cetobacterium,Clostridium, and Bacteroides.
Moreover, the canine intestine also hosts non-
bacterial microorganisms. In their work,
Swanson et al. (2011) identified archea (about
1% of all sequencing reads), fungi (about
0.01% of all sequences) and viruses (less than
1% of all sequencing reads).
With respect to the variability of the compo-
sition of canine intestinal microbiota, consid-
erable intraspecies differences have been
observed in dogs housed under identical condi-
tions and receiving the same diet, with very
marked variations in the microbial species
residing in the large intestine compared to
those found in the small intestine. Moreover,
there are large differences between the bacte-
rial species that inhabit the different sections
of the intestine and faecal microbiota
(Suchodolski et al., 2005).
The animal’s age is one of the factors influ-
Corresponding author: Prof. Giacomo Biagi,
Dipartimento di Scienze Mediche Veterinarie,
Università di Bologna, Via Tolara di Sopra 50,
40064 Ozzano dell’Emilia (BO), Italy.
Tel. +39.051.2097379 - Fax: +39.051.2097373.
Key words: Dog, Immune system, Intestinal
microbiota, Prebiotics, Synbiotics.
Received for publication: 16 September 2013.
Accepted for publication: 28 December 2013.
This work is licensed under a Creative Commons
Attribution NonCommercial 3.0 License (CC BY-
NC 3.0).
©Copyright C. Pinna and G. Biagi, 2014
Licensee PAGEPress, Italy
Italian Journal of Animal Science 2014; 13:3107
Italian Journal of Animal Science 2014; volume 13:3107
Non-commercial use only
[page 170] [Ital J Anim Sci vol.13:2014]
encing the composition of faecal microbiota: in
older animals, lecithinase-positive clostridia
and bacteria belonging to the class bacilli are
found in higher concentrations than lacto-
bacilli, pepto-streptococci and bifidobacteria
(Benno and Mitsuoka, 1989; Benno et al., 1992;
Mitsuoka, 1992); furthermore, faecal microbio-
ta seems to be influenced not only by age, but
also by the dog breed (Simpson et al., 2002).
Unfortunately, studies that investigated the
effect of age on canine intestinal microbiota
were conducted using traditional culturing
techniques and no research was done using
current assays.
Main effects of intestinal
microbiota on the host’s health
Gastrointestinal microbiota is a complex
ecosystem made up of hundreds of bacterial
species, some of which are potentially patho-
genic, while others are considered good for the
host (Roberfroid et al., 1995). The beneficial
microorganisms that reside in the large intes-
tine influence gastrointestinal functionality
and the host’s health in general, in virtue of
some principal mechanisms: i) detoxification
of some toxic substances introduced through
the diet or newly formed as a result of metabol-
ic processes of the body and of intestinal
microbiota (Tomomatsu, 1994); ii) barrier
effect against the proliferation of potentially
pathogenic bacteria and their adhesion to the
intestinal mucosa, thanks to occupation of the
attack sites of these microorganisms and pro-
duction of selective antimicrobial substances
(Liévin-Le Moal and Servin, 2006); iii) uptake
of ammonia and amine used as a source of
nitrogen to support microbial protein synthe-
sis, with a consequent reduction in the intes-
tinal absorption of these undesirable sub-
stances (Howard et al., 2000); iv) interaction
with the host immune system (Round and
Mazmanian, 2009; Cerf-Bensussan and
Gaboriau-Routhiau, 2010); and v) production
of vitamins (LeBlanc et al., 2012).
The short-chain fatty acids (SCFA) that
derive from microbial fermentation of carbohy-
drates represent a source of energy that the
host can use. In particular, SCFA are used as
energy substrates by colonocytes (butyric
acid), hepatocytes (propionic acid and lactic
acid) and peripheral tissues (acetic acid;
Cummings and Englyst, 1987). It has been esti-
mated that microbial fermentations can cover
between 2 and 7% of the maintenance energy
requirements of an adult dog (Herschel et al.,
1981; Stevens and Hume, 1998). Besides creat-
ing a favourable environment for beneficial
microbial species, the pH reduction caused by
SCFA induces a shift from ammonia to ammo-
nium ions, thus preventing absorption by the
intestine (McQuaid, 2005).
Prebiotics and synbiotics
According to a recent definition, a prebiotic
is a selectively fermented ingredient that allows
specific changes, both in the composition
and/or activity in the gastrointestinal microbio-
ta that confers benefits upon host well-being
and health (Roberfroid, 2007). To be effective,
a prebiotic has to withstand digestion and
reach the colon where it selectively stimulates
the growth and/or metabolic activity of micro-
bial species that promote evident beneficial
effects for the host.
Prebiotics are non-digestible carbohydrates,
mainly oligosaccharides with a low degree of
polymerisation, obtained by extraction from
vegetable raw materials (for example, hot
water extraction of inulin from chicory, arti-
chokes, bananas and wheat and of specific
oligosaccharides from soybeans; Franck and
Bosscher, 2009), by enzymatic synthesis [for
example, the fructooligosaccharides (FOS)
produced from sucrose and galactooligosac-
charides (GOS) obtained from lactose (Fujita
et al., 1992; Spiegel et al., 1994)] or else by par-
tial enzymatic hydrolysis of oligosaccharides
and polysaccharides [for example, the hydroly-
sis of inulin to FOS and of xylan polymers to
xylooligosaccharides (XOS) under the action
of xylanase (Imaizumi et al., 1991; De Bruyn et
al., 1992)]. Main characteristics of some prebi-
otic substances are presented in Table 1.
However, fructans such as inulin (a long-chain
fructan, up to 60 units), oligofructose (OF;
fructans chains with 8 to 10 units, often
referred to as long-chain FOS) and short-chain
FOS (fructans chains with 3-5 units) have
been widely tested in companion animals
(Hernot et al., 2008) and seem to be the most
frequently used prebiotic substances in the pet
food industry. Moreover, pet food ingredients
may contain certain amounts of natural prebi-
otic substances (Van Loo et al., 1995; Campbell
Pinna and Biagi
Table 1. Main characteristics of some non-digestible oligosaccharides with prebiotic potential.
Name Chemical composition Production process dp
Inulin β(2-1) fructans with a terminal glucose Extraction from chicory root, artichokes, 11-60
bananas and wheat
Oligofructose (long-chain β(2-1) fructans Enzymatic (β-fructosidase) synthesis from sucrose 8-10
fructo-oligosaccharides) or partial enzymatic or chemical hydrolysis from inulin
Short-chain β(2-1) fructans Enzymatic (β-fructosidase) synthesis from sucrose 3-5
fructo-oligosaccharides or partial enzymatic or chemical hydrolysis from inulin
Galacto-oligosaccharides Chains of galactose with some glucose Enzymatic (β-galactosidases) synthesis 2-5
(oligogalactose) from lactose
Soybean-oligosaccharides Mainly galactose with presence of mannose, Extraction from soybeans 3-4
glucose, fructose, arabinose and xylose
Xylo-oligosaccharides β(1-4)-linked xylose Partial enzymatic (xylanases) hydrolysis of 2-10
polyxylans polymers from vegetables and fruits
Lactitol 4-O-β-D-galactopyranosyl-D-glucitol Hydrogenation of lactose 2
Lactulose Galactose and fructose Isomerisation of lactose 2
dp, degree of polymerisation.
Non-commercial use only
[Ital J Anim Sci vol.13:2014] [page 171]
et al., 1997; Hussein et al., 1998; Moshfegh et
al., 1999). The fructan content of some veg-
etable raw materials is presented in Table 2.
The combination of a prebiotic and one or
more probiotic bacterial strains is defined as a
synbiotic (Schrezenmeir and De Vrese, 2001).
The simultaneous combination of probiotic
strains and a source of prebiotic molecules
that they can metabolise might offer the
administered bacterial strains greater possibil-
ities of growing and colonising the host, thus
promoting the potential beneficial effects.
Effects of prebiotic substances
in healthy dogs
Effects on composition of intestinal
Flickinger et al. (2003b) reviewed the
effects of inulin and OF in domesticated ani-
mals. The effects of prebiotics in dogs and
other companion animals were recently
reviewed by Swanson and Fahey (2006) and
Hernot et al. (2008). A brief summary of the
effects of prebiotics on canine intestinal
microbiota is reported in Table 3.
The effects on canine intestinal microbiota
which result from the administration of sub-
stances with prebiotic action have been stud-
ied by various authors, but with sometimes
conflicting results. For example, in a study
with adult beagles, Flickinger et al. (2003a)
found that the use of OF [fructose chains
obtained from hydrolysed inuline, degree of
polymerisation (dp) of 3 to 10] at different
doses (3, 6 and 9 g/kg of diet) linearly
Prebiotics and synbiotics in dogs
Table 2. Fructan content of some vegetable raw materials.
Vegetable Moshfegh et al. (1999) Campbell et al. (1997)
Inulin, g/100 g of as is OF, g/100 g of as is Short-chain FOS, g/100 g of DM
Artichoke, globe 4.4 0.4 2.2
Banana 0.5 0.5 0.6
Barley 0.8 0.8 1.9
Chicory root 41.6 22.9 2.1
Jerusalem artichoke 18.0 13.5 28.6
Oats -- 0.4
Onion powder 18.3 18.3 4.8
Peas -- 0.8
Potato, sweet -- 0.1
Rye -- 4.1
Wheat - 1.4
Wheat bran 2.5 2.5 4.0
OF, oligofructose; FOS, fructooligosaccharides; DM, dry matter.
Table 3. Effects of prebiotic administration on composition of canine faecal microbiota.
Reference Prebiotic used Level of Method of Lactobacilli Bifidobacteria C. perfringens Total clostridia E. coli/coliforms
inclusion, g/kg determination
Howard et al., 200 scFOS 15 Selective media ↔↔ ND ↑↔
Strickling et al., 2000 FOS 5 ↔↔ ↔
MOS 5 Selective media ↔↔ ↓ ND
XOS 5 ↔↔ ↔
Willard et al., 2000 FOS 10 Selective media ↔↔ ND ↔↔
Flickinger et al., 2003b OF 9 Selective media ↔↔ ↓ ND ND
Middelbos et al., 2007a scFOS+dried yeast 12+3 DNA analysis ↑↑
scFOS+dried yeast 9+6 ↑↑↔ ↔
Barry et al., 2009 scFOS 2 and 4 DNA analysis ↔↔ ND
Inulin 2 and 4 ↔↔ ↔
Biagi et al., 2010 Lactitol 10 Selective media NR ND
Beloshapka et al., 2012 Polydextrose 5, 10 and 15 DNA analysis ↔↔ ↓ ND
scFOS, short-chain fructooligosaccharides; ND, not determined; FOS, fructooligosaccharides; MOS, mannanoligosaccharides; XOS, xylooligosaccharides; OF, oligofructose; NR, not recovered.
°Bacterial counts were conducted on intestinal digesta.
Non-commercial use only
[page 172] [Ital J Anim Sci vol.13:2014]
increased the aerobic population and reduced
C. perfringens in faeces [respectively, +0.8 and
-0.3 log10 cfu/g of faecal dry matter (DM) with
9 g/kg of OF, compared with control], without
exerting any influence on the faecal popula-
tion of lactobacilli and bifidobacteria. The lat-
ter result was also observed by Swanson et al.
(2002b) when adult dogs were fed FOS at 2 g/d.
In another study (Howard et al., 2000), the
administration of short-chain FOS (at 15 g/kg
of diet) increased aerobic population in the
distal colon of adult dogs (+1.8 log10 cfu/g of
faecal DM, compared with a diet containing
cellulose at 60 g/kg). In the study by Grieshop
et al. (2004), feeding adult dogs with chicory
(10 g/kg of diet) or mannanoligosaccharides
(MOS; 10 g/kg of diet) increased faecal bifi-
dobacteria (+0.4 and +0.5 log10 cfu/g of faecal
DM, respectively) and MOS also resulted in a
decrease of faecal E. coli concentrations.
In a study by Strickling et al. (2000), the use
of FOS (OF from chicory root), MOS (from
yeast cell wall of Saccharomyces cerevisiae) or
XOS (mainly made of xylobiose and xylotriose,
which are dimers and trimers of xylose, respec-
tively) at a dietary concentration of 5 g/kg DM
did not affect the number of faecal bifidobacte-
ria in adult dogs; compared with animals
administered FOS and XOS, those receiving the
diet supplemented with MOS showed a numer-
ical reduction in C. perfringens in the faeces (-
0.26 and -0.68 log10 cfu/g of faecal DM, respec-
tively). Although MOS are often described as
prebiotic non-digestible oligosaccharides, they
are not fermented by beneficial bacteria;
instead, MOS act by binding and removing
pathogens from the gastrointestinal tract and
stimulating the immune system (Spring et al.,
2000). In a study by Vickers et al. (2001), in
vitro fermentation of different sources of inulin
and FOS increased concentrations of SCFA,
whereas fermentation of MOS resulted in mod-
erate production of SCFA.
In another study, Barry et al. (2009) did not
observe any effect on the faecal microbiota of
dogs after administering short-chain FOS or
inulin at relatively low doses (2 and 4 g/kg of
diet). Vanhoutte et al. (2005), in contrast,
highlighted the positive role played by a combi-
nation of OF (4.5 g/d) and inulin (5.6 g/d) on
the intestinal microbiota of dogs; their find-
ings included, in particular, an increase in the
populations of streptococci; interestingly, no
bifidobacteria were detected in any of the
seven dogs that were involved in the study.
Similarly, Willard et al. (2000) reported that
bifidobacteria and lactobacilli were inconsis-
tently isolated from faeces of dogs during a
study in which FOS were used as a dietary sup-
plement at 10 g/kg of diet.
When administered to a group of adult shep-
herd dogs, lactosucrose (1.5 g/d), a bifidogenic
fibre enzymatically synthesised from D-galac-
tose, D-fructose and D-glucose, showed to be
effective in increasing bifidobacteria (+0.5
log10 cfu/g of faeces) and decreasing C. perfrin-
gens (-1.6 log10 cfu/g of faeces) in the faeces
(Terada et al., 1992).
In a recent study (Beloshapka et al., 2012),
the utilisation of polydextrose (a polysaccha-
ride synthesised by random polymerisation of
glucose and sorbitol with an average dp of 12)
at dietary concentrations of 5, 10 and 15 g/kg of
diet linearly reduced faecal concentrations of
C. perfringens in healthy adult dogs (-0.3, -0.4
and -0.8 log10 cfu/g of faecal DM with polydex-
trose at 5, 10 and 15 g/kg of diet, respectively),
without affecting the faecal concentrations of
E. coli, lactobacilli and bifidobacteria.
In a study by Biagi et al. (2010), various
fibre sources and prebiotic substances were
tested in the dog, both in vitro and in vivo.
Among the substrates used in the in vitro test,
FOS (two different sources: from partially
hydrolysed inulin from chicory with dp 3 to 7
and from chicory with dp 2 to 10), lactitol,
inulin from chicory (two sources: one with
dp>20 and the other one with dp 2 to 60), cit-
rus and apple pectins and psyllium fibre
showed to be rapidly fermentable by canine
intestinal microbiota, resulting in a reduction
in the pH of faecal inocula. Among the sub-
stances tested, lactitol had an evident positive
effect on undesirable bacterial populations, as
reflected in an in vivo reduction in the concen-
trations of coliform bacteria and C. perfringens
(-2.2 and -1.0 log10 cfu/g of faeces, respective-
ly) when lactitol was fed to adult dogs at 10
g/kg of diet for 30 d. Middelbos et al. (2010)
reported that supplementing the diet with beet
pulp had the effect of significantly increasing
the clostridia count in dog faecal specimens
(from 83 to 90% of bacteria-assigned
sequences obtained using pyrosequencing). In
the previously cited study by Biagi et al.
(2010), compared with control, beet pulp
induced an increase in the pH (+0.13) and
counts of coliforms (+0.5 log10 CFU/mL) of fae-
cal inocula. Moreover, Middelbos et al. (2010)
observed that beet pulp also induced a reduc-
tion in the concentration of bacteria belonging
to the phylum Actinobacteria (from 1.4 to 0.8%
of total sequences), which includes bifidobac-
teria, without, however, affecting the number
of bacilli, among which we find numerous bac-
terial species considered to be beneficial and
belonging to the genus Lactobacillus spp.
According to what emerged during the study
conducted by Middelbos et al. (2007a), the
dietary inclusion of two combinations of short-
chain FOS and dried yeast as a source of MOS
(12 g/kg FOS+3 g/kg yeast cell wall and 9 g/kg
FOS+6 g/kg yeast cell wall, respectively) result-
ed in an increase in the faecal populations of
bifidobacteria (+1.0 and +1.4 log10 CFU/g of
feacal DM, respectively) and lactobacilli (+0.9
log10 CFU/g of feacal DM for both treatments)
and, consequently, a lowering of the faecal pH
(-0.3 and -0.4, respectively). The authors also
highlighted a tendency toward a reduction in
the faecal counts of E. coli, hypothesising that
MOS had the ability to bind to the fimbriae of
some pathogenic bacteria, such as, precisely,
coliform bacteria and Salmonella spp., thus
preventing them from colonising the intestinal
wall. In another study with adult dogs
(Middelbos et al., 2007b), a yeast cell wall
preparation fed at different levels of inclusion
(0.5, 2.5, 4.5 and 6.5 g/kg of diet) as a source of
MOS linearly reduced faecal counts of E. coli
(-0.9 log10 CFU/g of feacal DM in dogs receiv-
ing 6.5 g/kg of yeast cell wall).
Beloshapka et al. (2013) investigated the
effect of inulin (14 g/kg of diet) or a yeast cell
wall extract (14 g/kg of diet) in adult dogs
receiving raw meat-based diets [containing
approximately per kg of diet 250 to 300 g of
crude protein (CP) and 450 to 500 g of fat].
Administration of inulin resulted in lower fae-
cal abundance of Enterobacteriaceae and
Escherichia and higher faecal lactobacilli while
the yeast cell wall extract increased faecal bifi-
dobacteria. Moreover, inulin reduced faecal
abundance of some Bacteroides and
Fusobacterium species.
Based on results from the cited studies,
despite some discrepancies, the use of prebiot-
ic substances seems to represent an efficient
way to manipulate the gastrointestinal ecosys-
tem of dogs, increasing the abundance of ben-
eficial bacteria and reducing the presence of
undesired microbes. Among the prebiotics that
have been tested, short-chain FOS and OF,
when used at concentrations higher than 10
g/kg of diet, seem to be the most effective in
modulating the canine intestinal ecosystem.
Effects on intestinal ammonia
and other bacterial catabolites
In general, limitation of carbohydrates as a
source of energy in the hindgut leads to micro-
bial proteolysis with consequent release of
toxic substances, such as ammonia and
amines (Russell et al., 1983).
Prebiotics might reduce concentrations of
ammonia in the animal intestine, as increased
fermentation leads to higher amounts of nitro-
gen converted into bacterial protein (Howard
et al., 2000). Moreover, the use of prebiotics
might reduce intestinal proteolysis and pro-
Pinna and Biagi
Non-commercial use only
[Ital J Anim Sci vol.13:2014] [page 173]
duction of putrefactive compounds by increas-
ing the number of beneficial bacteria, enhanc-
ing SCFA production and reducing luminal pH
(Terada et al., 1992). In the study by Biagi et al.
(2010), compared with control, the ammonia
concentration was lower in the inocula to
which citrus pectin was added (-23%) and
higher in those treated with gluconic acid and
inulin (+17 and 20%, respectively). In the
same study, FOS and lactitol had no effect on
ammonia concentrations. In a previous in vitro
study that used swine cecal inoculum, gluconic
acid instead brought about a reduction in the
ammonia concentration (Biagi et al., 2006).
Terada et al. (1992) reported a significant
decrease of faecal ammonia (-60%) and bad
smell of faeces in dogs receiving 1.5 g/d of lac-
tosucrose. Similarly, in the study by Flickinger
et al. (2003a), faecal ammonia concentrations
tended to be reduced by OF but concentrations
of other protein catabolites remained unaffect-
ed. In contrast, ammonia intestinal and faecal
concentrations were not influenced by diet in
the already cited studies by Strickling et al.
(2000) and Barry et al. (2009); the same result
was observed in the study by Beynen et al.
(2002) in which adult dogs received a diet sup-
plemented with OF (dp from 3 to 20) at 10 g/kg
for 30 d. Similarly, the use of FOS at 30 g/kg in
adult dogs did not reduce faecal ammonia
(Hesta et al., 2003). In the study by Swanson et
al. (2002b), the use of FOS reduced faecal con-
centrations of indole (a protein catabolite of
bacterial origin) by 1.2 mol/g of faecal DM but
faecal ammonia and biogenic amines were
unaffected. Beloshapka et al. (2012) reported
that faecal indole concentrations tended to
decrease with increasing dietary levels of poly-
dextrose but other protein catabolites (ammo-
nia, phenol and branched-chain fatty acids)
were not influenced by treatment.
Finally, Propst et al. (2003) reported that the
use of different concentrations (3, 6 and 9 g/kg
of diet) of OF or inulin in adult dogs resulted in
increased faecal ammonia and isovalerate (a
branched-chain fatty acid that derives from
protein fermentation) concentrations. In the
same study, OF also resulted in increased fae-
cal concentrations of total biogenic amines
and SCFA and reduced faecal phenols. Zentek
et al. (2002) found that the intake of MOS (1
g/kg BW/d) had the effect of lowering both the
pH (-0.3) and the ammonia concentration (-38
µmol/g of faeces) in canine faeces. The same
authors also noted that the utilisation of MOS
significantly decreased faecal unbound water
content (from 165 to 55 g/kg of faeces) and
apparent digestibility of protein, the latter
result presumably as a consequence of the
increased viscosity of the intestinal chyme.
The conflicting results that are observed
when prebiotics are fed to dogs are not easy to
explain. First, different basal diets might
cause some discrepancy: diets that are rich in
wheat, barley or oats are likely to contain sig-
nificant amounts of soluble fiber (including
short-chain fructans; Van Loo et al., 1995)
that might mask the effect of prebiotics.
Another cause of conflicting results might
reside in the type of prebiotics that are used:
in fact, within the same category, prebiotic
substances may differ based on their origin,
degree of polymerisation, etc. Obviously, the
level of dietary inclusion of prebiotics also
has an influence on their effects: in particu-
lar, FOS seem to be effective at concentra-
tions higher than 10 g/kg of diet. Moreover, in
many studies the effects of prebiotics on
intestinal microbiota were evaluated based
only on faecal analyses. This is very common
today, as most scientists try to avoid for ethi-
cal reasons any type of invasive methods of
analysis when a study is conducted with dogs.
Unfortunately, it is well known that the con-
centration of bacterial metabolites able to
cross the intestinal mucosa can vary while
digesta move along the intestine (Stevens
and Hume, 1998). Therefore, faeces might
not reflect the changes in the concentration
of ammonia, SCFA and other molecules that
the prebiotic may have induced in the colon.
Finally, another reason for discrepancies in
the effect of prebiotics might reside in the
inconsistent presence of their target bacteria
in dogs, namely bifidobacteria and lactobacil-
li. In fact, while some authors reported high
average concentrations of bifidobacteria in
the faeces of experimental dogs (Flickinger et
al., 2003a; Middelbos et al., 2007a), bifidobac-
teria were inconsistently isolated from canine
faeces in the studies by Willard et al. (2000),
Greetham et al. (2002), Apanavicius et al.
(2007), Biagi et al. (2007, 2010), Lamendella
et al. (2008). Similarly, Willard et al. (2000)
reported that lactobacilli were inconsistently
isolated from dog faeces.
In the study by Beloshapka et al. (2013),
according to 454 pyrosequencing, bifidobacteria
were not detectable and lactobacilli were pres-
ent at less than 0.05% of total sequences. In the
same study, when faecal samples were analysed
by quantitative polymerase chain reaction both
Bifidobacterium and Lactobacillus were
detectable, even if at low levels. Authors con-
cluded that bifidobacteria and lactobacilli might
be underestimated using these 16S rRNA gene-
based sequencing approaches due to the pres-
ence of several sources of bias, as already high-
lighted by other authors (Garcia-Mazcorro et al.,
2011; Handl et al., 2011).
Effects on intestinal short-chain
fatty acids
Short-chain fatty acids (acetate, propionate,
lactate and butyrate) are the main products of
carbohydrate fermentation. There is evidence
that butyric acid is the preferred fuel substrate
of the terminal ileal mucosa (Chapman et al.,
1995) and the epithelial cells of the large intes-
tine (Roediger, 1980). Moreover, these organic
acids possess antibacterial properties
(Knarreborg et al., 2002) and reduce luminal
pH thus improving animal intestinal health.
In the in vitro study by Biagi et al. (2010),
total SCFA in the inocula were increased by
lactitol (+18%), inulin from chicory (+17%),
pectins from apple (+15%), psyllium fiber
(+21%) and partially hydrolysed guar gum
(+69%). The higher SCFA concentrations lead
to significantly lower pH values of inocula.
Similarly, faecal propionic acid and total SCFA
were increased in dogs fed OF at 6 g/kg of diet
(+55 and +31%, respectively; Flickinger et al.,
2003a). These results agree with those
obtained by Propst et al. (2003), who reported
higher faecal concentrations of acetic, propi-
onic and butyric acids in dogs receiving inulin
or OF at different levels of inclusion (3, 6 and
9 g/kg of diet). Similarly, the utilisation of poly-
dextrose at 5, 10 and 15 g/kg of diet in adult
dogs resulted in lower faecal pH and higher
faecal concentrations of acetate, propionate
and total SCFA (Beloshapka et al., 2012).
Conversely, Barry et al. (2009) reported
decreased faecal concentrations of acetic acid,
propionic acid and total SCFA in dogs fed inulin
at 2 and 4 g/kg of diet. In a study by Twomey et
al. (2003), the administration of FOS at 30 or 60
g/kg of diet to dogs resulted in higher faecal lac-
tate concentrations (85, 143 and 289 mmol/kg of
faeces for control, FOS at 30 g/kg and FOS at 60
g/kg, respectively) and lower faecal pH (5.4, 5.3
and 5.0 for control, FOS at 30 g/kg and FOS at 60
g/kg, respectively).
Effects on faecal quality
It has been observed that the utilisation of
prebiotics can result in humans in increased
stool weight and decreased stool transit time
(Macfarlane et al., 2006). Prebiotics are some-
times proposed in humans as mild laxatives
despite the fact that a clear scientific evidence
of this effect is still lacking (Cummings and
Macfarlane, 2002).
Twomey et al. (2003) observed that adminis-
tration of FOS at 30 or 60 g/kg of diet to dogs
resulted in decreased faecal dry matter (DM;
327, 303 and 296 g/kg of faeces for control, FOS
at 30 g/kg and FOS at 60 g/kg of diet, respective-
ly). Conversely, several authors (Strickling et
al., 2000; Swanson et al., 2002b; Flickinger et al.,
Prebiotics and synbiotics in dogs
Non-commercial use only
[page 174] [Ital J Anim Sci vol.13:2014]
2003a; Beloshapka et al., 2012) did not observe
any effect of prebiotic administration on canine
faecal dry matter when prebiotics were admin-
istered at lower doses than those used by
Twomey et al. (2003). Based on the literature, it
seems evident that high dietary concentrations
of prebiotics may have an influence on faecal
volume and consistency. Because, in general,
pet owners expect their dogs to excrete small
and firm faeces, prebiotics should be adminis-
tered to dogs at relatively low concentrations
(less than 20 g/kg of dietary DM).
Effects on nutrient digestibility
Several authors reported that prebiotic con-
sumption by dogs resulted in lower organic
matter (OM) and CP total tract apparent
digestibility (Diez et al., 1997, 1998a, 1998b;
Zentek et al., 2002; Flickinger et al., 2003a;
Hesta et al., 2003; Propst et al., 2003;
Middelbos et al., 2007a; Beloshapka et al.,
2012). Conversely, Middelbos et al. (2007b)
reported higher ileal digestibility of OM (79.4
vs 74.5%) and CP (72.4 vs 65.3%) in dogs fed
spray-dried yeast cell wall at 6.5 g/kg of diet. In
the study by Twomey et al. (2003), total tract
apparent digestibility of protein in dogs receiv-
ing FOS at 30 or 60 g/kg of diet was unaffected.
In general, prebiotic consumption leads to
higher faecal nitrogen concentrations because
faecal bacterial mass is increased (Hesta et al.,
2003; Karr-Lilienthal et al., 2004) thus leading
to lower apparent digestibility of OM and CP. As
already mentioned, conversion of ammonia
nitrogen into bacterial protein is a positive
effect that can improve intestinal health.
Another possible effect of prebiotics is an
improved intestinal absorption of minerals. In a
study with adult dogs, Beynen et al. (2002) found
that the use of OF at 10 g/kg increased apparent
calcium (+86%) and magnesium (+67%) absorp-
tion, whereas phosphorus absorption was unaf-
fected. Similarly, the use of lactulose at 1 or 3 g/MJ
of metabolisable energy in adult dogs increased
apparent calcium (+63 and +83%, respectively)
and magnesium (+27 and +52%, respectively)
absorption in a dose-dependent manner, but not
phosphorus (Beynen et al., 2001). Results from
these two studies seem to confirm that, similarly
to what has been observed in other animal
species and humans (Scholz-Ahrens et al., 2007),
prebiotics may have a positive influence on calci-
um and magnesium intestinal absorption in dogs.
The positive effects of prebiotics on mineral
absorption have been attributed to several mech-
anisms, including increased solubility of minerals
and enterocytes proliferation because of
increased bacterial production of SCFA and
increased expression of calcium binding proteins
(Scholz-Ahrens et al., 2007).
Effects on immune system
The gastrointestinal tract is the main site of
interaction between the immune system and
microorganisms. While the immune system
plays a very important role in maintaining
homeostasis with intestinal microbiota, bacte-
ria residing in the gut influence development of
gut-associated lymphoid tissues and shape ani-
mal immunity (Round and Mazmanian, 2009).
The effects of prebiotics on immune system
of dogs and other animal species were recently
reviewed by Lomax and Calder (2009). While
the utilisation of 8.7 g/kg of diet of a combina-
tion of high fermentable fiber sources (contain-
ing a mixture beet pulp, FOS and gum arabic;
Field et al., 1999), short-chain FOS at 9.1 g/kg of
diet (Adogony et al., 2007) or inulin (30 g/kg of
diet; Verlinden et al., 2006) had only little or no
effect on canine immune system, the utilisation
of FOS in combination with MOS increased ileal
IgA concentrations (+1.5 mg/g DM; both FOS
and MOS were used at 1 g/d; Swanson et al.,
2002b). In another study (Swanson et al.,
2002c), dietary supplementation with FOS at 2
g/d plus MOS at 1 g/d increased blood lympho-
cytes and reduced blood neutrophils in adult
dogs. Conversely, in the study by Grieshop et al.
(2004), a combination of chicory (10 g/kg of
diet) and MOS (10 g/kg of diet) reduced periph-
eral blood lymphocyte concentration with no
other effect on immune system. Similarly,
Middelbos et al. (2007b) observed only limited
effects on canine immune system when a yeast
cell wall preparation was fed to adult dogs. At
present, the prebiotic effects on canine immu-
nity have not been well studied and more
research is needed. Nevertheless, based on the
cited studies, despite some discrepancies, the
utilisation of MOS seems to enhance immune
system in dogs. Conversely, based on current
knowledge, the influence of FOS and inulin on
canine immune system might be negligible.
Effects of synbiotics
in healthy dogs
Ogué-Bon et al. (2010) conducted in vitro
tests to assess the synergistic potential of some
prebiotic substrates (FOS, GOS and inulin) and
several probiotic strains (Bifidobacterium
bifidum, B. longum, Lactobacillus plantarum, L.
acidophilus and L. rhamnosus). In this study, a
specificity between bacterial strain and fer-
mentable substrate emerged clearly; for exam-
ple, GOS were rapidly used by bifidobacteria
(thanks to their ability to synthesise -galactosi-
dase), as had already been highlighted by other
authors (Gopal et al., 2001; Rada et al., 2008;
Zanoni et al., 2008). FOS, on the other hand,
were shown to be easily metabolised by all the
test strains with the exception of L. rhamnosus;
this latter finding confirms what had been pre-
viously observed by Kaplan and Hutkins (2000)
and is probably ascribable to a deficiency of the
enzyme -fructosidase in L. rhamnosus strains.
Results from the study by Ogué-Bon et al.
(2010) also indicated that the synbiotic combi-
nation GOS+B. bifidum induced greater modu-
lation of canine faecal microbiota compared
with GOS alone.
In a study by Swanson et al. (2002a), two
experiments were performed with a group of
dogs receiving for 28 d short-chain FOS (4 g/d),
a strain of Lactobacillus acidophilus (2 x 109
cfu/d) or their combination. In the second exper-
iment, compared with control, FOS supplemen-
tation increased faecal total aerobes (+0.6 log10
cfu/g of faecal DM), bifidobacteria (+0.6 log10
cfu/g of faecal DM) and lactobacilli (+0.7 log10
cfu/g of faecal DM). The combination of FOS and
L. acidophilus resulted in effects of larger entity
on the concentration of bacterial metabolites
compared to administration of either of the two
preparations alone. More specifically, the synbi-
otic was particularly effective in reducing the
faecal concentrations of ammonia (compared
with control, -5% in the second experiment) and
of some catabolites (branched-chain fatty acids;
compared with control, -8 and -22% in experi-
ment 1 and 2, respectively) deriving from pro-
tein fermentation.
Tzortzis et al. (2004b) carried out an in vitro
investigation into the effects on canine gut
microbiota of several prebiotic substances,
including a particular galactooligosaccharide
[galactosyl melibiose mixture (GMM); synthe-
sised using -galactosidase isolated from L.
reuteri], in association with L. acidophilus and
L. reuteri strains. The authors observed that all
of the various tested substrates (FOS with dp 2
to 9, GMM, melibiose and raffinose) possessed
prebiotic properties, but GMM showed a higher
increase in bifidobacteria and lactobacilli as
well as a higher decrease in clostridia com-
pared to the other prebiotics (FOS, melibiose
and raffinose). Furthermore, the increase in
the counts of bifidobacteria was highest for the
combination of GMM and L. reuteri (compared
with inoculum at start, +1.3 log10 CFU/mL).
During another in vitro study, Tzortzis et al.
(2004a) investigated the effect of various car-
bon sources on the production of extracellular
antagonistic compounds against two
Escherichia coli strains and Salmonella enteri-
ca serotype Typhimurium by three canine-
derived lactobacilli strains (L. mucosae,L. aci-
dophilus and L. reuteri). Results showed that
Pinna and Biagi
Non-commercial use only
[Ital J Anim Sci vol.13:2014] [page 175]
production of antimicrobial compounds by lac-
tobacilli strains was influenced by substrate in
a synergistic mode of action.
In another study (Garcia-Mazcorro et al.,
2011), the administration for 21 d of a com-
mercial synbiotic containing 7 different pro-
biotic species (Enterococcus faecium,
Streptococcus salivarius ssp. termophilus,
Bifidobacterium longum, Lactobacillus aci-
dophilus,L. casei ssp. rhamnosus,L. plan-
tarum and L. delbrueckii ssp. bulgaricus) and
a mixture of FOS and arabinogalactans
induced a significant increase in the concen-
trations of Enterococcus and Streptococcus
spp. (species present in the probiotic supple-
ment) in dog faeces during synbiotic admin-
istration. In the same study, none of the eval-
uated serum (cobalamin, folate, IgA, trypsin-
like immunoreactivity and pancreatic lipase
immunoreactivity) or faecal (IgA and a1-pro-
teinase inhibitor) markers of gastrointestinal
and immune function were influenced by syn-
biotic administration. The association
between commercially available probiotic
strains (Lactobacillus plantarum, two strains
of L. acidophilus, L. rhamnosus,Bifidobac -
terium longum and B. bifidum) and commer-
cially available fibre blends (rice bran, citrus
pectin and barley and maize starch) was stud-
ied by Ogué-Bon et al. (2011). The authors
observed that rice bran was capable of increas-
ing SCFA production and stimulating the
growth of probiotic strains. This finding is par-
ticularly interesting since rice bran is com-
monly used as a fibre supplement in the pet
food industry and could therefore add a prebi-
otic effect to the known dietary effects tied to
the use of this type of fibre, which include
increasing the faecal mass and providing a lax-
ative action. Finally, the authors noted that rice
bran on its own had the same effect on the fae-
cal counts of bifidobacteria and lactobacilli and
concentrations of SCFA as the various synbiot-
ic combinations, thus revealing that in this
case no synergism existed between the probi-
otic strains and fibre source used. Despite the
relatively low number of studies that have been
conducted with synbiotics in the canine
species, there is some evidence that the proper
combination of a prebiotic with one or more
probiotic strains might result in a synergistic
effect on dog intestinal microbiota.
Roles of prebiotic substances
in canine disease
One potential benefit from the utilisation of
prebiotics in humans and monogastric ani-
mals is to reduce infection by intestinal
pathogens (Callaway et al., 2008). In fact, pre-
biotics can stimulate the growth of bacteria
that compete against pathogens (Roberfroid,
2007) and also modulate activity of the
immune system (Seifert and Waltz, 2007;
Lomax and Calder, 2009).
By increasing the number of lactobacilli in
the intestine, inulin at 10 g/kg of diet could
provide positive action against Salmonella
typhimurium infections, based on what was
observed by Apanavicius et al. (2007) in exper-
imentally infected puppies. The antagonist
action of lactobacilli against Salmonella
typhimurium (de Moreno de LeBlanc et al.,
2010) is in fact well known. In the already cited
study by Apanavicius et al. (2007), inuline sup-
plementation decreased enterocyte sloughing,
an indicator of intestinal damage, and
increased acetate intestinal concentrations
whereas the utilisation of FOS at 10 g/kg of
diet resulted in decreased enterocyte slough-
ing but did not affect lactobacilli counts.
As already mentioned, the use of prebiotics
might reduce the intestinal concentrations of
ammonia and, as a consequence, the amount of
ammonia that is absorbed into circulation and
burdens liver and kidneys (Howard et al., 2000).
Dogs with hepatic failure do not metabolise
ammonia well and might not be able to convert
ammonia into urea. On the other hand, dogs
with renal functional impairment lose their
ability to excrete nitrogen wastes. For these rea-
sons, prebiotics such as lactulose (McQuaid,
2005) could be used in the treatment of dogs
with renal or liver failure to prevent uremia and
hepatic encephalopathy, respectively.
The utilisation of prebiotics can produce
some benefits in humans in the management of
constipation by increasing stool weight and
decreasing stool transit time (Macfarlane et al.,
2006); moreover, there is some evidence that
prebiotics might be helpful in the treatment of
inflammatory bowel disease in humans and ani-
mal models (Hedin et al., 2007). At present, no
studies have been done to verify these prebiotic
effects in dogs. In general, more research needs
to be done to investigate the possible role of pre-
biotics in canine disease.
A reading of the literature shows that by
relying on the use of prebiotic substances it
may be possible to manipulate the gastroin-
testinal ecosystem of dogs with the aim of
improving their intestinal wellbeing and
enhancing their immune function. Utilisation
of prebiotics has several beneficial effects in
the canine intestine, including improved com-
position of intestinal microbiota, reduced con-
centrations of protein catabolites and
enhanced production of SCFA. Among prebi-
otics, short-chain FOS and OF seem to be the
most effective in modulating canine intestinal
microbiota and improving intestinal absorp-
tion of minerals but with little or no effect on
canine immune system. Conversely, MOS may
have a positive influence on the immune sys-
tem of dogs but more research is needed on
this subject. Furthermore, evidence exists that
some positive effects of prebiotics in dogs
might be enhanced if these are used in combi-
nation with specific probiotic strains, in the
form of a synbiotic. Unfortunately, to date,
most studies with prebiotics in dogs were con-
ducted with healthy adult animals so that little
is known about the interaction between prebi-
otic administration and factors such as age
and health status.
Clinical effects of prebiotics have been
widely investigated in humans but, at present,
little evidence exists that prebiotics may be
helpful in canine diseases such as infections
by intestinal pathogens, intestinal constipa-
tion and hepatic and renal failure. More
research needs to be done to investigate the
possible role of prebiotics in canine disease
and possibly to link prebiotic-induced changes
in the intestinal microbiota to significant
physiological outcomes.
Finally, most studies on canine intestinal
microbiota were conducted using traditional
culture methods, so that more research
remains to be done with modern molecular
identification methods to investigate the
effects of prebiotic substances in dogs.
Adogony, V., Respondek, F., Biourge, V.,
Rudeaux, F., Delaval, J., Bind, J.L., Salmon,
H., 2007. Effects of dietary scFOS on
immunoglobulins in colostrums and milk of
bitches. J. Anim. Physiol. An. N. 91:169-174.
Apanavicius, C.J., Powell, K.L., Vester, B.M.,
Karr-Lilienthal, L.K, Pope, L.L., Fastinger,
N.D., Wallig, M.A., Tappenden, K.A.,
Swanson, K.S., 2007. Fructan supplemen-
tation and infection affect food intake,
fever, and epithelial sloughing from
Salmonella challenge in weanling puppies.
J. Nutr. 137:1923-1930.
Barry, K.A., Hernot, D.C., Middelbos, I.S.,
Francis C., Dunsford, B., Swanson, K.S.,
Prebiotics and synbiotics in dogs
Non-commercial use only
[page 176] [Ital J Anim Sci vol.13:2014]
Fahey Jr., G.C., 2009. Low-level fructan
supplementation of dogs enhances nutri-
ent digestion and modifies stool metabo-
lite concentrations, but does not alter fecal
microbiota populations. J. Anim. Sci.
Beloshapka, A.N., Dowd, S.E., Suchodolski, J.S.,
Steiner, J.M., Duclos, L., Swanson, K.S.,
2013. Fecal microbial communities of
healthy adult dogs fed raw meat-based diets
with or without inulin or yeast cell wall
extracts as assessed by 454 pyrosequenc-
ing. FEMS Microbiol. Ecol. 84:532-541.
Beloshapka, A.N., Wolff, A.K., Swanson, K.S.,
2012. Effects of feeding polydextrose on
faecal characteristics, microbiota and fer-
mentative end products in healthy adult
dogs. Brit. J. Nutr. 108:638-644.
Benno, Y., Mitsuoka, T., 1989. Effect of
advances in age on intestinal microflora of
beagle dogs. Microecol. T. 19:85-91.
Benno, Y., Nakao, H., Uchida, K., Mitsuoka, T.,
1992. Impact of the advances in age on the
gastrointestinal microflora of beagle dogs.
J. Vet. Med. Sci. 54:703-706.
Beynen, A.C., Baas, J.C., Hoekemeijer, P.E.,
Kappert, H.J., Bakker, M.H., Koopman, J.P.,
Lemmens, A.G., 2002. Faecal bacterial pro-
file, nitrogen excretion and mineral
absorption in healthy dogs fed supplemen-
tal oligofructose. J. Anim. Physiol. An. N.
Beynen, A.C., Kappert, H.J., Yu, S., 2001. Dietary
lactulose decreases apparent nitrogen
absorption and increases apparent calcium
and magnesium absorption in healthy dogs.
J. Anim. Physiol. An. N. 85:67-72.
Biagi, G., Cipollini, I., Grandi, M., Zaghini, G.,
2010. Influence of some potential prebiotics
and fibre-rich foodstuffs on composition
and activity of canine intestinal microbiota.
Anim. Feed Sci. Tech. 159:50-58.
Biagi, G., Cipollini, I., Pompei, A., Zaghini, G.,
Matteuzzi, D., 2007. Effect of a Lactobacillus
animalis strain on composition and metab-
olism of the intestinal microflora in adult
dogs. Vet. Microbiol.124:160-165.
Biagi, G., Piva, A., Moschini, M., Vezzali, E.,
Roth, F.X., 2006. Effect of gluconic acid on
piglet growth performance, intestinal
microflora, and intestinal wall morphology.
J. Anim. Sci. 84:370-378.
Buddington, R.K., 2003. Postnatal changes in
bacterial populations in the gastrointestinal
tract of dogs. Am. J. Vet. Res. 64:646-651.
Callaway, T.R., Edrington, T.S., Anderson, R.C.,
Harvey, R.B., Genovese, K.J., Kennedy,
C.N., Venn, D.W., Nisbet, D.J., 2008.
Probiotics, prebiotics and competitive
exclusion for prophylaxis against bacterial
disease. Anim. Health Res. Rev. 9:217-225.
Campbell, J.M., Bauer, L.L., Fahey Jr., G.C.,
Lewis Hogarth, A.J.C., Wolf, B.W., Hunter,
D.E., 1997. Selected fructooligosaccharide
(1-kestose, nystose, and 1F--fructofura-
nosylnystose) composition of foods and
feeds. J. Agr. Food Chem. 45:3076-3082.
Cerf-Bensussan, N., Gaboriau-Routhiau, V.,
2010. The immune system and the gut
microbiota: friends or foes? Nat. Rev.
Immunol. 10:735-744.
Chapman, M.A., Grahn, M.F., Hutton, M.,
Williams, N.S., 1995. Butyrate metabolism
in the terminal ileal mucosa of patients with
ulcerative colitis. Brit. J. Surg. 82:36-38.
Cummings, J.H., Englyst, H.N., 1987.
Fermentation in the human large intes-
tine and the available substrates. Am. J.
Clin. Nutr. 45:1243-1255.
Cummings, J.H., Macfarlane, G.T., 2002.
Gastrointestinal effects of prebiotics. Brit.
J. Nutr. 87:145-151.
De Bruyn, A., Alvarez, A.P., Sandra, P., De
Leenheer, L., 1992. Isolation and identifi-
cation of O--D-fructofuranosyl-(2,1)-D-
fructose, a product of the enzymatic
hydrolysis of the inulin from Cichorium
intybus. Carbohyd. Res. 235:303-308.
de Moreno de LeBlanc, A., Castillo, N.A.,
Perdigon, G., 2010. Anti-infective mecha-
nisms induced by a probiotic Lactobacillus
strain against Salmonella enterica serovar
Typhimurium infection. Int. J. Food
Microbiol. 138:223-231.
Diez, M., Hornick, J.L., Baldwin, P., Istasse, L.,
1997. Influence of a blend of fruc-
tooligosaccharides on nutrient digestibili-
ty and plasma metabolite concentrations
in healthy beagles. Am. J. Vet. Res.
Diez, M., Hornick, J.L., Baldwin, P., Van
Eenaeme, C., Istasse, L., 1998a. Etude des
fibres alimentaires chez le chien: présen-
tation des résultats de 7 essais expérimen-
taux. Ann. Med. Vet. 142:185-201.
Diez, M., Hornick, J.L., Baldwin, P., Van
Eenaeme, C., Istasse, L., 1998b. The influ-
ence of sugar-beet fibre, guar gum and
inulin on nutrient digestibility, water con-
sumption and plasma metabolites in
healthy beagle dogs. Res. Vet. Sci. 64:91-96.
Field, C.J., McBurney, M.I., Massimino, S.,
Hayek, M.G., Sunvold, G.D., 1999. The fer-
mentable fiber content of the diet alters
the function and composition of canine
gut associated lymphoid tissue. Vet.
Immunol. Immunop. 72:325-341.
Flickinger, E.A., Schreijen, E.M., Patil, A.R.,
Hussein, H.S., Grieshop, C.M., Merchen,
N.R., Fahey Jr., G.C., 2003a. Nutrient
digestibilities, microbial population and
protein catabolites as affected by fructan
supplementation of dog diets. J. Anim. Sci.
Flickinger, E.A., Van Loo, J., Fahey Jr., G.C.,
2003b. Nutritional responses to the pres-
ence of inulin and oligofructose in the
diets of domesticated animals: a review.
Crit. Rev. Food Sci. 43:19-60.
Franck, A., Bosscher, D., 2009. Inulin. In: S.S.
Cho and P. Samuel (eds.) Fiber ingredi-
ents: food applications and health bene-
fits. CRC Press, Taylor and Francis Group,
Boca Raton, FL, USA, pp 41-60.
Fujita, K., Kitahata, S., Kozo, H., Hotoshi, H.,
1992. Production of lactosucrose and its
properties. In: M.A. Clarke (ed.)
Carbohydrates in industrial synthesis.
Verlag Bartens, Berlin, Germany, pp 68-76.
Garcia-Mazcorro, J.F., Lanerie, D.J., Dowd,
S.E., Paddock, C.G., Grützner, N., Steiner,
J.M., Ivanek, R., Suchodolski, J.S., 2011.
Effect of a multi-species synbiotic formula-
tion on fecal bacterial microbiota of
healthy cats and dogs as evaluated by
pyrosequencing. FEMS Microbiol. Ecol.
Gopal, P.K., Sullivan, P.A., Smart, J.B., 2001.
Utilisation of galacto-oligosaccharides as
selective substrates for growth by lactic
acid bacteria including B. lactis DR10 and
Lactobacillus rhamnosus DR20. Int. Dairy
J. 11:19-25.
Greetham, H.L., Giffard, C., Hutson, R.A.,
Collins, M.D, Gibson, G.R., 2002.
Bacteriology of the Labrador dog gut: a cul-
tural and genotypic approach. J. Appl.
Microbiol. 93:640-646.
Grieshop, C.M., Flickinger, E.A., Bruce, K.J.,
Patil, A.R., Czarnecki-Maulden, G.L., Fahey
Jr., G.C., 2004. Gastrointestinal and
immunological responses of senior dogs to
chicory and mannan-oligosaccharides.
Arch. Anim. Nutr. 58:483-493.
Handl, S., Dowd, S.E., Garcia-Mazcorro, J.F.,
Steiner, J.M., Suchodolski, J.S., 2011.
Massive parallel16S rRNA gene pyrose-
quencing reveals highly diverse fecal bac-
terial and fungal communities in healthy
dogs and cats. FEMS Microbiol. Ecol.
Harmsen, H.J.M., Gibson, G.R., Elfferrich, P.,
Raangs, G.C., Wildeboer-Veloo, A.C.M.,
Argaiz, A., Roberfroid, M.B., Welling, G.W.,
2000. Comparison of viable counts and flu-
orescent in situ hybridization using spe-
cific rRNA-based probes for the quantifica-
tion of human faecal bacteria. FEMS
Microbiol. Lett. 183:125-129.
Hedin, C., Whelan, K., Lindsay, J.O., 2007.
Pinna and Biagi
Non-commercial use only
[Ital J Anim Sci vol.13:2014] [page 177]
Evidence for the use of probiotics and pre-
biotics in inflammatory bowel disease: a
review of clinical trials. Proc. Nutr. Soc.
Hernot, D., Ogué, E., Fahey, G., Rastall, R.A.,
2008. Prebiotics and synbiotics in compan-
ion animal science. In: J. Versalovic, M.
Wilson (eds.) Therapeutic microbiology:
probiotics and related strategies. ASM
Press, Washington, DC, pp 357-370.
Herschel, D.A., Argenzio, R.A., Southworth, M.,
Stevens, C.E., 1981. Absorption of volatile
fatty acid, Na and H2O by the colon of the
dog. Am. J. Vet. Res. 42:1118-1124.
Hesta, M., Janssens, G.P.J., Millet, S., De Wilde,
R., 2003. Prebiotics affect nutrient
digestibility but not faecal ammonia in
dogs fed increased dietary protein levels.
Brit. J. Nutr. 90:1007-1014.
Hooda, S., Minamoto, Y., Suchodolski, J.S.,
Swanson, K.S., 2012. Current state of knowl-
edge: the canine gastrointestinal microbio-
me. Anim. Health Res. Rev.13:78-88.
Howard, M.D., Kerley, M.S., Sundvold, G.D.,
Reinhart, G.A., 2000. Source of dietary
fiber fed to dogs affects nitrogen and ener-
gy metabolism and intestinal microflora
populations. Nutr. Res. 20:1473-1484.
Hussein, H.S., Campbell, J.M., Bauer, L.L.,
Fahey Jr., G.C., Lewis Hogarth, A.J.C., Wolf,
B.W., Hunter, D.E., 1998. Selected fruc-
tooligosaccharide composition of pet-food
ingredients. J. Nutr. 128:2803-2805.
Imaizumi, K., Nakatsu, Y., Sato, M.,
Sedarnawati, Y., Sugano, M., 1991. Effects
of xylooligosaccharides on blood glucose,
serum and liver lipids and cecum short-
chain fatty acids in diabetic rats. Agr. Biol.
Chem. Tokyo 55:199-205.
Kaplan, H., Hutkins, R.W., 2000. Fermentation
of fructoligosaccharides by lactic acid bac-
teria and bifidobacteria. Appl. Environ.
Microb. 66:2682-2684.
Karr-Lilienthal, L.K., Grieshop, C.M., Spears,
J.K., Patil, A.R., Czarnecki-Maulden, G.L.,
Merchen, N.R., Fahey Jr., G.C., 2004.
Estimation of the proportion of bacterial
nitrogen in canine feces using
diaminopimelic acid as an internal bacter-
ial marker. J. Anim. Sci. 82:1707-1712.
Knarreborg, A., Miquel, N., Granli, T., Jensen,
B.B., 2002. Establishment and application
of an in vitro methodology to study the
effects of organic acids on coliform and
lactic acid bacteria in the proximal part of
the gastrointestinal tract of piglets. Anim.
Feed Sci. Tech. 99:131-140.
Lamendella, R., Santo Domingo, J.W., Kelty, C.,
Oerther, D.B., 2008. Bifidobacteria in feces
and environmental waters. Appl. Environ.
Microb. 74:575-584.
Langendijk, P.S, Schut, F., Jansen, G.J., Raangs,
G.C., Kamphuis, G.R., Wilkinson, M.H.F.,
Welling, G.W., 1995. Quantitative fluores-
cence in situ hybridization of
Bifidobacterium spp. with genus-specific
16S rRNA-targeted probes and its applica-
tion in fecal samples. Appl. Environ.
Microb. 61:3069-3075.
LeBlanc, J.G., Milani, C., de Giori, G.S., Sesma,
F., van Sinderen, D., Ventura, M., 2013.
Bacteria as vitamin suppliers to their host:
a gut microbiota perspective. Curr. Opin.
Biotech. 24:160-168.
Liévin-Le Moal, V., Servin, A.L., 2006. The front
line of enteric host defense against unwel-
come intrusion of harmful microorganisms:
mucins, antimicrobial peptides, and micro-
biota. Clin. Microbiol. Rev. 19:315-337.
Lomax, A.R., Calder, P.C., 2009. Prebiotics,
immune function, infection and inflam-
mation: a review of the evidence. Brit. J.
Nutr. 101:633-658.
Macfarlane, S., Macfarlane, G.T., Cummings,
J.H., 2006. Review article: prebiotics in the
gastrointestinal tract. Aliment. Pharm.
Ther. 24:701-714.
McQuaid, T.S., 2005. Medical management of a
patent ductus venosus in a dog. Canadian
Vet. J. 46:352-356.
Middelbos, I.S., Fastinger, N.D., Fahey Jr., G.C.,
2007a. Evaluation of fermentable oligosac-
charides in diets fed to dogs in comparison
to fiber standards. J. Anim. Sci. 85:3033-
Middelbos, I.S., Godoy, M.R., Fastinger, N.D.,
Fahey Jr., G.C., 2007b. A dose-response
evaluation of spray-dried yeast cell wall
supplementation of diets fed to adult dogs:
effects on nutrient digestibility, immune
indices, and fecal microbial populations. J.
Anim. Sci. 85:3022-3032.
Middelbos, I.S., Vester Boler, B.M., Qu, A.,
White, B.A., Swanson, K.S., Fahey Jr., G.C.,
2010. Phylogenetic characterization of
fecal microbial communities of dogs fed
diets with or without supplemental dietary
fiber using 454 pyrosequencing. PLoS ONE
Mitsuoka, T., 1992. Intestinal flora and aging.
Nutr. Rev. 50:438-446.
Moshfegh, A.J., Friday, J.E., Goldman, J.P.,
Ahuja, J.K.C., 1999. Presence of inulin and
oligofructose in the diets of Americans. J.
Nutr. 129:1407-1411.
Ogué-Bon, E., Khoo, C., Hoyles, L., McCartney,
A.L., Gibson, G.R., Rastall, R.A., 2011. In
vitro fermentation of rice bran combined
with Lactobacillus acidophilus 14 150B or
Bifidobacterium longum 05 by the canine
faecal microbiota. FEMS Microbiol. Ecol.
Ogué-Bon, E., Khoo, C., McCartney, A.L.,
Gibson, G.R., Rastall, R.A., 2010. In vitro
effects of synbiotic fermentation on the
canine faecal microbiota. FEMS Microbiol.
Ecol. 73:587-600.
Propst, E.L., Flickinger, E.A., Bauer, L.L.,
Merchen, N.R., Fahey Jr., G.C., 2003. A
dose-response experiment evaluating the
effects of oligofructose and inulin on
nutrient digestibility, stool quality, and
fecal protein catabolites in healthy adult
dogs. J. Anim. Sci. 81:3057-3066.
Rada, V., Nevoral, J., Trojanová, I., Tománková,
E., Smehilová, M., Killer, J., 2008. Growth
of infant faecal bifidobacteria and
clostridia on prebiotic oligosaccharides in
in vitro conditions. Anaerobe 14:205-208.
Roberfroid, M.B., 2007. Prebiotics: the concept
revisited. J. Nutr. 137:830-837.
Roberfroid, M.B., Bornet, F., Bouley, C.,
Cummings, J.H., 1995. Colonic microflora:
nutrition and health. Nutr. Rev. 53:127-130.
Roediger, W.E., 1980. Role of anaerobic bacte-
ria in the metabolic welfare of the colonic
mucosa in man. Gut 21:793-798.
Round, J.L., Mazmanian, S.K., 2009. The gut
microbiota shapes intestinal immune
responses during health and disease. Nat.
Rev. Immunol. 9:313-323.
Russell, J.B., Sniffen, C.J., Van Soest, P.J.,
1983. Effect of carbohydrate limitation on
degradation and utilization of casein by
mixed rumen bacteria. J. Dairy Sci.
Schaible, U.E., Kaufmann, S.H., 2005. A nutri-
tive view on the host-pathogen interplay.
Trends Microbiol. 13:373-380.
Scholz-Ahrens, K.E., Ade, P., Marten, B., Weber,
P., Timm, W., Açil, Y., Glüer, CC.,
Schrezenmeir, J., 2007. Prebiotics, probi-
otics, and synbiotics affect mineral absorp-
tion, bone mineral content, and bone
structure. J. Nutr. 137:838-846.
Schrezenmeir, J., De Vrese, M., 2001. Probiotics,
prebiotics and synbiotics: approaching a
definition. Am. J. Clin. Nutr. 73:361-364.
Seifert, S., Watzl, B., 2007. Inulin and
oligofructose: review of experimental
data on immune modulation. J. Nutr.
Simpson, J.M., Martineau, B., Jones, W.E.,
Ballam, J.M., Mackie, R.I., 2002.
Characterization of fecal bacterial popula-
tions in canines: effects of age, breed and
dietary fiber. Microb. Ecol. 44:186-197.
Spiegel, J.E., Rose, R., Karabell, P., Frankos, V.H.,
Schmitt, D.F., 1994. Safety and benefits of
fructooligosaccharides as food ingredients.
Prebiotics and synbiotics in dogs
Non-commercial use only
[page 178] [Ital J Anim Sci vol.13:2014]
Food Technol.-Chicago 48:85-89.
Spring, P., Wenk, C., Dawson, K.A., Newman,
K.E., 2000. The effect of dietary mannano-
ligosaccharides on cecal parameters and
the concentrations of enteric bacteria in
the ceca of Salmonella-challenged broiler
chicks. Poultry Sci. 79:205-211.
Stevens, C.S., Hume, I.D., 1998. Contributions
of microbes in vertebrate gastrointestinal
tract to production and conservation of
nutrients. Physiol. Rev. 78:393-427.
Strickling, J.A., Harmon, D.L., Dawson, K.A.,
Gross, K.L., 2000. Evaluation of oligosac-
charide addition to dog diets: influences
on nutrient digestion and microbial popu-
lations. Anim. Feed Sci. Tech. 86:205-219.
Suchodolski, J.S., 2011. Companion animals
symposium: microbes and gastrointestinal
health of dogs and cats. J. Anim. Sci.
Suchodolski, J.S., Dowd, S.E., Westermarck, E.,
Steiner, J.M., Wolcott, R.D., Spillmann, T.,
Harmoinen, J.A., 2009. The effect of the
macrolide antibiotic tylosin on microbial
diversity in the canine small intestine as
demonstrated by massive parallel 16s rRNA
gene sequencing. BMC Microbiol. 9:210.
Suchodolski, J.S., Ruaux, C.G., Steiner, J.M.,
Fetz, K., Williams, D.A., 2005. Assessment
of the qualitative variation in bacterial
microflora among compartments of the
intestinal tract of dogs by use of a molecu-
lar fingerprinting technique. Am. J. Vet.
Res. 66:1556-1562.
Swanson, K.S., Fahey, G.C., 2006. Prebiotic
impacts on companion animals. In: G.R.
Gibson, R.A. Rastall (eds.) Prebiotics
development and application. John Wiley
and Sons, Chichester, UK, pp 217-236.
Swanson, K.S., Dowd, S.E., Suchodolski, J.S.,
Middelbos, I.S., Vester, B.M., Barry, K.A.,
Nelson, K.E., Torralba, M., Henrissat, B.,
Coutinho, P.M., Cann, I.K.O., White, B.A.,
Fahey Jr., G.C., 2011. Phylogenetic and
gene-centric metagenomics of the canine
intestinal microbiome reveals similarities
with humans and mice. ISME J. 5:639-649.
Swanson, K.S., Grieshop, C.M., Flickinger,
E.A., Bauer, L.L., Chow, J., Wolf, B.W.,
Garleb, K.A., Fahey Jr., G.C., 2002a.
Fructooligosaccharides and Lactobacillus
acidophilus modify gut microbial popula-
tions, total tract nutrient digestibilities
and fecal protein catabolite concentra-
tions in healthy adult dogs. J. Nutr.
Swanson, K.S., Grieshop, C.M., Flickinger, E.A.,
Bauer, L.L., Healy, H.P., Dawson, K.A.,
Merchen, N.R., Fahey Jr., G.C., 2002b.
Supplemental fructooligosaccharides and
mannanoligosaccharides influence immu -
ne function, ileal and total tract nutrient
digestibilities, microbial populations and
concentrations of protein catabolites in
the large bowel of dogs. J. Nutr. 132:980-
Swanson, K.S., Grieshop, C.M., Flickinger, E.A.,
Healy, H.P., Dawson, K.A., Merchen, N.R.,
Fahey Jr., G.C., 2002c. Effects of supplemen-
tal fructooligosaccharides plus mannano-
ligosaccharides on immune function and
ileal and fecal microbial populations in
adult dogs. Arch. Tiererernahr. 56:309-318.
Terada, A., Hara, H., Oishi, T., Matsui, T.,
Mitsuoka, T., Nakajyo, S., Fujimori, I., Hara,
K., 1992. Effect of dietary lactosucrose on
faecal flora and faecal metabolites of dogs.
Microb. Ecol. Health D. 5:87-92.
Tomomatsu, H., 1994. Health effects of
oligosaccharides. Food Technol.-Chicago
Twomey, L.N., Pluske, J.R., Rowe, J.B., Choct,
M., Brown, W., Pethick, D.W., 2003. The
effects of added fructooligosaccharide
(Raftilose®P95) and inulinase on faecal
quality and digestibility in dogs. Anim.
Feed Sci. Tech. 108:83-93.
Tzortzis, G., Baillon, M.L., Gibson, G.R., Rastall,
R.A., 2004a. Modulation of antipathogenic
activity in caninederived Lactobacillus
species by carbohydrate growth substrate.
J. Appl. Microbiol. 96:552-559.
Tzortzis, G., Goulas, A.K., Baillon, M.L.A.,
Gibson, G.R., Rastall, R.A., 2004b. In vitro
evaluation of the fermentation properties
of galactooligosaccharides synthesized by
-galactosidase from Lactobacillus reuteri.
Appl. Microbiol. Biot. 64:106-111.
Van Loo, J., Coussement, P., De Leenheer, L.,
Hoebregs, H., Smits, G., 1995. On the pres-
ence of inulin and oligofructose as natural
ingredients in the western diet. Crit. Rev.
Food Sci. 35:525-552.
Vanhoutte, T., Huys, G., De Brandt, E., Fahey
Jr., G.C., Swings, J., 2005. Molecular moni-
toring and characterization of the faecal
microbiota of healthy dogs during fructan
supplementation. FEMS Microbiol. Lett.
Verlinden, A., Hesta, M., Hermans, J., Janssens,
G., 2006. The effects of inulin supplementa-
tion of diets with or without protein sources
on digestibility, faecal characteristics,
haematology and immunoglobulins in dogs.
Brit. J. Nutr. 96:936-944.
Vickers, R.J., Sunvold, G.D., Kelley, R.L.,
Reinhart, G.A., 2001. Comparison of fermen-
tation of selected fructooligosaccharides
and other fiber substrates by canine colonic
microflora. Am. J. Vet. Res. 62:609-615.
Willard, M.D., Simpson, R.B., Cohen, N.D.,
Clancy, J.S., 2000. Effects of dietary fruc-
tooligosaccharide on selected bacterial
populations in feces of dogs. Am. J. Vet.
Res. 61:820-825.
Zanoni, S., Pompei, A., Cordisco, L., Amaretti,
A., Rossi, M., Matteuzzi, D., 2008. Growth
kinetics on oligo- and polysaccharides and
promising features of three antioxidative
potential probiotic strains. J. Appl.
Microbiol. 105:1266-1276.
Zentek, J., Marquart, B., Pietrzak, T., 2002.
Intestinal effects of mannanoligosaccha-
rides, transgalactooligosaccharides, lac-
tose and lactulose in dogs. J. Nutr.
Pinna and Biagi
Non-commercial use only
... The fermentation parameter results registered for inulin and cellulose are in accordance with a previous study [34]. These results confirm the prebiotic effect of inulin [35]. Otherwise, the limited volume of gas registered during the incubation with MOS could indicate that the highest organic matter degradability might be due to filtration problems related to the specific particle dimension, as indicated by Calabrò et al. [36]. ...
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Lipids represent a significant energy source in dogs’ diets. Moreover, dogs need some essential fatty acids, such as linoleic and α-linolenic fatty acids, because they are not able to produce them endogenously. This study aimed to evaluate the effect of different dietary lipid sources on faecal microbial populations and activities using different evaluations. Hemp seed oil and swine tallow were tested as lipid supplements in a commercial canned diet at a ratio of 3.5% (HL1 and HL2, respectively). These diets were compared with one rich in starch (HS). Twelve dogs were recruited and equally divided into three groups. Faeces samples at 30 days were used as inoculum and incubated with three different substrates (MOS, inulin, and cellulose) using the in vitro gas production technique. The faecal cell numbers of relevant bacteria and secondary metabolites were analysed (in vivo trial). In vitro evaluation showed that the faeces of the group fed the diet with hemp supplementation had better fermentability despite lower gas production. The in vivo faecal bacterial count showed an increase in Lactobacillus spp. In the HL1 group. Moreover, a higher level of acetate was observed in both evaluations (in vitro and in vivo). These results seem to indicate a significant effect of the dietary fatty acid profile on the faecal microbial population.
... Certain feed additives can improve and stabilize the composition of the intestinal microbiota, reducing the presence of pathogens as well as toxins [27]. In addition, prebiotics may lead to enhanced immune function and can be used safely as a secondary treatment of diseases, such as certain bacterial intestinal infections, constipation, kidney or liver diseases, especially hepatic encephalopathy caused by PSS, explaining the increasing interest in the application of fiber and prebiotics such as lactulose and psyllium in animal feed [11,[28][29][30][31][32][33]. ...
Full-text available
The intestinal microbiome of dogs can be influenced by a number of factors such as non-starch polysaccharides as well as some non-digestible oligo- and disaccharides. These molecules are only decomposed by intestinal anaerobic microbial fermentation, resulting in the formation of volatile fatty acids (VFAs), which play a central role in maintaining the balance of the intestinal flora and affecting the health status of the host organism. In the present study, the effects of lactulose and psyllium husk (Plantago ovata) were investigated regarding their influence on concentrations of various VFAs produced by the canine intestinal microbiome. Thirty dogs were kept on a standard diet for 15 days, during which time half of the animals received oral lactulose once a day, while the other group was given a psyllium-supplemented diet (in 0.67 and in 0.2 g/kg body weight concentrations, respectively). On days 0, 5, 10 and 15 of the experiment, feces were sampled from the rectum, and the concentration of each VFA was determined by GC-MS (gas chromatography–mass spectrometry). Lactulose administration caused a significant increase in the total VFA concentration of the feces on days 10 and 15 of the experiment (p = 0.035 and p < 0.001, respectively); however, in the case of psyllium supplementation, the concentration of VFAs showed a significant elevation only on day 15 (p = 0.003). Concentrations of acetate and propionate increased significantly on days 5, 10 and 15 after lactulose treatment (p = 0.044, p = 0.048 and p < 0.001, respectively). Following psyllium administration, intestinal acetate, propionate and n-butyrate production were stimulated on day 15, as indicated by the fecal VFA levels (p = 0.002, p = 0.035 and p = 0.02, respectively). It can be concluded that both lactulose and psyllium are suitable for enhancing the synthesis of VFAs in the intestines of dogs. Increased acetate and propionate concentrations were observed following the administration of both supplements; however, elevated n-butyrate production was found only after psyllium treatment, suggesting that the applied prebiotics may exert slightly different effects in the hindgut of dogs. These findings can be also of great importance regarding the treatment and management of patients suffering from intestinal disorders as well as hepatic encephalopathy due to portosystemic shunt.
... The author concluded that feeding prebiotic substances at doses as high as 1.4% (DM basis) seems to be a valid means to beneficially manipulate intestinal microbiota composition and its functionality. In a more recent report, Pinna and Biagi [155] exhaustively reviewed the scientific literature regarding the use of prebiotics in the canine species. In spite of the fact that several inconsistencies were found when comparing study results among each other, the investigators confirmed the positive impact of feeding prebiotics on canine fitness, as testified by an overall enhanced composition of the gut microbial ecosystem, augmented synthesis of SCFAs and mitigated production of certain protein fermentation metabolites. ...
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Chronic inflammatory enteropathy (CIE) refers to a heterogeneous group of idiopathic diseases of the dog characterised by persistent gastrointestinal (GI) clinical signs. If conventional dietary treatment alone would be unsuccessful, management of CIE is traditionally attained by the use of pharmaceuticals, such as antibiotics and immunosuppressive drugs. While being rather effective, however, these drugs are endowed with side effects, which may impact negatively on the animal’s quality of life. Therefore, novel, safe and effective therapies for CIE are highly sought after. As gut microbiota imbalances are often associated with GI disorders, a compelling rationale exists for the use of nonpharmacological methods of microbial manipulation in CIE, such as faecal microbiota transplantation and administration of pre-, pro-, syn- and postbiotics. In addition to providing direct health benefits to the host via a gentle modulation of the intestinal microbiota composition and function, these treatments may also possess immunomodulatory and epithelial barrier-enhancing actions. Likewise, intestinal barrier integrity, along with mucosal inflammation, are deemed to be two chief therapeutic targets of mesenchymal stem cells and selected vegetable-derived bioactive compounds. Although pioneering studies have revealed encouraging findings regarding the use of novel treatment agents in CIE, a larger body of research is needed to address fully their mode of action, efficacy and safety.
... An example of nutraceutical are prebiotics that can be defined as a non-digestible food ingredient that beneficially affects the host by selectively stimulating growth and/or activity of a limited number of bacteria in the colon [1,6,[9][10][11]. In this context of food promoting health, prebiotics have been the subject of numerous scientific studies and there are publications which have demonstrated their therapeutic effectiveness on both systemic and gastrointestinal tract [11][12][13][14][15][16]. ...
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Background: This study aimed to evaluate the effects of increasing dosages of a commercial product composed by Saccharomyces cerevisiae yeast (YAM), with active metabolites, which are beta glucans, nucleotides, organic acids, polyphenols, amino acids, vitamins and minerals (Original XPCtm, Diamond V, IOWA, USA) added to a commercially available dry cat food. Apparent digestibility of dietary nutrients, fecal microbiota, fecal fermentation products and immunological parameters were evaluated. Twenty-seven healthy cats of mixed sexes, with a mean body weight of 4.19 ± 0.83 kg and a mean age of 9.44 ± 5.35 years were distributed by age in an unbalanced randomized block design, consisting of three experimental treatments: CD (control diet), YAM 0.3 (control diet with 0.3% yeast with active metabolites) and YAM 0.6 (control diet with 0.6% yeast with active metabolites). Results: The inclusion of the additive elevated the apparent digestibility of crude fiber (p = 0.013) and ash (p < 0.001) without interfering feed consumption, fecal production and fecal characteristics. Regarding fermentation products present in the feces, prebiotic inclusion increased lactic acid concentration (p = 0.004) while reducing isovaleric acid (p = 0.014), only in the treatment YAM 0.3. No differences were noticed on biogenic amines (BA), fecal pH, ammonia concentration, total and individuals short-chain fatty acids (SCFA) and total and individuals branched-chain fatty acids (BCFA) (except isovaleric acid in YAM 0.3). As regards to fecal microbiota, prebiotic inclusion has resulted in the reduction of Clostridium perfringens (p = 0.023). No differences were found in the immunological parameters evaluated. Conclusion: It can be concluded that the additive, at the levels of inclusion assessed shows prebiotic potential and it has effects on fecal fermentation products and microbiota without interfering on crude protein and dry matter digestibility. More studies evaluating grater inclusion levels of the prebiotic are necessary to determine optimal concentration.
... The definition of prebiotic indicates that it is a substrate selectively utilized by the host's microorganisms conferring a health benefit. 115 They are essentially non-digestible carbohydrates for the host, mainly oligosaccharides with a low degree of polymerization derived from natural products such as fructooligosaccharides (FOS), inulin, and mannanoligosaccharides. 116 Galactooligosaccharides are a complex mixture of oligosaccharides usually derived from lactose via enzymatic transgalactosylation. 117 Ide et al. 118 reported that the administration of kestose, a FOS with one fructose monomer linked to sucrose, to dogs for 8 weeks had a bifidogenic activity, with an increased fecal concentration of butyrate and reduction in the relative abundance of Bacteroides spp., C. perfringens, and Sutterella spp., that returned to initial levels 4 weeks after discontinuing the treatment. In another study conducted in dogs, supplementation of inulin and yeast cell wall (fermentable fibers) to raw meat diets for 14 days promoted an increase of fecal DNA concentration of Lactobacillus and Bifidobacterium, respectively, without substantial effects on diversity and similarity of communities. ...
Microbiota and microbiome, which refers, respectively, to the microorganisms and conjoint of microorganisms and genes are known to live in symbiosis with hosts, being implicated in health and disease. The advancements and cost reduction associated with high-throughput sequencing techniques have allowed expanding the knowledge of microbial communities in several species, including dogs. Throughout their body, dogs harbor distinct microbial communities according to the location (e.g., skin, ear canal, conjunctiva, respiratory tract, genitourinary tract, gut), which have been a target of study mostly in the last couple of years. Although there might be a core microbiota for different body sites, shared by dogs, it is likely influenced by intrinsic factors such as age, breed, and sex, but also by extrinsic factors such as the environment (e.g., lifestyle, urban vs rural), and diet. It starts to become clear that some medical conditions are mediated by alterations in microbiota namely dysbiosis. Moreover, understanding microbial colonization and function can be used to prevent medical conditions, for instance, modulation of gut microbiota of puppies is more effective to ensure a healthy gut than interventions in adults. This paper gathers current knowledge of dogs’ microbial communities, exploring their function, implications in the development of diseases, and potential interactions among communities while providing hints for further research.
... Possessing a healthy microbiome and maintaining gut barrier integrity are important for canine health and disease prevention. Many plant components influence the microbiota by increasing potentially beneficial bacteria and minimizing pathogenic microbes(Kil & Swanson, 2011;Pinna & Biagi, 2014; Suchodolski, 2011a,b).To illustrate, dogs with inflammatory bowel disease, whose clinical symptoms are commonly characterized by chronic vomiting and diarrhoea, were revealed to have decreased abundance of Firmicutes and Bacteroidetes, as well as lower gut microbial diversity, specifically in the genus Clostridium(Honneffer et al., 2014;Minamoto et al., 2015).Substances which can promote selected bacterial growth and alter the microbiome structure, benefiting the host's health, are commonly known as prebiotics(Garcia-Mazcorro et al., 2017). While traditionally prebiotics were considered to be subsets of fermentable fibres(Garcia-Mazcorro et al., 2017), the definition has since broadened to encompass a wide variety of ingredients(Gibson et al., 2010(Gibson et al., , 2017, including non-carbohydrate plant-based ingredients, notably polyphenols(Gibson et al., 2017;Moorthy et al., 2020). ...
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Dogs possess the ability to obtain essential nutrients, established by the Association of American Feed Control Officials (AAFCO), from both animal- and plant-based ingredients. There has been a recent increase in the popularity of diets that limit or completely exclude certain plant-based ingredients. Examples of these diets include ‘ancestral’ or ‘evolutionary’ diets, raw meat-based diets and grain-free diets. As compared to animal sources, plant-derived ingredients (including vegetables, fruits, grains, legumes, nuts and seeds) provide many non-essential phytonutrients with some data suggesting they confer health benefits. This review aims to assess the strength of current evidence on the relationship between the consumption of plant-based foods and phytonutrients (such as plant-derived carotenoids, polyphenols and phytosterols) and biomarkers of health and diseases (such as body weight/condition, gastrointestinal health, immune health, cardiovascular health, visual function and cognitive function) from clinical trials and epidemiological studies. This review highlights the potential nutritional and health benefits of including plant-based ingredients as a part of balanced canine diets. We also highlight current research gaps in existing studies and provide future research directions to inform the impact of incorporating plant-based ingredients in commercial or home-prepared diets.
... The crucial role that the intestinal microbiota plays in supporting host health is a well-established concept [1] and in recent decades scientific research has widely investigated different nutritional strategies aimed to positively influence the microbial ecosystem of the gastrointestinal tract [2]. Among the several dietary components investigated in this context, in particular, undigestible carbohydrates (i.e., oligosaccharides) have been explored both in humans [3,4] and other animal species such as dogs [5,6], mostly for their potential benefits on the composition and activity of the gut microbiota, leading the way to the nutritional "prebiotic" approach aimed to maintain or improve host health [7]. ...
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The present study investigated in dogs the dietary effects of intact seaweeds on some fecal bacterial populations and metabolites, fecal IgA and apparent total tract digestibility (ATTD). Ten healthy adult dogs were enrolled in a 5 × 5 replicated Latin square design to evaluate five dietary treatments: control diet (CD); CD + Ascophyllum nodosum; CD + Undaria pinnatifida; CD + Saccharina japonica; CD + Palmaria palmata (n replicates per treatment = 10). Seaweeds were added to food at a daily dose of 15 g/kg. The CD contained silica as a digestion marker. Each feeding period lasted 28 d, with a 7 d wash-out in between. Feces were collected at days 21 and 28 of each period for chemical and microbiological analyses. Fecal samples were collected during the last five days of each period for ATTD assessment. Dogs showed good health conditions throughout the study. The fecal chemical parameters, fecal IgA and nutrient ATTD were not influenced by algal supplementation. Similarly, microbiological analyses did not reveal any effect by seaweed ingestion. In conclusion, algal supplementation at a dose of 15 g/kg of diet failed to exert noticeable effects on the canine fecal parameters evaluated in the present study.
... Several nondigestible carbohydrates are known to possess prebiotic features and range from the disaccharide lactulose to oligo-or polysaccharides such as fructo-oligosaccharides (FOS), mannan-oligosaccharides (MOS), xylooligosaccharides (XOS) and galacto-oligosaccharides (GOS) and inulin (Roberfroid et al., 2010;Slavin, 2013). To be effective, prebiotics have to withstand digestion by host enzymes and reach the distal part of the intestine where they favour the proliferation and metabolic activities of specific bacterial species able to promote evident beneficial effects to the host (Pinna and Biagi, 2016). By escaping upper intestinal hydrolysis and absorption and reaching the hindgut compartments, these complex carbohydrates will be selectively fermented by those microorganisms that possess genes encoding specific extracellular and/or intracellular glycosyl-hydrolases (GH) and transport systems, required for the breakdown and uptake, respectively, of these carbohydrates (Vieira et al., 2013). ...
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Dogs and cats have gained a special position in human society by becoming our principal companion animals. In this context, efforts to ensure their health and welfare have increased exponentially, with in recent times a growing interest in assessing the impact of the gut microbiota on canine and feline health. Recent technological advances have generated new tools to not only examine the intestinal microbial composition of dogs and cats, but also to scrutinize the genetic repertoire and associated metabolic functions of this microbial community. The application of high-throughput sequencing techniques to canine and feline faecal samples revealed similarities in their bacterial composition, with Fusobacteria, Firmicutes and Bacteroidetes as the most prevalent and abundant phyla, followed by Proteobacteria and Actinobacteria. Although key bacterial members were consistently present in their gut microbiota, the taxonomic composition and the metabolic repertoire of the intestinal microbial population may be influenced by several factors, including diet, age and anthropogenic aspects, as well as intestinal dysbiosis. The current review aims to provide a comprehensive overview of the multitude of factors which play a role in the modulation of the canine and feline gut microbiota and that of their human owners with whom they share the same environment.
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Background The increased prevalence of atopic dermatitis (AD) in dogs necessitates research in its disease etiology. Objectives To explore the association between puppyhood dietary exposures and prevalence of owner-reported allergy/atopy skin signs (AASS) after the age of 1 year. Animals Four thousand and twenty-two dogs were eligible, 1158 cases, and 2864 controls. Methods This cross-sectional hypothesis-driven observational study was extracted from the DogRisk food frequency questionnaire. Forty-six food items and the ratio of 4 major diet types were tested for their association with AASS incidence later in life. Potential puppyhood dietary risk factors for AASS incidence were specified using binary multivariable logistic regression. The model was adjusted for age and sex. Results Eating raw tripe (odds ratio, 95% confidence intervals OR, 95% CI = 0.36, 0.16-0.79; P = .01), raw organ meats (OR, 95% CI = 0.23, 0.08-0.67; P = .007), human meal leftovers, and fish oil supplements as well as eating more that 20% of the diet as raw and/or <80% of the diet as dry, in general, were associated with significantly lower AASS incidence in adulthood. In contrast, dogs fed fruits (OR, 95% CI = 2.01, 1.31-3.07; P = .001), mixed-oil supplements, dried animal parts, and dogs that drank from puddles showed significantly higher AASS incidence in adulthood. Conclusions and Clinical Importance Puppyhood exposure to raw animal-based foods might have a protective influence on AASS incidence in adulthood, while puppyhood exposure to mixed oils, heat processed foods and sugary fruits might be a potential risk factor of AASS incidence later. The study suggests a causal relationship but does not prove it.
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This study aimed to evaluate the effects of two prebiotics in different concentrations on nutrient digestibility, fermentative products and immunological variables in adult dogs. Twenty-four adult dogs were randomly divided into six blocks according to their metabolic body weights (BW0.75); within these groups, dogs were randomized to four treatments: control without prebiotics (CO); inclusion of 0.5% prebiotic blend Yes-Golf (B1); inclusion of 1.0% galactooligosaccharide (GOS); and inclusion of 1.0% prebiotic blend Yes-Golf (B2). The experiment lasted 30 days, with 20 days adaptation and 10 days stool and blood collection. Results were analyzed for normality and means were separated by ANOVA and adjusted by the Tukey test at the significance level of 5.0%. Prebiotic supplementation had no effect on apparent digestibility coefficients (ADC), total stool production and fecal scores (p > 0.05). Prebiotics evaluated also did not alter fecal pH, nor the concentrations of ammonia, lactic acid, short chain fatty acids (SCFA) and most fecal branched chain fatty acids (BCFA) (p > 0.05). The addition of GOS decreased the concentration of iso-valeric acid (p = 0.0423). Regarding immunological variables, concentrations of fecal IgA were not influenced by the treatments. Treatments GOS and B2 increased the total number of polymorphonuclear cells, as well as the oxidative burst in relation to treatments B1 and CO (p < 0.0001). Treatment B2 improved the rate of S. aureus phagocytosis in relation to CO (p = 0.0111), and both the GOS and B2 treatments had a better index for E. coli phagocytosis than the CO treatment (p = 0.0067). In conclusion, there was indication that both prebiotics GOS and B2 at 1.0% inclusion improved the immunity of healthy dogs.
Inulin, a non-digestible carbohydrate, is a fructan that has been part of our daily diet for some centuries and naturally occurs in many plants as storage carbohydrate. It is present for example in leeks, onions, garlic, wheat, chicory.
Fructooligosaccharides (FOS) are naturally occurring sugars with potentially beneficial nutritional effects. They are widely distributed throughout the plant kingdom. An ion chromatographic method was developed to rapidly and accurately measure FOS in selected food and feed ingredients ingested by humans and animals. The objective of this study was to determine the 1-kestose (1-kestotriose; GF2) nystose (1,1-kestotetraose; GF3), and 1F-β-fructofuranosylnystose (1,1,1-kestopentaose; GF4) content of a wide variety of foods and feedstuffs. After extraction with water and appropriate filtration samples were chromatographed, using an alkaline sodium acetate gradient, through an ion exchange column and guard fitted to a Dionex chromatography unit equipped with a pulsed electrochemical detector. All samples were prepared both with and without spikes of standards to verify recovery and peak identification. Samples of the Compositae family were highest in total FOS followed by Allium species of the Amaryllidadeae family. The method provided excellent separation, recovery, and quantification of the GFn units of FOS. Accurate quantitation of FOS will allow more precise nutritional formulations to be developed with respect to inclusion of this functional food component in human and animal diets.
This article discuss the serious consequences of formation of toxic fermentation products in the colon and the counteracting health benefits of oligosaccharide ingestion. The benefits arise from increased population of indigenous bifidobacteria in the colon which, by their antagonistic effect, suppress the activity of putrefactive bacteria and reduce the formation of toxic fermentation products. In addition, the many advantages oligosaccharides have over dictary fiber are enumerated, as well as the natural foods that contain the sugar and its dosages and side effects.