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Japanese Citrus Fruit (Sudachi) Juice Is Associated with Increased Bioavailability of Calcium from Whole Small Fish and Suppressed Bone Resorption in Rats

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J Nutr Sci Vitaminol, 50, 177-183, 2004 Japanese Citrus Fruit (Sudachi) Juice Is Associated with Increased Bioavailability of Calcium from Whole Small Fish and Suppressed Bone Resorption in Rats Yoshitaka NIT1, Kazuhiro FUKUTA1, Kentaro SAKAI2 and Shigeru YAMAMOTO3 1Food TechnologyDivision , TokushimaPrefectural Industrial TechnologyCenter, Tokushima770-8021, Japan 2Department of Nutrition and Health Promotion, Faculty of Human Life Science,Hiroshima Jogakuin Univer sity, Hiroshima 732-0063, Japan 3Department of Nutrition, School of Medicine,The University of Tokushima, Tokushima770-8503, Japan (Received October 11, 2003) Summary Shirasuboshi (boiled and semi-dried whitebait) is a processed fish food that con tains abundant calcium. It is eaten whole and commonly consumed in Japan. In this study, the effect of sudachi (Citrus sudachi) juice on calcium, magnesium and phosphorus bioavail ability, and bone metabolism in rats was examined. After 14 d of diets low in calcium and phosphorus, male Sprague-Dawley rats were fed shirasuboshi diets containing dried shira suboshi powder treated with 20% (S20) or 40% (S40) sudachi juice, or distilled water (C) (0.5% Ca; 0.3% P) for 14 d. The apparent absorptions and retentions of calcium, magne sium and phosphorus from shirasuboshi were determined. Bone formation was calculated by measuring serum osteocalcin, and bone resorption by measuring urinary pyridinoline and deoxypyridinoline. The apparent absorption and retention of calcium and magnesium in the S20 group were significantly higher than in the C and S40 groups. Although serum osteo calcin was not affected by the addition of sudachi juice, the urinary pyridinoline and deoxy pyridinoline concentrations in the S40 group were significantly lower than in the C and S20 groups. Our results indicate that sudachi juice added to shirasuboshi was associated with increased calcium bioavailability and suppressed bone resorption in rats. Key Words calcium-absorption, citrus fruit, fish, bone resorption, rats The importance of adequate calcium intake for the solubilizing dietary calcium. development and maintenance of peak bone mass is Sudachi (Citrus sudachi) is a major citrus fruit grown well established (1). Insufficient calcium intake increas in Tokushima Prefecture, which is located on Shikoku es bone resorption (1, 2), decreases bone mass (3) and Island in Japan. There is a dietary habit of squeezing increases the risk of osteoporosis after menopause (4). sudachi juice on shirasuboshi in this area. The major A sufficient calcium intake is therefore required to pre organic acid component of sudachi juice is citric acid. vent bone loss. For these reasons, promoting diets high Previously, we found that sudachi juice solubilizes cal in calcium and exploring new ways of increasing the cium from shirasuboshi in vitro (11). Furthermore, we bioavailability of dietary calcium are very important. observed solubilization of calcium by sudachi juice fol Shirasuboshi (boiled and semi-dried whitebait) is a lowing in vitro peptic and peptic-pancreatic digestions processed fish food that is eaten whole and commonly of shirasuboshi (11). These results suggest that sudachi consumed in Japan. Although whole small fish with juice treatment may enhance the bioavailability of cal bones are potentially a good source of dietary calcium, cium from shirasuboshi. The present study was therefore bone calcium is unavailable for absorption due to its designed to examine the effect of sudachi juice on cal incorporation in insoluble hydroxyapatite crystals (5). cium, magnesium and phosphorus bioavailability, and There is very little information on the availability of cal bone metabolism in young male rats fed shirasuboshi cium from the bones of small fish (5, 6), and methods to diets. efficiently increase calcium availability from small fish MATERIALS AND METHODS have not been fully examined. It is thought that calcium must be ionized in order to Preparation of dried shirasuboshi powder. Shirasuboshi be absorbed in the intestine (7). Several reports have were purchased from Yoshimi Kaisan Co., Ltd. (Komat dealt with the significant effects of citric acid and citric sushima, Tokushima, Japan). The content of water in acid salts on the bioavailability of calcium (8, 9). the shirasuboshi was 38.7g/100g. Sudachi juice (pH Mehansho et al. (10) demonstrated that CCM (a combi 2.2) was purchased from Tokushima City Agricultural nation of calcium carbonate, citric acid and malic acid) Cooperatives (Tokushima, Japan). The concentrations of in orange juice enhances the bioavailability of calcium. citric acid and malic acid in the sudachi juice were These results suggest that citric acid is very effective in 60mg/mL and 3.5mg/mL, respectively. To 100g of 177 178 Nu Y et al. Table 1. Composition of experimental diets. 1C , the diet containing dried shirasuboshi powder treated with distilled water; S20 , the diet containing dried shirasuboshi powder treated with 20% sudachi juice; S40, the diet containing dried shirasuboshi powder treated with 40% sudachi juice .2 Containing (g/100g): protein, 63.6; fat, 5.2; carbohydrate, 0.2; (mg/100g): calcium , 750; magnesium, 190; phospho rus, 950. 3Prepared according to AIN -93G formulation except for calcium and phosphorus . fresh shirasuboshi, 20 or 40mL of sudachi juice was with the Guideline for the Care and Use of Laboratory added to make the experimental diets. Distilled water Animals at the University of Tokushima. was added to an equivalent amount of sudachi juice to Metabolism studies. During the periods of 11-14 d make the control diet. The shirasuboshi treated with and 25-28 d, the rats were placed in metabolic cages sudachi juice or distilled water was then dried for 12h at (Try Tec Co., Ltd., Osaka, Japan). The food intake was 80•Ž. Dried shirasuboshi were ground to a powder using measured, and feces and urine were collected separately a food cutter (DLC-XG; Conair Corp., Stamford, CN, USA) . for each period for the determination of apparent Animals and diets. Male Sprague-Dawley rats, 3 wk absorption and retention. The 0.1% carmine was added of age (Japan SLC Co., Ltd., Hamamatsu, Shizuoka, to each diet as a marker, and the feces were collected Japan) were preliminarily maintained on a stock diet until the marker was all excreted. Feces collected were (MF; Oriental Yeast Co., Ltd., Tokyo, Japan) for 7 d, and dried for 24h at 105•Ž, weighed, and ground with a the rats were then fed ad libitum a low-calcium blender. Contaminants, including hairs, were removed (0.01%), low-phosphorus (0.15%) diet for 14 d (Table by filtering through an 80-mesh stainless steel sieve . 1). The rats were then divided into three groups of six Urine was collected in a glass flask containing 1 N rats each. The three groups were fed ad libitum the hydrochloric acid, and filtered with No. 7 filter paper shirasuboshi diets containing dried shirasuboshi powder (Toyo Roshi Co., Ltd., Tokyo, Japan). treated with 20% (S20) or 40% (S40) sudachi juice, or Analytical methods. At the end of the study period , distilled water (C) (0.5% Ca; 0.3% P) for 14 d (Table 1) . the rats were anesthetized by ethyl ether and killed, and The diets were based on the AIN-93 G formulation (12) . blood samples and femurs were collected. Serum was The dried shirasuboshi powder was the main source of aliquoted after centrifugation (1, 500•~g) for 15min at protein, calcium and phosphorus in each diet, and the 4•Ž and stored at -40•Ž until analysis. Feces, right total level of fat was adjusted to 7% (w/w) with soybean femurs and food samples were dried, and then ashed for oil. The contents of energy, protein, fat, fiber, calcium 24h at 550•Ž in a muffle furnace (FO300; Yamato Sci and phosphorus were constant in each diet. The rats entific Co., Ltd., Tokyo, Japan). The temperature was were housed individually in stainless steel cages at gradually raised until 550•Ž. The ashed samples were room temperature (24•Ž) and 55% humidity with a dissolved in 1% hydrochloric acid. 12h light-dark cycle. All rats were given distilled water Calcium and magnesium concentrations were deter ad libitum. The animals were maintained in accordance mined by atomic absorption spectrophotometry (Z Effect of Citrus Fruit on Calcium Absorption 179 Table 2. Body weight gain, food intake and food efficiency in rats fed low Ca and P diet or dried shirasuboshi diet. Values are means•}SD, n=18 in (A) and n=6 per group in (B). 8100; Hitachi, Ltd., Tokyo, Japan) with strontium add Table 3. The apparent absorption and retention of cal ed to the sample at a final concentration of 3,000mg/L. cium, magnesium and phosphorus in rats fed low Ca Phosphorus was determined by a colorimetric method and P diet. using ammonium molybdenate (13). The apparent ab sorption and retention of calcium, magnesium and phosphorus were calculated by the following formulae: Apparent absorption (%)=[(intake-fecal excretion)/ (intake)]•~100, and apparent retention (%)=[(intake -fecal excretion-urinary excretion)/(intake)]•~100 . Values are means•}SD, n=18. Citric acid and malic acid in sudachi juice were mea sured by high-performance liquid chromatography (Organic Acids Analytic System; Japan Spectroscopic dex (SSI), which is an indicator of whole bone strength Co., Ltd., Tokyo, Japan) (14). (16-18). Biochemical analysis. The concentrations of cal In vitro solubilization of calcium from dried shirasuboshi cium, magnesium and inorganic phosphorus in serum powder. To 20mL of Ultra Pure Water (Milli-Q SO; Mil were measured by a colorimetric method using assay lipore Corp., Tokyo, Japan), 1g of dried shirasuboshi kits for each mineral (Calcium C, Magnesium B and powder was added and incubated on a shaker for 1h at Phosphor C; wako Pure Chemical Industries, Ltd.,. 37•Ž. Samples were centrifuged (18,000•~g) for 10 min Osaka, Japan). at 4•Ž and the amount of calcium in the supernatant The concentrations of calcitonin and osteocalcin in was determined by atomic absorption spectrophotome serum were measured by enzyme immunoassay (Penin try (Z-8100; Hitachi, Ltd.).
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