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Danish Institute of Agricultural Sciences, Department of Animal Nutrition and Physiology, Research Center Foulum, DK-8830 Tjele, Denmark
4To whom correspondence and reprint requests should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • sweetener • sugar • digestibility • fermentation • pigs • D-tagatose
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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), patented as a low energy
carbohydrate sweetener and bulking agent (Zehner 1988
),
and as an antihyperglycemic agent (Zehner et al. 1994
).
The net energy value has been estimated at slightly <0 on the basis of
a study in rats (Livesey and Brown 1996
).
D-Tagatose may thus have a use as a sugar substitute of
particular benefit because of its lower energy value. Studies in vitro
have also indicated that D-tagatose can inhibit the
activity of carbohydrases in the small intestine (Hertel 1997
, Seri et al. 1995
) with a possible further
reduction of the energy value of the diet and a depression of the
glycemic response (Seri et al. 1995
).
A metabolism study in rats has shown that carbon of orally administered
14C-labeled D-tagatose is excreted in
the urine (5–6%), breath (49–68%) and feces (11–29%) with
variation in the urinary and fecal excretion depending on whether the
rats are adapted to dietary D-tagatose (Levin et al. 1995
). However, there is little information to date on the
route by which carbon from D-tagatose appears in the
peripheral tissues and in the urine; however, it appears that events
taking place in the gastrointestinal tract are of great importance. A
study with only one ileum-fistulated pig supplemented with
antibiotics to eliminate any microflora residing in the small intestine
indicates that 78 ± 8% of D-tagatose could be
absorbed, in contrast to lactitol, which had an ileal digestibility of
5 ± 7% (Levin et al. 1995
). However, given the
limited number of observations, these values should be interpreted with
great caution.
We have performed an experiment with normal pigs designed to study the apparent ileal and fecal digestibility of D-tagatose, its influence on the apparent ileal and fecal digestibilities of starch, sucrose, protein, fat and energy, and changes in microbial activity [ATP concentrations and adenylate energy charge, (AEC)6 ], pH and concentration of short-chain fatty acids (SCFA) in the gut contents.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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At 7-d intervals, two series of experiments were performed with eight castrated male Danish Landrace x Yorkshire pigs. The pigs were obtained from the herd at the Danish Institute of Agricultural Sciences, Foulum, Denmark. The pigs for the first series of experiments came from two sows (2 x 4 littermates) and for the second series from four sows (4 x 2 littermates). The pigs in series 1 were 67–69 d old and weighed 26.1 ± 1.1 kg. The pigs in series 2 were 62–75 d old and weighed 24.6 ± 1.9 kg. The pigs were housed individually in 4 m2 pens with concrete floors.
Diets and feeding.
Two experimental diets were used for the experiments (control and
tagatose diet in the following). The composition is given in
Table 1. Chromic oxide was used as a digestibility marker. Because
D-tagatose is soluble in water, polyethylene glycol 4000
(PEG) was also tested as a digestibility marker but was not found
useful. For each series, four pigs were given the same experimental
diet, with littermates fed different experimental diets. The average
weight of the pigs was balanced between the groups. The pigs had an
adaptation period of 2 d during which they were fed a traditional
Danish pig's diet (d-4 and d-3), followed by 2 d of consuming a
1:1 mixture of the standard feed and the experimental diet (d-2 and
d-1). Subsequently, the pigs were fed the experimental diet for 18 d (d 0–17). The pigs were fed twice a day at 0700 and 1500 h. The
feed intake was restricted to 40 g/(kg body weight · d).
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For collection of feces, a plastic bag was mounted on the rump of the pigs for three consecutive days just before slaughter (d 14–16). The bags were changed twice a day at feeding, and the collected feces were frozen to -18°C. The feces samples from each day were pooled for each pig and freeze-dried for further analysis.
Collections of samples after slaughter.
On d 17, the pigs were killed 3 h after the morning meal with a
lethal injection of pentobarbital sodium (200 g/L). Immediately after
slaughter, the gastrointestinal tract was removed and divided into
eight segments by ligatures, essentially as described by Clemens et al. (1975)
. The segments were as follows: the stomach, three
equal parts of the small intestine (SI1, SI2,
SI3), the cecum and three equal parts of the large
intestine including the rectum (LI1, LI2,
LI3). The luminal contents of each segment were carefully
collected by gently squeezing the material out of the gut segment. The
collected material was weighed and a sample taken for analysis.
Analyses.
The concentrations of ATP, SCFA and dry matter and pH were determined in wet intestinal contents (digesta). All other chemical analyses were conducted on freeze-dried samples.
The concentration of ATP and the AEC ratio were determined by the
luciferin-luciferase method as described by Jensen and Jørgensen (1994)
. The concentration and composition of SCFA
and the concentration of lactate were determined as described by
Jensen et al. (1995)
. Luminal pH was determined with a
combined pH-electrode (GK 2401C, Radiometer, Copenhagen, Denmark).
Gross energy was analyzed by a LECO AC 300 automated calorimeter system
(LECO, St. Joseph, MI) and crude protein by the Kjeldahl-method as
N x 6.25 (AOAC 1990
). HCl-fat was analyzed by
extraction in diethyl ether after hydrolysis with 3 mol/L HCl
(Stoldt 1952
). Chromic oxide was determined by the
method of Schurch et al. (1950)
.
Without prior extraction of low-molecular-weight sugars (which are not
hydrolyzed to liberate glucose in the analytical procedure), starch was
determined by gelatinization and simultaneous hydrolysis with
thermostable 
-amylase (EC 3.2.1.1; Termamyl®, Novo Nordisk A/S,
Copenhagen, Denmark) for 1 h followed by a 2-h incubation with
ß-glucanase-free amyloglucosidase (EC 3.2.1.3; cat. no. 1202 367,
Boehringer Mannheim, Mannheim, Germany); the resulting glucose monomers
were quantified with a glucose oxidase reagent (EC 1.1.3.4; cat. no.
K-GLUC, Megazyme International Ireland, Wicklow, Ireland) as
described by Bach Knudsen and Hessov (1995)
. Free
glucose from enzymatic degradation of sucrose was considered negligible
because this degradation takes place on the brush border and not in the
intestinal lumen.
Sucrose and D-tagatose in freeze-dried samples were
determined essentially as described by Johansen et al. (1996)
. Briefly, the sample (125–250 mg) was extracted with 5
mL 50% (v/v) methanol containing 1 g/L sorbitol (internal standard)
under constant mixing in a heating block (50°C) and subsequently
centrifuged at 2000 x g for 10 min. The
supernatant was filtered by using a Waters Sep-Pak C18
(Waters Corporation, Milford, MA) filter with a Vac Elut SPS 24
(Analytichem International, Harbor City, CA). Before filtration of the
sample, the Sep-Pak filter was pretreated with 1 volume 100%
methanol, 3 volumes water and 1 volume 50% (v/v) methanol. A volume of
1.5 mL of the filtrate was evaporated overnight in a vacuum centrifuge
at 50°C and redissolved in 1.5 mL HPLC grade water. Before injection
on the HPLC column, the sample was filtered using a 0.2
µm Sartorius filter (Sartorius AG, Goettingen,
Germany). The sugars were separated on a calcium-based resin column
(Aminex HPX-87C, BioRad Laboratories, Herkules, CA), kept at 85°C, by
injection of 25 µL filtrate using a Waters HPLC LC
Module1 (Waters Corporation) at a flow rate of 0.6 mL/min and a Waters
410 RI detector (Waters Corporation), internal temperature 45°C,
sensitivity 64. The samples were calibrated against a standard mixture
(4 g/L). Preliminary experiments showed linearity in the range
0.05–8.0 g/L (corresponding to a detection limit of 0.3 g
D-tagatose/kg dry matter). D-Tagatose and
sorbitol were quantified on the basis of peak area. Sucrose was
quantified on the basis of peak height because of insufficient baseline
separation from other components.
Calculations.
The digestibility in the distal third of the small intestine
(SI3) and in feces was calculated as follows:
 |
where MD and MI/F are the concentrations of marker in the diet (D), and intestine (I) or feces (F). CD and CI/F are the corresponding concentrations of the feed component, for which the digestibility is to be calculated.
Statistical analysis.
Two kinds of analyses were conducted. One concerned comparison of
treatment effects (i.e., diets) in a given intestinal segment. This was
accomplished using a simple ANOVA based on the following general linear
model (GLM):
 |
where Ydi is the dependent
variable, µ is the overall mean,
d is the effect of diet, d= 1,2,
and 
di ~ N(0,
2)
represents the unexplained random error.
The effect of treatment over a range of segments was analyzed using
multivariate ANOVA with diet as the between-animal effect and
segment as the within-animal effect by using the following general
linear model:
 |
where d denotes the effect of diet,
d=1,2, ßs is the effect of segment,
s= 1,...4, ßds is the
interaction between diet and segment, and i refers to an
individual pig. The variance component 
i ~
N(0,
2) accounts for the fact that the repeated
measurements were made on the same individual, thereby rendering these
observations correlated, whereas the term dsi
~ N(0,2) represents the unexplained random
error (SAS Institute 1989
).
Because the digestive processes in the upper and lower gut are quite different, the stomach and small intestine were considered as one compartment (upper gut), the cecum and colon as another (lower gut), and the compartments were analyzed separately.
The experimental diets were balanced between the two series of experiments; thus series were not included in the statistical analyses. The analyses were performed with SAS for Windows version 6.12 (SAS Institute, Cary, NC).
In tables and figures, significance of difference (P < 0.05) refers to univariate analysis. SEM values were calculated for each group separately. When effects of the dietary treatment in a specific segment are referred to, probability levels stated in the text refer to the univariate analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. Except for some of the SCFA, which were present in very low
amounts, all variables were significantly different (P
< 0.05) among segments in the upper gut. In the lower gut, there
were significant differences among the segments, except for the pH and
concentrations of formate, lactate, acetate, propionate and total SCFA.
Statistically significant effects of the diet (P < 0.05),
demonstrated an overall difference between the two diet groups,
although the effect of diet was not significant in all segments when
analyzed separately in the univariate analyses. Significant
interactions (P < 0.05) between the diet and segment
(D x S) indicate that the differences between one segment and
another along the gastrointestinal tract followed a different pattern
for pigs fed the two experimental diets.
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Significantly larger amounts of digesta were collected from the stomach
(P = 0.04), SI1 (P
= 0.02), SI2 and SI3 (P
= 0.0001) of tagatose-fed pigs compared with pigs fed the
control diet (Table 3). In the large intestine, there was also a significantly larger
amount of digesta in LI1 of the tagatose group than the
control group (P = 0.03), but there was no overall
significant effect of diet in the multivariate analysis of the amount
of digesta in the lower gut (Table 2)
.
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), but no overall effect of diet
was detected in the multivariate analysis of the upper gut. There was
no significant effect of experimental diet on the amount of dry matter
collected from the lower gut. The total amount of digesta present in the upper gut was significantly higher in the tagatose group than in the control group (2540 g vs. 1675 g, P = 0.0001), whereas no significant difference was seen in the amount of dry matter collected from the pigs in the control group (380 g) and the tagatose group (416 g, P = 0.10).
The dry matter concentration (g/kg digesta) in the upper gut was lower
for the tagatose group in the stomach, SI2 and
SI3 (Table 3)
, which led to an overall significant effect
of diet and an interaction between segment and diet in the multivariate
analysis (Table 2)
. In addition to a greater reduction of dry matter
concentration from the stomach to SI1, the dry matter
concentration decreased further from SI1 to SI2
in the pigs fed the tagatose diet. In contrast, in the control group,
the dry matter concentration in the small intestine increased through
passage of the small intestine. No overall effect of diet was seen in
the dry matter concentration in the lower gut, but there was an
interaction between diet and segment (Table 2)
.
Apparent digestibility of D-tagatose and nutrients.
The apparent digestibility of dry matter in the distal third of the
small intestine was lower for the tagatose diet than the control diet
(P = 0.01). This was reflected by a lower
digestibility of gross energy (P = 0.02)
(Table 4). There were no differences between groups in the small intestinal
digestibilities of protein, fat or starch, but there was a lower
digestibility of sucrose (P = 0.009) in pigs fed
the tagatose diet. The digestibility of D-tagatose in
SI3 was 25.8 ± 5.6%, whereas no
D-tagatose was recovered from feces (Table 4)
.
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pH of the gut content at slaughter.
There was no difference between diet groups in the pH of the stomach or
small intestinal contents (Fig. 1
). The pH increased from 4.6 in the stomach to 6.1 in
SI1 and 7.1 in SI3 with significant differences
among segments (Table 2)
. Along the large intestine, there were no
significant changes in pH; overall, however, the tagatose diet resulted
in a lower pH than did the control diet in the lower gut (Table 2)
.
This difference was significant in the cecum (P = 0.03) and in LI1 (P = 0.004).
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The microbial activity expressed by the concentration of ATP (Fig. 1)
was generally very low in the stomach and the two first segments of the
small intestine (<0.4 mg/kg digesta), but increased subsequently in
SI3 to 1.3 mg/kg digesta in pigs fed the tagatose diet and
4.2 mg/kg digesta in those fed the control diet (P
= 0.0006). The microbial activity increased in the cecum to 17.1
mg/kg digesta without any difference between the two diet groups.
However, in the following segment (LI1), there was a
reduction in the microbial activity to 6.8 mg/kg digesta for the pigs
fed the control diet, whereas the activity remained high (16.8 mg/kg
digesta) in pigs fed the tagatose diet (P = 0.0007). There was no difference between groups in segments
LI2 and LI3 but overall, the activity was
higher in the lower gut of the tagatose-fed pigs compared with
those fed the control diet (Table 2)
.
The higher specific activity (mg/kg digesta) in the distal small
intestine of the pigs fed the control diet did not reflect a higher
total activity in this part of the small intestine. When accounting for
the different amounts of digesta collected from the segment, the total
amounts of ATP in the stomach and small intestine were not
significantly different for pigs fed the two diets (Table 5). The total microbial activity, on the other hand, was
considerably higher in the cecum (P = 0.03) and
colon (P = 0.003) of the tagatose-fed pigs
compared with pigs fed the control diet.
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. The difference
between the diet groups in SI3 was significant
(P = 0.0003); in the multivariate analysis, it gave
overall significant effects of diet (P = 0.003)
along with significant differences between segments and an interaction
between diet and segment (P = 0.02, Table 2
). The
tagatose diet resulted in higher AEC in the cecum (P
= 0.03) and LI1 (P = 0.003)
compared with the control diet. The AEC then declined through the large
intestine for both dietary groups, and in LI2, there was no
difference between the two groups (Fig. 1)
. Thus, in the multivariate
analysis of AEC in the lower gut, there were significant differences
between segments, diets, and an interaction between segment and diet
(Table 2)
. Concentration of lactate and short-chain fatty acids in gut contents at slaughter.
There was a notable increase in the concentration of lactate from the
stomach (0.6 mmol/kg digesta) through the small intestine to 11.2
mmol/kg digesta in SI3 of the pigs fed the control diet
(Fig. 2
). In the pigs fed the tagatose diet, lactate increased from 0.9 in
the stomach to only 3.1 mmol/kg digesta in SI1, with a
further small increment through the remainder of the small intestine to
3.8 mmol/kg digesta in SI3. This gave a significantly lower
lactate concentration in SI2 (P = 0.02)
and SI3 (P = 0.005) of the
tagatose-fed pigs compared with the pigs fed the control diet, and
there was a significant interaction between segment and diet in the
multivariate analysis (P = 0.0004, Table 2
).
However, the differences in concentration did not reflect differences
in lactate production because the amount of digesta in the
tagatose-fed group was higher than that in the control group,
especially in SI3. Therefore, there was no significant
difference between the two diet groups in the total amount of lactate
in the distal third of the small intestine (P = 0.7).
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. There was
no significant effect of diet on the level of formate in the upper gut,
but a significant difference between the segments (Table 2)
. No lactate
was detected in the cecum and colon, and the level of formate was
similar to that of the stomach and almost constant throughout the large
intestine. The apparent higher mean concentration of formate in the
large intestine in the tagatose-fed group (1.7 mmol/kg digesta)
than in the control group (0.6 mmol/kg digesta) was not significant
(P = 0.15).
There was no acetate in the stomach, SI1 or
SI2, but the concentrations in SI3 were 1.9
mmol/kg digesta in pigs fed the tagatose diet and 7.0 mmol/kg digesta
in those fed the control diet (P = 0.0001,
Fig. 3
). This gave overall significant effects of diet, segment and an
interaction between diet and segment in the multivariate analysis
(Table 2)
. Propionate and butyrate were present in very low
concentrations, and valerate was totally absent from the upper gut of
the pigs in both dietary groups (Fig. 3)
.
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and 4). The concentration of acetate increased in the cecum to 41.1
mmol/kg digesta in the control group and 32.5 mmol/kg digesta in the
tagatose-fed group (P = 0.03, Fig. 3
). For the
control group, the concentration decreased subsequently through the
large intestine to 33.5 mmol/kg digesta in the LI3. For the
tagatose-fed group, there was a slight increase to a maximal
concentration in LI2 (39.0 mmol/kg digesta). However, the
concentration in the cecum was the only case in which there was a
significant difference between the two diet groups (P
= 0.02). In the multivariate analysis, this led to a significant
interaction between segment and diet, but no significant main effects
of segment or diet (Table 2)
.
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. This gave an overall
significantly higher concentration in pigs fed the tagatose diet
(P = 0.009), whereas the differences between
segments were not significant (P = 0.055, Table 2
).
The concentration of butyrate was 9.7–11.9 mmol/kg digesta in
the cecum, and D-tagatose induced an increase of the
concentration to 13.2 mmol/kg digesta in LI1, followed by a
reduction in the following segments. In contrast, in pigs fed the
control diet, there was a slight reduction in the concentration of
butyrate along the large intestine to 7.7 mmol/kg digesta in
LI3. There was only a significant difference between the
diet groups in LI1 (P = 0.03), but no
overall effect of diet in the lower gut (P = 0.06,
Table 2
).
There was a >1.3 times higher concentration of valerate in the cecum
and colon of tagatose-fed pigs compared with pigs fed the control
diet (P = 0.0002, Fig. 3
). In addition, there was a
small but significant difference between the segments of the lower gut
(P = 0.03).
The branched-chain SCFA, which are produced from fermentation of
protein, also increased in the lower gut (Fig. 4)
. For the
tagatose-fed pigs, the concentration of isobutyrate increased from
0.63 mmol/kg digesta in the cecum to 1.63 mmol/kg digesta in
LI1 and further to 2.56 mmol/kg digesta in LI3.
For the control pigs, the concentration changed from 1.04 mmol/kg
digesta in the cecum to 1.99 mmol/kg digesta in LI1 and
2.19 mmol/kg digesta in LI3. Similar results were obtained
for isovalerate whose concentration increased from 0.53 mmol/kg digesta
in the cecum of tagatose-fed pigs to 2.33 mmol/kg digesta in
LI3. For the pigs fed the control diet, the corresponding
values were 0.86 and 2.06 mmol/kg digesta. There was no significant
difference between the diet groups, but there were significant
differences among segments (Table 2)
.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). For this
reason, we present the digestibility results only in the distal third
of the small intestine. However, if a difference in flow between the
dietary component and the marker continues throughout the small
intestine, the use of chromic oxide as a digestibility marker may lead
to an overestimation of the digestibility. On the basis of the amount
of ATP and SCFA, and the pH at slaughter, the microbial activity in the
gastrointestinal tract appears to be minimal in the upper
gastrointestinal tract and does not contribute to the small intestinal
digestibility to any appreciable extent. Although differences were seen
between diet groups in the specific microbial activity (expressed by
the ATP concentration) and the concentrations of lactate, formate and
acetate in the upper gut, there were no indications of a difference in
the total microbial activity when the results were corrected for the
"dilution" of digesta in these segments. Only the AEC ratio,
expressing the relative microbial activity, indicated a lower activity
in the small intestine of the pigs fed the tagatose diet. Therefore, it
is plausible that most of the missing D-tagatose, relative
to chromic oxide, was absorbed and not fermented by bacteria residing
in the ileum of the pigs.
The small intestinal digestibility of sucrose was reduced by ~10% in
the group fed the tagatose diet compared with the control group. On a
quantitative basis, this reflected a malabsorption of 3.0 g
sucrose/kg ingested for the control diet group compared with 4.8 g
malabsorbed sucrose from the diet supplemented with
D-tagatose. The presence of D-tagatose may have
reduced the absorption of sucrose by inhibiting the sucrase activity in
the small intestine as suggested by Seri et al. (1995)
.
Such an inhibitory effect of D-tagatose on carbohydrases in
the small intestine has not been demonstrated previously in vivo;
however, in vitro results with pure enzymes indicate that
D-tagatose may inhibit pig intestinal sucrase/isomaltase
activity, but not the glucoamylase/maltase activity (Hertel 1997
). In contrast, studies with homogenates of mucous
membranes of the small intestine of rabbits have suggested that
D-tagatose inhibits both enzyme complexes in a
dose-dependent manner (Seri et al. 1995
). In this
study, there were no measurable effects of D-tagatose on
the in vivo digestibility of starch, protein or fat in the distal small
intestine. The lack of effect on starch digestibility is consistent
with a lack of effect on maltase in vitro as demonstrated by
Hertel (1997)
, and the lower digestibility of dry matter
and energy of the tagatose diet compared with the control diet was due
primarily to the low digestibility of D-tagatose itself.
The difference between diets in the digestibilities of dry matter,
energy and sucrose in the small intestine was totally abolished in
feces as a result of microbial fermentation of the substrates in the
large intestine. Starch, sucrose and D-tagatose were
totally digested by the end of the large intestine. Introducing larger
amounts of fermentable material into the large intestine of the
tagatose-fed pigs led to a higher microbial activity and an
increased excretion of fecal nitrogen. This is the reason for the lower
apparent fecal digestibility of nitrogen as previously demonstrated
with other easily fermentable carbohydrates (Tetens et al. 1996
).
As for most other sugar substitutes, laxation is an adverse effect that
may limit the use of D-tagatose in food products. In this
study, inclusion of 10% D-tagatose in the diet increased
markedly the amount of digesta in the small intestine, but the moisture
content was also higher. Therefore, there were no differences between
the groups in the amounts of dry matter collected from the segments of
the upper gastrointestinal tract. These results indicate that the
effect of D-tagatose on volume in the small intestine is
primarily an effect on the liquid phase, presumably through a higher
osmotic pressure. In the lower gut, there was no significant difference
between the two diet groups in the amounts of digesta and dry matter
collected. Too high an osmolarity in the gut lumen can lead to
diarrhea; in this study, we observed that two pigs had loose stools
temporarily 1–2 d after exposure to D-tagatose. This is in
agreement with previous results in rats in which low levels (5%) of
D-tagatose did not cause any adverse effects, whereas
higher levels (10–20%) led to temporary signs of diarrhea
(Levin et al. 1995
).
The present study demonstrated that D-tagatose has strong influences on the microbial activity (ATP concentration, concentration and composition of SCFA, and pH) in the lower gut. Generally, these effects were most extensive in the cecum and the proximal part of the colon, whereas the effects in the distal part of the colon were less evident. The main effects were reduction in luminal pH, increased ATP concentration and AEC-ratio, and higher concentrations of propionate and butyrate in the cecum and colon of the tagatose-fed pigs compared with pigs fed the control diet. For the distal colon and rectum, there were significant differences between diet groups only in the concentrations of propionate, valerate and caproate. These results indicate that the ingested D-tagatose is almost completely fermented in the cecum and proximal colon, whereas only small amounts reach the more distal parts of the colon.
A particularly interesting observation was the high concentration of valerate found in the large intestine of the pigs fed D-tagatose, suggesting that D-tagatose may specifically stimulate the production of this acid.
Presumably, the bacteria of the gastrointestinal tract have to adapt to
fermentation of D-tagatose. Indirectly, this was shown in a
rat study in which adapted rats had a 17.3% lower fecal output of
14C-labeled D-tagatose (11.4%) and an 18.5%
higher excretion of 14C via the breath compared
with unadapted rats (Levin et al. 1995
). Although the
14C-containing components were not identified in
the study, the results clearly suggest that D-tagatose is
metabolized more efficiently in adapted than unadapted rats, again
suggesting that gastrointestinal microflora have to adapt to this
monosaccharide. Whether similar adaptation is necessary for the
microflora in the gastrointestinal tract of other monogastrics (such as
pigs and humans) should be investigated.
The concentrations of SCFA found in the gut contents of the pigs in
these experiments suggest that, in particular, the microbial production
of C3–C5 is elevated in pigs fed D-tagatose. However, the
concentrations of SCFA in the gut do not reflect the actual production
because some SCFA have already been absorbed and metabolized in the gut
wall or transferred to the peripheral tissues. Because butyrate is the
preferred fuel for the gut tissues (Scheppach 1994
), the
production of butyrate may be even greater than what appears from the
composition of SCFA in the gastrointestinal contents. Butyrate has been
suggested as beneficial in the prevention of colon cancer (Van Munster and Nagengast 1993
). Propionate and valerate have
recently been shown to resemble butyrate in their ability to inhibit
cell proliferation and increase alkaline phosphatase activity in human
colonic adenocarcinoma cell lines (Siavoshian et al. 1997
), although the effects are weaker. Thus,
D-tagatose may serve as a substrate to produce high amounts
of propionate, butyrate and valerate, a feature that is of interest if
D-tagatose is under consideration as a functional food
ingredient.
Partial replacement of easily digestible carbohydrates with
D-tagatose could have several nutritional implications. The
zero net energy value calculated on the basis of a study with rats by
Livesey and Brown (1996)
has been suggested to stem from
a thermogenic effect, but a recent study with humans has not been able
to confirm this (Buemann et al. 1998
). If such a
thermogenic effect does not occur in humans, the zero net energy value
may be questioned. However, D-tagatose may be expected to
have a lower energy value than monosaccharides that are completely
absorbed in the small intestine because a large part (>74%) of the
D-tagatose is fermented in the large intestine. The energy
obtained from microbial fermentation is generally used less efficiently
than the energy obtained through direct digestion and absorption of
carbohydrates in the small intestine (Livesey 1992
).
Furthermore, in the fermentation process, there are losses through
production of heat and various gases (hydrogen, methane), and some SCFA
are lost in feces. Additionally, fecal excretion of fat and nitrogen in
microbial biomass may reduce the retained energy, although this was not
detected in this study.
In conclusion, D-tagatose is digested and absorbed to only a small extent in the small intestine of pigs and shows some hyperosmotic effect in this part of the gastrointestinal tract. In adapted pigs, D-tagatose is completely fermented in the large intestine and contributes to the overall energy balance with a high production of short-chain fatty acids. In particular, the increases in the concentrations of propionate, butyrate and valerate draw attention toward possible specific health benefits resulting from incorporation of these monosaccharides into food products.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Presented in part at the 8th European Congress
on Obesity, 18–21 June, 1997, Trinity College, Dublin, Ireland
[Johansen, H. N. & Jensen, B. B. (1997). Recovery of energy
as SCFA after microbial fermentation of D-tagatose. Int. J.
Obes. 21 (suppl. 2): S50].
3 Submission of this paper was approved by the
Danish Institute of Agricultural Sciences.
6 Abbreviations used: AEC, adenylate energy
charge; Ce, cecum; LI1, LI2, LI3,
three equal parts of large intestine (proximal, mid- and distal
including rectum); SCFA, short-chain fatty acids; SI1,
SI2, SI3, three equal parts of the small
intestine (proximal, mid- and distal); St, stomach.
Manuscript received July 13, 1998. Initial review completed August 29, 1998. Revision accepted January 25, 1999.
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