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The Journal of Nutrition Vol. 128 No. 11 November 1998,
pp. 2028-2031
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* School of Food and Nutritional Sciences, The University of Shizuoka, Shizuoka 422-8526, Japan and Department of Food and Nutrition, School of Home Economics, Japan Women's University, Tokyo 112, Japan
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ABSTRACT |
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Abstract
Introduction
Methods
Results
Discussion
References
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Maltitol is a disaccharide alcohol that is produced by hydrogenation of maltose and exhibits resistance to intestinal disaccharidases. We demonstrated previously that maltitol stimulated transepithelial diffusional calcium transfer in the ileum, accompanied by an elevation of intestinal calcium absorption as well as calcium retention in the body. In this study we examined whether the maltitol-induced increase in the diffusional transfer of intestinal calcium absorption leads to an alteration of the physical properties of bones in the weanling rats which exhibit the maximal level of intestinal active calcium absorption. Rat pups were removed from dams at 24 d of age and were fed the diets containing either maltose (control) or maltitol and a requisite amount of calcium (0.52%) for 21 d. Balance studies performed during the final 5-d period showed that maltitol-fed rats had greater calcium retention and calcium absorption. The breaking force of femoral bones was 13% greater in the rats fed the maltitol diet than in controls. The calcium content and dry weight of both femurs and tibias, as well as the bone mineral density of tibias, were elevated in the rats fed the maltitol diet. In a separate experiment, gastric intubation of maltitol-containing diet increased the serum calcium concentration in the portal vein at 2 and 4 h compared to controls. These results indicate that the maltitol-induced increase in the intestinal calcium absorption through paracellular pathway leads to enhancement of the calcium content and the breaking strength in the bone of weanling rats.
KEY WORDS: calcium · maltitol · intestinal absorption · bone · rats
Maltitol, a hydrogenated derivative of maltose, is a disaccharide alcohol which exhibits resistance to intestinal disaccharidases (Yoshizawa et al. 1975 In the present study, we demonstrate evidence that maltitol elicits a stimulation of calcium retention in weanling rats, and it eventually enhances the calcium content as well as the breaking strength of the femoral bones even in this developing stage, which is characteristic of a maximal level of intestinal active calcium transport.
Animals and diet.
Twenty female rats of Wistar strain (Japan SLC, Hamamatsu, Japan) were removed from dams at 24 d of age and were housed in individual wire cages in a temperature- and humidity-controlled room (23°C and 50% relative humidity, respectively). They received free access to the diet containing either maltose (control) or maltitol together with a normal level (0.52%; AIN 1977) of calcium (Table 1) for 21 d. The concentrations of maltose and maltitol were increased stepwise during the experimental period at the expense of cornstarch, i.e., 2, 5 and 10% for the first 3, the next 4, and the final 14 d, respectively. Because a preliminary study showed that weanling rats consumed 10% maltitol diet slightly less than those fed the 10% maltose diet, the control rats fed the 10% maltose diet received the same amount of diet that the rats fed the 10% maltitol diet consumed during the previous day, i.e., pair-feeding was performed during the final 14-d period.
Determinations of the breaking force of the bone.
The fresh femoral bones were isolated and the muscles and connective tissues were removed. The breaking force of the femoral diaphysis (the center of the femur) was determined using a dynagraph (type DYN-1255, Iio, Tokyo, Japan) according to the procedure described by Ezawa et al. (1979) Measurement of bone mineral density.
The tibial bones were isolated, and the bone mineral density of the proximal and distal metaphysis and the diaphysis of right tibia was measured by the dual-energy X-ray absorptiometry (Hologic QDR-1000 X-ray bone densitometer, Waltham, MA). Because the bone mineral density of rats is much lower than that of humans, all scans were performed using the ultrahigh resolution scan mode (rat mode, Version 2.0 software, Hologic, Waltham, MA) as previously reported (Omi et al. 1994 Determinations of calcium.
Calcium amounts in the diets, feces, urine, femurs and tibias were determined by a Zeeman polarized atomic absorption spectrophotometer (Hitachi Z-8000, Tokyo, Japan) using a graphite atomizer. Diets and feces were first dried and micropulverized, from which 100-mg samples were ashed at 600°C for 24 h in the presence of 1 mL of nitric acid. The ashed samples were dissolved in 4 mL of 12 mol/L HC1 and diluted with distilled water, 20 µL of which was subjected to atomization at 2700°C for 10 s, and the atomic absorbance was monitored at 422.7 nm. Urine was diluted with distilled water and directly subjected to atomization. Right femurs and right tibias free of the bone marrow were cut into pieces and dried at 105°C for 12 h. The dried material was ashed and the calcium content was determined by atomic absorption spectrophotometry as described above. Calcium absorption and calcium retention were computed by the following formula: calcium absorption, % = (Ca intake Chemicals.
Maltitol was generously provided by Towa Chemical Industry, Tokyo, Japan. All other reagents were of analytical grade.
Statistical analysis.
All results were subjected to one-way analysis of variance and presented with individual SEM. Differences in mean values between the groups were considered significant at P < 0.05.
The rats weaned to the maltitol-containing diet exhibited no sign of diarrhea and gained weight at a rate similar to that of control animals. The total food intakes during the entire experimental period (21 d) of the animals fed the control diet and the maltitol-containing diet were 173 ± 1 g and 173 ± 2 g (n = 10), respectively.
Previous studies showed that sugar alcohols including sorbitol (Suzuki et al. 1985
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
). When maltitol is consumed with a meal, it reaches the lower part of the small intestine. We previously reported that maltitol increased transepithelial diffusional transfer of calcium in rat ileum (Goda et al. 1993, Kishi et al. 1996), and that the consumption of a diet containing maltitol enhanced the intestinal calcium absorption and calcium retention in normal adult rats (Goda et al. 1992) as well as in ovariectomized rats (Goda et al. 1995). We further showed that the maltitol-induced increase in intestinal diffusional calcium transfer led to an increase in the calcium content and the breaking force of femoral bones in ovariectomized rats (Goda et al. 1995), suggesting that the modulation of intestinal diffusional calcium transfer might be an effective measure of preventing bone mineral loss in the postmenopausal state. This result prompted us to determine whether the maltitol-induced alteration of the diffusional transfer of calcium in the small intestine may give potential benefit of the calcium accumulation in the bone-growing rats.
MATERIALS AND METHODS
Abstract
Introduction
Methods
Results
Discussion
References
View this table:
Table 1.
Composition of the diets1
. The force necessary for the break at the center of the femoral diaphysis was measured under the conditions of 1.0-cm sample space, 100 mm/min plunger speed and 50-kg load range. The breaking force was expressed as dyne.
).
fecal Ca excretion)/(Ca intake) × 100, and calcium retention, % = (Ca intake fecal Ca excretion urinary Ca excretion)/(Ca intake) × 100. Serum calcium concentration was determined by the method of Connerty and Briggs (1966) using 0-cresolphthalein complexone (Calcium C-test, Wako, Osaka, Japan).
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
View this table:
Table 2.
Effects of feeding maltitol-containing diet on calcium excretion in feces and urine of weanling rats1
View larger version (30K):
[in a new window]
Fig 1.
Effect of feeding a maltitol diet on dry weight, calcium content and the breaking force of the femoral bone in weanling rats. Values are means ± SEM, n = 8. * Significantly different from controls, P < 0.05.
View this table:
Table 3.
Effect of feeding a maltitol-containing diet on bone mineral density of the tibia in weanling rats1
View this table:
Table 4.
Effect of gastric intubation of a maltitol-containing diet on
the serum calcium concentration in the portal vein of
weanling rats1,2
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
, Vaughan and Filer 1960), mannitol (Armbrecht and Wasserman 1976) and maltitol (Goda et al. 1993) enhanced calcium absorption in the lower part of the small intestine in rats. The results of the present study demonstrated that the stimulatory effect of maltitol on calcium absorption and retention occurs in weanling rats, in which a maximal level of intestinal active calcium absorption exists (Pansu et al. 1983a). The enhanced calcium retention in the maltitol-fed weanling rats was accompanied by a slight, but significant increase (13%) in the resisting strength of femoral bones against the administration of a breaking force (Fig. 1). This increase in bone-breaking force seems to be due to an elevation of calcium content in the bone segment of the maltitol-fed weanling rats. Indeed, the calcium balance study indicated that the rats fed the maltitol diet gained 70 mg more of calcium than did the controls during the 21-d experimental period. This accounts for 10% of the expected gain in skeletal calcium over this period, and it corresponds to 7% of the total calcium in the whole skeleton of the control rats (DeMoss and Wright 1998). This increase in calcium retention most likely accounts for the 9% increase in the calcium contents of the femurs and tibias, and also for the 5-8% increase in the mineral density of the tibias.
), it seems reasonable that the experimental period we selected (21d) was long enough to examine the effect of the dietary manipulation on the calcium content, mineral density and the mechanical strength of the bones of weanling rats. Based on the literature, we estimated that 24-d-old weanling female rats gain ca. three times the calcium in the body during the subsequent 21 d (DeMoss and Wright 1998). This may well explain why the degree of maltitol-induced increase in the calcium contents in the bones (9%) reflected the increase in calcium retention (9%). Thus, our results suggest that enhancement of calcium absorption and retention induced by a maltitol-containing diet might cause an alteration of calcium metabolism in weanling rats, resulting in an elevation of the calcium content and the mineral density in the bones, and eventually an increase in resisting strength against a breaking force.
), the nonsaturable component of calcium absorption was shown to be unchanged by vitamin-D deficiency, and to be quantitatively similar throughout the intestine (Pansu et al. 1983b). Because calbindin is essentially absent in the rat ileum (Pansu et al. 1983b), active transport of calcium through the transcellular route should be minimal in this segment. Indeed, Nellans and Kimberg (1978) showed that in the ileum, 90% of the calcium is moved by a paracellular pathway. However, little is known about the modulation of the paracellular pathway of calcium. Using everted gut sacs, we previously demonstrated that maltitol enhanced the rate of transepithelial diffusional transfer of calcium in the ileum by modulating the paracellular pathway, presumably through the activation of calmodulin (Kishi et al. 1996). Our previous studies (Goda et al. 1995) showed that dietary maltitol stimulated not only intestinal calcium absorption but also calcium retention. This led to an increase in the calcium content of the femoral bones and an elevation of the breaking strength of the bones in ovariectomized rats, which was used as a simulation model for postmenopausal females at risk for osteoporosis. In this experiment, we demonstrated that the increase in the paracellular calcium transport by dietary maltitol elevates the calcium content of the bones and consequently enhances the resisting strength of the bone against a breaking force in weanling rats. Taken together, it is most likely that the nonsaturable component of calcium transport through paracellular pathway contributes to a considerable extent to overall intestinal calcium absorption in weanling rats (this study) as well as in ovariectomized rats (Goda et al. 1995), and that the enhancement of this component causes an increase in calcium retention as well as a rise in the calcium content and the mineral density of the bones.
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FOOTNOTES |
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Manuscript received 22 April 1998. Initial reviews completed 21 May 1998. Revision accepted 14 July 1998.
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LITERATURE CITED |
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Abstract
Introduction
Methods
Results
Discussion
References
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