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© 2003 The American Society for Nutritional Sciences J. Nutr. 133:4207-4211, December 2003

Nutrient Metabolism

Ingestion of Difructose Anhydride III and Voluntary Running Exercise Independently Increase Femoral and Tibial Bone Mineral Density and Bone Strength with Increasing Calcium Absorption in Rats

Kazuki Shiga*,{dagger}, Hiroshi Hara{dagger},1, Goroh Okano**, Manabu Ito{ddagger}, Akio Minami{ddagger} and Fusao Tomita{dagger}

* Northern Advancement Center for Science and Technology, Colabo-Hokkaido, Sapporo 001-0021, Japan; {dagger} Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan; ** Division of Exercise Science, Sapporo Medical University, Sapporo, 060-8556, Japan; and {ddagger} Department of Orthopedic Surgery, Hokkaido University Graduate School of Medicine, Sapporo 060-8638, Japan

1To whom correspondence should be addressed. E-mail: hara{at}chem.agr.hokudai.ac.jp.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Difructose anhydride III (DFAIII), a nondigestible disaccharide, promotes intestinal calcium absorption. Exercise-induced mechanical stimuli are essential for bone growth. In the present study, we examined the effects of consuming DFAIII and voluntary running exercise on calcium absorption and bone characteristics using male Sprague-Dawley rats (4 wk old). The study was designed in a 2 x 2 factorial arrangement with two conditions (sedentary or exercised) and two diets [AIN-93G diet with or without DFAIII (30 g/kg diet)]. Both consuming DFAIII and running exercise increased net calcium absorption, and the effects of DFAIII and exercise were additive. Both consuming DFAIII and exercise also increased femoral variables such as calcium content and total bone mineral density (BMD); however, only consuming DFAIII increased bone strength in the femur. Conversely, running exercise augmented tibial calcium content, total BMD and bone strength, but consuming DFAIII did not. We conclude that consuming DFAIII and running exercise additively enhance calcium absorption and differentially stimulate femoral and tibial BMD and mechanical properties in rats.

KEY WORDS: • difructose anhydride III • voluntary running exercise • calcium absorption • bone • rats

Adequate calcium intake and physical exercise are recommended for the development of high peak bone mass and the prevention of osteoporosis (1). Also, we should consider not only adequate calcium intake, but also the absorptive efficiency of ingested calcium, because intestinal calcium absorption is influenced by many factors such as age (2), the source of ingested calcium (3) and coingested nutrients (4).

Nondigestible carbohydrates such as dietary fiber, oligosaccharides and resistant starch have various physiologic functions (5,6), and the promotive effects of several nondigestible carbohydrates on calcium absorption have been well examined (7–11). We previously reported that difructose anhydride III (DFAIII),2 a nondigestible disaccharide, enhances calcium absorption in in vivo (12,13) and in vitro experiments (14,15). The proposed mechanisms for the promotion of calcium absorption are the following: 1) intact DFAIII stimulates paracellular calcium absorption by increasing the passage of tight junctions in the small and large intestine (14,15) and 2) ingested DFAIII is fermented in the large intestine, producing SCFA that promote calcium absorption (13,16). We also showed that consuming DFAIII partially prevents ovariectomy-induced (13) and gastrectomy-induced (unpublished data) osteopenia with improvement of calcium absorption in rats. However, in normal healthy rats, the effects of DFAIII ingestion on bone growth have not yet been fully clarified.

Physical exercise–induced mechanical stress plays an important role in the maintenance and increase of bone mass (17). Many researchers have shown that exercise interventions increase bone mineral density (BMD) and bone strength in humans (18–20) and rats (21–23). However, there are very few reports regarding the effects of exercise training on intestinal calcium absorption (24,25).

This study examined the effects of DFAIII ingestion and exercise on calcium absorption and bone characteristics in rats. To date, the combined effects of calcium absorption enhancers such as DFAIII and exercise are unknown. We investigated whether BMD and bone strength in the femur and tibia are increased by DFAIII ingestion and loading exercise.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Test material.

Difructose anhydride III (DFAIII; Nippon Beet Sugar Manufacturing, Tokyo, Japan) is a nondigestible disaccharide consisting of two fructose residues with a molecular weight of 324; it is prepared from inulin with Arthrobacter sp. H65–7 inulin fructotransferase (Inulinase II; EC 2.4.1.93) (26). Recently, a procedure was established for the mass production of DFAIII using this bacterial enzyme (27).

Animals and diets.

Male Sprague-Dawley rats (n = 36; 4 wk old; Clea Japan, Tokyo, Japan) were housed in individual stainless steel cages (17.5 x 25 x 17 cm) in a room with controlled temperature (22 ± 2°C), relative humidity (40 to 60%) and lighting (0800 to 2000 h). The rats were fed the stock diet for an acclimation period of 4 to 5 d, and were then divided into four groups of nine rats using a randomized block design based on body weight. The rats in two groups were fed the test diet containing DFAIII (DFAIII diet). The rats in the other two groups were fed the test diet without DFAIII (control diet). Stock and control diets were prepared according to the AIN-93G formulation (5.0 g Ca and 80 g cellulose per kg of diet) (28). The DFAIII portion (30 g) replaced part of the cellulose portion in the test diet (i.e., 30 g DFAIII and 50 g cellulose per kg of diet). All rats were allowed free access to the assigned test diets and deionized water for 28 d. On d 4 of the feeding period, the rats in one group from each dietary division were transferred to cages (27 x 35 x 35 cm) equipped with a rotary wheel and a counter for recording distances run; these rats were allowed to exercise voluntarily until d 27 of the feeding period (exercised group). We chose voluntary running as the type of exercise (29) because the effect of electrical stimulus cannot be excluded with a motor-driven treadmill. In addition, voluntary running is a more natural and easily monitored exercise than other types of exercise training. Distances run in each 24-h period were measured daily. The remaining groups were transferred to cages one-third smaller (17.5 x 8 x 17 cm) than the cages used in the acclimation period (17.5 x 25 x 17 cm) to reduce voluntary activity (sedentary group). Body weight and food intake were measured daily. Spilled food was collected carefully and weighed, and food intakes were corrected accordingly. Whole feces were collected for 5 consecutive days in two sampling periods, from d 9 (sample 1) and from d 23 (sample 2) of the feeding period, and were freeze-dried to evaluate net absorption of calcium. On d 27 of the feeding period, all rats were transferred to metabolic cages (17.5 x 25 x 17 cm), and urine was collected for 24 h to measure the urinary excretion of deoxypyridinoline (D-Pyr) as a marker of bone resorption (30). At the end of the experiment, the rats were killed under sodium pentobarbital anesthesia (50 mg/kg body weight; Nembutal, Abbott Laboratories, North Chicago, IL). The left and right femur and tibia were removed, carefully cleaned of adherent tissue, wrapped with paper (Kimwipe, CRECIA, Tokyo, Japan) soaked with saline, and stored at 4°C. Bone strength (left side) and BMD (right side) of the femur and tibia were measured within the next few days. The right femur and tibia were freeze-dried for measurement of dry weight and calcium content after measuring BMD. The cecum was removed with its contents, and the contents were collected, weighed, frozen immediately with liquid nitrogen and stored at -40°C for subsequent analysis. The cecal wall was washed with saline and weighed.

This study was approved by the Hokkaido University Animal Committee, and animals were maintained in accordance with Hokkaido University’s guidelines for the care and use of laboratory animals.

Analytical methods.

Freeze-dried feces were milled to a fine powder, and the powdered feces (~1.5 g) were dry-ashed in an electric furnace (EYELA TMF-3200, Tokyo Rikakikai, Tokyo, Japan) at temperatures elevated linearly to 550°C for 6 h, then held at 550°C for 18 h. The ashed samples were treated with 5.49 mol/L HCl at 200°C for 30 min and were dissolved in 0.82 mol/L HCl. Calcium concentration of the ashed solutions was measured with a polarizing Zeeman-effect atomic absorption spectrometer (Z-5310, Hitachi, Tokyo, Japan) after suitable dilution. Calcium content of the test diets and the right femur and tibia was determined in the same manner. We performed recovery tests to confirm the accuracy of above-mentioned method, and the recovery of calcium was 108 ± 1.1% (n = 5, CV = 2.3%).

Total BMD of the right femur and tibia was measured by dual-energy X-ray absorptiometry (DEXA) with a small animal high resolution scan module (QDR-4500A, Hologic, Bedford, MA). The regional difference was estimated by evaluation of the regional BMD [25% proximal, 50% middle (midshaft) and 25% distal of each bone]. Bone strength was measured by a three-point bending test (11,31) performed with a rheometer (RE-3305 Rheoner, Yamaden, Tokyo, Japan). The center of the left femur and tibia was fractured under the following conditions: 1-cm sample space, 30-mm/min plunger speed and 20-kg load range. The maximum breaking force was recorded as the bone strength.

Urinary D-Pyr concentration was evaluated using a commercial assay kit (Osteolinks DPD, Sumitomo Pharmaceuticals, Osaka, Japan). Urinary creatinine concentration was measured using the Jaffe reaction, as described by Lustgarten and Wenk (32). Urinary D-Pyr excretion values were corrected with the urinary creatinine values.

The cecal contents were diluted with 4 volumes of deionized water and homogenized using a Teflon homogenizer. The pH of the cecal contents was measured by testing this homogenate with a semiconducting electrode (ISFET pH sensor 0010–15C, HORIBA, Kyoto, Japan). Pools of total SCFA (the sum of acetic, propionic and butyric acid levels) in the homogenate of cecal contents were measured by the procedure described previously (33,34).

Calculations and statistical analyses.

Net absorption of calcium was calculated by the following formula: Net Ca absorption (%) = 100 x (total Ca intake - fecal Ca excretion)/total Ca intake.

Data were analyzed for the two factors (exercise and diet) and their interactions by two-way ANOVA. Student’s t test was used to determine whether distances run differed between the two groups of exercised rats (P < 0.05). Correlation coefficients for the relationships between net calcium absorption and several femoral and cecal variables were calculated by the least squares method (35). Statistical analyses were done using the SAS General Linear Models procedure (SAS Version 6.07, SAS Institute, Cary, NC).


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Body weight gain tended to be lower in exercised rats (6.65 ± 0.174 g/d) than in sedentary rats (7.16 ± 0.201 g/d, P = 0.064), and food intake in exercised rats (24.7 ± 0.485 g/d) was higher than that in sedentary rats (22.7 ± 0.462 g/d, P = 0.004). The distances run by exercised rats did not differ between the two dietary groups (control group, 4646 ± 531 m/d; DFAIII group, 3855 ± 488 m/d; P = 0.294).

Net calcium absorption in rats fed the DFAIII diet was higher than that in rats fed the control diet at 2 wk (Fig. 1A) and at 4 wk (Fig. 1B) after the start of the feeding period. Calcium absorption was higher in exercised rats than in sedentary rats at 2 and 4 wk.



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  		FIGURE 1 Net calcium absorption in sedentary and exercised rats fed the control diet or difructose anhydride III (DFAIII) diet at (A) 2 wk (d 9–13) and (B) 4 wk (d 23–27) after the start of the feeding period. Values are means ± SEM, n = 9. P-values were estimated by two-way ANOVA: (A) exercise, P < 0.001; diet, P = 0.002; exercise x diet, P = 0.767 and (B) exercise, P = 0.002; diet, P < 0.001; exercise x diet, P = 0.496.

 
Femoral dry weight and calcium content were higher in exercised rats than in sedentary rats, and were also higher in rats fed the DFAIII diet than in rats fed the control diet (Table 1). The calcium concentration of the femur was not affected by voluntary running exercise and DFAIII ingestion. Tibial dry weight and calcium content were higher in exercised rats than in sedentary rats. The calcium concentration of the tibia was not affected by exercise. DFAIII ingestion did not influence these tibial variables.


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  		TABLE 1 Femoral and tibial weight, calcium content and calcium concentration of sedentary and exercised rats fed the control diet or difructose anhydride III (DFAIII) diet for 28 d1

 
The BMD of the whole femur evaluated by DEXA was higher in exercised rats than in sedentary rats, and was higher in rats fed the DFAIII diet than in rats fed the control diet (Table 2). Whole tibial BMD was higher in exercised rats than in sedentary rats. Voluntary running exercise and DFAIII ingestion increased femoral distal BMD, but not proximal and midshaft BMD. Proximal tibia BMD was higher in the DFAIII group than in the control group. Diet did not affect the midshaft and distal parts of the tibia. Exercise clearly influenced all regional parts of the tibia.


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  		TABLE 2 Femoral and tibial bone mineral density (BMD) of the total, proximal region, midshaft region and distal region of sedentary and exercised rats fed the control diet or difructose anhydride III (DFAIII) diet for 28 d1

 
Bone strength (maximum breaking force) of the femur was higher in rats fed the DFAIII diet than in rats fed the control diet (Fig. 2A). Femoral strength was not affected by running exercise. Tibial bone strength was greater in the exercised groups than in the sedentary groups (Fig. 2B). DFAIII ingestion did not affect tibial bone strength.



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  		FIGURE 2 Bone strength (maximum breaking force) of (A) the femur and (B) the tibia in sedentary and exercised rats fed the control diet or difructose anhydride III (DFAIII) diet for 28 d. Values are means ± SEM, n = 9. P-values were estimated by two-way ANOVA: (A) exercise, P = 0.102; diet, P = 0.041; exercise x diet, P = 0.213 and (B) exercise, P < 0.001; diet, P = 0.422; exercise x diet, P = 0.069.

 
Urinary D-Pyr excretion was reduced by voluntary running exercise (Table 3), and it tended to be higher in rats fed the DFAIII diet than in rats fed the control diet (P = 0.098).


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  		TABLE 3 Urinary deoxypyridinoline (D-Pyr) excretion of sedentary and exercised rats fed the control diet or difructose anhydride III (DFAIII) diet for 28 d1

 
Cecal wall weight and the pool of total SCFA (the sum of acetic, propionic, and butyric acid levels) were higher in rats fed the DFAIII diet than in rats fed the control diet. The pH of cecal contents in rats fed the DFAIII diet (6.10 ± 0.063) was lower than that in rats fed the control diet (7.38 ± 0.081, P < 0.001). Exercise did not affect these variables (data not shown).


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Ingestion of DFAIII and exercise enhanced intestinal calcium absorption (Fig. 1); however, the increases in calcium content (Table 1), BMD (Table 2) and bone strength (Fig. 2) differed between the femur and tibia. In the femur, DFAIII ingestion augmented bone strength with increasing calcium content and whole BMD; however, running exercise did not augment the mechanical properties despite the increase in calcium content and whole BMD (Table 4). In contrast, running exercise, but not DFAIII ingestion, increased tibial bone strength with increasing calcium content and whole BMD. These findings reveal that a combination of DFAIII ingestion and running exercise promotes bone growth in the leg. Clinical observation shows the femur to be the most common fracture site in patients with osteoporosis (36). Ingestion of DFAIII combined with exercise may effectively decrease the risk of femoral fracture. Femoral dry weight, calcium content, whole femoral BMD and bone strength correlated positively with net calcium absorption at 4 wk [n = 36; r = 0.408, P < 0.05 (dry weight); r = 0.401, P < 0.05 (Ca content); r = 0.414, P < 0.05 (total BMD) and r = 0.368, P < 0.05 (bone strength)], suggesting that DFAIII ingestion and exercise promotes bone growth at least partly by increasing calcium absorption.


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  		TABLE 4 Summary of the two-way ANOVA of bone-related variables1

 
Both DFAIII ingestion and exercise increased calcium absorption (Fig. 1). The effect of DFAIII ingestion and exercise on calcium absorption is probably additive, not synergistic. We previously demonstrated that DFAIII increases calcium absorption in both the small and large intestine (14,15). In the small intestine, DFAIII activates the passage of tight junctions (15). The present study showed that ingesting DFAIII increases the total SCFA (sum of acetic, propionic and butyric acid levels) pool and decreases the pH value of the cecal contents. Calcium absorption at 4 wk correlated positively (n = 36, r = 0.429, P < 0.01) with the total SCFA pool in cecal contents, suggesting that cecal fermentation of DFAIII is involved in the increased calcium absorption in the large intestine. It has been reported that forced running exercise for 9 wk stimulates the active transport of calcium via a transcellular pathway in in vivo and in situ experiments (24). These results suggest that DFAIII ingestion and exercise training promote calcium absorption via different mechanisms. The effect of exercise on calcium absorption has not yet been fully clarified. To our knowledge, only three published papers demonstrate that forced running exercise increases calcium absorption in rats (24,25) and humans (37). Our results show that voluntary running exercise also increases intestinal calcium absorption in rats.

Exercise-induced bone growth is site specific (22,38–40). Voluntary tower climbing (22) and forced treadmill exercise (38) promote growth in the femur and tibia in rats, rather than the lumbar vertebra. Iuliano-Burns et al. (39) showed that moderate jumping exercise increases bone mineral content in the tibia-fibula (loaded sites) in pubertal girls but not in the humerus or radius-ulna (nonloaded sites). It is likely that factors such as the type of exercise, the magnitude of loaded mechanical stress and bone architecture influence the effects of exercise on various skeletal sites. In this study, the effects of exercise on bone characteristics differed between the femur (upper part of the leg) and the tibia (lower part of the leg) (Tables 1, , 2, , 4; Fig. 2). In the case of the tibia, voluntary running exercise increased calcium content (Table 1), total and regional BMD (Table 2) and bone strength (Fig. 2); however, running exercise did not strengthen the mechanical properties of the femur despite the increased calcium content and total BMD. Possibly, the mechanical stress loaded to the femur was less than that loaded to the tibia because of the type of exercise chosen for this study. This might also be related to the quadruped posture of rats.

We measured the regional BMD of the femur and tibia [25% proximal, 50% middle (midshaft) and 25% distal] to assess the local effects of DFAIII ingestion and voluntary running exercise (Table 2). Ingestion of DFAIII and exercise increased distal femur BMD and proximal tibia BMD. We found that these bone regions had lower BMD than the other four regions; the proximal and midshaft femur and midshaft and distal tibia. This suggests that the ratio of trabecular bone in these bone regions was higher than that of cortical bone. Trabecular bone is reported to be more sensitive to aging and to drugs that modulate bone metabolism (41). The additional calcium absorbed because of DFAIII ingestion and exercise might be used preferentially in areas of trabecular bone.

As described earlier, running exercise did not increase femoral bone strength despite the increased calcium content and total BMD of the femur (Table 1, , 4; Fig. 2). This may be related to the effect of exercise on femoral midshaft BMD. Briefly, in this study, exercise did not augment femoral midshaft BMD (Table 2), and bone strength was assessed with a three-point bending test; that is, the center of the femur (femoral midshaft) was fractured. However, the mechanical properties of bone depend not only on BMD but also on bone architecture (42). Actually, DFAIII ingestion augmented femoral bone strength without increasing the midshaft BMD. Further studies are needed to clarify the effects of exercise and DFAIII ingestion on bone strength and bone architecture.

In the present study, voluntary running exercise decreased urinary excretion of D-Pyr (Table 3). This indicates that running exercise increases bone mass by suppressing bone resorption in addition to enhancing calcium absorption (Fig. 1). Our result is consistent with previous reports that exercise-induced mechanical stress stimulates bone growth by increasing bone formation and decreasing bone resorption (18,23) although we did not evaluate bone formation.

In conclusion, a combination of DFAIII ingestion and running exercise enhances calcium absorption and increases femoral and tibial calcium content, BMD and bone strength in rats. The beneficial effects of DFAIII ingestion and exercise on bone growth differ between the femur and tibia in rats.


   FOOTNOTES
 
2 Abbreviations used: BMD, bone mineral density; DEXA, dual-energy X-ray absorptiometry; DFAIII, difructose anhydride III; D-Pyr, deoxypyridinoline. Back

Manuscript received 2 July 2003. Initial review completed 28 July 2003. Revision accepted 15 September 2003.


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 MATERIALS AND METHODS
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 DISCUSSION
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