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Unité des Maladies Métaboliques et Micro-nutriments,
*
Unité des Métabolismes Energétique et Lipidique, Centre de Recherche en Nutrition Humaine d’Auvergne, INRA, Centre de Recherche de Clermont-Ferrand/Theix, Champanelle, France,
Roquette Frères, Lestrem Cedex, France and
Laboratoire de Nutrition Humaine, Centre de Recherche en Nutrition Humaine d’Auvergne, Clermont-Ferrand, France
1To whom correspondence should be addressed. E-mail: coudray{at}clermont.inra.fr
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • calcium • magnesium • fermentation • polyol carbohydrates • mineral balance
There is now overwhelming evidence that low digestible carbohydrates are a necessary component of human and animal diets and play an important role in human health (1
). Recently, attention has increasingly focused on fermentable carbohydrates, and more especially on fermentable polyols (sugar alcohols), currently used in various agro-food industries (2
). Polyols, low digestible carbohydrates, are almost completely degradable in the large intestine by fermentation. Polyols are key food ingredients because they permit the development of sugar-free confectionery, which offers the benefits of noncariogenicity, reduced energy intake and low glycemia. Increasing not only dietary intake of Ca and Mg, but also their intestinal absorption, is of great interest for different categories of populations at risk of deficiency such as postmenopausal women, the elderly and diabetics (3
). In previous animal studies, we showed that fermentable carbohydrates enhanced Ca and Mg absorption (4
). This observation was recently confirmed by other authors (5
). Moreover, the polyols, maltitol, lactitol and isomalt, were shown to enhance mineral bioavailability in rats (6
). To date, no human data reporting the effect of polyols on mineral bioavailability are available. As part of a larger project concerning the effects of dietary fiber in human nutrition, we studied the consequences of an increased intake of two polyols. The criteria used were food tolerance, stool characteristics, nutrient digestibility, energy metabolism (7
) and mineral balance. Here, we report the results of the ingestion of these polyols on the apparent absorption and the balance of Ca and Mg.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Nine healthy young men with no medical history of renal, vascular, digestive, endocrine or currently evolving disease were enlisted after a normal physical examination. The subject characteristics were as follows (means ± SEM): age, 20.0 ± 0.5 y; weight, 68.4 ± 2.7 kg; height, 1.76 ± 0.02 m; body mass index, 22.1 ± 0.5 kg/m2; lean mass, 58.5 ± 2.1 kg. Each subject received a complete explanation of the purpose and procedures of the investigation and signed an informed consent form. The study protocol was approved by the regional Medical Faculty Ethical Committee (CCPPRB no. AU205). The subjects had lunch and dinner at the Human Nutrition Laboratory throughout the control period. Breakfasts were provided that consisted of 20 g sweetened instant cocoa powder, 280 g semiskimmed milk, 65 g sandwich loaf bread, 10 g butter and 60 g jam. In addition, the volunteers were given a 70 g milk roll for a snack. Extra food items such as alcoholic and energy-containing beverages were not allowed.
Experimental design.
The subjects were offered three diets according to a Latin-square design (3 x 3) with three repetitions. Each experimental period comprised 32 d, starting with a daily progressive adaptation to a maximum of 100 g dry matter per day of the tested products (until d 18) followed by 14 d with a constant intake of the tested products. Duplicate meals were prepared by a staff member for each day of the experimental balance periods, including breakfast and snacks. The balance period involved food intake determination and total collection of feces and urine. Duplicate meals and all individual leftovers were homogenized, freeze-dried and analyzed separately. Urine and feces was collected during the last 10 d of each experimental period. The collected urine per subject was pooled and representative samples were saved in acid-washed bottles and stored at -18°C until analysis. Feces were collected in plastic pots, stored at -18°C, pooled, homogenized, freeze-dried and stored at -18°C until analysis.
Experimental diets.
Four daily balanced menus were distributed in rotation to subjects during each balance period (Table 1
). The planned macro- and micronutrients contents of the offered diets corresponded to nutritional recommendations. The estimated energy intake from these diets was between 12.0 and 12.5 MJ/d, including the tested products. The tested products were provided by the Roquette Frères Company (Lestrem, France). The maltitol syrup Lycasin®HBC (LHBC2 diet) consisted of 50% of maltitol and 50% of a hydrogenated polysaccharide fraction of Lycasin®HBC (HPFL diet); the latter was also tested. In this study, the tested products were diluted in water and offered in six equal doses at breakfast (1000 h), lunch (1600 h) and dinner (2200 h) to prevent a bulky input of fermentable carbohydrates in the large intestine. Information on food tolerance and net energy value of these products and their impact on nutrient digestive utilization may be found in Sinaud et al. (7
).
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Food intake was monitored by collection of duplicate meals by the laboratory staff. Composite samples of food were prepared using metal-free materials. About 0.5 g of tested products or diets or 0.25 g of feces were dry-ashed at 500°C for 10 h and the dry residue was added to HCl (6 mol/L), diluted adequately and analyzed for Ca and Mg. Urine was analyzed directly with dilution in 1 g/L of lanthanum chloride solution. Ca and Mg were assayed by flame atomic absorption spectrometry (Perkin-Elmer 560, Paris, France) with an air-acetylene flame and hollow cathode lamps at wavelengths 422 and 285 nm, respectively. Mineral levels were calculated from standard curves of mineral solutions (Merck, Lyon, France). Analytical quality was checked using total diet control standards (NIST) for dietary mineral measurements, home constructed human feces for fecal mineral measurements and Seronorm® urine (Nycomed, Oslo, Norway) for urinary mineral measurements. The Ca measurements were 102 ± 2, 97 ± 4 and 99 ± 3% of certified values for these three quality controls. The Mg measurements were 101 ± 3, 98 ± 2 and 99 ± 4% of certified values for the three quality controls. All measurements were performed at least in duplicate. Cecal short-chain fatty acid (SCFA) levels were determined by gas-liquid chromatography (8
).
Calculations.
Absolute apparent absorption (mg/d) was calculated as follows: daily mineral intake - daily mineral fecal excretion. Relative apparent absorption (%) was calculated as follows: 100 x [(daily mineral intake - daily mineral fecal excretion)/(daily mineral intake)]. Mineral retention (mg/d) was calculated as follows: (daily mineral intake) - (daily mineral fecal excretion + daily mineral urinary excretion).
Statistical analysis.
Data were analyzed statistically according to a Latin-square design (3 x 3) with three repetitions. Comparisons between experimental diets were made by ANOVA using the general linear model procedure of Statistical Analysis Systems (9
), according to the following model: µ + 
diet + ß repetition + 
subject + 
. For each experimental treatment, the data are presented as adjusted means ± adjusted SEM. Differences were considered significant at P < 0.05.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Total daily Ca intake was from 1200 to 1300 mg for each of the three experimental periods. The tap water Ca concentration was 0.62 mmol/L, the consumption of which represented about 2.5% of daily Ca intake. Ca fecal excretion was similar in all three treatments and varied from 840 to 860 mg/d. Consequently, both absolute (mg/d) and relative (%) apparent Ca absorptions were unaffected by diet treatment. The relative apparent absorption of Ca was between 32 and 37%. Neither daily Ca urinary excretion (
180 mg) nor daily Ca retention (230 mg) differed among the three experimental treatments.
Magnesium.
Total daily Mg intake was from 320 to 330 mg for each of the three experimental periods. The tap water Mg concentration was 0.37 mmol/L, the consumption of which represented about 5% of total Mg intake. Mg fecal excretion was lower when the polyols were consumed than when dextrose was consumed (Table 2
). Consequently, both relative and absolute apparent Mg absorptions were greater after ingestion of HPFL and relative apparent absorption was greater after intake of LHBC than after dextrose intake (Table 2)
. Eight out of nine subjects had higher apparent Mg absorption when fed the HPFL diet than when fed the control diet, and six of nine subjects had higher apparent Mg absorption when fed the LHBC diet than when fed the control diet. This improvement in apparent Mg absorption was accompanied by a significant increase in Mg urinary excretion when given the LHBC treatment (Table 2)
.
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). This study design mimics consumption of confectionery and avoids possible adverse effects. Both studied products were accepted by the volunteers with no difficulty. The main result of this work was that these polyols significantly improved apparent Mg absorption, whereas the intestinal absorption and balance of Ca were not altered.
Since 1977 the potential beneficial effects of fermentable carbohydrates on mineral absorption and status, in particular Ca and Mg, have been largely investigated by our group (10
,11
) and by other workers (5
,12
). The animal studies clearly showed a beneficial effect of fermentable carbohydrates on intestinal absorption of Ca and Mg, although this effect is less marked for Ca than for Mg and often depends on experimental conditions.
The positive effect of fermentable carbohydrates on intestinal mineral absorption is attributed mainly to the high production of SCFA (13
), which produces a decrease in the luminal pH and an increase in the concentration of ionized minerals in the cecum. Consequently, the mineral solubility is increased and the active and passive diffusion of minerals across the intestinal cells is enhanced. As a consequence, these fermentation-induced changes theoretically ought to improve the intestinal absorption of nearly all minerals in the hindgut. However, in this study, apparent Mg absorption was increased, whereas that of Ca was unchanged. The intestinal absorption mechanism and site of Mg largely differ from those of Ca, which may explain the different impact of fermentable carbohydrates on the apparent absorption of these two minerals.
The absorption efficiency of dietary Ca depends on two major factors: its regulation by physiological factors including hormones and its interaction with the other dietary constituents (14
). A possible explanation for the lack of an effect of fermentable carbohydrates on Ca intestinal absorption in this study is downregulation of its active intestinal absorption in the upper part of intestine after several weeks of fermentable carbohydrate intake (15
). We speculate that fermentable carbohydrate feeding increased Ca intestinal absorption in the lower parts of the intestine, but fermentable carbohydrate feeding for several weeks may result in a "feedback" effect decreasing Ca intestinal absorption in the high parts of the intestine. Experimental data obtained from rat studies seem to confirm such an adaptation effect. Chonan and Watanuki (16
) noted that galacto-oligosaccharide supplementation increased apparent Ca absorption in ovariectomized rats at the beginning (9 d) but not at the end of their experiment at 28 d. In human studies fructo-saccharides and lactulose increased intestinal Ca absorption in adolescent and postmenopausal women when the supplementation lasted only 9 d (17
,18
), whereas other studies conducted in adults showed no effect after a 21-d supplementation (19
,20
). Lack of an effect on the absorption of Ca is also likely attributable to the status and requirement of the subjects; this is more probably attributable to a higher requirement or less feedback than to the longer duration of the treatment in men.
Intestinal Mg absorption occurs mainly in the lower parts of the intestine, especially in the jejunum and ileum (21
). The mechanisms involved in intestinal Mg absorption are a saturable process and passive diffusion. The component of intestinal Mg absorption from the distal part of the intestine by passive diffusion is very large. The results of this study clearly showed a significant increase in the relative apparent Mg absorption during the consumption of both fermentable polyols. This was accompanied by an increase in urinary Mg excretion during LHBC intake, in which the kidney is the organ that most closely regulates Mg metabolism. This increase confirms the positive effect of fermentable carbohydrates on apparent Mg absorption. In previous work in which chemical balance was employed, we showed that 40 g/d of inulin tended to increase apparent Mg absorption in young men by 10% (22
).
Recently, in an isotopic study, we showed that short-chain oligosaccharides increased intestinal Mg absorption in postmenopausal women (12%) (23
). Van den Heuvel (24
) investigated the effect of 15 g/d of FOS consumption, for 9 d, on Mg absorption in adolescents by measurement of urinary excretion of orally administered 25Mg. Moreover, this study failed to show an effect of FOS, although the observed increase in urinary excretion of 25Mg was 18% after FOS ingestion. To our knowledge, this is the first time that such a beneficial effect of a sugar alcohol on apparent Mg absorption has been demonstrated in humans.
In conclusion, a significant positive effect of two low digestible fermentable carbohydrates, LHBC and HPFL, on apparent Mg absorption was demonstrated in this study. The improvement in intestinal Mg absorption may be of special interest for people with large Mg needs or at risk of Mg deficiency. Although both products were without effect on Ca absorption and balance, fermentable carbohydrate feeding may improve intestinal absorption of Ca only in populations who show a high need for this mineral, such as adolescents, or in populations with impaired mineral absorption, such as women during late menopause and older populations. Further human studies are therefore still needed to confirm the effects of these products in other populations.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Manuscript received 25 July 2002. Initial review completed 3 September 2002. Revision accepted 1 October 2002.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1. Briel, F., Achour, L. & Fourié, B. (1995) Les fibres alimentaires. Cah. Nutr. Diét. 30:132-136.
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5. 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]
6. Goda, T., Yamada, M., Takase, S. & Hosoya, N. (1992) Effect of maltitol intake on intestinal calcium absorption in the rat. J. Nutr. Sci. Vitaminol. (Tokyo) 38:277-286.
7. Sinaud, S., Montaurier, C., Wils, D., Vernet, J., Brandolini, M., Bouteloup-Demange, C. & Vermorel, M. (2002) Net energy value of two low-digestible polysaccharides (Lycasin®HBC) and the hydrogenated polysaccharide constituant of Lycasin®HBC in healthy human subjects and their impact on nutrient digestive utilisation. Br. J. Nutr. 87:131-139.[Medline]
8. Demigne, C., Remesy, C. & Rayssiguier, Y. (1980) Effects of fermentable carbohydrates on volatile fatty acids (VFA), ammonia and mineral absorption in the rat caecum. Reprod. Nutr. Dévelop. 20:1351-1359.
9. SAS Institute Inc. (1988) SAS/STAT User’s Guide, Release 6.03 1988 SAS Institute Cary, NC.
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11. Lopez, W. H., Coudray, C., Bellanger, J., Younes, H., Demigne, C. & Remesy, C. (1998) Intestinal fermentation lessens the inhibitory effects of phytic acid on mineral utilization in rats. J. Nutr. 128:1192-1198.
12. Ohta, A., Ohtsuki, M., Baba, S., Adachi, T., Sakata, T. & Sakaguchi, E. (1995) Calcium and magnesium absorption from the colon and rectum are increased in rats fed fructo-oligosaccharides. J. Nutr. 125:2417-2424.
13. Lutz, T. & Scharrer, E. (1991) Effect of short-chain fatty acids (SCFA) on calcium absorption by the rat colon. Exp. Physiol. 76:615-618.[Abstract]
14. Bronner, F. (1998) Calcium absorption: a paradigm for mineral absorption. J. Nutr. 128:917-920.
15. Bronner, F., Pansu, D. & Stein, W. D. (1986) An analysis of intestinal calcium transport across the rat intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 250:G561-G569.
16. Chonan, O. & Watanuki, M. (1995) Effect of galactooligosaccharides on calcium absorption in rats. J. Nutr. Sci. Vitaminol. (Tokyo) 41:95-104.
17. Van den Heuvel, E. G., Muys, T., Van Dokkum, W. & Schaafsma, G. (1999a) Lactulose stimulates calcium absorption in postmenopausal women. J. Bone Miner. Res. 14:1211-1216.[Medline]
18. Van den Heuvel, E. G., Muys, T., van Dokkum, W. & Schaafsma, G. (1999b) Oligofructose stimulates calcium absorption in adolescents. Am. J. Clin. Nutr. 69:544-548.
19. Van den Heuvel, E. G., Schaafsma, G., Muys, T. & van Dokkum, W. (1998) Nondigestible oligosaccharides do not interfere with calcium and nonheme-iron absorption in young, healthy men. Am. J. Clin. Nutr. 67:445-451.[Abstract]
20. Barclay, D., Kastenmayer, P., Couzy, F., Mettraux, C., Clough, J., Vigo, M. & Rochat, F. (2000) Effect of fructooligosacchrides on calcium absorption in healthy men. Abstract presented on the occasion of 4th International Symposium on Nutritional Aspects of Osteoporosis, May 17–20, Lausanne, Switzerland 2000.
21. Brink, E. J. & Beynen, A. C. (1992) Nutrition and magnesium absorption: a review. Prog. Food Nutr. Sci. 16:125-162.[Medline]
22. Coudray, C., Bellanger, J., Castiglia-Delavaud, C., Remesy, C., Vermorel, M. & Rayssiguier, Y. (1997) 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. 51:375-380.[Medline]
23. Tahiri, M., Tressol, J. C., Arnaud, J., Bornet, F., Bouteloup-Demange, C., Feillet-Coudray, C., Ducros, V., Pepin, D., Brouns, F., Roussel, A. M., Rayssiguier, Y. & Coudray, C. (2001) Five week intake of short-chain fructo-oligosaccharides increases intestinal absorption and status of magnesium in postmenopausal women. J. Bone Miner. Res. 16:2152-2160.[Medline]
24. 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 The Netherlands.
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