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Unité Maladies Métaboliques et Micronutriments, Centre de Recherche en Nutrition Humaine d’Auvergne, Centre de Recherche INRA Clermont-Ferrand/Theix, F-63122 Saint Genès Champanelle, France
2To whom correspondence should be addressed. E-mail: coudray{at}clermont.inra.fr.
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ABSTRACT |
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 TOP ABSTRACT Effects of Dietary Fibers...Absorption and Homeostasis of...Effect of Fermentable...How Do Fermentable Carbohydrates...Effect of Fermentable...Conclusion.LITERATURE CITED |
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KEY WORDS: • magnesium • dietary fiber • absorption • fermentation • rats • humans
There is experimental and clinical evidence showing that the amount of magnesium (Mg) in typical Western diets is often insufficient to meet individual needs. Because Mg, the second most abundant intracellular cation, plays an essential role in a wide range of fundamental reactions, it is not surprising that its deficiency in the organism may lead to severe biochemical changes. Increased intake of dietary fiber is now being recommended for good health, and cereals, fruits and vegetables make a major contribution to Mg intake. However, fiber and some of the associated substances have strong in vitro mineral-binding or complexing capacities; hence fiber has been suspected of impairing Mg absorption. Alternatively, there have been many reports indicating that products of fiber fermentation may enhance Mg absorption from the large intestine. Thus, it is important to identify factors that either reduce or improve intestinal Mg absorption. In this review, the effects of fibers on Mg absorption are summarized.
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Effects of Dietary Fibers on Mg Absorption. |
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TOPABSTRACTEffects of Dietary Fibers...Absorption and Homeostasis of...Effect of Fermentable...How Do Fermentable Carbohydrates...Effect of Fermentable...Conclusion.LITERATURE CITED |
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16 g/d (1
). This low fiber intake has been observed in most Western countries, with ranges of 15–20 g/d, whereas a dietary fiber intake of 25–30 g/d is generally advocated, based on epidemiologic, ecologic and ethnogeographic data. This could be achieved by consuming more plant foods and/or possibly by supplementing different foods with fiber concentrates. In staple foods, 50% of the dietary fibers consumed are relatively soluble and fermentable. However, dietary fibers and some associated substances, such as phytate, have in vitro mineral-binding capacities and may thus alter mineral bioavailability. Recently, attention has been focused on fermentable poly- or oligosaccharides; the latter are used in various industrial food products for both structural proprieties and potential health effects.
Earlier work suggested that diets rich in dietary fibers might have unfavorable effects on mineral absorption (2
–4
). However, the data reported must be interpreted in their specific context. For example, the widely cited work (2
) reporting that Bazari bread consumption significantly decreased Mg absorption and balance in humans was based on only two subjects, and the negative Mg balance was due mainly to high urinary Mg excretion. It must be noted that the Bazari bread diet contained, in addition to the insoluble fibers, high amounts of phytate and phosphorus, liable to impair Mg absorption. Another study (3
) reported that the consumption of Mg-rich oat bran decreased fractional Mg absorption, whereas net Mg absorption was significantly increased, without significant changes in Mg balance. Purified fiber ingestion (cellulose or carboxymethyl-cellulose) decreased the Mg balance only nonsignificantly (4
), whereas the control diet was supplemented with 200 mg Mg/d to satisfy the dietary Mg recommendation. The supplemental Mg was likely to be more available than the dietary Mg present in the fiber diet, which might explain in part the results obtained. More recently, the effects of sugar beet fiber on Mg absorption and balance in healthy young men were examined (5
). This fiber concentrate did not reduce Mg absorption, urinary Mg excretion or Mg balance. From the studies conducted during the last 20 years, it is clear that the observed effects of fibers on mineral absorption depend largely 1) on the nature of the fibers (soluble/insoluble, fermentable/nonfermentable); 2) on the amount of dietary fibers; 3) especially on the presence of associated components in the diet such as phytates; 4) and on the homeostasis of concerned minerals.
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Absorption and Homeostasis of Mg. |
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TOPABSTRACTEffects of Dietary Fibers...Absorption and Homeostasis of...Effect of Fermentable...How Do Fermentable Carbohydrates...Effect of Fermentable...Conclusion.LITERATURE CITED |
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). This conclusion could be drawn independently of the experimental methods used, diet, age or Mg status. Some studies showed that Mg absorption is related to the luminal Mg concentration in a curvilinear fashion. This has been interpreted to reflect the presence of a transcellular, saturable absorptive process. However, there is a direct correlation between Mg absorption and the luminal or dietary Mg levels (7
). The saturable absorptive process seems thus to function only at very low dietary Mg intakes. At usual Mg intakes, Mg absorption occurs primarily by intercellular diffusional and solvent drag mechanisms (8
). Mg absorption in animal and humans may vary between 35 and 70% of Mg intake.
The main mechanism of Mg homeostasis takes place at the renal level (9
). During Mg deprivation, the kidney avidly conserves the body Mg. Conversely, when excess Mg is taken, it is rapidly excreted into the urine. That is why Mg absorption is loosely regulated. In kidneys, the main site of Mg reabsorption is the proximal tubule and thick ascending limb of Henle’s loop, which reabsorb 70% of the filtered Mg. The excretory side of Mg balance involves appropriate changes in renal Mg handling. Despite the extensive capacities of regulation of Mg homeostasis by the kidneys, no hormone or factor appears to be responsible for renal Mg homeostasis.
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Effect of Fermentable Carbohydrates on Mg Absorption in Animals. |
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TOPABSTRACTEffects of Dietary Fibers...Absorption and Homeostasis of...Effect of Fermentable...How Do Fermentable Carbohydrates...Effect of Fermentable...Conclusion.LITERATURE CITED |
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). Subsequently, different types of fermentable carbohydrates (RS, OS, lactulose, hydrocolloids and pectin) were investigated throughout the world (11
–20
). All of these studies have confirmed the beneficial effect of such carbohydrates on Mg absorption in rats. RS in particular has been investigated for its effects on Mg absorption. RS is defined as the sum of starches and products of starch degradation that escape small intestinal digestion and reach the large bowel (21
). They are classified into four main types: physically inaccessible starch (RS1), native resistant granules and high amylose starches (RS2), retrograded starches (RS3) and chemically modified starches (RS4). Daily RS intake generally ranges between 5 and 10 g (22
). There have been only a few investigations of the effects of RS on Mg absorption, and these concern RS2 or RS3 in particular. The first study (10
) explored the effects of raw potato resistant starch (RS) on Mg absorption in rats. Both relative and net Mg absorption values were significantly higher in the RS group than in controls, in parallel with an enlarged cecum and greater short-chain fatty acid (SCFA) production than in control rats. This was accompanied by a significant acidification of cecal pH and a greater degree of cecal Mg solubilization. A series of investigations showed that RS, together with an enlargement of the cecum and enhanced SCFA production, significantly increased Mg absorption and counteracted the inhibitory effects of phytic acid when present in the diets as pure compound or in phytic acid-rich foods (13
,14
,23
–25
). Other investigators have also investigated this issue and have shown that RS2, but not retrograded resistant starch (RS3), raised apparent Mg absorption in rats (17
,26
). All of these studies showed clearly that RS and in particular RS2 increases Mg absorption in rats.
Another important family of fermentable carbohydrates are inulin-type fructans and many types of OS. They are natural food compounds, commonly found in varying amounts in cereals, chicory, artichokes and onions; some of the OS may also be of synthetic origin. Human consumption of these compounds varies between 3 and 10 g/d (27
). They have been studied extensively in the last decade for their potential beneficial effects on mineral metabolism, particularly Ca and Mg. One study determined the effect of different doses of inulin and the production of SCFA and mineral accumulation in the rat cecum (12
). Then, the effect of different dietary levels of Ca on the cecal fermentation intensity of inulin (5–20%) was examined in rats (26
). Recently, the fermentation effect of 3-wk consumption of inulin (10%) on the inhibitory action of phytic acid on mineral utilization was studied in rats (14
). Finally, the effects of raw potato starch, inulin and their combination on Ca and Mg balance were compared in rats (24
). In all of these studies, the rats fed the inulin diet showed a significant cecal hypertrophy and an accumulation of SCFA, low cecal pH and greater cecal blood flow, together with enhanced cecal Mg absorption and significantly improved Mg absorption and balance.
Different OS, including fructo-OS (FOS), galacto-OS and lactitol-OS, have also been studied for their effects on Mg absorption. Delzenne et al. (18
) compared the effect of inulin and oligofructose (OF) on mineral, nitrogen and energy digestive balance in rats. They found that OF increased Mg absorption by 68%. More recently, the effects of inulin and OF and their combination were compared on mineral absorption and balance (16
). OF increased Mg absorption by 46%, whereas the combination with inulin was slightly more efficient with an increase of 57% compared with controls. They showed that FOS feeding increased Mg absorption from the colon and rectum in rats (20
). Ohta et al. (28
) also showed that FOS increased further Mg absorption in Mg-deficient rats. To identify the segment of lumen in which FOS affects Mg absorption, they performed a mineral-balance study using cecectomized rats (29
). The FOS-diet lowered the luminal pH in the cecum and colon in the sham-operated rats, as well as colonic pH in cecectomized rats. The FOS diet increased the absorption of both Ca and Mg in the sham-operated rats, but in the cecectomized rats, only Mg absorption was enhanced by FOS, whereas Ca absorption was unchanged.
The high isotonicity due to the presence of small sugars, such as lactose and lactulose, may increase the intercellular permeability and facilitate Mg absorption in the jejunum and ileum. A large proportion of lactose reaches the colon and is fermented by the microflora. Lactulose shares with lactose the characteristic of being poorly digestible and fermentable. It was shown that feeding 10% lactulose elicited a marked enlargement of the cecum, a drop in cecal pH and an increase in the SCFA pool in rats (11
). Replacement of glucose by lactose or lactulose (100 g/kg) significantly stimulated apparent Mg absorption in rats (30
). Lactose or lactulose vs. glucose lowered the pH of the ileal lumen. There was a negative relationship between ileal pH and apparent absorption of Mg. It is suggested that lactose- or lactulose-induced stimulation of Mg absorption in rats is caused, to a large extent, by a lowering of ileal pH. However, because lactose is partly digestible, it is generally less effective than lactulose or other indigestible fermentable carbohydrates.
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How Do Fermentable Carbohydrates Increase Mg Absorption? |
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TOPABSTRACTEffects of Dietary Fibers...Absorption and Homeostasis of...Effect of Fermentable...How Do Fermentable Carbohydrates...Effect of Fermentable...Conclusion.LITERATURE CITED |
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). A second possible mechanism is that SCFA contribute directly to the enhancement of Mg absorption via a cation exchange mechanism, as proposed for Ca in the form of calcium acetate (31
). Kashimura et al. (19
) examined the effect of adding various organic acids to the mucosal fluid in vitro, using a rat hindgut segment. The addition of acetic acid and butyric acid actually enhanced the intestinal uptake of Ca, Mg and phosphorus. It was postulated that SCFA can stimulate the flux of Mg2+ ions in the mucosal to serosal direction most probably by activation of an apical Mg2+/2H+ antiporte through the provision of protons within the epithelial cell (32
). Among the SCFA tested, n-butyrate was more effective in stimulating Mg (2
) flux than acetate, propionate or isobutyrate. The question that should now be addressed is: what are the possible molecular changes that may accompany the ingestion of fermentable carbohydrates at the level of the intestinal cell? |
Effect of Fermentable Carbohydrates on Mg Absorption in Humans. |
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TOPABSTRACTEffects of Dietary Fibers...Absorption and Homeostasis of...Effect of Fermentable...How Do Fermentable Carbohydrates...Effect of Fermentable...Conclusion.LITERATURE CITED |
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). Daily Mg intake, Mg absorption, urinary Mg and Mg balance did not differ between the groups. However, Mg absorption, urinary Mg excretion and Mg balance tended to increase (+8 to 10%) when the subjects consumed the inulin diet. In another study, administration of 15 g of FOS (Raftilose P95%) for 9 d in 12 adolescents increased urinary excretion of the stable isotope 25Mg by 18% (33
). However, this result did not differ significantly from the control group.
More recent studies have shown a positive effect of fermentable carbohydrates on Mg absorption in postmenopausal women and in adult men. The first study investigated the effect of short-chain FOS on the absorption and status of Mg in postmenopausal women, using stable isotopes (34
). In that study, ingestion of a moderate dose of FOS (10 g/d) for 5 wk resulted in a significant increase in Mg absorption (+12%). Although urinary Mg was also increased, the body isotope retention was greater with FOS treatment than with placebo treatment. In another study, the effect of feeding 100 g/d of maltitol syrup or its hydrogenated polysaccharide fraction on the apparent absorption and balance of Mg was investigated in healthy young men, using the chemical balance technique. Both products significantly increased Mg absorption in the subjects (35
). We also studied the effect of feeding 100 g/d of DOS 6, a fermentable pectin, on the apparent absorption and balance of Mg in healthy young men, using the chemical balance technique. Ingestion of this carbohydrate for 4 wk increased Mg absorption by 47% compared with the placebo group (unpublished data). The principal results of these studies are shown in Table 1
. They indicate that, overall, fermentable carbohydrates can improve Mg absorption in humans. However, the effect must be discussed in the context of the experimental conditions (product dose, experiment duration, studied population) and the balance method applied (classic balance or stable isotope balance). The increase in Mg absorption due to these fermentable carbohydrates is generally accompanied by an increase in urinary Mg excretion. The latter greatly depends on the body Mg store. In spite of this increase in urinary Mg excretion, the overall balance of Mg (Mg retention) was improved in some of these cases.
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Conclusion. |
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TOPABSTRACTEffects of Dietary Fibers...Absorption and Homeostasis of...Effect of Fermentable...How Do Fermentable Carbohydrates...Effect of Fermentable...Conclusion.LITERATURE CITED |
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FOOTNOTES |
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3 Abbreviations used: FOS, fructooligosaccharides; OF, oligofructose; OS, oligosaccharides; RS, resistant starch; SCFA, short-chain fatty acid.
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LITERATURE CITED |
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TOPABSTRACTEffects of Dietary Fibers...Absorption and Homeostasis of...Effect of Fermentable...How Do Fermentable Carbohydrates...Effect of Fermentable...Conclusion.LITERATURE CITED |
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17. Schulz, A. G., Van Amelsvoort, J. M. & Beynen, A. C. (1993) Dietary native resistant starch but not retrograded resistant starch raises magnesium and calcium absorption in rats. J. Nutr. 123:1724-1731.
18. Delzenne, N., Aertssens, J., Verplaetse, H., Roccaro, M. & Roberfroid, M. (1995) Effect of fermentable fructo-oligosaccharides on mineral, nitrogen and energy digestive balance in the rat. Life Sci. 57:1579-1587.[Medline]
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22. Stephen, A. M., Sieber, G. M., Gerster, Y. A. & Morgan, D. R. (1995) Intake of carbohydrate and its components—international comparisons, trends over time, and effects of changing to low-fat diets. [Review]Am. J. Clin. Nutr. 62:851S-867S.
23. Lopez, H. W., Levrat-Verny, M. A., Coudray, C., Besson, C., Krespine, V., Messager, A., Demigné, C. & Rémésy, C. (2001) Class 2 resistant starches lower plasma and liver lipids and improve mineral retention in rats. J. Nutr. 131:1283-1289.
24. Younes, H., Coudray, C., Bellanger, J., Demigné, C., Rayssiguier, Y. & Rémésy, C. (2001) Effects of two fermentable carbohydrates (inulin and resistant starch) and their combination on calcium and magnesium balance in rats. Br. J. Nutr. 86:479-485.[Medline]
25. Heijnen, M. L., van den Berg, G. J. & Beynen, A. C. (1996) Dietary raw versus retrograded resistant starch enhances apparent but not true magnesium absorption in rats. J. Nutr. 126:2253-2259.
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27. Van Loo, J., Coussement, P., de Leenheer, L., Hoebregs, H. & Smits, G. (1995) On the presence of inulin and oligofructose as natural ingredients in the western diet. [Review]Crit. Rev. Food Sci. Nutr. 35:525-552.[Medline]
28. Ohta, A., Baba, S., Takizawa, T. & Adachi, T. (1994) Effects of fructooligosaccharides on the absorption of magnesium in the magnesium-deficient rat model. J. Nutr. Sci. Vitaminol. 40:171-180.
29. Ohta, A., Ohtuki, M., Takizawa, T., Inaba, H., Adachi, T. & Kimura, S. (1994) Effects of fructooligosaccharides on the absorption of magnesium and calcium by cecectomized rats. Int. J. Vitam. Nutr. Res. 64:316-323.[Medline]
30. Heijnen, A. M., Brink, E. J., Lemmens, A. G. & Beynen, A. C. (1993) Ileal pH and apparent absorption of magnesium in rats fed on diets containing either lactose or lactulose. Br. J. Nutr. 70:747-756.[Medline]
31. Trinidad, P. T., Wolever, T. M. S. & Thompson, L. U. (1993) Interactive effects of Ca and short chain fatty acid on absorption in the distal colon of man. Nutr. Res. 13:417-425.
32. Leonhard-Marek, S., Gabel, G. & Martens, H. (1998) Effects of short chain fatty acids and carbon dioxide on magnesium transport across sheep rumen epithelium. Exp. Physiol. 83:155-164.[Abstract]
33. Van den Heuvel, E. G. (1998) Application of Dual Stable Isotope Techniques to Measure Absorption of Calcium, Magnesium and Iron in Man. Doctoral thesis 1998 University of Maastricht Maastricht, The Netherlands.
34. Tahiri, M., Tressol, J. C., Arnaud, J., Bornet, F., Bouteloup-Demange, C., Feillet-Coudray, C., Ducros, V., Pepin, D., Brouns, F., Rayssiguier, A. M. & Coudray, C. (2001) Five week intake of short-chain fructo-oligosaccharides increases intestinal absorption and status of magnesium in post-menopausal women. J. Bone Miner. Res. 16:2152-2160.[Medline]
35. Coudray, C., Bellanger, J., Vermorel, M., Sinaud, S., Wils, D., Feillet-Coudray, C., Brandolini, M., Bouteloup-Demange, C. & Rayssiguier, Y. (2003) Two polyol, low digestible carbohydrates improve apparent absorption of magnesium but not of calcium in healthy young men. J. Nutr. 133(in press).
36. Ellegard, L., Andersson, H. & Bosaeus, I. (1997) Inulin and oligofructose do not influence the absorption of cholesterol, or the excretion of cholesterol, Ca, Mg, Zn, Fe, or bile acids but increases energy excretion in ileostomy subjects. Eur. J. Clin. Nutr. 51:1-5.[Medline]
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