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Departments of 2 Animal Science and 3 Food Science and 4 USDA-ARS, U.S. Plant, Soil, and Nutrition Laboratory, Cornell University, Ithaca, NY 14853
* To whom correspondence should be addressed. E-mail: xl20{at}cornell.edu.
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ABSTRACT |
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 TOP ABSTRACT IntroductionMaterials and MethodsResultsDiscussionLITERATURE CITED |
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Introduction |
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TOPABSTRACTIntroductionMaterials and MethodsResultsDiscussionLITERATURE CITED |
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Iron bioavailability of staple crops may be improved by removing or reducing inhibitors of iron utilization (e.g., phytate and polyphenolics) and/or enriching enhancers of iron utilization (4). Recently, inulin and short-chain fructooligosaccharides (FOS)5 have been studied as possible candidates of such enhancers (5–9). These compounds are unique D-fructofuranose polymers linked by a ß2
1 bond at the anomeric C2, and are accumulated in the tissues of many plant species (10). The general assumption is that these compounds are indigestible in the upper digestive tract of simple-stomached animals and humans (11), but that they pass to their lower gut to be fermented by microbes (10).
Positive effects of supplemental inulin or FOS on bioavailability of dietary calcium and magnesium in animals and humans have been reported (12–17). However, only a few studies (5–9,18) have been conducted to determine such effects on bioavailability of dietary iron. Consequently, several major issues remain to be clarified. First, the effects of inulin or FOS on dietary iron utilization are inconclusive, as benefits to blood hemoglobin (Hb) concentration and hematocrit were shown in rats fed diets containing 5 or 7.5% FOS (6,7), whereas no improvement in iron utilization was produced by supplementation of inulin or FOS in healthy men (8,9). Second, all experimental animals or tested subjects in past studies were fed inorganic iron supplements (6,7,18). Thus, the exclusive effects of supplemental inulin or FOS on the bioavailability of iron intrinsically present in foods of plant origin have not been studied. Lastly, there is little information on the mode of action of inulin for its possible enhancement of iron bioavailability.
Because in vivo and in vitro studies have demonstrated that inulin and FOS stimulated the proliferation of certain types of colonic bacteria, such as bifidobacteria and lactobacilli (19–26), most inulin studies on mineral nutrition have been focused on the possible changes of these microbial populations (19–25) or the fermentation products of inulin such as short-chain fatty acids in the hindgut (19,21,22). However, effects of inulin on microbial production of 2 putative iron solubility and/or bioavailability determinants, hydrogen sulfide and phytase, in the digesta of various segments have not been well studied. Hydrogen sulfide generated from sulfate and sulfur amino acids by gut microbes (27) may react with ferrous iron to form insoluble ferrous sulfide, inhibiting its absorption. In contrast, microbial phytase releases phytate-bound iron from the digesta and renders the element available for absorption (28–30). In addition, there is little evidence for the direct impact of inulin on iron concentration or solubility in the digesta, particularly in the upper digestive tract.
Young pigs are an excellent model for the study of human iron nutrition because of similarities in the anatomy of their gastrointestinal tracts, digestive physiology, and diets between the 2 species (31). The iron status of young pigs can be readily manipulated by adjusting the dosage of the iron injections routinely given shortly after birth. The tremendous growth rate of weanling pigs (10-fold increase of birth weight in the first 6 wk of life), the low iron body store, and the low iron intake from sow's milk (1 mg/L) allows these animals to develop an "iron-deficient state" in a relatively short period of time (31). Therefore, the objectives of this study were to determine whether supplemental 2 and 4% dietary inulin: 1) improved utilization of iron intrinsically present in a corn and soybean meal basal diet by young pigs for hemoglobin synthesis; and 2) affected sulfide and soluble Fe concentrations, phytase activity, and pH of digesta from different segments of the gastrointestinal tracts of young pigs.
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Materials and Methods |
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TOPABSTRACTIntroductionMaterials and MethodsResultsDiscussionLITERATURE CITED |
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-D-glucopyranosyl-(ß-D-fructofuranosyl)n-1-ß-D-fructofuranosides (n = 10–60, mean of 25), and oligofructose, -D-fructopyranosyl-(ß-D-fructofuranosyl)n-1-ß-D-fructofuranosides (n = 2–7, mean of 4).
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25°C) with a light:dark cycle of 12:12 h, given free access to feed and water, and checked daily. In Expt. 1, 24 weanling pigs (with body weights of 9.23 ± 0.03 kg) were allotted into 3 groups (n = 8), and were fed the BD, BD + 2% inulin, or BD + 4% inulin for 5 wk. In Expt. 2, 12 weanling pigs (with body weights of 7.70 ± 0.19 kg) were allotted into 2 groups (n = 6), and were fed the BD or BD + 4% inulin for 6 wk. Prior to the beginning of both experiments, all pigs were fed the BD for 2 wk to adjust their body iron stores. Growth performance and sample collection. In both experiments, feed intake of individual pigs was recorded daily and body weight of individual pigs was measured weekly. Blood samples of all individual pigs (fasted overnight for 8 h) were collected weekly from the anterior vena cava using 5-mL heparin syringes to assay for blood Hb and hematocrit. At the end of Expt. 2, all pigs were killed by electrical stunning and exsanguinations. Based on a preliminary experiment, pigs were first fasted for 8 h and then were given free access to feed for 10 h prior to slaughter for us to collect comparable and sufficient digesta samples from all designated segments. The digestive tracts were quickly removed from the carcass and separated into various sections for digesta sampling. Digesta samples for the stomach were collected from the entire contents and thoroughly mixed using a blender. Digesta samples for different parts of intestines were collected from a 12 cm segment each, and the excisions were as follows: upper jejunum, 2 m posterior to the pylorus; lower jejunum, 2 m anterior to the ileo-caecal junction; proximal colon, immediately posterior to the ileo-caecal junction; mid colon, equal length up and down the mid transverse colon; and distal colon, immediately anterior to the rectum. The samples were immediately frozen in liquid nitrogen, and stored in a –20°C freezer. After 48 h, all samples were freeze-dried (20 SRC-X, Virtis) and stored in a –20°C freezer until analysis. All the assayed values were expressed on a dry matter basis, and moisture contents in the fresh digesta samples were calculated from the weight difference before and after freeze drying.
Blood sample analyses.
Blood Hb concentrations were measured spectrophotometrically using the cyanomethemoglobin method following the manufacturer's instructions (Pointe Scientific). Hematocrit values were determined using heparinized microcapillary tubes (Fisher Scientific). Hemoglobin repletion efficiency (HRE) was determined using the following formula (35):
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and total body Hb iron content was estimated using the following formula:
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Digesta sample analyses. Total digesta Fe concentration was measured using the same method for dietary Fe concentrations. To determine pH and soluble iron of digesta and fecal samples, 2 g of fresh wet samples were suspended in 18 mL of distilled water and mixed on an rotator stirrer for 30 min at the room temperature and centrifuged at 3,000 x g for 15 min at 4°C (GS-6KR Centrifuge, Beckman Instruments). The pH in the homogenates was determined using a glass electrode (Accumet Tris Compatible Combination Electrode, Model 630, Fisher Scientific). Soluble iron concentration in the prepared homogenates was measured using a ferrozine assay (36). After 0.1 mL of homogenate was diluted in 0.9 mL of deionized water, 0.1 mL of ferrozine chromogen solution was added for color development. The absorbance was measured at 562 nm using KC-4 version 2.6 microplate scanning spectrophotometer (BIO-TEK Instruments). Total soluble sulfide concentration in the fresh digesta was determined as previously described (37–39). Digesta phytase activities were measured using a spin column method as described by Kim and Lei (40) at 2 pH levels: the actual digesta pH for each segment and the commonly used pH (5.5) for phytase activity assay.
Statistical analyses.
Data were analyzed as a randomized block design using the Proc General Linear Models procedure of SAS (version 6.12, SAS). Effects of dietary inulin on various measures were analyzed using 1-way ANOVA with or without time-repeated measurements. Dose-dependent effects of inulin in Expt. 1 were analyzed using Proc Reg procedure of SAS. Each individually penned pig was used as the experimental unit. The Bonferroni/Dunn t-test was used to compare treatment means, and the significance level was set at P 
0.05 (41). Values in the text are means ± SEM.
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Results |
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TOPABSTRACTIntroductionMaterials and MethodsResultsDiscussionLITERATURE CITED |
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Expt. 2. There was no difference in overall growth performance or final hematocrit between pigs fed BD and 4% inulin. Pigs fed 4% inulin had 14% higher (94.4 ± 4.5 vs. 107.8 ± 3.7 g/L, P = 0.06) blood Hb concentrations at wk 6, and 22% higher (20.4 ± 1.4 vs. 24.9 ± 0.7%, P < 0.05) overall HRE than pigs fed BD. The changes in Hb concentrations over the 6-wk period were greater (P < 0.05) in pigs fed 4% inulin than those fed the BD. Although total iron concentrations of digesta from various segments were not significantly different (Fig. 2A), pigs fed 4% inulin had 45% higher (P < 0.01) soluble Fe concentrations in the 3 segments of colon than those of pigs fed BD (Fig. 2B). In contrast, digesta soluble sulfide concentration in pigs fed 4% inulin was 32% lower (P < 0.01) in digesta of distal colon and marginally lower (17%, P = 0.08) in mid colon than pigs fed BD (Fig. 3). The pH of digesta samples from various segments did not differ between the x and y groups at the end of the study (stomach: 3.2 ± 0.2 vs. 3.3 ± 0.2; upper jejunum: 6.6 ± 0.2 vs. 6.5 ± 0.1; lower jejunum: 7.3 ± 0.1 vs. 7.2 ± 0.1; proximal colon: 6.6 ± 0.2 vs. 6.6 ± 0.2; mid colon: 6.8 ± 0.1 vs. 6.8 ± 0.03; and distal colon: 6.8 ± 0.1 vs. 6.7 ± 0.1) or fecal samples (6.0 ± 0.2 vs. 6.1 ± 0.2). When phytase activity in digesta was assayed at pH 5.5, the 2 groups of pigs did not differ in digesta from any segment except for lower jejunum, where pigs fed 4% inulin had a slightly higher activity than pigs fed the BD (Table 3). When phytase activity in digesta was assayed at the actual digesta pH of each segment, only stomach digesta showed detectable activity (BD, 52.9 ± 11.5 units/g; 4% inulin, 29.2 ± 7.5 units/g; P = 0.10).
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Discussion |
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TOPABSTRACTIntroductionMaterials and MethodsResultsDiscussionLITERATURE CITED |
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The positive effect of inulin on HRE in pigs in the present study is consistent with that of FOS in rats reported by Ohta et al. (6). However, other groups did not observe a positive effect of inulin or FOS in humans (8,9). This discrepancy does not seem to be simply explained by differences in inulin or FOS doses between these experiments. The positive effects in rats was produced by 5–10% inulin or FOS (5–7, 14), whereas human subjects who did not show a response were given 3% (15 g of inulin/d) (8) or 8% (40 g of inulin/d) (9) inulin. Alternatively, initial iron status of the experimental animals or human subjects might be the key determinant of the treatment outcomes. Our pigs experienced moderate iron-deficient anemia and grew normally, which provided an appropriate physiological condition for inulin to show its effect on iron bioavailability. However, healthy, non-Fe–deficient subjects were used in human studies (8,9).
Thus, supplemental inulin may exert a greater role in iron-deficient animals than in iron-adequate humans (6,8). If so, enriching inulin in staple crops may benefit the iron-deficient population without putting the iron-adequate population at risk of iron excess. As the positive effects of 4% inulin on blood Hb and HRE were not significant until wk 5, a minimal length of time was needed for supplemental inulin to show its maximum effect. In addition, the type of inulin may affect the outcome. The inulin used in our study was a mixture of long and short-chain oligofructose polymers, whereas van den Huvel et al. (8) used short-chain oligofructose consisting of glucose linked to 2–4 fructose units, and Coudray et al. (9) used inulin of longer chain length (DP = 15). Different types of inulin or FOS fare differently in the digestive tracts and affect different types of microbial populations, leading to different digestive or metabolic impacts (22,44–46). It is also interesting to mention that soybean meal contains 4–6% galactooligosaccharides (47). As we and others have still observed an enhanced iron bioavailability by supplementing inulin or FOS into the basal diets containing up to 30% soybean meal, this again suggests the specificity of oligosaccharides in impacting select biochemical and metabolic responses.
Compared with pigs fed the BD, pigs fed 4% inulin had higher concentrations of soluble iron and lower concentrations of sulfide in digesta of the colon. To the best of our knowledge, the effect of inulin on digesta sulfide concentrations has not been reported, although Sakai et al. (7) observed an increased soluble iron concentration in the colon of rats fed 7.5% short-chain FOS. The increased solubility of iron in colon digesta would promote absorption of iron if mineral absorption takes place in the large intestine (7,16,48). Although it is still a subject of debate as to whether a significant amount of iron can be absorbed in the colon (49), a few recent studies have shown the expression of iron absorption-related genes in the large intestines of rats and mice (50,51). Furthermore, Ohta et al. (48) have reported that dietary inulin supplementation resulted in a positive correlation between apparent calcium absorption and the relative amounts of calbindin (calbindin-D9k) and strongly induced CaBP expression in large intestines of rats. Our group is actively investigating whether inulin can upregulate iron transporter in the colon of pigs.
As sulfide is generated from microbial fermentation (27), the reduced concentration of sulfide in the distal colon digesta may be interpreted as a modified microbial population in the colon of the inulin-fed pigs, leading to an attenuated hydrogen sulfide production (27,52). Consequently, lowering sulfide would reduce its binding to iron (53), leaving more iron soluble or available for possible absorption. Our data are in agreement with Swanson et al. (22) and Flickinger et al. (45) who observed a reduction in fecal hydrogen sulfide and other fecal putrefactive agents (protein fermentative catabolites) in dogs fed FOS. Reduction of such moieties, if verified, would be extremely important in human and companion animal gut health because these subjects may ingest excess protein, and indoles, phenols, and S-containing compounds have large bowel disease implications (27).
Because we did not see an effect of supplemental inulin on fecal or digesta pH, and virtually no effect of supplemental inulin on phytase activity in digesta of various segments at either actual digesta pH or pH 5.5, the inulin-produced improvements in HRE of pigs was not associated with intestinal pH or digesta phytase activity. Reported changes of digesta pH by supplemental inulin or FOS have been controversial. Loh et al. (54) showed an elevated colonic pH in pigs fed 3% inulin, whereas Kleessen et al. (44) observed a decreased cecal and colonic pH in rats fed 5% short or long-chain FOS. Meanwhile, Mikkelsen et al. (55) found no changes of digesta pH in pigs fed 4% FOS. Thus, supplemental inulin or FOS does not always affect digesta pH, and their effect on iron bioavailability is not necessarily associated with lowering intestinal pH. Although stomach digesta had detectable phytase activity at its actual pH, and lower jejunum digesta phytase activity showed an inulin effect at pH 5.5, their activities were low compared with those in colon digesta. Thus, the detected phytase activity in upper gut was due to mainly the plant phytase present in the diet and probably did not have a major impact on iron bioavailability. Clearly, supplemental inulin did not seem to promote phytase-producing microbes in the gastrointestinal tracts of pigs.
In conclusion, our results indicate that supplemental 4% inulin improved utilization of iron intrinsically present in corn and soybean meal by young pigs for hemoglobin synthesis. This positive effect of inulin was associated with deceased concentrations of sulfide and increased concentrations of soluble iron in colon digesta, but not with digesta pH or phytase activity across different segments of the gastrointestinal tracts of pigs. The supplemental inulin concentration used in the present study is close to the tolerable threshold of humans (42), above the level that caused dramatic positive shifts in the composition of microbiota in humans (56), and achievable in staple crops by plant breeding (42). Thus, our findings are highly relevant to improving iron nutrition in anemic population through biofortification. The combined effectiveness of inulin with other approaches in improving iron nutrition merits future research.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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5 Abbreviations used: BD, basal diet; FOS, fructooligosaccharide; Hb, hemoglobin; HRE, hemoglobin repletion efficiency.
Manuscript received 18 May 2006. Initial review completed 29 June 2006. Revision accepted 6 September 2006.
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LITERATURE CITED |
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1. Diet WHO. Nutrition and the prevention of chronic diseases. In: World Health Organization Technical Report Series. Geneva: World Health Organization; 2003.
2. Yip R. The challenge of improving iron nutrition: limitations and potentials of major intervention approaches. Eur J Clin Nutr. 1997;51: Suppl 4:S16–24.
3. Graham R, Welch R, Bouis H. Addressing micronutrient malnutrition through enhancing the nutritional quality of staple foods: principles, perspectives and knowledge gaps. Adv Agron. 2001;70:77–142.
4. Welch RM. Breeding strategies for biofortified staple plant foods to reduce micronutrient malnutrition globally. J Nutr. 2002;132:495S–9S.
5. Delzenne N, Aertssens J, Verplaetse H, Roccaro M, Roberfroid M. Effect of fermentable fructo-oligosaccharides on mineral, nitrogen and energy digestive balance in the rat. Life Sci. 1995;57:1579–87.[Medline]
6. Ohta A, Ohtsuki M, Baba S, Takizawa T, Adachi T, Kimura S. Effects of fructooligosaccharides on the absorption of iron, calcium and magnesium in iron-deficient anemic rats. J Nutr Sci Vitaminol (Tokyo). 1995;41:281–91.[Medline]
7. Sakai K, Ohta A, Shiga K, Takasaki M, Tokunaga T, Hara H. The cecum and dietary short-chain fructooligosaccharides are involved in preventing postgastrectomy anemia in rats. J Nutr. 2000;130:1608–12.
8. van den Heuvel EG, Schaafsma G, Muys T, van Dokkum W. Nondigestible oligosaccharides do not interfere with calcium and nonheme-iron absorption in young, healthy men. Am J Clin Nutr. 1998;67:445–51.[Abstract]
9. Coudray C, Bellanger J, Castiglia-Delavaud C, Remesy C, Vermorel M, Rayssignuier Y. Effect of soluble or partly soluble dietary fibres supplementation on absorption and balance of calcium, magnesium, iron and zinc in healthy young men. Eur J Clin Nutr. 1997;51:375–80.[Medline]
10. Delzenne NM. Oligosaccharides: state of the art. Proc Nutr Soc. 2003;62:177–82.[Medline]
11. Fishbein L, Kaplan M, Gough M. Fructooligosaccharides: a review. Vet Hum Toxicol. 1988;30:104–7.[Medline]
12. Coudray C, Feillet-Coudray C, Tressol JC, Gueux E, Thien S, Jaffrelo L, Mazur A, Rayssiguier Y. Stimulatory effect of inulin on intestinal absorption of calcium and magnesium in rats is modulated by dietary calcium intakes short- and long-term balance studies. Eur J Nutr. 2005;44:293–302.[Medline]
13. Griffin I, Hicks P, Heaney R, Abrams S. Enriched chicory inulin increases calcium absorption mainly in girls with lower calcium absorption. Nutr Res. 2003;23:901–9.
14. Lopez HW, Coudray C, Levrat-Verny MA, Feillet-Coudray C, Demigne C, Remesy C. Fructooligosaccharides enhance mineral apparent absorption and counteract the deleterious effects of phytic acid on mineral homeostasis in rats. J Nutr Biochem. 2000;11:500–8.[Medline]
15. Morohashi T, Sano T, Ohta A, Yamada S. True calcium absorption in the intestine is enhanced by fructooligosaccharide feeding in rats. J Nutr. 1998;128:1815–8.
16. Ohta A, Baba S, Takizawa T, Adachi T. Effects of fructooligosaccharides on the absorption of magnesium in the magnesium-deficient rat model. J Nutr Sci Vitaminol (Tokyo). 1994;40:171–80.[Medline]
17. Younes H, Coudray C, Bellanger J, Demigne C, Rayssiguier Y, Remesy C. Effects of two fermentable carbohydrates (inulin and resistant starch) and their combination on calcium and magnesium balance in rats. Br J Nutr. 2001;86:479–85.[Medline]
18. Ohta A, Ohtsuki M, Uehara M, Hosono A, Hirayama M, Adachi T, Hara H. Dietary fructooligosaccharides prevent postgastrectomy anemia and osteopenia in rats. J Nutr. 1998;128:485–90.
19. Campbell JM, Fahey GC, Jr., Wolf BW. Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. J Nutr. 1997;127:130–6.
20. Mikkelsen L, Knudsen K, Jensen B. In vitro fermentation of fructo-oligosaccharides and transgalacto-oligosaccharides by adapted and unadapted bacterial populations from the gasterointestinal tract of piglets. Anim Feed Sci Technol. 2004;116:225–38.
21. Sghir A, Chow JM, Mackie RI. Continuous culture selection of bifidobacteria and lactobacilli from human faecal samples using fructooligosaccharide as selective substrate. J Appl Microbiol. 1998;85:769–77.[Medline]
22. Swanson KS, Grieshop CM, Flickinger EA, Bauer LL, Chow J, Wolf BW, Garleb KA, Fahey GC, Jr. Fructooligosaccharides and Lactobacillus acidophilus modify gut microbial populations, total tract nutrient digestibilities and fecal protein catabolite concentrations in healthy adult dogs. J Nutr. 2002;132:3721–31.
23. Grasten S, Pajari A, Likkonen K, Karppinen S, Mykkanen H. Fibers with different solubility characteristics alter similarly the metabolic activity of intestinal microbiota in rats fed cereal brands and inulin. Nutr Res. 2002;22:1435–44.
24. Gibson G, Beatty E, Wang X, Cummings J. Selective Stimulation of Bifidobacteria in the Human Colon by Oligofructose and Inulin. Gastroenterology. 1995;108:975–82.[Medline]
25. Mikkelsen LL, Bendixen C, Jakobsen M, Jensen BB. Enumeration of bifidobacteria in gastrointestinal samples from piglets. Appl Environ Microbiol. 2003;69:654–8.
26. Wang X, Gibson GR. Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J Appl Bacteriol. 1993;75:373–80.[Medline]
27. Magee EA, Richardson CJ, Hughes R, Cummings JH. Contribution of dietary protein to sulfide production in the large intestine: an in vitro and a controlled feeding study in humans. Am J Clin Nutr. 2000;72:1488–94.
28. Stahl CH, Han YM, Roneker KR, House WA, Lei XG. Phytase improves iron bioavailability for hemoglobin synthesis in young pigs. J Anim Sci. 1999;77:2135–42.
29. Lopez HW, Coudray C, Bellanger J, Younes H, Demigne C, Remesy C. Intestinal fermentation lessens the inhibitory effects of phytic acid on mineral utilization in rats. J Nutr. 1998;128:1192–8.
30. Hurrell RF, Reddy MB, Juillerat MA, Cook JD. Degradation of phytic acid in cereal porridges improves iron absorption by human subjects. Am J Clin Nutr. 2003;77:1213–9.
31. Miller ER, Ullrey DE. The pig as a model for human nutrition. Annu Rev Nutr. 1987;7:361–82.[Medline]
32. NRC. Nutrition requirements of swine, 10th ed. Washington (DC): National Academy Press; 1998.
33. Eppard PJ, Bauman DE, Bitman J, Wood DL, Akers RM, House WA. Effect of dose of bovine growth hormone on milk composition: alpha-lactalbumin, fatty acids, and mineral elements. J Dairy Sci. 1985;68:3047–54.
34. Quemer B, Thibault JF, Coussement P. Determineration of inulin and oligofructose in food products, integration in the AOAC method for measurement of total dietary fibre. Lebensm Wiss-Technol. 1994;27:125–32.
35. Miller J. Assessment of dietary iron availability by rat Hb repletion assay. Nutr Rep Int. 1982;26:993–1005.
36. Stookey L. Ferrozine-a new spectrophotometric reagent for iron. Anal Chem. 1970;42:779–81.
37. Simpson SL. A rapid screening method for acid-volatile sulfide in sediments. Environ Toxicol Chem. 2001;20:2657–61.[Medline]
38. Jeffery G, Bassett J, Mendham J, Denney R. Vogel's textbook of quantitative analysis of chemical analysis., 9th ed. Essex, England: Longman Scientific & Technical; 1989.
39. Cline J. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr. 1969;14:454–8.
40. Kim TW, Lei XG. An improved method for a rapid determination of phytase activity in animal feed. J Anim Sci. 2005;83:1062–7.
41. Gill JL. Repeated measurement: sensitive tests for experiments with few animals. J Anim Sci. 1986;63:943–54.
42. Briet F, Achour L, Flourie B, Beaugerie L, Pellier P, Franchisseur C, Bornet F, Rambaud JC. Symptomatic response to varying levels of fructo-oligosaccharides consumed occasionally or regularly. Eur J Clin Nutr. 1995;49:501–7.[Medline]
43. Moshfegh AJ, Friday JE, Goldman JP, Ahuja JK. Presence of inulin and oligofructose in the diets of Americans. J Nutr. 1999;129:1407S–11S.[Medline]
44. Kleessen B, Hartmann L, Blaut M. Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. Br J Nutr. 2001;86:291–300.[Medline]
45. Flickinger EA, Schreijen EM, Patil AR, Hussein HS, Grieshop CM, Merchen NR, Fahey GC, Jr. Nutrient digestibilities, microbial populations, and protein catabolites as affected by fructan supplementation of dog diets. J Anim Sci. 2003;81:2008–18.
46. Coudray C, Tressol JC, Gueux E, Rayssiguier Y. Effects of inulin-type fructans of different chain length and type of branching on intestinal absorption and balance of calcium and magnesium in rats. Eur J Nutr. 2003;42:91–8.[Medline]
47. Smiricky MR, Grieshop CM, Albin DM, Wubben JE, Gabert VM, Fahey GC, Jr. The influence of soy oligosaccharides on apparent and true ileal amino acid digestibilities and fecal consistency in growing pigs. J Anim Sci. 2002;80:2433–41.
48. Ohta A, Motohashi Y, Ohtsuki M, Hirayama M, Adachi T, Sakuma K. Dietary fructooligosaccharides change the concentration of calbindin-D9k differently in the mucosa of the small and large intestine of rats. J Nutr. 1998;128:934–9.
49. Roberfroid M. Inulin-type fructas: functional food ingredients. Boca Raton (FL): CRC Press; 2005.
50. Johnston KL, Johnson DM, Marks J, Srai SK, Debnam ES, Sharp PA. Non-haem iron transport in the rat proximal colon. Eur J Clin Invest. 2006;36:35–40.[Medline]
51. Takeuchi K, Bjarnason I, Laftah AH, Latunde-Dada GO, Simpson RJ, McKie AT. Expression of iron absorption genes in mouse large intestine. Scand J Gastroenterol. 2005;40:169–77.[Medline]
52. Gibson G, Cummings J, Macfarlane G. Growth and activities of sulphate-reducing bacteria in gut contents of healthy subjects and patients with ulcerative colitis. FEMS Microbiol Lett. 1991;86:103–11.
53. Rickard D. Kinetics of FeS precipitation: Part 1. Competing reaction mechanisms. Geochim Cosmochim Acta. 1995;59:4367–79.
54. Loh G, Eberhard M, Brunner RM, Hennig U, Kuhla S, Kleessen B, Metges CC. Inulin alters the intestinal microbiota and short-chain Fatty Acid concentrations in growing pigs regardless of their basal diet. J Nutr. 2006;136:1198–202.
55. Mikkelsen LL, Jakobsen M, Jensen BB. Effects of dietary oligosaccharides on microbial diversity and fructo-oligosaccharides on microbial diversity and fructo-oligosaccharide degrading bacteria in faeces of pigs post-weaning. Anim Feed Sci Technol. 2003;109:133–50.
56. Niness KR. Inulin and oligofructose: what are they? J Nutr. 1999;129:1402S–6S.
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