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Nutritional Science Center, Bioscience Laboratories, Meiji Seika Kaisha, Ltd., Saitama 350-0289, Japan and * Department of Bioscience and Chemistry, Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
1To whom correspondence should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • gastrectomy • cecectomy • anemia • rats • fructooligosaccharides
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Chonan et al. 1995
, Goda et al. 1993
), hydrolyzed dietary
fiber (Hara et al. 1997
) and resistant starch
(Schulz et al. 1993
), have been shown to have a
stimulatory effect on intestinal calcium (Ca) and magnesium (Mg)
absorption. Most of the authors speculated that these indigestible
carbohydrates exert their effect in the large intestine, as suggested
by the results of previous studies (Demigné et al. 1980
, Rémésy et al. 1993
,
Schulz et al. 1993
). The effects of short-chain
fructooligosaccharides
(Sc-FOS)2
have been well examined (Ohta et al. 1993
). Previously,
we confirmed that the stimulatory effect of Sc-FOS on Ca and Mg
absorption takes place in the large intestine in rats, as shown by four
different methods (Baba et al. 1996
, Ohta et al. 1994
, 1995a
and 1997
). Also, we showed that dietary Sc-FOS
stimulate iron absorption in rats (Ohta et al. 1995b
and 1998c
). In previous studies, we found that dietary Sc-FOS
improved recovery from anemia due to iron deficiency (Ohta et al. 1995b
) or gastrectomy (Ohta et al. 1998c
and 1999
) in rats. In that study, we also observed that
Sc-FOS feeding resulted in an increase in net iron absorption and
an increase in soluble iron in the cecal contents in rats (Ohta et al. 1995b
). Therefore, we speculate that Sc-FOS may
stimulate iron absorption in the large intestine. To the best of our
knowledge, there is little reported evidence concerning iron absorption
in the large intestine (Ebihara et al. 1994
and 1995
).
However, we expected that we could assess the role of the cecum, which
is the proximal site in the large intestine in which Sc-FOS are
thought to exert a stimulatory effect on iron absorption, by monitoring
recovery from postgastrectomy anemia in rats with or without cecectomy. |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Male Sprague-Dawley rats (n = 56, aged 4 wk;
Clea Japan, Tokyo, Japan) were housed in individual stainless steel
wire-mesh cages in a room maintained at 25°C and 55% relative
humidity. The rats were fed a pelleted diet (MF, Oriental Yeast, Tokyo,
Japan) for 1 wk before the operation as the adaptation period. The rats
were randomly assigned to four groups of 14 rats each. All rats were
anesthetized by Nembutal injection (sodium pentobarbital, 35 mg/kg body
weight; Abbot Laboratories, North Chicago, IL) before surgery. The rats
in the first group were subjected to a sham operation; the abdominal
cavity was opened for ~45 min, the same length of time as required
for the gastrectomy and cecectomy procedure. In the second group, the
cecum was removed surgically (Lambert 1965
), and in
third group, the stomach was removed surgically (Billroth II)
(Lambert 1965
, Oscarson et al. 1979
). In
the final group, both the cecum and the stomach were removed
surgically. All rats were given an intramuscular injection of vitamin
B-12 (Wako Pure Chemical, Tokyo, Japan) at 0.5 mg/kg every other week,
starting on the initial day of the feeding period. After the
operations, the rats were deprived of food for 24 h and then were
allowed free access to homogenized and pasteurized cow’s milk (Meiji
Milk Products, Tokyo, Japan) for 48 h.
Three days after the operations, the rats were fed the assigned
experimental diets for 4 wk. During the first 2 wk, the rats were fed
15 g diet/d; thereafter, they were fed 20 g/d for the remaining 2
wk. The rats had free access to deionized water throughout the
experimental period. In each surgical treatment group, rats were
divided randomly into two groups; one half of the rats were fed a
control diet (control) and the remaining half were fed a
Sc-FOS-containing diet (Sc-FOS). The control diet was prepared
according to the AIN-93G formulation (Reeves et al. 1993
). Sc-FOS, which is a mixture of 34% 1-kestose, 53%
nystose and 9% 1F-ß-fructofuranosylnystose (Meioligo-P,
Meiji Seika Kaisha, Tokyo, Japan) (Hidaka et al. 1988
and1991
), was added at 75g/kg diet by replacing sucrose in the
control diet. The iron source in both experimental diets was iron (III)
citrate (Wako Pure Chemical, Tokyo, Japan), and the iron concentration
was 806 µmol/kg diet (Reeves et al. 1993
). Other dietary components, apart from minerals, were
obtained from Oriental Yeast (Tokyo, Japan). All other reagents were of
analytical grade from Wako Pure Chemical. On the final day of the
study, all rats were anesthetized by exposure to diethyl ether. After
laparotomy, whole blood was collected by abdominal vein puncture and
the rats were killed. The cecum and colon were removed with their
contents; the contents were collected, weighed, frozen immediately with
liquid nitrogen and stored at -40°C until subsequent analyses. The
cecal wall was washed with saline and weighed. The contents weight was
evaluated as the difference in weight between the cecum with and
without the contents.
Ethical consideration.
This study was approved by the Animal Committee of Meiji Seika Bioscience Laboratories, and the animals were maintained in accordance with the guidelines for the care and use of laboratory animals of Meiji Seika Bioscience Laboratories.
Measurement of anemia-related biochemical variables.
Blood was collected by tail vein puncture every other week during the
experimental period. Blood samples were analyzed to determine the
hematocrit (Ht) and hemoglobin (Hb) concentration. Using the serum
samples obtained on the final day of the study, serum iron (SI) and
unsaturated iron-binding capacity (UIBC) were determined by means
of commercial assay kits (Fe c-test, UIBC-test, Wako Pure
Chemical). Hemoglobin-iron (Hb-Fe) and hemoglobin regeneration
efficiency (HRE) were calculated from the following formulas by the
method of Miller (1982)
.
 |
 |
 |
 |
 |
 |
Analysis of cecal and colorectal contents.
The cecal and colorectal contents were brought to a volume of 20 mL with deionized water and homogenized by means of a teflon homogenizer. Amounts of total iron in the homogenates were determined by atomic absorption spectrophotometry (Shimadzu AA-6400F, Shimadzu Seisakusho, Kyoto, Japan) after wet-ashing with an acid mixture (16 mol/L nitric acid/9 mol/L perchloric acid = 3:1). Soluble iron in the supernatant obtained upon centrifugation (30,000 x g for 20 min at 4°C) of the homogenate was determined by atomic absorption spectrophotometry after deproteinizing with 9 mol/L perchloric acid. The pH of these homogenates was measured with a glass electrode as the pH of the cecal and colorectal contents.
The solubility of iron in the cecal contents was estimated from the ratio of the iron level in the liquid phase to that in the solid phase by the following formula: liquid/solid = iron content in the liquid phase (µmol)/iron content in the solid phase (µmol). The solubility of iron in the colorectal contents was estimated in a similar manner.
Statistics.
Data were analyzed by three- or four-way ANOVA for the three or
four main factors (diet, cecectomy, gastrectomy and time) and their
interaction, and significant differences among groups were determined
by Tukey’s test (Dawson-Saunder and Trapp 1994
) (SPSS
Version 6.0, SPSS, Chicago, IL). Differences were considered
significant at P < 0.05. If the variances were
unequal, log transformations of the data were performed before ANOVA.
Values in the text are untransformed means ± SD
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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On the day experimental diet feeding was started, the body weights of the rats with cecectomy and/or gastrectomy were significantly lower than that of the sham-operated rats (P < 0.01). On the final day of the experiment, the body weight of the gastrectomized rats was significantly lower than that of the rats that had the sham operation or those with cecectomy alone (P < 0.01). The total body weight gain and food intake of the gastrectomized rats were lower than those of rats that had the sham operation or those with cecectomy alone (P < 0.01). Among the rats with both cecectomy and gastrectomy, the total body weight gain of the rats fed the control diet was lower than that of the rats fed the Sc-FOS diet. Among the rats with gastrectomy alone, the food intake of the rats fed the control diet was lower than that of the rats fed the Sc-FOS diet.
Anemia-related biochemical values.
Cecectomy alone did not affect Hb or Ht (Table 1
). Both Hb and Ht in rats with gastrectomy, except for those with
gastrectomy alone and fed the Sc-FOS diet, were significantly lower
than those of the sham-operated rats or the rats with cecectomy
alone. On the other hand, Hb and Ht in the gastrectomized rats without
cecectomy and fed the Sc-FOS diet did not differ those of the
sham-operated rats. Hb and Ht in the gastrectomized rats without
cecectomy and fed the Sc-FOS diet were higher than those in the
gastrectomized rats without cecectomy and fed the control diet
(P < 0.05), but in the gastrectomized rats with
cecectomy, Hb and Ht were not affected by the experimental diet.
|
). HRE in the gastrectomized rats without cecectomy and fed the
Sc-FOS diet was significantly higher than that in the
gastrectomized rats without cecectomy and fed the control diet. HRE in
the gastrectomized rats with cecectomy and fed the Sc-FOS diet did
not differ from that in the gastrectomized rats with cecectomy and fed
the control diet.
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In every surgical treatment group, the pH of the cecal contents and
that of the colorectal contents of the rats fed the Sc-FOS diet
were significantly lower than those in the rats fed the control diet,
and the wet weight of the cecal contents of the rats fed the Sc-FOS
diet were significantly higher than those in the rats fed the control
diet (Table 2
). In the rats with gastrectomy alone, the iron concentration in the
liquid phase of the cecal contents and the ratio of the iron
concentration in the liquid phase to that in the solid phase of the
cecal contents in the rats fed the Sc-FOS diet were significantly
higher than those in the rats fed the control diet.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). In this study,
we observed an increase in the soluble iron fraction in the cecal
contents of rats. Therefore, we thought that the effect of Sc-FOS
in increasing iron absorption may occur in the large intestine,
including the cecum. We have also confirmed that dietary Sc-FOS
prevent the anemia observed in gastrectomized rats (Ohta et al. 1998c
). The postgastrectomy anemia in rats is due to iron
malabsorption because rats with this anemia exhibit typical symptoms of
iron deficiency such as a decrease in the level of serum iron and an
increase in UIBC and TIBC. Therefore, in gastrectomized rats, dietary
Sc-FOS may stimulate intestinal iron absorption. It is very hard to
prevent postgastrectomy anemia. We know of no way other than Sc-FOS
feeding to prevent this anemia. Therefore, we expected that
gastrectomized rats may be useful to examine the mechanism of the
stimulatory effect of Sc-FOS on intestinal iron absorption. On the
other hand, we have shown that the effect of Sc-FOS in increasing
Ca and Mg absorption takes place mainly in the large intestine in rats
as determined by four different experimental methods (Baba et al. 1996
, Ohta et al. 1994
, 1995a
and 1997
). One
of these methods was cecectomy (Ohta et al. 1994
). The
ingested Sc-FOS are fermented by luminal bacteria, mainly in the
cecum of rats; thus we can assess the role of luminal fermentation of
indigestible carbohydrates and the role of the cecum by cecectomy.
Indeed, the stimulatory effect of Sc-FOS on Ca and Mg absorption
was shown previously to be decreased in cecectomized rats (Ohta et al. 1994
). Therefore, we expected that we could confirm
whether the stimulatory effect of Sc-FOS on iron absorption occurs
in the large intestine by observing the difference in recovery from
postgastrectomy anemia in rats with and without cecectomy.
In this study, Ht, Hb and SI concentrations in gastrectomized rats
without cecectomy and fed the Sc-FOS diet were higher than those in
the gastrectomized rats with cecectomy and fed the Sc-FOS diet, by
~15, 18 and 35%, respectively. A significant increase in HRE as a
result of Sc-FOS feeding was observed in gastrectomized rats, but
this was not observed in gastrectomized rats with cecectomy. These
findings indicate that cecectomy delayed the recovery from
postgastrectomy anemia promoted by Sc-FOS. In our previous study, a
significant correlation was observed between the apparent iron
absorption and HRE in gastrectomized rats (Ohta et al. 1999
). Therefore, the results of this study strongly suggest
that the stimulatory effect of Sc-FOS on iron absorption takes
place in the large intestine of gastrectomized rats. However, there is
another possible explanation for this result. Surgical treatment such
as cecectomy may shorten the small intestine transit time. It has been
reported that short-chain fatty acids, which are produced through
fermentation in the large intestine, change the small intestine transit
time, e.g., the ileal brake (Cherbut at al. 1997
). The
hypothesis that Sc-FOS feeding also prolongs the small intestine
transit time, thereby increasing iron absorption from the small
intestine, cannot be rejected on the basis of our findings. However,
one of the reasons for the ileal brake is the inhibition of
transpyloric flow (Cuche and Malbert 1999
).
There is no transpyloric flow control in gastrectomized rats.
Therefore, it seems that this explanation is not correct. The results
of this study do show that the cecum plays an important role in the
mechanism by which Sc-FOS prevent postgastrectomy anemia.
To our knowledge, there is very little information available about iron
absorption in the large intestine. There are a few reports indicating
that the large intestine has the potential to absorb iron
(Ebihara et al. 1994
and1995
). However, the main
intestinal segment involved in iron absorption is the proximal small
intestine, especially the duodenum. Indeed, it has been reported that a
divalent-cation transporter (DCT1), which functions as an
intestinal iron transport protein, is strongly expressed in the small
intestine, but poorly expressed in the large intestine (Gunshin et al. 1997
). In this study, cecectomy alone did not affect any
of the anemia-related variables examined, indicating that iron
absorption usually does not occur in the large intestine. However, iron
absorption in the large intestine may have occurred as a result of
Sc-FOS feeding.
The mechanism of iron absorption in the large intestine has not yet
been clarified; thus, we have no further explanation for the
stimulatory effect of Sc-FOS on iron absorption other than that it
takes place at least in part in the cecum. However, several phenomena
that suggest characteristics of the mechanism were observed. The first
limiting step of iron absorption in both the small intestine and the
large intestine may be the solubilization of dietary iron. A
significant increase in the level of iron in the liquid phase of the
cecal contents was observed in the gastrectomized rats. In the previous
and present studies, Sc-FOS feeding significantly increased the
concentration of iron in the liquid phase of the cecal contents in
iron-deficient (Ohta et al. 1995b
) and
gastrectomized rats. These phenomena may occur as a result of the
lowering of the pH of the cecal contents by the luminal bacterial
fermentation of Sc-FOS and/or Sc-FOS may stimulate the
absorption of Ca, which forms an insoluble complex with iron
(Barton et al. 1995, Hallberg et al. 1991
, Prather and Miller 1992
). These changes
would increase the diffusive movement of iron into mucosal cells from
the luminal contents. It remains to be proven whether cecal intestinal
iron absorption occurs via a diffusive pathway.
In a previous study, cecectomy alone did not decrease calcium
absorption in rats fed a normal purified diet without Sc-FOS
(Ohta et al. 1994
), similar to the case of iron
absorption in this study. Calbindin-D9k (CaBP), which plays a role in
intracellular Ca transport, is expressed mainly in the small intestine
(Duflos et al. 1996
). However, we have observed that
dietary Sc-FOS strongly induced CaBP expression in the large
intestine (Ohta et al. 1998a
and 1998b
). It remains to
be confirmed whether Sc-FOS feeding results in the induction of
other intestinal transport proteins for iron, e.g., DCT1, as in the
case of CaBP.
In the gastrectomized rats with cecectomy, Sc-FOS feeding increased the mean HRE by ~0.053. Also, an increase in the iron concentration in the liquid phase of the cecal contents was observed. It seems that iron absorption may occur not only in the cecum but also in the colorectum, i.e., throughout the entire large intestine.
The cecum plays an important role in the mechanism by which Sc-FOS prevent postgastrectomy anemia. Our findings suggest that Sc-FOS stimulate iron absorption from the large intestine, at least in gastrectomized rats, and the large intestine may have the ability to absorb iron at a nutritionally important level.
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FOOTNOTES |
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Manuscript received November 1, 1999. Initial review completed December 21, 1999. Revision accepted February 16, 2000.
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