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Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan and * Division of Exercise Science, Sapporo Medical University, Sapporo 060-8556, 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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KEY WORDS: • gastrectomy • iron absorption • anemia • dietary fiber • voluntary running exercise • rats
Postgastrectomy anemia is a common complication in patients after gastric resection (1 ,2 ). It has been reported that iron (3 ) and/or vitamin B-12 (4 ) deficiencies after gastrectomy contribute to this anemia in humans. In the early stages right after gastrectomy, iron-deficient anemia occurs (2 ) because gastric acid plays an important role in intestinal iron absorption through solubilization of dietary insoluble iron salts (5 ). Recently, total gastrectomy has been shown to induce iron malabsorption and anemia also in rats (6 ,7 ), indicating that iron deficiency in humans and rats is a factor in gastrectomy-induced anemia.
Iron deficiency also impairs exercise performance primarily because of the failure of the oxygen delivery system as a result of anemia (8 ,9 ). Several researchers have reported that endurance capacity, as measured by time to exhaustion during treadmill running, is lowered by severe anemia (8 ,10 ,11 ). However, the effects of iron-deficiency anemia on voluntary activity have not been elucidated (12 ,13 ). We chose to monitor voluntary running as a way of observing exercise performance in totally gastrectomized rats.
Indigestible carbohydrates such as dietary fibers, oligosaccharides and resistant starch promote calcium absorption in rats (14 –17 ) and humans (18 ,19 ). In particular, the fermentable carbohydrates exert effects in the large intestine (17 ). We previously reported that ingestion of water-soluble soybean fiber (WSSF), a highly fermentable dietary fiber with low viscosity, partially prevents the diminished calcium absorption that follows total gastrectomy in rats, resulting in an improvement in postgastrectomy osteopenia (20 ). In contrast, there is little reported evidence concerning whether these indigestible carbohydrates stimulate iron absorption (7 ,21 ,22 ). Feeding fructooligosaccharides increased iron absorption in totally gastrectomized rats (7 ). However, the effects of dietary fiber on iron malabsorption and anemia after gastric resection are not known. We speculated that if ingestion of WSSF increases iron absorption, postgastrectomy anemia could be also improved. WSSF is widely used in foods and beverages for its stabilization and emulsification properties and to prevent the adhesion of cooked rice and noodles (23 ). However, the physiologic functions of WSSF have not yet been fully clarified.
The aims of this study were to examine the effects of feeding WSSF on gastrectomy-induced iron malabsorption and anemia in rats (Experiment 1) and to examine the effect of total gastrectomy on voluntary running exercise performance in rats fed diets with or without WSSF (Experiment 2). We also evaluated the effects of voluntary running exercise on iron absorption and hematological variables by comparing Experiments 1 and 2.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Water-soluble soybean fiber (WSSF; SOYAFIBES, Fuji Oil, Tokyo, Japan) is a novel polysaccharide consisting mainly of galactose, arabinose and galacturonic acids, with an average molecular weight of 
500,000 (23
,24
). The preparation of WSSF was as follows. Defatted soybeans were treated with hot water (50°C) to remove water-soluble components; the WSSF was extracted under weakly acidic conditions (pH 5.0 by HCl) at 120°C for 1.5 h. WSSF contains 6.7% moisture, 6.1% crude protein, 6.8% ash and 80.4% soluble dietary fiber consisting of 100% water-soluble acidic hemicellulose high in galacturonic acids; the iron concentration was 8.85 mg/kg WSSF.
Animals and diets.
Male Sprague-Dawley rats (4 wk old; Clea Japan, Tokyo, Japan) were housed in individual stainless steel cages (17.5 cm x 25 cm x 17 cm) in a room with controlled temperature (22 ± 2°C), relative humidity (40–60%) and lighting (light 800-2000 h). Rats were fed the stock diet (25 ) shown in Table 1 for an acclimation period of 4–5 d, and were divided into two groups using a randomized block design based on body weight in two separate experiments (Experiment 1 and 2). After 24 h of food deprivation, the rats of one group were subjected to total gastrectomy (20 ,26 ) in which the stomach was removed after ligation of several vessels that supply blood to the stomach; in addition, an end-to-side anastomosis was carried out between the cut edge of the esophagus and the upper jejunum 8 cm distal from the ligament of Treitz (Gastrectomized group). The rats in the other group were subjected to laparotomy in which the abdominal cavity was opened (Sham-operated group). Both operations were performed under the same anesthetic procedure (Nembutal/sodium pentobarbital, 40 mg/kg body, Abbott Laboratories, North Chicago, IL). All rats were deprived of food and water for 24 h after the operations, and were then fed cow’s milk for 2–3 d.
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In Experiment 2 (effects of total gastrectomy and WSSF feeding on voluntary running, Sham/Control group; n = 7, Sham/WSSF group; n = 6, Gastrectomized/Control group; n = 9, Gastrectomized/WSSF group; n = 9), rats were allowed voluntary exercise. On d 8 after the start of the feeding period, all rats were moved into cages (27 cm x 35 cm x 35 cm) equipped with a rotary wheel and a counter for recording distances run; they were allowed to exercise voluntarily until the final day of the feeding period. Distances run for each 24-h period were measured every day. Other details were as in Experiment 1.
This study was approved by the Hokkaido University Animal Committee, and animals were maintained in accordance with the guidelines for the care and use of laboratory animals of Hokkaido University.
Analytical methods.
Hemoglobin concentration was evaluated using a commercial assay kit (Hemoglobin B-test, Wako Pure Chemical Industries, Osaka, Japan). Freeze-dried feces were ground with a pestle and mortar to a fine powder and the powdered feces (1.5 g) were ashed at temperatures elevated linearly to 550°C for 6 h, and then at 550°C for 18 h with an electric furnace (EYELA TMF-3200, Tokyo Rikakikai, Tokyo, Japan). The ashed samples were treated with 5.49 mol/L HCl at 200°C for 30 min and dissolved in 0.82 mol/L HCl. Iron concentrations in the ashed solutions were measured by atomic absorption spectrometry (Shimadzu AA-6400F, Shimadzu Seisakusyo, Kyoto, Japan) after suitable dilution. The amount of iron in the test diets was determined in the same manner. We performed recovery tests to confirm the accuracy of the above-mentioned method, and the recovery of iron was 105 ± 5.1% (n = 5, CV = 5.7%).
The cecal contents were diluted with 4 volumes of deionized water and homogenized using a Teflon homogenizer. The pH of these homogenates was measured with a semiconducting electrode (ISFET pH sensor 0010–15C, HORIBA, Kyoto, Japan) as the pH of cecal contents. The amount of total iron in the homogenates was determined by the above-mentioned atomic absorption spectrometry after dry-ashing with an electric furnace. 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 spectrometry after deproteinizing with 9 mol/L perchloric acid. Concentrations of organic acids (acetic, propionic, butyric, succinic and lactic acids) in the homogenate of cecal contents were measured after sample preparation by the procedure described previously (28 ,29 ) using a HPLC (LC-10ADvp, Shimadzu Seisakusyo, Kyoto, Japan) equipped with two Shim-pack SCR-102H columns (8 mm i.d. x 30 cm long, Shimadzu Seisakusyo) and an electroconductibility detector (CDD-6A, Shimadzu Seisakusyo).
Calculations and statistical analyses.
Net absorption of iron was calculated by the following formula: amount of net Fe absorption (µmol) = total Fe intake - fecal Fe excretion. Net Fe absorption ratio (%) = 100 x (total Fe intake - fecal Fe excretion)/total Fe intake.
Hemoglobin regeneration efficiency (HRE) was estimated from the following formulas (30 ): HRE = [Hemoglobin-Fe (mol) at the end of the feeding period - Hemoglobin-Fe (mol) at the beginning of the feeding period]/total Fe intake during the feeding period. Hemoglobin-Fe (mol) = [body weight (g)] x [mL blood/g body weight (assumed to be 0.067 mL)] x [(g hemoglobin/L blood)/1000] x [mol Fe/g hemoglobin (assumed to be 0.06)].
Data were analyzed by two- or three-way ANOVA for the two or three factors (operation, diet and time, or operation, diet and exercise) and their interactions. Duncan’s multiple range test (31 ) was used to determine whether mean values were significantly different between groups (P < 0.05). Correlation coefficients for the relationships between net iron absorption or HRE and several cecal variables (Experiment 1) and between cumulative running distance and several hematological variables (Experiment 2) were calculated by the least-squares method (32 ). These statistical analyses were done using the General Linear Models procedure of SAS (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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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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As shown in Figure 1 , gastrectomy markedly reduced iron absorption in rats. It has been widely accepted that iron absorption occurs mainly in the small intestine (33 ). Many researchers have reported that solubilization of dietary iron salts by gastric acid is an important step in intestinal iron absorption (5 ,34 ). In this study, the iron source in the test diets was ferric citrate [AIN-93G formulation, (25 )], an iron salt that dissolves very slowly (35 ). In the case of sham-operated rats, dietary ferric citrates might dissolve sufficiently in the stomach; however, in gastrectomized rats, ingested ferric citrates would flow directly into the small intestine, and pass through before sufficient solubilization could took place.
WSSF feeding completely prevented iron malabsorption as a result of total gastrectomy (Fig. 1) . We showed previously that ingestion of WSSF improves gastrectomy-induced calcium malabsorption and osteopenia (20 ). Proposed mechanisms for the promotion of calcium absorption are as follows: 1) organic acids produced by fermentation solubilize calcium salts in the large intestine (14 ,36 ); and 2) the SCFA themselves promote calcium transport (37 –39 ). Soluble iron in the cecal contents was increased by WSSF consumption, although the speciation of the soluble iron in the intestine is not known (Table 3) . However, iron absorption was more strongly correlated with the pools of acetic acid, propionic acid and total SCFA (sum of acetic, propionic and butyric acids) than with the soluble iron pool or cecal pH (Table 5 ). These results suggest that SCFA produced from WSSF promote iron absorption. Cecal fermentation differed between sham-operated and gastrectomized rats fed the WSSF diet (Table 4) ; the pools of acetic, propionic, butyric and total SCFA in the cecal contents were 40–70% higher, whereas the pools of succinic and lactic acids were much higher in the sham-operated rats than in the gastrectomized rats. Net iron absorption was not enhanced by WSSF feeding in sham-operated rats (Fig. 1) , in spite of the increase in cecal organic acids pools resulting from WSSF feeding (Table 4) . This result suggests that the cecal fermentation pattern of WSSF is an important factor in the stimulatory effect on iron absorption after WSSF feeding, and that succinic and lactic acids may not be involved in iron absorption in the cecum.
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There are conflicting reports concerning the impairment of exercise performance as a result of iron deficiency (8 ,10 ,41 ). Several reports have shown that the decreased exercise performance after iron deficiency is attributable mainly to the lowered capacity to deliver oxygen from lungs to tissues as a result of anemia (8 ,9 ). In contrast, transfusions to restore the decreased hemoglobin did not fully improve endurance capacity in iron-deficient humans (42 ) and rats (10 ), suggesting that not only anemia but other factors as well are involved in the impairment of exercise performance caused by iron deficiency. In this study, total gastrectomy led to iron-deficiency anemia (Figs. 2 , 3) and a severe reduction in running exercise performance (Fig. 4 , Table 6 ); however, WSSF feeding ameliorated these effects. In gastrectomized rats, the distance run was positively correlated with hemoglobin concentration (r = 0.730, P < 0.001) and hematocrit (r = 0.740, P < 0.001) at 5 wk. However, running performance did not recover completely even when the anemia was fully reversed by WSSF feeding (Figs. 2 3 4 , Table 6 ). Our results suggest that iron-deficiency anemia is primarily responsible for the impaired running performance; however, latent iron deficiency, which leads to inadequacies in the iron-related metabolism, (43 ) may also be responsible for this impairment.
Voluntary running exercise suppressed body weight gain in sham-operated rats and in gastrectomized rats fed the WSSF diet (Table 2) . This phenomenon probably depends on the energy expenditure associated with running exercise. In this study, running decreased net iron absorption (Fig. 1) . Gastrointestinal bleeding might contribute to the negative effects of exercise on intestinal iron absorption (44 ). Hemoglobin concentration and hematocrit in gastrectomized rats fed the control diet were diminished by voluntary running exercise (Fig. 2) , in spite of much shorter distances run compared with the other three groups (Fig. 4 , Table 6 ), suggesting that running exercise under iron deficiency conditions worsens the anemia. In Experiment 1 (under sedentary condition) of this study, body weight gain in rats fed the WSSF diet was higher than that in rats fed the control diet in the sham groups (Table 1) . The reasons for this greater gain are not known. The difference in body weights between control and WSSF groups could not be explained by the weight of the cecal contents (Table 3) .
In conclusion, ingestion of WSSF completely prevents postgastrectomy iron malabsorption and anemia, and cecal fermentation of WSSF may be involved in improving these gastrectomy-induced complications. Total gastrectomy severely impairs running exercise performance, and the lowered performance is dramatically improved by feeding WSSF.
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FOOTNOTES |
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Manuscript received 7 August 2002. Initial review completed 29 November 2002. Revision accepted 9 January 2003.
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LITERATURE CITED |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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