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The Journal of Nutrition Vol. 128 No. 1 January 1998,
pp. 106-110
Nutritional Science Center, Bioscience Laboratories, Meiji Seika Kaisha, Ltd., Saitama 350-02, Japan, * Department of Bioscience and Chemistry, Faculty of Agriculture, Hokkaido University, Sapporo 060, Japan, and Department of Basic Sciences, Ishinomaki Senshu University, Ishinomaki 986-80, Japan
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ABSTRACT |
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Abstract
Introduction
Methods
Results
Discussion
References
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Postgastrectomy osteopenia is observed generally in humans. Fructooligosaccharides increase the absorption of calcium from the large intestine of healthy rats. Thus, we have examined whether they stimulate calcium absorption and prevent osteopenia in rats following total gastrectomy. Rats were subjected to either a sham surgical operation or Billoth II gastrectomy. Seven rats from each surgical treatment group were fed a control diet, and another seven rats of each treatment group were fed a diet containing fructooligosaccharides (75 g/kg diet) for 4 wk. For 5 d each week, feces were collected, and the calcium and phosphorus contents were measured for calculation of the absorption of these minerals. At the end of the experiment, the rats were killed and bones were collected. The net calcium absorption, calcium content and bone mineral density of the femur and tibia in gastrectomized rats fed the control diet were significantly less than those in sham-operated rats fed control diet. The net calcium absorption in rats fed the fructooligosaccharides diet was greater than that in rats fed control diet. Moreover, dietary fructooligosaccharides prevented the decrease in the calcium content and bone mineral density in gastrectomized rats. Dietary fructooligosaccharides enhanced calcium absorption and prevented the changes indicative of postgastrectomy osteopenia such as decreases in bone calcium content and bone mineral density in gastrectomized rats.
KEY WORDS: · rats · gastrectomy · fructooligosaccharides · calcium · bone mineral density
Osteopenia develops in patients after gastric resection (Morgan et al. 1965, Pääkkönen et al. 1984 Recent studies suggest a novel way to improve the Ca balance. Indigestible oligosaccharides, resistant starch, guar gum hydrolysate and inulin increase Ca absorption (Ohta et al. 1993, 1994a, Schulz et al. 1993 Accordingly, this study was performed to test whether FOS increase Ca absorption in gastrectomized rats and prevent postgastrectomy osteopenia. We also assessed the contribution of calcium malabsorption to postgastrectomy osteopenia.
Animals and surgical procedures.
Thirty 4-wk-old male Sprague-Dawley rats (Clea Japan, Tokyo, Japan) were housed in individual stainless-steel wire-mesh cages in a room at 25°C and 55% relative humidity. Rats were fed a pelleted diet (MF, Oriental Yeast, Tokyo, Japan) for a 1-wk adaptation period before operation. All rats were anesthetized by intraperitoneal injection of Nembutal (sodium pentobarbital, 35 mg/kg body weight; Abbot Laboratories, North Chicago, IL). The rats were randomly assigned to two groups of 14 or 16 rats. In the group of 16 rats, the stomach was surgically removed (Lambert 1965
Experimental groups and diets.
After these operations, the rats were deprived of food for 24 h and then were allowed free access to homogenized, pasteurized cows' milk (Meiji Milk Products Co. Ltd., Tokyo, Japan) for 48 h. The rats were then fed the purified control diet at 15 g/d for the next four days. Dietary treatments began on d 7 postoperation at which time the 14 rats in each surgical treatment group were randomly divided into two diet groups. The compositions of the control and FOS diets are listed in Table 1. FOS (Meioligo-P®, Meiji Seika Kaisha, Ltd., Tokyo, Japan) is a mixture of 42% 1-kestose, 46% nystose and 9% 1F- Determination of Ca and P content of diets, feces and bones.
The amounts of Ca and P in diets, feces, left femur and left tibia were quantified with an inductive-coupled plasma emission spectrometer (ICPS-5000, Shimadzu, Kyoto, Japan). The diets, feces and bones were first dried, and then the diets and feces were micropulverized. Whole bones and about 100 mg of diets and feces were ashed at 550°C for 24 h. The ashed samples were dissolved in 4 mL of HCl solution (2 mol/L) then diluted appropriately with distilled water for atomization. The apparent absorption of Ca and P were calculated by the following formula: Apparent absorption (mmol/day) = intake Measurement of bone mineral density.
Bone mineral density (BMD, mg/cm2) of right femur and right tibia of each rat was measured by dual-energy X-ray absorptiometry (DEXA DCS-600A, Aroca, Chicago, IL).
Statistics.
Data are expressed as the means ± SD. Data were analyzed by two-way (diet and gastrectomy) or three-way (diet, gastrectomy and time) ANOVA, and significant differences between groups were determined by Tukey-q test (Dawson-Saunders and Trapp 1994; SPSS Ver. 6.0, SPSS, Inc. Chicago, IL). Differences were considered significant at P < 0.05. A correlation coefficient between apparent absorption of Ca and BMD of femur or tibia was calculated by the least squares method (Ichihara 1991 Body weights and food intakes.
Initial and final body weights in gastrectomized rats fed FOS diet were lower than those of sham-operated rats fed control diet (Table 2). Body weight gains and total food intakes did not vary among the experimental groups.
Apparent absorption of Ca and P.
Apparent absorption of Ca in rats fed the FOS diet was higher than that in rats fed control diet (Fig. 1, Table 3). Apparent absorption in gastrectomized rats fed control diet was significantly lower than that in rats of other three groups throughout the four absorption study periods. In the gastrectomized rats, the apparent absorption of Ca was significantly higher in rats fed FOS than in those fed control diet.
Ca and P content and BMD of the femur and tibia.
The Ca and P levels per whole bone and per g dry weight of femur and tibia did not differ in sham-operated rats of both dietary groups (Table 4). Ca per whole bone and per g dry weight of femur and tibia in gastrectomized rats fed the control diet were significantly lower than in other groups. The Ca and P level per whole bone and per g dry weight of femur and tibia in gastrectomized rats fed FOS diet were significantly higher than those in gastrectomized rats fed control diet. The Ca level per whole bone and per g dry weight of tibia in gastrectomized rats fed FOS diet did not differ from those in sham-operated rats of either dietary group.
The apparent absorption ratio of Ca in this study (Fig. 1), was markedly decreased by gastrectomy to a level similar to previous studies (Fries et al. 1992
The authors are indebted to assistant professor M. Uehara of the Faculty of Agriculture, Tokyo University of Agriculture, for her valuable suggestions concerning this paper, and thank H. Inage, M. Koizumi and T. Iguchi of Showa Women's University for their assistance in the preparation of bone samples.
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
, Tovey et al. 1990), suggesting the importance of the stomach in calcium homeostasis (Axelson et al. 1991, Fries et al. 1992, Håkanson et al. 1990). The mechanism of postgastrectomy osteopenia has not been clarified, and nutritional therapy for postgastrectomy osteopenia has not been developed (Axelson et al. 1991, Bisballe et al. 1991). Calcium malabsorption has been reported to be a cause of osteopenia. It is thought that gastric acid dissolves insoluble Ca in the diet, and thereby facilitates the absorption of Ca in the small intestine (Allen 1982, Eastell 1985, Ivanovich et al. 1967, Mahoney et al. 1975, Nordin 1968, Sheikh 1987). However, the above hypothesis is debatable. Water-insoluble Ca compounds such as calcium carbonate can be absorbed by humans without gastric acid secretion (Bo-Linn et al. 1984), suggesting that gastric acid secretion is not essential for calcium absorption in the small intestine. Further, subcutaneous Ca supplementation failed to prevent bone loss in gastrectomized rats (Persson et al. 1993). This study led us to consider the stomach as the source of a calcinotropic hormone, gastrocalcin (Persson et al. 1989 and 1993). On the other hand, the gastric hormone gastrin has no effect on duodenal Ca absorption in short-term experiments in rats (Rümenapf et al. 1990). The stomach plays an important role in Ca homeostasis, but the mechanism of gastric action is not yet understood.
, Hara et al. 1996, Rémésy et al. 1993). Among these, the effect of fructooligosaccharides (FOS),2 a mixture of indigestible and fermentable sugars (Hidaka et al. 1991), has been well examined. FOS increase Ca and Mg absorption (Ohta et al. 1993 and 1994a) and stimulate bone calcification in healthy rats (Ohta et al. 1993). A considerable part of the effects of FOS feeding take place in the large intestine (Baba et al. 1996, Ohta et al. 1994b, 1995 and 1997). Thus, it may be reasonable to propose that FOS stimulate Ca absorption in gastrectomized rats and prevent postgastrectomy osteopenia.
MATERIALS AND METHODS
Abstract
Introduction
Methods
Results
Discussion
References
, Oscarson et al. 1979). The other group of 14 rats was subjected to sham operation; the abdominal cavity was opened for approximately 45 min, the same length of time required for the gastrectomy procedure. Two gastrectomized rats died before the start of the experiment.
View this table:
Table 1.
Composition of experimental diets
View this table:
Table 2.
Initial and final body weights, total body weight gain and food intake of rats with or without gastrectomy fed control or fructooligosaccharides (FOS) diets for 28d1
-fructofuranosyl nystose (Hidaka et al. 1988 and 1991). Other dietary components, apart from minerals, were obtained from Oriental Yeast Co., (Tokyo, Japan).
fecal excretion.
) using Microsoft Excel Version 7.0 (Microsoft, Tokyo, Japan).
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
View larger version (42K):
[in a new window]
Fig 1.
Apparent absorption of Ca in rats subjected to sham operation or gastrectomy and fed diets with or without fructooligosaccharides. With d 1 corresponding to the start of feeding experimental diets, the testing periods were: 1, d 4-d 8; 2, d 11-d 15; 3, d 18-d 22; 4, d 25-d 29. Values are means ± SD, n = 7. Within each testing period, values with different superscript letters are significantly different, P 
0.05.
View this table:
Table 3.
The results of three way ANOVA of the apparent absorption of calcium and phosphorus data1
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[in a new window]
Fig 2.
Apparent absorption of P in rats subjected to sham operation or gastrectomy and fed diets with or without fructooligosaccharides. With d 1 corresponding to the start of feeding experimental diets, the testing periods were: 1, d 4-d 8; 2, d 11-d 15; 3, d 18-d 22; 4, d 25-d 29. Values are means ± SD, n = 7. Within each testing period, values with different superscript letters are significantly different, P 0.05.
View this table:
Table 4.
Ca, P contents and bone mineral density (BMD) in the femur and tibia of rats with or without gastrectomy fed control or fructooligosaccharide (FOS) diets for 4 wk1
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
). The decrease in Ca absorption appeared within one week and continued for at least four weeks in this study. One previous report suggested that gastric acid secretion is not essential for Ca absorption in humans (Bo-Linn et al. 1984). Thus, insufficient gastric acid secretion may not be the only cause for markedly decreased Ca absorption after gastrectomy. Functions of the stomach other than acid secretion may facilitate Ca absorption. Our previous study clearly demonstrated that the large intestine of intact rats is able to absorb nutritionally sufficient Ca from an insoluble Ca compound (CaCO3) infused into the cecum (Ohta et al. 1997). The net absorption of Ca infused into the cecum was reduced from 0.55 mmol/day (Ohta et al. 1997) to 0.30 mmol/day by gastrectomy. These results suggest that the large intestine of gastrectomized rats could not absorb Ca sufficiently. These results suggest that the stomach is involved in Ca absorption from the large intestine.
). We speculate that the CaCO3 in our experimental diet was not dissolved in the case of the gastrectomized rats, and the amount of insoluble phosphate in the small intestine was reduced and P absorption was increased.
, Schulz et al. 1993). This mechanism should be activated without gastric acid secretion.
). FOS feeding prevented the decrease of both Ca content in bones and BMD. In this study, a significant correlation between the BMD and the whole bone Ca content of both femur (r = 0.9690) and tibia (r = 0.8843) was observed (Table 4). Perrson et al. (1993) speculated that the main cause of postgastrectomy osteopenia is a lack of gastric hormones such as gastrin or gastrocalcin, since subcutaneous Ca supplementation failed to prevent postgastrectomy osteopenia in rats. However, a significant positive correlation between the apparent Ca absorption and BMD (Table 5) may suggest that the malabsorption of Ca is an important risk factor of postgastrectomy osteopenia. Also, it seems that postgastrectomy osteopenia is not prevented by only Ca supplementation. We think it is necessary to enhance Ca absorption in order to prevent postgastrectomy osteopenia.
View this table:
Table 5.
Correlations between apparent absorption of Ca of each balance period and bone mineral density (BMD) of femur or tibia in all rats
ACKNOWLEDGMENT
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FOOTNOTES |
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Manuscript received 25 April 1997. Initial reviews completed 19 May 1997. Revision accepted 19 August 1997.
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LITERATURE CITED |
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Abstract
Introduction
Methods
Results
Discussion
References
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