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Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
1To whom correspondence should be addressed. E-mail: hara{at}chem.agr.hokudai.ac.jp.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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18% of the ingested TA was recovered in the feces. Our results demonstrate that TA reduces iron absorption and induces anemia, conditions that are partially prevented by the feeding of DFA III, but not FOS.
KEY WORDS: • difructose anhydride III • fructooligosaccharide • tannic acid • iron • intestinal absorption
Iron deficiency is one of the most common nutritional problems in the world (1) and is a major cause of anemia. The low bioavailability of dietary iron is an important factor in iron deficiency. Some dietary components, such as phytates or polyphenols, decrease the bioavailability of nonheme iron (2–4). Polyphenols are present in a variety of vegetable origin foods and constitute an integral part of the human diet. Recently, owing to possible beneficial human health effects, interest in food phenolics and recommended daily intakes has increased. However, vegetable tannin [tannic acid (TA)1], a large polyphenol, has been shown to reduce the bioavailability of iron in many vegetable foods because of its galloyl-containing group (3), which binds iron and thus inhibits its absorption from food (5,6). The literature shows that the chemical properties of TA inhibit iron absorption (7,8). We also previously found that TA induces severe anemia by decreasing iron absorption, but does not affect other trace minerals such as Zn, Cu and Mn in rats (Afsana, K. & Hara, H., unpublished data). Moreover, in iron-deficient humans, polyphenol consumption has been shown to affect iron status (9); however, there have been no studies investigating the prevention of polyphenolic compound-induced iron-deficiency anemia.
Recently, the nutritional importance of several indigestible carbohydrates such as difructose anhydride III [DFA III (10)], fructooligosaccharide [FOS (11–13)], resistant starch (14,15) and guar gum hydrolysate (16,17) has received attention because they promote mineral absorption. DFA III is an indigestible disaccharide (Fig. 1), and a process for mass production of DFA III from inulin with Arthrobacter sp. H65–7 inulin fructotransferase [EC 2.4.1.93; Inulinase II (18)] has been developed. This compound has two glycoside bonds between two fructose molecules. DFA III is very stable at high temperatures in acidic conditions (pH 2.0 at 100°C for 30 min), and this sugar has one-half the sweetness of sucrose (19). We previously showed that ingestion of DFA III stimulates Ca absorption in in vivo and in vitro studies (10,20–22). In contrast, very few reports show the enhancing effects of indigestible saccharides on iron absorption (23). The feeding of water-soluble soybean fiber (24) or short-chain fructooligosaccharide (25) has been shown to prevent iron-deficiency anemia induced by gastric resection in rats. These fermentative carbohydrates have been reported to stimulate iron absorption from the large intestine. However, there is no proposed mechanism for the promotion of iron absorption by indigestible saccharides. To our knowledge, there is no information on whether the iron-deficiency anemia and iron malabsorption induced by dietary TA in rats could be prevented by these carbohydrate sources. Furthermore, DFA III has a greater effect on calcium absorption than does FOS (10), although the effects of DFA III on iron absorption have yet to be determined.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Male Sprague-Dawley rats (Clea Japan, Tokyo, Japan), 5-wk-old and weighing 90–110 g, were given free access to a stock diet (Table 1) and deionized water during a 5–6 d acclimation period. Rats were housed individually in wire-bottom stainless steel cages at a controlled temperature of 22–24°C, relative humidity of 40–60% and light cycle of 0800–2000 h throughout the experiment.
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The acclimated rats were assigned to three groups of eight using a randomized block design based on body weight, hemoglobin concentration and hematocrit. A control, FOS or DFA III (30 g/kg) diet was fed to the rats for 3 wk (Table 1) (26). The FOS and DFA III were added to the stock diets at the expense of the whole diet. Diets were prepared according to AIN-93G formulation (27) except for the iron concentration (30 mg/kg diet). We evaluated this minimum requirement iron level for rats in a previous study (Table 1). Feces were collected for three consecutive days from d 8 and 19 of the test period and were freeze-dried for subsequent iron absorption evaluation. Body weight and food intake were measured daily in both experiments. Blood samples were obtained from the tail vein for the determination of hemoglobin concentrations and hematocrits at 0, 1, 2 and 3 wk after the start of test diet feeding.
At the end of the experiment, rats were anesthetized by an intraperitonial injection of pentobarbital solution (Nembutal, 50 mg/kg body; Abbott, Chicago, IL), and blood was collected from the abdominal aorta. The serum was stored at -40°C until analysis of iron concentration. The cecum with its contents and the liver after a perfusion of saline from the portal vein to exclude the blood were removed. Both were weighed, frozen immediately and stored at -40°C for subsequent analyses. The weight of the cecal contents was determined by the subtraction of the cecal wall weight from that of the total cecum.
Experiment 2.
The rats were divided into four groups of eight as in expt. 1 and were fed control, TAcontrol, TAFOS or TADFA III diets (FOS and DFA III, 30 g/kg diet; TA, 15 g/kg diet) for 3 wk. Other details were the same as in expt. 1. The TA level was set at the amount that significantly reduced hemoglobin concentration, hematocrit and iron absorption based on the results of a previous study (Afsana, K. & Hara, H., unpublished data).
All experiments were approved by the Hokkaido University Animal Use Committee, and the rats were maintained according to the guidelines for the care of laboratory animals at Hokkaido University.
Analytical methods.
Hemoglobin concentrations were measured using a commercial assay kit (Hemoglobin B-test; Wako Pure Chemical Industries, Osaka, Japan). Hematocrits were determined after centrifugation (15,000 x g) of blood. (Centrifuge Hematocrit MC-201, Hitachi, Tokyo, Japan).
Serum iron concentrations and unsaturated iron binding capacities (UIBC) were determined using an assay kit (Wako Pure Chemical Industries). The total iron-binding capacities (TIBC) and transferrin saturations (Tf) were calculated from the obtained values.
Freeze-dried feces were weighed and milled to fine powder. Diets (5 g) and the powdered feces (1.5 g) were dry-ashed at linearly increased temperatures up to 550°C for 6 h and then at 550°C for 18 h by a muffle furnace (EYELA, TMF-3200; Tokyo Rikakikai, Tokyo, Japan). Samples were heated with 5.49 mol/L of HCl until drying and diluted with 0.82 mol/L of HCl. Iron concentrations of the samples were measured with an atomic absorption spectrophotometer (Shimadzu AA-6400F; Shimadzu Seisakusyo, Kyoto, Japan) after appropriate dilution. The dried liver sample (1.8 g) was analyzed to determine iron concentrations in a similar manner to the feces. We estimated the analytical accuracy by performing the recovery tests of iron and determined the recovery rate to be 105 ± 5.11% (n = 5).
The cecal weight including its contents was measured and the contents collected after cutting off the cecal wall. The cecal wall was washed with saline and weighed. The cecal contents were diluted with four volumes of deionized water and homogenized using a teflon homogenizer. The homogenate was measured as the cecal pH with a semiconducting electrode (ISFET pH sensor 0010–15C; Horiba, Kyoto, Japan). The total iron in the homogenate was determined after dry-ashing using the same procedure as that for feces. The cecal supernatant was obtained after centrifugation of the homogenate (30,000 x g at 4°C for 20 min), and deproteinized with 9 mol/L of perchloric acid. The iron concentrations in the dry-ashed cecal homogenate (total iron) and the deproteinized supernatant fractions (soluble iron) were measured by atomic absorption spectrometry. After washing the homogenate with chloroform, the concentrations of individual organic acids (acetic, propionic, butyric, lactic and succinic acid) in the cecal homogenate were measured by ion-exclusion chromatography using an HPLC system equipped with a solvent delivery system (SLC-10 AVP; Shimadzu), a double ion-exchange column (Shim-pack SCR-102h, 8 x 300 mm; Shimadzu) and an electroconductivity detector (CDD-6A; Shimadzu) (28).
The TA concentrations in feces were determined by the Association of Official Analytical Chemist’s procedure (29). However, TA was extracted from feces (0.5 g) at 60°C for 45 min with methanol (5 mL). The extract was then measured spectrophotometrically using the Folin-Denish reagent to determine the fecal TA concentrations.
Calculations and statistical analyses.
Each value was calculated as follows:
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The total TA concentrations in fecal extracts (mg) were determined by the absorbance of each of the samples of the TA groups subtracted by the mean absorbance of the extract in the TA-free control group.
The data were analyzed by two-way (diet and time, Figs. 2and 3) or one-way ANOVA (diet, Tables 2, 3, 4, 5;Fig. 4). To determine differences from wk 0, the Scheffé test (30) was performed. The Kruskal-Wallis test was performed to analyze the lactic acid pool data [expt. 2, Table 5 (P < 0.001)]. The Duncan multiple range test (31) was used to determine whether the means differed among groups (P < 0.05). The correlation coefficients for iron absorption and several cecal variables were calculated by the least squares method (32). These statistical analyses were performed using the general linear models procedure of the Statistical Analysis Systems program (SAS version 6.07; SAS Institute, Cary, NC).
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Hemoglobin concentrations in all groups (Fig. 2A) and hematocrits only in the DFA III-fed group (Fig. 2B) increased from 0 to 3 wk (P < 0.001), however, the three groups did not differ (expt. 1). Serum iron concentrations, UIBC, TIBC and Tf in the three groups fed diets without TA also did not differ (data not shown).
In expt. 2, the hemoglobin concentrations of rats fed the control TA diet were lower (P < 0.001) than in rats fed the TA-free control diet at wk 2 and 3 (Fig. 3A). The concentrations at wk 2 and 3 in the TADFA III groups were higher (P < 0.001) than in the TAcontrol group, but lower (P < 0.001) than in the control (TA-free) group. Rats fed the TADFA III diet had higher (P < 0.001) hemoglobin concentrations than the TAFOS-fed group at wk 2, but not at wk 3. The hematocrits of the TA-fed rats were lower (P < 0.001) than that of the control at wk 1 as well as at wk 2 and 3 (Fig. 3B). Rats fed the TADFA III diet had higher (P < 0.001) hematocrits than the control-fed rats at wk 2, but not at wk 3. The hematocrits at wk 2 and 3 in the TADFA III-fed groups were higher (P < 0.001) than in the TAFOS-fed group and were not different from the values of the TA-free–fed group. Serum iron concentrations and Tf were lower (P < 0.001) and UIBC and TIBC were higher (P < 0.005) in the TA-fed groups, and there was no effect of indigestible saccharide on these variables (Table 3).
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The feeding of indigestible saccharide did not influence the wet weights and iron concentrations of liver in expt. 1 (Table 2). The wet weights and iron concentrations of the liver of rats fed the TA-containing diet were lower (P < 0.001) than those fed the TA-free diet in expt. 2, and the feeding of the DFA III and FOS diets did not affect the reduced liver variables.
The weight of cecal contents was higher (P < 0.001) in the rats fed both the indigestible sugar (expt. 1) and TA (expt. 2) (Table 4). However, the cecal contents weight of TAFOS-fed rat was higher (P < 0.001) than those of the TAcontrol- and TADFA III-fed rats (expt. 2).
The total iron pool, but not the soluble iron pool, was higher (P < 0.001) in the DFAIII- and FOS-fed groups compared with the control group (expt. 1). In expt. 2, the total iron pool was higher (P < 0.001) in all TA-fed groups than in the control, whereas the feeding of FOS and DFAIII had no effect. Soluble iron pool in the TAFOS-fed group was higher (P < 0.001) than other groups in expt. 2.
Cecal pH was lower (P < 0.001) in both indigestible sugar-fed groups than in the control group (expt. 1). However, in expt. 2, the cecal pH of the TAcontrol group was lower (P < 0.001) than the pH of TA-free control group. Moreover, the pH in the TAFOS-fed group, but not in the TADFA III-fed group, was lower (P < 0.001) than the TAcontrol group.
Acetic and propionic acid and total SCFA pools were higher (P < 0.001) in the DFA III-fed groups than the other groups (expt. 1, Table 5). In expt. 2, the TAcontrol group showed larger acetic acid pools than that of the TA-free group (P < 0.005). The lactic acid pool was higher in the FOS-fed compared with other groups (P < 0.001) in both the experiments (Table 5).
The fecal recovery rates of TA at d 19–21 were 15.5, 21.9 and 17.3% in TAcontrol-, TAFOS- and TADFA III-fed groups, respectively (P = 0.354, n = 24).
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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A DFA III diet enhanced the iron absorption in TA-fed rats throughout the feeding period (d 8–10 and 19–21), whereas TAFOS feeding increased iron absorption only at d 8–10 (expt. 2). Sakai et al. (25) showed that the cecal fermentation of FOS is involved in the prevention of anemia induced by gastric resection. These results suggest that FOS increases iron absorption in the large intestine. However, there is no report on an iron transporter, such as DCT-1, in the large intestinal mucosa. There is evidence that DFA III increases Ca absorption via a paracellular pathway in the small intestine (22). Possibly both the small intestine and cecal fermentation are involved in the sustained increase in iron absorption by the feeding of DFA III. It remains to be determined which part of the intestine is involved in the DFA III effects and what mechanism is associated with the promotion of iron absorption by DFA III.
The effect of DFA III on iron absorption has not yet been clarified and this is the first report showing that DFA III increases iron absorption. Decreases in hemoglobin and serum iron concentrations and increases in UIBC and TIBC are symptoms of iron-deficiency anemia (33). In this study, iron-deficiency anemia occurred in the TA-fed rats throughout the test period. At the final week, the feeding of DFA III, but not FOS, improved hemoglobin concentrations and hematocrits in rats fed TA (Fig. 3A, B). However, the feeding of DFA III did not change the serum iron variables (Table 3). The amount of absorbed iron in rats fed TADFA III was not sufficient to increase these variables to the same level as in the control rats (expt. 2). Liver iron stores, which also did not change by the feeding of DFA III, agreed with the results of the serum variable (Table 2). Previous results showed that FOS feeding could prevent anemia in totally gastrectomized rats (25), which does not agree with the results for FOS feeding in the present study. This may be due to differences in the dose of FOS, i.e., 75 g of FOS/kg diet used in the previous work, but only 30 g of FOS/kg diet in the present study.
The DFA III feeding increased cecal SCFA in expt. 1 (TA-free diet), but not in expt. 2 (TA feeding). The fermentation product, SCFA (21,34), released by cecal bacteria contributes to an increase in Ca absorption (35). Mitamura et al. (20) demonstrated that the large intestine is involved in the promotive effect of DFA III on Ca absorption. Iron absorption rate was correlated with many cecal fermentation variables; a positive correlation with SCFA and a negative correlation with cecal pH in expt. 1 (Table 6). These correlations support the hypothesis that cecal fermentation is involved in the increase in iron absorption induced by indigestible saccharides in rats fed a TA-free diet. A low level of FOS feeding did not induce a sustained increase in iron absorption (Fig. 4A, B, d 19–21) in spite of lower pH and higher soluble iron in the cecum (Table 4). We also found high levels of cecal lactic acid in the FOS-fed groups (expts. 1 and 2, Table 5). It has been shown that FOS increases lactic acid-producing bacteria throughout the cecocolon (36). A large increase in lactic acid was responsible for the low cecal pH in the FOS group fed TA or TA-free control, demonstrating that lower pH and soluble iron (P < 0.001) in the cecum were not important factors in increased iron absorption (Table 4). In rats fed TA, feeding DFA III promoted iron absorption during d 19–21 without any changes in cecal variables. The possible mechanisms involved in promoting iron absorption are increases in iron absorption in the small intestine by DFA III or induction of some bacteria to degrade TA in the cecum by DFA III without obvious changes in organic acid production (Table 5). There is evidence that TA is hydrolyzed by bacterial tannase enzyme to gallic acid (37). However, we showed that fecal recovery of TA was 15–20% and there were no differences among the groups. It is unlikely that TA metabolism in the cecum is changed by feeding DFA III and FOS. The involvement of cecal fermentation in the effect of DFA III on iron absorption in TA-fed rats need further investigation.
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In conclusion, the feeding DFA III increases iron absorption and partially prevents iron-deficiency anemia induced by TA. Cecal fermentation may be partly involved in the increase in iron absorption induced by the feeding of DFA III.
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FOOTNOTES |
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Manuscript received 22 June 2003. Initial review completed 27 June 2003. Revision accepted 9 August 2003.
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LITERATURE CITED |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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