Short-chain Fatty Acid Formation In The Hindgut Of Rats Fed Native And ...

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Short-chain fatty acid formation in the hindgut of rats fed native
and fermented oat fibre concentrates
Adele M. Lambo-Fodje*, Rickard Öste and Margareta E. G.-L. Nyman
Division of Applied Nutrition and Food Chemistry, Department of Food Technology, Engineering and Nutrition, Center
for Chemistry and Chemical Engineering, Lund University, PO Box 124, SE-221 00, Lund, Sweden
(Received 21 September 2005 – Revised 1 March 2006 – Accepted 1 March 2006)
The formation of SCFA in rats fed fermented oat fibre concentrates was compared with that of rats fed native oat fibre concentrate. The cultures
used were lactic acid bacteria consisting of Lactobacillus bulgaricus and Streptococcus thermophilus (V2), the exopolysaccharide-producing strain
Pediococcus damnosus 2.6 (Pd) and L. reuteri (Lr). The materials were incorporated into test diets yielding a concentration of indigestible carbohydrates of 80 g/kg (dry weight). Rats fed the V2-fermented fibre-concentrate diet yielded higher caecal and distal concentrations of acetic acid
(P,0·01) than rats fed the native fibre concentrate. All the fermented fibre concentrates resulted in a higher propionic acid concentration in the
distal colon (P,0·05), while rats fed Pd-fermented fibre concentrate resulted in lower concentration of butyric acid (P,0·05, P,0·01) in all parts
of the hindgut as compared with rats fed the native fibre concentrates. Butyrate concentrations ranged between 5–11mmol/g (distal colon) and
6–8mmol/g (13 d faeces). Higher proportions of acetic acid (P,0·05; P,0·01) were observed in the caecum of rats fed the fermented fibre concentrates. Rats fed Pd- and Lr-fermented fibre concentrates produced higher proportions of propionic acid (P,0·05; P,0·01) in the caecum.
Changes in SCFA formation in the caecum, distal colon and faeces of rats fed the fermented samples compared with the native sample indicate
that these microbes probably survive in the hindgut and that modification of the microflora composition with fermented foods is possible. This may
be important for the gastrointestinal flora balance in relation to colonic diseases.
Short-chain fatty acids: Fermented oat fibre concentrate: Lactic acid bacteria: Rat hindgut
The colon is one of the least understood and most metabolically active organs (Eastwood, 1991). It is a tubular contractile
reservoir that retains water, electrolytes, and ions and has a
complex assemblage of micro-organisms that are responsible
for the colon’s degradative abilities. The main carbon and
energy sources for colonic microflora are certain types of
carbohydrates usually referred to as indigestible carbohydrates. The type and amount of endproducts formed by
colonic bacteria depend on the chemical structure, composition and amounts of the available substrate, as well as the
biochemical characteristics and catabolite regulatory mechanisms of the bacteria involved (Macfarlane & Macfarlane,
1997). The main endproducts from microbial degradation in
the hindgut of dietary carbohydrates that escape digestion
are SCFA, mainly acetic, propionic and butyric acid (Ruppin
et al. 1980). Gases such as CO2, H2 and CH4 are also produced. There is increasing evidence that some SCFA have
specific physiological effects. Acetic and propionic acid are
quickly absorbed through the colonic mucosa, stimulating
salt and water uptake (Ruppin et al. 1980). A high production
of SCFA may also lower colonic pH, resulting in an increased
mineral solubility and reduced formation of secondary bile
acids (Nagengast et al. 1988; Delzenne et al. 1995). Further,
the proliferation of unwanted pathogens may decrease as a
result of lower colonic pH. Butyric acid and to some extent
propionic acid are important energy substrates for the colonocytes (Roediger, 1982), and butyric acid especially has been
suggested to play a part in the prevention and treatment of
ulcerative colitis (Cummings, 1997) and cancer (Scheppach
et al. 1995). Studies in vitro have also shown that butyric
acid may inhibit the growth of human cancer cells (Whitehead
et al. 1986; Gamet et al. 1992) and can induce apoptosis
(Hague et al. 1995) in colonic tumour cell lines. Propionic
acid may lower plasma cholesterol concentrations by inhibiting cholesterol synthesis from acetic acid in the liver (Wolever
et al. 1991) and also enhances colonic muscular contraction,
relieving constipation and contributing to laxation (Yajima,
1985). Acetic acid promotes the relaxation of resistance
vessels in the colonic vasculature, thus helping in the maintenance of blood flow to the liver and colon (Mortensen et al.
1990).
The amount and pattern of SCFA formed in the colon are
highly dependent on the type of carbohydrate available.
Some types of resistant starch, barley b-glucans, raffinose
and oligofructose appear to promote butyric acid production
both in vitro (Casterline et al. 1997; Karppinen et al. 2000)
and in rats (Berggren et al. 1993; Mathers et al. 1997; Nilsson
& Nyman, 2005). Arabinogalactans and guar gum result in
*Corresponding author: Dr Adele M. Lambo-Fodje, fax þ46 46 222 45 32, email adele.lambo@inl.lth.se
Abbreviations: EPS, exopolysaccharides; Lr, Lactobacillus reuteri; Pd, Pediococcus damnosus 2.6; V2, Lactobacillus bulgaricus and Streptococcus thermophilus.
British Journal of Nutrition (2006), 96, 47–55 DOI: 10.1079/BJN20061797
q The Authors 2006
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high yields of propionic acid (Berggren et al. 1993; Edwards,
1993) in rats. Oat dietary fibre has been shown to result in a
higher amount of butyric acid (1·44 mmol/g) by in vitro fermentation with human faecal inocula as compared with oneautoclaved cycle-resistant starch (0·94 mmol/g) (Casterline
et al. 1997). The formation of SCFA is dependent on physico-chemical characteristics of the carbohydrate reaching
the colon, such as monomeric composition, glycosidic linkages, molecular weight and solubility (Henningsson et al.
2001; Nilsson & Nyman, 2005), which in turn can be affected
by heat treatment (Goodlad & Mathers, 1992) and
fermentation.
Oat-based media could be suitable for the growth of lactic
acid bacteria and also for the formation of microbial or
exopolysaccharides (EPS) (Mårtensson et al. 2002a,b). A
straight-chained b-(1 ! 3) glucan polymer with b-(1 ! 2)
glucose monomers linked to the interior chain has also been
isolated from Pediococcus damnosus 2.6 (Pd) (DueñasChasco et al. 1997). This EPS can be produced in an oatbased medium after incubation with Pd (Mårtensson et al.
2002a,b). The production of EPS with a-(1 ! 3) glucan and
a-(2 ! 6) fructan structures has also been observed in Lactobacillus reuteri (Lr) LB 121 growing on sucrose (van GeelSchutten et al. 1999). However, there is yet no evidence that
Lr ATCC 55 730 used in the present study produces EPS in
an oat-based medium. EPS are capable of improving the texture and viscosity of the final product (Ricciardi et al. 1994)
and may also improve the sensory and nutritional properties.
The dairy industry uses some cultures that have been
described as promoters of ropiness or mouthfeel because of
their texture-enhancing properties (Sutherland, 1998; Folkenberg et al. 2005). Further, Nakajima et al. (1992) reported
that there was a reduction in serum lipids in rats fed a ropy
milk product containing a phospho-polysaccharide. The physiological effects of lactic acid bacteria-produced EPS may
depend on their ability to resist degradation by gastrointestinal
enzymes, and thus behave like a type of dietary fibre.
The objective of the present study was to evaluate the formation of SCFA along the hindgut of rats fed a b-glucanenriched oat fibre concentrate fermented with different lactic
acid bacteria. Commercial yoghurt strains consisting of a mixture of (a) L. delbrueckii subsp. bulgaricus and Streptococcus
salivarius subsp. thermophilus (V2), (b) Lr ATCC 55 730 and
(c) the EPS-producing bacteria Pd were used in the fermentations
of the oat fibre concentrate. The effects of the diets on food intake
and weight gain, weight of the caecum contents, bulking effect
and SCFA production were investigated.
Materials and methods
Bacterial strains
The probiotic culture Lr, the EPS-producing culture Pd and
the commercial yoghurt strain, V2, were used. Lr was
obtained from Biogaia Biologics (Stockholm, Sweden). Pd
was received from the collection at the University of San
Sebastian (Universidad del Paı́s Vasco, Spain). Pd and Lr
strains were stored at 2808C in De Man–Rogosa–Sharpe
broth (De Man et al. 1960) containing 25 % (v/v) glycerol.
The commercial yoghurt culture V2 was a 1:1 mixture of
L. delbrueckii subsp. bulgaricus and S. salivarius subsp.
thermophilus (Visby Tønder A/S, Tønder, Denmark); V2
was stored at 2808C according to the recommendation of
the manufacturer. V2 was chosen because it is the starter
culture commonly used in Sweden and improves aroma and
acidity in the final product.
Preparation of the oat fibre concentrates
Oat fibre concentrate in powder form was obtained from Ceba
Foods AB (Lund, Sweden). The powder was reconstituted to a
DM of 10 %, with aqueous distilled water. Glucose (2 %, w/v)
was added to the concentrate as an additional substrate for
microbial growth and the mixture was sterilised at 808C for
20 min. The concentrate was then cooled to fermentation temperature (288C for Pd and 378C for V2 and Lr) and inoculated.
The fermentations were performed over a period of between
16 and 20 h (due to the different growth rate of the various
lactic acid bacteria) under anaerobic conditions. The amount
of V2 culture used as inoculum was 0·02 % (w/v). Inoculates
for Pd and Lr (5 %, v/v) were taken from a fresh (20 h incubation) pre-inoculum in De Man–Rogosa–Sharpe broth
(Merck, Darmstadt, Germany) and the cells were collected
and washed with 0·9 % (w/v) NaCl solution. The final pH of
the fermented fibre concentrates was 4·2 ^ 0·5. All samples
were lyophilised using a Labconco lyphlock 12 freeze-dry
system (Ninolab AB, Väsby, Sweden) and milled to a particle
size less than 0·3 mm in a Cyclotec mill (Tecator AB,
Höganäs, Sweden). The chemical composition of the oat
fibre concentrates is shown in Table 1.
Animals and experimental design
Male Wistar rats with an average weight of 91·0 (SEM 3) g were
purchased from B&K Universal (Stockholm, Sweden). The rats
were randomly divided into groups of seven in order to obtain
Table 1. Composition of oat fibre concentrates (g/100 g dry weight)
Native Fermented with V2 Fermented with Pd Fermented with Lr
Protein 28·0 29·0 29·0 28·0
Lipids 14·0 13·0 14·0 13·5
Starch 21·4 21·0 22·3 23·3
Dietary fibre 25·0 24·5 24·8 25·3
Ash 2·6 2·4 3·0 1·2
NA* 9·0 10·1 6·9 8·7
V2, Lactobacillus bulgaricus and Streptococcus thermophilus; Pd, Pediococcus damnosus 2.6; Lr, L. reuteri;
NA, not analysed.
*Likely to be low-molecular-weight carbohydrates.
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a similar average weight between the different test groups (91·0
(SEM 2·0), 90 (SEM 3·0), 90·5 (SEM 3·0), 92·8 (SEM 3·0) g for rats
fed the native, V2-fermented, Pd- and Lr-fermented fibre concentrates respectively). The rats were housed individually in
metabolism cages, with free access to water (Berggren et al.
1993). The feed intake was restricted to 12 g dry weight per d.
After 7 d of adaptation to the diets, a 5 d experimental period followed when faeces were collected daily for the determination of
faecal dry and wet weights, fermentability and bulking effect.
Faeces were kept at 2208C and then freeze-dried and milled
before analysis of total fermentability. Fresh faeces were collected on dry ice on day 6, to determine the faecal excretion of
SCFA (13 d). At the end of the experiment, the animals were
killed using CO2. The caecum and colon were immediately
removed and the colon was divided into the proximal and the
distal parts and kept frozen (2208C) until analysed for SCFA.
The caecal tissue, content weight and pH were measured
before freezing the caecal content. The Ethics Committee for
Animal Studies at Lund University (Sweden) approved the
animal experiment.
Diets were formulated from four test products. These products were the native oat fibre concentrate, the V2-fermented
oat fibre concentrate, Pd-fermented oat fibre concentrate and
Lr-fermented oat fibre concentrate. All diets had a concentration of indigestible carbohydrates of 80 g/kg dry weight
(corresponding to a total intake of about 4·8 g for each rat
during the 5 d experimental period). Components of the test
diets are shown in Table 2. The DM content of the diets
was adjusted with wheat starch, a starch source that has
been shown to be completely digested and absorbed in the
upper intestinal tract and therefore does not contribute to
any hindgut fermentation (Björck et al. 1987). The amount
of SCFA excreted on a wheat starch diet has also been
shown to be negligible (Berggren et al. 1993).
Analytical methods
Indigestible carbohydrates. The content of indigestible
carbohydrates (dietary fibre) in the oat fibre concentrates
was isolated in duplicate using the centrifugation–dialysis
method (as described before in Lambo et al. 2005), in
which molecules with a molecular weight $1000 Da will be
recovered. The fibre values were corrected for remaining
proteins, lipids, starch and ash (Table 1). The monomeric
composition of the dietary fibre in the isolated fibre residues
and in faeces was analysed by GLC on a DB-225 column
(J&W Scientific, Folsom, CA, USA) for the neutral sugars
as their alditol acetates and spectrophotometrically for the
uronic acids (Theander et al. 1995).
Crude protein, lipids, starch and minerals. The N was
assayed by the Kjeldahl procedure (Kjeltec System 1003;
Tecator AB, Höganäs, Sweden) according to the manual.
Crude protein was calculated as N £ 6·25.
Total lipid content was determined gravimetrically by extraction in diethyl ether and petroleum ether (boiling point 40–608C;
1:1) after hydrolysis with 7·7 M-HCl at 70–808C for 60 min
(Association of Official Analytical Chemists, 1980).
Total starch in the fibre residues and faeces from the rats
was quantified as described by Björck & Siljeström (1992).
No starch could be detected in the faeces.
Ash content was determined by incineration at 5508C for at
least 5 h, cooling in a desiccator and then weighing.
Determination of short-chain fatty acids. The amount of
SCFA (acetic, propionic, iso-butyric, butyric, iso-valeric, valeric, caproic, and heptanoic acid), lactic acid and succinic acid
in the caecum, colon and 13 d faeces were analysed by GLC
(Richardson et al. 1989). The intestinal content was homogenised (Polytronw; Kinematica AG, Lucerne, Switzerland) with
2-ethylbutyric acid as internal standard. Hydrochloric acid
was added to protonise the SCFA, which were then extracted
with diethyl ether and silyated with n-(tert-butyldimethylsilyl)-n-methyltrifluoroacetamide (Sigma Chemical Company,
MO, USA). The samples were allowed to stand for 24–48 h
in order for complete derivatisation to occur and then they
were analysed using an HP-5 column (Hewlett-Packard,
Wilmington, DE, USA), and integrated by Chem Station software (Hewlett-Packard).
Calculations and statistical analyses
Bulking capacity of the indigestible carbohydrates was calculated as:
Faecal dry weighttest diet ðgÞ
Indigestible carbohydrates ingestedtest diet ðgÞ :
Table 2. Components of test diets (g/kg dry weight)
Component Native Fermented with V2 Fermented with Pd Fermented with Lr
Dietary fibre source 320 320 320 320
Casein 80 80 80 80
Maize oil 10 10 10 10
Sucrose 100 100 100 100
DL-Methionine 1 1 1 1
Mineral mixture* 48 48 48 48
Vitamin mixture† 8 8 8 8
Choline chloride 2 2 2 2
Wheat starch 431 431 431 431
V2, Lactobacillus bulgaricus and Streptococcus thermophilus; Pd, Pediococcus damnosus 2.6; Lr, L. reuteri.
*Contained (g/kg): CuSO4.5H2O, 0·37; ZnSO4.7H2O, 1·4; KH2PO4, 332·1; NaH2PO4.2H2O, 171·8; CaCO3, 324·4; KI,
0·068; MgSO4, 57·2; FeSO4.7H2O, 7·7; MnSO4.H2O, 3·4; CoCl.6H2O, 0·020; NaCl, 101·7.
† Contained (g/kg): menadione, 0·62; thiamine hydrochloride, 2·5; riboflavin, 2·5; pyridoxine hydrochloride, 1·25; calcium
pantothenate, 6·25; nicotinic acid, 6·25; folic acid, 0·25; inositol, 12·5; p-aminobenzoic acid, 1·25; biotin, 0·05; cyanocobalamin, 0·00 375; retinal, 0·187; vitamin D, 0·000613; vitamin E, 25; maize starch, 941·25.
Short-chain fatty acids in rats fed oats 49
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Fermentability (%) of the indigestible carbohydrates was calculated as:
1 2
Indigestible carbohydrates in faecestest diet ðgÞ
Indigestible carbohydrates ingestedtest diet ðgÞ
 
£ 100:
The molar proportion of SCFA was calculated as a ratio of the
total concentration of organic acids analysed to the individual
acid concentration and expressed as a percentage.
All statistical analyses were performed with the Minitabw
software package version 13 (Minitab Inc., State College,
PA, USA). The means and standard deviations were analysed
using the two-sided Student’s t test. Significance of difference
between the means of the fermented fibre concentrates and the
native fibre concentrates was determined (P,0·05 and
P,0·01).
Results
Monomeric composition of the indigestible carbohydrate
The monomeric composition of the indigestible carbohydrate
in the native and fermented fibre concentrates is shown in
Table 3. The main monomer in all materials was glucose.
The distribution between the neutral sugars and uronic acids
was quite similar in all the concentrates.
Basal data
The feed intake was almost complete and the rats gained
weight throughout the experiment (Table 4). Body-weight
gain, wet and dry faecal outputs, caecal contents, bulking
capacity and fermentability were similar among the different
groups and no significant differences could be seen.
Short-chain fatty acid concentrations
Acetic acid was the major metabolite in rats fed the oat fibre
concentrates, followed by propionic and butyric acids.
Approximately 80 % of the organic acids analysed in the
caecum of rats could be attributed to these acids. Some
lactic acid could also be detected (Table 5).
A significantly higher concentration of acetic acid was
observed in the caecum and distal colon of rats fed the V2-fermented fibre concentrate (51 and 29mmol/g, respectively;
P,0·01) as compared with the native fibre concentrate (39
and 21mmol/g, respectively) (Fig. 1).
The propionic acid concentrations were similar in rats fed
the different fibre concentrates. The exception was in the
distal colon of rats fed the fermented fibre concentrates and
the 13 d faeces of the rats fed the Pd-fermented fibre concentrate, where significantly higher (P,0·05) concentrations of
propionic acid were obtained, as compared with the native
fibre concentrate (Fig. 1).
The caecal butyric acid concentrations in rats fed the Pd(9mmol/g) and Lr- (15mmol/g) fermented fibre concentrates
were significantly lower (P,0·05) than in those fed the
native fibre concentrate (24mmol/g). In the proximal and
distal colon, only the Pd-fermented fibre concentrate yielded
a significantly lower (P,0·05) butyric acid concentration as
compared with the native fibre concentrate.
Proportions of short-chain fatty acids
Some differences were also observed in the proportions of
SCFA among the rats fed the different fibre concentrates
(Fig. 2). The rats fed the fermented fibre concentrates yielded
significantly higher (P,0·05; P,0·01) proportions of acetic
acid in the caecum than the native fibre concentrate. A
higher proportion of acetic acid (P¼0·014) was formed in
the distal colon of rats fed the Pd-fermented fibre concentrate
as compared with the rats fed the native fibre concentrate.
Proportions of propionic acid were higher (P,0·05;
P,0·01) in the caecum of rats fed the Pd- (P¼0·043) and
Lr- (P¼0·004) fermented fibre concentrates than in the
caecum of rats fed the native fibre concentrate. There was
also a tendency for rats fed the Pd-fermented fibre concentrate
to yield higher proportions of propionic acid in the distal colon
and 13 d faeces as compared with the rats fed the native fibre
concentrate (Fig. 2).
In the caecum, the rats fed the Pd- and Lr-fermented fibre
concentrates produced significantly lower (P,0·05; P,0·01)
butyric acid proportions than the rats fed the native fibre concentrate. In the distal colon, only the rats fed the Pd-fermented
fibre concentrate had a significantly lower (P¼0·010) butyric
acid proportion.
Caecal pools and faecal excretions
Caecal pool and faecal excretions of the organic acids are
shown in Table 5. The caecal pool of organic acids (SCFA þ
lactic acid) in rats fed the V2-fermented fibre concentrate was
higher (P¼0·026) than the caecal pool in rats fed the native
fibre concentrate due to higher amounts of acetic (P¼0·008)
and propionic acids (P¼0·048). Rats fed the Pd-fermented
fibre concentrate had lower caecal pools of butyric acid
(P¼0·007) and lactic acid (P¼0·010) than those fed native
fibre concentrate. However, the faecal excretion of propionic
acid was higher (P¼0·017) for rats fed the Pd-fermented
Table 3. Monomeric composition (%) of indigestible carbohydrates in the oat fibre concentrates
Native Fermented with V2 Fermented with Pd Fermented with Lr
Arabinose 2·5 3·0 3·2 2·6
Xylose 2·5 2·5 2·7 2·0
Glucose 81·0 83·0 82·9 82·2
Uronic acids 11·4 10·2 9·1 10·2
Minor components* 2·6 1·3 2·1 3·0
V2, Lactobacillus bulgaricus and Streptococcus thermophilus; Pd, Pediococcus damnosus 2.6; Lr, L. reuteri.
*Rhamnose, fucose, mannose and galactose.
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fibre concentrate as compared with those rats fed the native
fibre concentrate.
Faecal excretions were higher for rats fed the Lr-fermented
fibre concentrate (116mmol; P¼0·030) as compared with
those fed the native fibre concentrate (76mmol). This could
be explained by higher (P,0·05; P,0·01) excretions of
acetic, propionic and lactic acids in rats fed this diet.
Discussion
SCFA, especially propionic and butyric acids, have been
reported to have health-promoting properties and the desire
to develop functional food products with the ability to improve
health or prevent the incidence of certain diseases has become
a challenge for the food industry. In the present investigation,
oat fibre concentrate was fermented with different lactic acid
bacteria and used in a rat experiment, in order to observe
the SCFA formation in the hindgut. Oat fibre concentrates
were fed to rats for 13 d, which has been reported to be sufficiently long to yield optimal fermentation of dietary fibre
components (Nyman & Asp, 1985; Brunsgaard et al. 1995)
and a stable SCFA profile (Tulung et al. 1987; Levrat et al.
1991).
The total fermentability of the fibre was similar (about 92–
96 %) in the native and fermented oat fibre concentrates, and
was in agreement with previous studies, which revealed
values of about 90 % for a b-glucan-enriched oat fibre (Henningsson et al. 2002) and about 97 % for barley b-glucans
(Berggren et al. 1993). Rats fed the V2-fermented fibre concentrate were more prone to form SCFA in the caecum,
while those fed the Lr-fermented fibre concentrate resulted
in the highest faecal excretion of SCFA, indicating a slower
fermentation of the substrate with the presence of Lr (Table 5).
In the caecum and distal colon, the formation of acetic and
propionic acids seemed to be favoured by the rats fed the fermented fibre concentrates, while butyric acid formation was
comparatively higher in rats fed the native fibre concentrate.
V2 and Pd have been observed to be homofermenters in
vitro (convert glucose to lactic acid) (Axelsson, 1998; Battock
& Azam-Ali, 1998), whereas Lr has been observed to be a heterofermenter (converts glucose to lactic and acetic acid)
(Lindgren & Dobrogosz, 1990; Mitsuoka, 1992; Fujisawa
et al. 1996). The colonic sugar fermenters Clostridium spp.,
Table 4. Initial weight (g), feed intake (g/d) and body-weight gain (g/d) of rats, and faecal and caecal
contents (g/d), fibre intake (g/d), bulking capacity and fermentability (%) in rats fed native and
fermented oat fibre concentrates*
(Mean values with their standard errors for seven rats per group)
Native
Fermented
with V2
Fermented
with Pd
Fermented
with Lr
Mean SEM Mean SEM Mean SEM Mean SEM
Initial weight 91·0 2·0 90·0 3·0 90·5 3·4 92·8 3·0
Feed intake 11·4 0·7 11·3 0·8 11·6 0·2 11·6 0·4
Body-weight gain 3·8 1·0 3·1 1·4 4·0 1·4 3·5 1·0
Wet faeces 0·87 0·1 0·87 0·2 0·88 0·1 0·80 0·2
Dry faeces 0·54 0·02 0·60 0·03 0·60 0·06 0·53 0·07
Caecal content 2·3 0·1 2·5 0·6 2·0 0·3 2·5 0·5
Fibre intake 0·91 0·06 0·90 0·07 0·93 0·02 0·93 0·03
Bulking capacity 0·60 0·02 0·63 0·04 0·62 0·06 0·60 0·07
Fermentability 94·4 1·4 92·8 1·1 95·4 2·8 96·2 1·4
V2, Lactobacillus bulgaricus and Streptococcus thermophilus; Pd, Pediococcus damnosus 2.6; Lr, L. reuteri.
*No significant differences could be seen between the groups.
Table 5. Caecal pool (mmol) and faecal excretion of organic acids (mmol)†
(Mean values with their standard errors for seven rats per group)
Acetic acid Propionic acid Butyric acid Lactic acid Total pool
Mean SEM Mean SEM Mean SEM Mean SEM Mean SEM
Caecum
Native 94 4 32 2 61 8 22 2 236 16
Fermented with V2 142*** 12 54** 9 53 9 17 4 294** 15
Fermented with Pd 102 14 35 5 24*** 6 11** 2 186 19
Fermented with Lr 112 22 43 6 36 12 11** 3 217 32
13 d Faeces
Native 41 5 8 0·6 9 1 8 2 76 9
Fermented with V2 41 4 8 0·2 10 2 10 1 77 5
Fermented with Pd 53 6 13** 2 7 1 11 2 92 8
Fermented with Lr 61** 8 13** 2 12 4 20*** 4 116** 18
V2, Lactobacillus bulgaricus and Streptococcus thermophilus; Pd, Pediococcus damnosus 2.6; Lr, L. reuteri.
Mean values were significantly different from the corresponding value of the native fibre concentrate in the same part of the hindgut:
** P,0·05, *** P,0·01.
Short-chain fatty acids in rats fed oats 51
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Eubacterium spp., Fusobacterium spp., Butyrivibrio spp. and
acid utilisers, such as Megaspaera elsdenii, are all butyrateproducers (Holdeman et al. 1977; Tsukahara et al. 2002).
Sugar fermenters produce butyric acid as the major endproduct of fermentation, while the acid utilisers convert lactic
acid to butyric acid (Tsukahara et al. 2002). Bifidobacteria,
which are also present in the colon, produce both acetic and
lactic acid. Propionibacterium sp. and Veillonella sp. are
acetate and propionate producers (Mitsuoka, 1996; Ozadali
et al. 1996). The production of butyric acid generated by
acid converters such as M. elsdenii, for example, is stimulated
by lactic and acetic acids (Tsukahara et al. 2002). This conversion process seems to depend on the rate at which lactic acid is
produced. The varied amounts of acetic, propionic, butyric and
the other organic acids observed in the present study most
probably resulted from the metabolic activities of the
microflora in the colon as well as from the ingested microorganisms in the fermented fibre concentrates.
It may also be questioned if the ingested bacteria reach the
hindgut of rats in a live state. There has been some controversy as to whether V2 survives passage through the intestinal
tract. Bianchi-Salvadori et al. (1978) isolated viable V2 in the
faeces of human subjects after yoghurt consumption, whereas
Pedrosa et al. (1995) did not come to the same conclusion. In
conventional rats, one of the micro-organisms in V2, L. delbrueckii spp. bulgaricus was not always present, whereas
the other micro-organism, S. salivarius spp. thermophilus
did not survive beyond the upper small intestine (Hargrove
& Alford, 1978). Lr, on the other hand, inhabits the gastrointestinal tract of mammals and hence survives the passage and
reaches the colon (Casas & Dobrogosz, 2000), while there is
yet no report about the survival of Pd in vivo. However, in
vitro studies have shown that Pd can tolerate exposures to gastrointestinal juices (Immerstrand, 2005). The variations in the
0
10
20
30
40
50
60(a)
(b)
(c)
A
ce ti c ac id (
µm
o l/g
)
0
10
20
30
40
P
ro p io n ic a ci d (
µm
o l/g
)
0
10
20
30
Caecum Proximal Distal 13 d faeces
B
u ty ri c ac id (
µm
o l/g
)
***
***
**
**
**
**
***
**
** **
**
Fig. 1. Concentrations of (a) acetic acid, (b) propionic acid and (c) butyric
acid (mmol/g wet contents) in the caecum, proximal colon, distal colon and in
13 d faeces of rats fed native fibre concentrate (B), Lactobacillus bulgaricus
and Streptococcus thermophilus-fermented fibre concentrate ( ), Pediococcus damnosus 2.6-fermented fibre concentrate (A) or L. reuteri-fermented
fibre concentrate ( ). Data are means (n 7), with their standard errors represented by vertical bars. Mean values were significantly different from the
corresponding value of the native fibre concentrate in the same part of the
hindgut: ** P,0·05, *** P,0·001.
30
40
50
60(a)
(b)
(c)
A
ce ti c ac id (
%
)
5
7
9
11
13
15
17
19
21
23
P
ro p io n ic a ci d (
%
)
0
5
10
15
20
25
30
Caecum Proximal Distal 13 d faeces
B
u ty ri c ac id (
%
)
**
***
***
**
**
**
***
**
**
**
Fig. 2. Proportions of (a) acetic acid, (b) propionic acid and (c) butyric acid
(percentage of total SCFA) in the caecum, proximal colon, distal colon and in
13 d faeces of rats fed native fibre concentrate (W), Lactobacillus bulgaricus
and Streptococcus thermophilus-fermented fibre concentrate (X), Pediococcus damnosus 2.6-fermented fibre concentrate (A) or L. reuteri-fermented
fibre concentrate ( £ ). Data are means (n 7), with their standard errors represented by vertical bars. Mean values were significantly different from the
corresponding value of the native fibre concentrate in the same part of the
hindgut: ** P,0·05, *** P,0·001.
A. M. Lambo-Fodje et al.52
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formation of SCFA in the caecum and distal colon of rats fed
the different fermented fibre concentrates could also be interpreted as a probable indication that there is survival of these
microbes in the upper intestinal tract and that they reach the
hindgut. When ingested, these micro-organisms might
improve the balance of gastrointestinal flora by increasing
the number and activity of endogenous bacteria possessing
health-promoting properties.
The significantly higher concentration of propionic acid in
the distal colon and the13 d faeces, the 13 d faecal excretion
and the tendency towards higher proportions of propionic
acid in the distal colon and 13 d faeces of rats fed Pd-fermented fibre concentrate is evidence of the fact that this substrate
persisted to a higher extent beyond the proximal colon as compared with the native fibre concentrate. This observed trend
reveals that there was a tendency for propionic acid to be continuously formed to a higher degree in the distal part of the
hindgut of rats fed Pd-fermented fibre concentrate than of
rats fed the native fibre concentrate, which may be positive
towards maintaining colonic health. Propionic acid (like butyric acid) is an important energy substrate for the colonic
mucosa and, as most colonic diseases occur in the distal part
of the colon, it is important to increase the formation of
these acids distally. Furthermore, propionic acid has been
suggested to inhibit the synthesis of cholesterol from acetic
acid in the liver (Wright et al. 1990; Wolever et al. 1991).
Interestingly, in a clinical study on human subjects, a ropy
oat-based product (fermented with the strains V2 and Pd
2.6) significantly reduced total cholesterol (4·3 %) and
increased faecal Bifidobacterium ssp. count compared with a
fermented dairy-based product (Mårtensson et al. 2005). It
could be speculated that this was due to an increased formation of propionic acid.
In the caecum, the proportion of butyric acid was lower
(P,0·05; P,0·01) for rats fed the fermented (except for
V2) products (12–21 %) than for those fed the native fibre
concentrate (26 %). The values for the fermented products
were, however, in a similar region as those observed from earlier studies (15 %) for a b-glucan-enriched oat fibre and barley
b-glucan, i.e. substrates known to promote comparatively high
proportions of butyric acid (Berggren et al. 1993; Henningsson et al. 2002). The differences between the native and fermented fibre concentrates could probably be due to the
added bacteria and their capability of modifying the composition of the microflora in the hindgut and thus the SCFA profile. Furthermore, possible changes in the biochemical
characteristics of the substrates after in vitro fermentation
could also contribute to the observed results. Thus, Lambo
et al. (2005) observed that the physico-chemical properties,
such as the amount of oats and barley b-glucans and viscosity
of b-glucans solutions, were lowered after incubation with a
mixture of lactic acid bacteria. However, in the present
study the amount of dietary fibre including b-glucans was
not lowered after fermentation, which may have been due to
the fact that mixtures of lactic acid bacteria were not used
in the fermentation. Furthermore, a higher amount of substrate
(2 % glucose) was also used in the present study as compared
with 1 % in the previous study. On the other hand, it cannot,
however, be excluded that the molar mass of the dietary
fibres and b-glucans were not modified during fermentation
with the different lactic acid bacteria. Interestingly, Nilsson
& Nyman (2005) have shown that fructo-oligosaccharides
with a low degree of polymerisation yielded higher amounts
of butyric acid than those with a high degree of polymerisation, which instead yielded high amounts of propionic acid.
The proportions of butyric acid in the distal colon of rats fed
the fibre concentrates (10–16 %) were similar to earlier
reports on potato products (14 %) (Henningsson et al. 2002).
A high formation of butyric acid in the colon, especially in
the distal part, is interesting as it might protect against colon
cancer (Whitehead et al. 1986; McIntyre et al. 1993; Hague
et al. 1995; Thorup et al. 1995), and type III resistant starch
has been found to play such a protective role in rats (Perrin
et al. 2001). Colon cancer occurs mostly in the distal colon
in both man and experimentally induced rodent cancer
models (Bufill, 1990; Holt et al. 1996). Butyric acid may
also have therapeutic effects in distal ulcerative colitis (Scheppach et al. 1992). A human study showed that b-glucanenriched oat bran (20 g fibre) added to the diet of patients
with ulcerative colitis for 12 weeks increased the concentration of butyric acid in the faeces by 36 % and also improved
the symptoms of the disease (Hallert et al. 2003). Furthermore, Perrin et al. (2001) observed that only those indigestible
carbohydrates favouring a high and stable butyric acid production in the rat hindgut decreased the rate of aberrant
crypt foci, one of the most reliable intermediate biomarkers
of colon cancer (Pretlow et al. 1991, 1992; Konstantakos
et al. 1996; Young et al. 1996; Shivapurkar et al. 1997).
Prebiotic products that maintain SCFA formation (even in
small concentrations) in the distal colon are recommended.
Butyric acid concentrations of 1–5mmol/g (Scheppach et al.
2001) have been found to effectively suppress cell proliferation in cultured colonocytes, but it is still unclear how
these concentrations relate to conditions in vivo. This will
probably depend on the extent of butyric acid uptake along
the colon and the persistence of an active concentration
(Robertson et al. 2001). Butyrate concentrations in the present
study ranged between 4 and 9mmol/g in the proximal colon, 5
and 11mmol/g in the distal colon and 6 and 8mmol/g in the
13 d faeces. This implies that butyric acid formation persisted
along the hindgut.
In conclusion, the fermented fibre concentrates seemed to
favour the formation of acetic and propionic acids, while the
native fibre concentrate favoured the formation of butyric acid.
Acknowledgements
Ceba Foods AB (Lund, Sweden) financially supported the present study.
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