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Human Nutrition Research Centre, Institut National de la Recherche Agronomique, BP 71627, 44316 Nantes Cedex 03, France
2To whom correspondence should be addressed: C Cherbut INRA, BP 71627, 44316 Nantes Cedex 03, France. Fax: 33–2-40–67-50–12. E-mail: cherbut{at}nantes.inra.fr
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • butyrate • colonic microflora • fructo-oligosaccharides • long-term intake • rats
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). They are mainly known for their
ability to increase the endogenous growth of intestinal lactobacilli
and bifidobacteria in humans and animals (Bouhnik et al. 1996
, Campbell et al. 1997
, Gibson and Roberfroid 1995
), which has long been regarded as beneficial to
health (Gibson and Roberfroid 1995
, Macfarlane et al. 1997, Metchnikoff 1903
). Moreover, in vitro
(Gibson and Wang 1994
) and in vivo studies
(Campbell et al. 1997
) in rats showed that FOS
fermentation decreases intracolonic pH, produces SCFA and lactate, and
increases the proportion of butyrate. SCFA, especially butyrate, are
the main sources of energy for colonocytes (Roediger 1995
) and influence colonic function by stimulating water and
sodium absorption and modulating motility (Cherbut et al. 1997,
Roediger and Moore 1981
). Moreover,
butyrate induces differentiation and stimulates the apoptosis of
cancerous cells in vitro (Hague et al. 1996
).
Although FOS intake seems beneficial, its effect was studied only for
short periods of ingestion never exceeding 3–4 wk. Several authors
have suggested that gut adaptation could modify the gastrointestinal
effects of nondigestible carbohydrates (Rao et al. 1994
,
Weaver et al. 1996
). In rats fed different types of
indigestible polysaccharides, 3–12 wk were necessary to stabilize
cecal bacterial mass and metabolic activity and allow measurement of
stable digestibility of nonstarch polysaccharides and cecal SCFA
concentrations (Brunsgaard et al. 1995
, Walter et al. 1986
, Weaver et al. 1996
). In humans, a
similar adaptation seems to occur, since studies showed that a chronic
(8-d) load of lactulose was better digested than a single load
(Florent et al. 1985
) and reduced the diarrhea induced
by a single large dose (Flourié et al. 1993
).
Furthermore, Rao et al. (1994)
reported that fecal bacterial
composition was different after 15 wk than 2 wk of psyllium fiber
intake. In particular, the increase in bifidobacteria noted at wk 2
returned to baseline levels at wk 15. In this context, we tested the
hypothesis that the effects of FOS on cecal flora activities and
populations in rats would differ over short (2 wk), medium (8 wk) and
long (27 wk) periods of time.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Thirty-six male Wistar rats (Janvier, Le Genest Saint Isles, France),
with an initial mean weight of 115 ± 1 g (6 wk), were
divided into six groups of six rats each and fed two different diets
for 2, 8 or 27 wk. Control groups were fed a basal low-fiber diet
(Basal) containing (g/kg diet): pregelatinized corn starch 646, soluble
casein 204, DL-methionine 3.7, corn oil 18.5, lard 58.5, a
mineral mixture 43.7 [providing (g/kg diet):
Ca2(PO4)3 16.6,
K2(PO4)3 10.5, CaCO3
8.0, NaCl 3.1, MgSO4 3.9, FeSO4 0.3,
ZnSO4 0.2, MnSO4 0.2, CuSO4 0.04,
CoSO4 4.10-4, K2HSO4
4.10-4, NH3(SO4)2
4.10-4, MgO 0.9], a vitamin mixture 5.6 [providing (mg/kg
diet): all-rac-
–tocopherol (500 UI/g) 150,
all-trans-retinyl acetate (500,000 UI/g) 8,
cholecalciferol (400,000 UI/g) 2.5, nicotinic acid 45, calcium
pantothenate 15, thiamin hydrochloride 5, riboflavin 9, pyridoxine (PN)
hydrochloride 5, ascorbic acid 113, folic acid 2,
p-aminobenzoic acid 113, vitamin B-12 (1 g/kg) 67.8,
biotin 0.4, phylloquinone 2, myo-inositol 113] and
cellulose 20. Experimental groups received a diet containing 90 g/kg
short-chain FOS. FOS were included in the Basal diet at the expense
of corn starch, so that the two diets (Basal and FOS) differed only in
the proportions of corn starch and FOS. These FOS, composed of 44%
1-kestose (GF2), 46% nystose (GF3), and 10%
1F-ß-fructofuranosyl nystose (GF4), are considered to be
fully indigestible in the small intestine of rats (Nilsson et al. 1988
). Rats were individually housed in suspended
wire-mesh-bottomed cages and maintained at 23°C in an animal room
with a 12-h light-dark cycle. Food and water were consumed ad
libitum. Food intake and body weight were recorded every
2 to 3 d during the first period (2 wk) and then twice a month.
All experiments were in accordance with National Research Council
guidelines for the care and use of laboratory animals.
Transit time.
One wk before killing, rats were placed individually in metabolic cages
and acclimated for 2 d. On the 3rd d, they received 4 mL of
polyethylene glycol (PEG) 4000 (10%) by oral administration. Their
feces were then harvested and weighed every 3 h for 4 d.
Harvested feces were freeze-dried, weighed and pulverized to
determine PEG concentration according to the method of Hyden (1955)
.
Transit time was calculated as that required for the excretion of 50%
of the initial PEG.
Cecum collection.
At the end of each adaptation period, rats were killed by an intracardiac injection of sodium pentobarbital. The cecum was immediately removed, carefully dissected free from fat and mesentery, and weighed. The content was then removed and weighed. The empty tissue was washed with phosphate-buffered saline, blotted and weighed.
Cecal content was divided into four parts: 1) 0.8 g was collected into a sterile assay tube for bacterial enumeration; 2) 0.2 g was immediately frozen at -80°C for further analysis of lactate; 3) 0.3 g was supplemented with 0.75 mL of HgCl2 (1 g/L) and 0.105 mL of H3PO4 (50 g/L) and then frozen at -80°C for further analysis of SCFA; and 4) the residual material was used for dry matter determination. A portion of proximal and distal colonic contents was also sampled for SCFA and lactate analysis, and bacterial enumeration.
Bacterial enumeration.
Samples for enumeration of selected genera of colonic bacteria were serially diluted 10-fold with anaerobic one-fourth strength peptone-water within 2 h after collection. One hundred microliters of the appropriate dilutions were inoculated onto duplicate plates using unselective media for the enumeration of total anaerobes (Wilkins Chalgren Agar), and selective media for Lactobacillus sp. (Rogosa Agar) and total lactic acid-producing bacteria, i.e., Streptococcus sp., Lactobacillus sp. and Bifidobacterium sp. (Man Rogosa Sharp Agar). Plates were incubated aerobically or in an anaerobic chamber (H2/CO2/N2, 5:10:85) for 24 or 72 h as appropriate. After incubation, single colonies were counted, and the results were expressed as the log10 of the colony-forming unit (CFU) per gram of wet weight of cecal content.
SCFA and lactate analysis.
Lactate concentrations were determined by gas chromatography after
methylation and chloroformic extraction from cecal contents
(Holdeman et al. 1977
). Malonic acid was used as
internal standard. SCFA were analyzed by gas chromatography according
to Jouany (1982)
on supernatants of thawed samples centrifuged at 8,000
x g for 10 min. 4-Methyl valeric acid was used as
internal standard.
Chemicals.
Short-chain FOS (Actilight®) were provided by Eridania-Beghin Say (Vilvoorde, Belgium). Pregelatinized corn starch was purchased from Cerestar (Vilvoorde, Belgium), soluble casein from Touzart et Matignon (Vitry sur Seine, France), DL-methionine from Rhône-Poulenc (Commentry, France), cellulose arbocel from Rettenmaier und Sohne (Germany). Vitamin and mineral mixtures were prepared by the INRA (Jouy en Josas, France). Microbiological media were purchased from Oxoid (Uuipath, Dardilly, France). All other chemicals were obtained from the Sigma Chemical Co. (St. Quentin Fallavier, France).
Statistical analysis.
Statistical analysis was performed using the Statview F-4.11 package (Abacus Concepts, Berkeley, CA). Two-way ANOVA was used to assess the effects of diet (Basal or FOS), time of exposure to diet (2, 8 or 27 wk) and interactions between diet and time. When significant differences were found, individual means were compared by one-way ANOVA, to assess the effects of diet at each time and the effects of time for each diet. Statistical significance was accepted at the P < 0.05 level. Data are expressed as means and pooled SEM
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Food intake increased during the first 2 wk, then stabilized at about
16–17 g/d in both diet groups throughout the course of the experiment
(Table 1
). Rat body weight increased steadily until the end of the experiment,
with no difference between the two diet groups (Table 1)
. Cecal wall
weight was greater in rats fed FOS than in those fed Basal after 2 wk
of feeding, after which the effect decreased with time (Table 1)
. Cecal
wet content was greater in rats fed FOS regardless of the time period.
The percentage of dry matter was lower in rats fed FOS after 2 wk as
compared to those fed Basal and then became similar for both groups
(Table 1)
. Transit time was longer in rats fed FOS than in those fed
Basal at 2 and 8 wk (Table 1)
.
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FOS increased the cecal concentration of total SCFA throughout the
ingestion period, while Basal did not significantly change it. This
effect was mainly due to a strong increase in butyrate concentration,
whereas propionate concentration was not modified by diet (Table 2
). This resulted in a significantly higher proportion of butyrate in
rats fed FOS than in those fed Basal, regardless of the time period
(respectively, 15.8 ± 3.2 vs. 7.9 ± 1.5% at 2
wk, 25.8 ± 4.6 vs. 6.8 ± 1.2% at 8 wk, and 14.8 ± 0.6 vs. 6.7 ± 1.1% at 27 wk, P = 0.026). FOS
also increased lactate concentration (Table 2)
about 15-fold after 2 wk
of feeding but only 1–2-fold after 8 and 27 wk. Concurrently, cecal pH
was decreased by 2 U after 2 wk of FOS and by only 1
U after 8 and 27 wk (Table 2)
. Neither lactate
concentration nor pH were changed over time in rats fed Basal. Similar
trends were observed in colonic contents (Table 3
). The butyrate proportion was higher in the colon (proximal and distal
parts) in rats fed FOS than in those fed Basal throughout the course of
the experiment. On the contrary, lactate was elevated in both segments
only after 2 wk of FOS, then decreased at the same level than that
observed in rats fed Basal.
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After 2 wk of ingestion, the concentrations of total lactic acid
producers and Lactobacillus sp. were higher in rats fed FOS
than those fed Basal, whereas the concentrations of total anaerobes
were not different (Fig. 1
). However, the lactic acid producing bacteria increase induced by FOS
was not maintained with time and disappeared within 8 wk of ingestion
(Fig. 1)
. Similarly in the proximal and distal parts of the colon,
total lactic acid-producing bacteria counts were higher after 2 wk
in rats fed FOS as compared to rats fed Basal, whereas at 27 wk the
groups did not differ (Table 3)
.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In humans, pH, SCFA concentration and bacterial composition of contents
can be measured only in stools, which accounts imperfectly for
fermentation occurring mainly in the proximal part of the large
intestine (Florent et al. 1985
). Therefore, we chose to
work with rats, a model allowing accessibility to cecal contents, which
was validated for fermentation studies of nondigestible carbohydrates
(McIntyre et al. 1991
, Nyman et al. 1986
). Although the rapid growth rate of rats was a
disadvantage for a long-term experiment since their body and organ
weights increased with time, it is unlikely that bacterial populations
and fermentation products were modified due to animal growth. The
intestinal flora of rats is quickly stabilized after weaning
(Tannock 1997
) and no differences were observed in cecal
pH or SCFA concentrations between 4- and 27-mo-old rats fed an
oat-based diet (Mathers et al. 1993
). Furthermore,
in our experiment, the growth rate and body weight of the rats did not
differ in the control and experimental groups. Two-way ANOVA showed
that the effect of diet on cecal microbiota composition and SCFA
concentration was independent of rat body weight. We focused our study
in the cecum because this part of the cecocolonic tract is the major
site of fermentation in nonruminant species (Breves and Stück 1995
). The results we obtained in the proximal and
distal parts of the colon confirmed the relevance of this choice. As in
the cecum, we observed a sustained butyrogenic effect of FOS in the
colonic contents, while the increase in lactate and lactic
acid-producing bacteria was transient. Nevertheless, the magnitude
of these effects was lower in the colon than in the cecum.
Food intake was similar in both diet groups and stabilized around
16–17 g/d after 2 wk of feeding, regardless of body weight. Rats fed
the FOS diet consumed the same amount of FOS, about 1.5 g/d, throughout
the ingestion period. When expressed in g/kg rat weight, the FOS dose
thus decreased over time. We cannot exclude that this might be involved
in the disappearance of the initial effects of FOS on lactate and
lactic acid bacteria concentrations. However, the FOS dose ingested by
rats after 2 wk remained high and comparable to doses at which a
prebiotic effect was reported in rats of similar weight
(Campbell et al. 1997
) and in humans (Bouhnik et al. 1996,
Gibson et al. 1995
). Moreover, if the
FOS dose is expressed in g/kg cecum weight, which would be more
accurate, there was no significant change in FOS dose over time
(P = 0.32).
Although transit time was longer in rats fed FOS than those fed Basal,
the effect was more marked at the beginning of the experiment (2 and 8
wk) and not significant at the end. This may have been related to the
hypertrophy of the cecum. Numerous authors have already reported that
feeding fermentable polysaccharides increases cecal tissue weight and
area as well as the length of the colon (Brunsgaard et al. 1995
, Campbell et al. 1997
, Fontaine et al. 1996
). Accordingly, we observed a higher cecal wall weight
in rats fed FOS, which suggests that the cecum was larger in these rats
than in controls. This could explain the delay in transit time recorded
in rats fed FOS. Furthermore, the hypertrophy of the cecum decreased
with time, possibly accounting for the disappearance of the
difference in transit time between the two groups at 27 wk.
Cecal SCFA concentration was higher in rats fed FOS than in those fed
Basal. Moreover, the effect was enhanced by continuous ingestion of
FOS. While SCFA concentration was not significantly affected over time
in rats fed Basal, it was higher after 27 wk than after 2 wk in rats
fed FOS (P < 0.05). The hypothesis of a
time-dependent increase in FOS fermentation is unlikely. FOS are
rapidly and extensively fermented by the colonic bacteria, as
demonstrated in vitro (Gibson and Wang 1994
). No
residual FOS were recovered in stools of healthy humans (Molis et al. 1996
), and the apparent digestibility of FOS was 100%
in rats fed about 1 g/d for 4–9 d (Nilsson et al. 1988
). Another possible explanation is that more organic matter
reached the cecum after 8 and 27 wk. Indeed, the weight of cecal wet
and dry contents increased over time in rats fed both FOS and Basal.
Nevertheless, the time-dependent increase in SCFA concentration was
observed only in rats fed FOS, which suggests that another mechanism
was involved in this effect.
Among SCFA, butyrate was particularly elevated in rats fed FOS, which
is consistent with previous observations in vitro (Gibson and Wang 1994
) and in vivo in rat cecum (Campbell et al. 1997
). The reason for this butyrogenic effect is currently
unknown. The chemical structure of FOS may be partly involved, although
other sugars composed of fructose and glucose do not induce a similar
increase in butyrate (Campbell et al. 1997
). Other
factors, such as the pH of cecal contents (Gibson and Wang 1994
), transit time (El Oufir et al. 1996
) and
the intestinal mucins released (Fontaine et al. 1996
),
are probably involved. The growth and activity of
butyrate-producing bacteria are likely also promoted by FOS. These
bacteria may utilize FOS either directly or metabolize lactate produced
during FOS fermentation. In vitro fermentation of FOS yields lactate
(Gibson and Wang 1994
), and elevated concentrations or
pools of lactate were reported in vivo in the cecum of rats fed inulin
or FOS for 2–3 wk (Rémésy et al. 1993
,
Campbell et al. 1997
). Consistent with these
observations, we found a particularly high lactate concentration in the
cecum after 2 wk of FOS ingestion. However, this concentration
decreased over time, and after 8 and 27 wk of adaptation was only
slightly higher than that measured in rats fed Basal. This decrease of
lactate could be related to the increase in total SCFA and butyrate
concentrations observed during the same period in rats fed FOS. Several
intestinal bacteria, such as Propionibacterium sp.,
Veillonella sp., Clostridium sp. and
sulfate-reducers, can metabolize lactate into SCFA (Durand et al. 1996
, Macfarlane et al. 1994
).
Furthermore, some of these bacteria can tolerate the acidic pH induced
by FOS fermentation (Therion et al. 1982
) and produce
butyrate under certain conditions (Salyers, 1995
).
Possibly cecal microflora adapted to the continuous intake of FOS,
promoting the growth and/or metabolic activity of lactate-utilizing
bacteria. Such a mechanism would account for the decrease in lactate
parallel to the rise in SCFA and butyrate observed in the cecum of rats
fed FOS for 8 and 27 wk.
Moreover, this hypothesis could also explain the disappearance of the
FOS effect on lactic acid bacteria over time. As already reported
(Campbell et al. 1997
), we found that the intake of FOS
specifically increased lactic acid-producing bacteria counts in rat
cecum after 2 wk without modifying total anaerobe concentration.
However, this effect disappeared over time, so that after 27 wk of
adaptation, lactic acid producers counts in the cecum were not
different in rats fed Basal and those fed FOS. Lactate production by
these bacteria leads to a decrease in luminal pH. As an acidic
environment promotes the proliferation of lactic acid producers
(Veilleux and Rowland, 1981
), it may have contributed to
maintaining the increase in lactic acid-producing bacteria,
including Lactobacillus sp., observed during the first weeks
of FOS ingestion in our study as well as in others (Bouhnik et al. 1996
, Campbell et al. 1997
, Gibson et al. 1995
). However, as suggested above, the microflora probably
adapted to the prolonged intake of FOS, and lactate-utilizers may
have been able to metabolize lactate into SCFA, possibly through
progressive adaptation to acidic conditions. Consequently, lactate
concentration would decrease and pH increase, allowing
FOS-utilizing bacteria other than lactic acid-producing
bacteria, to compete for the available substrate. Actually, numerous
intestinal bacteria can degrade FOS, including members of
Bacteroides sp., Clostridium sp. and
Enterobacteriaceae (Hartemink et al. 1997
,
Hartemink and Rombouts 1997
). This competition could
result in the suppression of the specific increase in lactic acid
producers.
We conclude that the effects of FOS on cecal bacterial composition and activity change over time in rats and contend that the long-term "functional" effects of fermentable polysaccharides should be studied both in animals continuing to consume a polysaccharide-rich diet and after stopping. Furthermore, the persistence of the butyrogenic property of FOS compared to the disappearance of their prebiotic and pH-reducing effects over time should help to understand the mechanisms of action of FOS on the colon cancer-risk-reduction, which might be a future health claim for these substrates.
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FOOTNOTES |
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3 Abbreviations used: cfu, colony-forming unit; FOS, fructo-oligosaccharides; PEG, polyethylene glycol; SCFA, short-chain fatty acids.
Manuscript received May 24, 1999. Initial review completed July 5, 1999. Revision accepted August 31, 1999.
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  A. A. Santos Jr., P. R. Ferket, F. B. O. Santos, N. Nakamura, and C. Collier Change in the Ileal Bacterial Population of Turkeys Fed Different Diets and After Infection with Salmonella as Determined with Denaturing Gradient Gel Electrophoresis of Amplified 16S Ribosomal DNA Poult. Sci., July 1, 2008; 87(7): 1415 - 1427. [Abstract] [Full Text] [PDF]
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 F. Respondek, A. G. Goachet, and V. Julliand Effects of dietary short-chain fructooligosaccharides on the intestinal microflora of horses subjected to a sudden change in diet J Anim Sci, February 1, 2008; 86(2): 316 - 323. [Abstract] [Full Text] [PDF]
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 H. Xue, M. B. Sawyer, C. J. Field, L. A. Dieleman, and V. E. Baracos Nutritional Modulation of Antitumor Efficacy and Diarrhea Toxicity Related to Irinotecan Chemotherapy in Rats Bearing the Ward Colon Tumor Clin. Cancer Res., December 1, 2007; 13(23): 7146 - 7154. [Abstract] [Full Text] [PDF]
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 K. E. Scholz-Ahrens and J. Schrezenmeir Inulin and Oligofructose and Mineral Metabolism: The Evidence from Animal Trials J. Nutr., November 1, 2007; 137(11): 2513S - 2523S. [Abstract] [Full Text] [PDF]
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 D. M. A. Saulnier, D. Molenaar, W. M. de Vos, G. R. Gibson, and S. Kolida Identification of Prebiotic Fructooligosaccharide Metabolism in Lactobacillus plantarum WCFS1 through Microarrays Appl. Envir. Microbiol., March 15, 2007; 73(6): 1753 - 1765. [Abstract] [Full Text] [PDF]
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G. Falony, A. Vlachou, K. Verbrugghe, and L. D. Vuyst Cross-Feeding between Bifidobacterium longum BB536 and Acetate-Converting, Butyrate-Producing Colon Bacteria during Growth on Oligofructose Appl. Envir. Microbiol., December 1, 2006; 72(12): 7835 - 7841. [Abstract] [Full Text] [PDF]
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 A-P Bai and Q Ouyang Probiotics and inflammatory bowel diseases. Postgrad. Med. J., June 1, 2006; 82(968): 376 - 382. [Abstract] [Full Text] [PDF]
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A. Belenguer, S. H. Duncan, A. G. Calder, G. Holtrop, P. Louis, G. E. Lobley, and H. J. Flint Two Routes of Metabolic Cross-Feeding between Bifidobacterium adolescentis and Butyrate-Producing Anaerobes from the Human Gut. Appl. Envir. Microbiol., May 1, 2006; 72(5): 3593 - 3599. [Abstract] [Full Text] [PDF]
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A. W. Walker, S. H. Duncan, E. C. McWilliam Leitch, M. W. Child, and H. J. Flint pH and Peptide Supply Can Radically Alter Bacterial Populations and Short-Chain Fatty Acid Ratios within Microbial Communities from the Human Colon Appl. Envir. Microbiol., July 1, 2005; 71(7): 3692 - 3700. [Abstract] [Full Text] [PDF]
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 P. D Cani, C. A Daubioul, B. Reusens, C. Remacle, G. Catillon, and N. M Delzenne Involvement of endogenous glucagon-like peptide-1(7-36) amide on glycaemia-lowering effect of oligofructose in streptozotocin-treated rats J. Endocrinol., June 1, 2005; 185(3): 457 - 465. [Abstract] [Full Text] [PDF]
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S. J. M. Ten Bruggencate, I. M. J. Bovee-Oudenhoven, M. L. G. Lettink-Wissink, and R. Van der Meer Dietary Fructooligosaccharides Increase Intestinal Permeability in Rats J. Nutr., April 1, 2005; 135(4): 837 - 842. [Abstract] [Full Text] [PDF]
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S. J. M. Ten Bruggencate, I. M. J. Bovee-Oudenhoven, M. L. G. Lettink-Wissink, and R. Van der Meer Dietary Fructo-Oligosaccharides Dose-Dependently Increase Translocation of Salmonella in Rats J. Nutr., July 1, 2003; 133(7): 2313 - 2318. [Abstract] [Full Text] [PDF]
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M. Tieking, M. Korakli, M. A. Ehrmann, M. G. Ganzle, and R. F. Vogel In Situ Production of Exopolysaccharides during Sourdough Fermentation by Cereal and Intestinal Isolates of Lactic Acid Bacteria Appl. Envir. Microbiol., February 1, 2003; 69(2): 945 - 952. [Abstract] [Full Text] [PDF]
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C. Cherbut, C. Michel, and G. Lecannu The Prebiotic Characteristics of Fructooligosaccharides Are Necessary for Reduction of TNBS-Induced Colitis in Rats J. Nutr., January 1, 2003; 133(1): 21 - 27. [Abstract] [Full Text] [PDF]
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K. S. Swanson, C. M. Grieshop, E. A. Flickinger, L. L. Bauer, J. Chow, B. W. Wolf, K. A. Garleb, and G. C. Fahey Jr Fructooligosaccharides and Lactobacillus acidophilus Modify Gut Microbial Populations, Total Tract Nutrient Digestibilities and Fecal Protein Catabolite Concentrations in Healthy Adult Dogs J. Nutr., December 1, 2002; 132(12): 3721 - 3731. [Abstract] [Full Text] [PDF]
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T. Tsukahara, H. Koyama, M. Okada, and K. Ushida Stimulation of Butyrate Production by Gluconic Acid in Batch Culture of Pig Cecal Digesta and Identification of Butyrate-Producing Bacteria J. Nutr., August 1, 2002; 132(8): 2229 - 2234. [Abstract] [Full Text] [PDF]
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C. Daubioul, N. Rousseau, R. Demeure, B. Gallez, H. Taper, B. Declerck, and N. Delzenne Dietary Fructans, but Not Cellulose, Decrease Triglyceride Accumulation in the Liver of Obese Zucker fa/fa Rats J. Nutr., May 1, 2002; 132(5): 967 - 973. [Abstract] [Full Text] [PDF]
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K. S. Swanson, C. M. Grieshop, E. A. Flickinger, L. L. Bauer, H.-P. Healy, K. A. Dawson, N. R. Merchen, and G. C. Fahey Jr Supplemental Fructooligosaccharides and Mannanoligosaccharides Influence Immune Function, Ileal and Total Tract Nutrient Digestibilities, Microbial Populations and Concentrations of Protein Catabolites in the Large Bowel of Dogs J. Nutr., May 1, 2002; 132(5): 980 - 989. [Abstract] [Full Text] [PDF]
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K. K. Buddington, J. B. Donahoo, and R. K. Buddington Dietary Oligofructose and Inulin Protect Mice from Enteric and Systemic Pathogens and Tumor Inducers J. Nutr., March 1, 2002; 132(3): 472 - 477. [Abstract] [Full Text] [PDF]
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 A.J. McBAIN and G.T. MACFARLANE Modulation of genotoxic enzyme activities by non-digestible oligosaccharide metabolism in in-vitro human gut bacterial ecosystems J. Med. Microbiol., September 1, 2001; 50(9): 833 - 842. [Abstract] [Full Text] [PDF]
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P. J. Naughton, L. L. Mikkelsen, and B. B. Jensen Effects of Nondigestible Oligosaccharides on Salmonella enterica Serovar Typhimurium and Nonpathogenic Escherichia coli in the Pig Small Intestine In Vitro Appl. Envir. Microbiol., August 1, 2001; 67(8): 3391 - 3395. [Abstract] [Full Text] [PDF]
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V. J. McCracken, J. M. Simpson, R. I. Mackie, and H. R. Gaskins Molecular Ecological Analysis of Dietary and Antibiotic-Induced Alterations of the Mouse Intestinal Microbiota J. Nutr., June 1, 2001; 131(6): 1862 - 1870. [Abstract] [Full Text]
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H. N. Lærke, B. B. Jensen, and S. Højsgaard In Vitro Fermentation Pattern of D-Tagatose Is Affected by Adaptation of the Microbiota from the Gastrointestinal Tract of Pigs J. Nutr., July 1, 2000; 130(7): 1772 - 1779. [Abstract] [Full Text]
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