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Oligofructose stimulates calcium absorption in adolescents^1,2,3

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Background: In rats, nondigestible oligosaccharides stimulate calcium absorption. Recently, this effect was also found in human subjects.

Objective: The objective of the study was to investigate whether consumption of 15 g oligofructose/d stimulates calcium absorption in male adolescents.

Design: Twelve healthy, male adolescents aged 14–16 y received, for 9 d, 15 g oligofructose or sucrose (control treatment) daily over 3 main meals. The treatments were given according to a randomized, double-blind, crossover design, separated by a 19-d washout period. On the 8th day of each treatment period, ⁴⁴Ca was given orally with a standard breakfast containing 200 mg Ca. Within half an hour after administration of ⁴⁴Ca, ⁴⁸Ca was administered intravenously. Fractional calcium absorption was computed from the enrichment of ⁴⁴Ca:⁴³Ca and ⁴⁸Ca:⁴³Ca in 36-h urine samples, which was measured by inductively coupled plasma mass spectrometry.

Results: An increase in true fractional calcium absorption (%) was found after consumption of oligofructose (mean difference ± SE of difference: 10.8 ± 5.6; P < 0.05, one sided). The results are discussed in relation to the methods used.

Conclusion: Fifteen grams of oligofructose per day stimulates fractional calcium absorption in male adolescents.

Key Words: Oligofructose • true calcium absorption • male adolescents • double stable-isotope technique • nondigestible oligosaccharides

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Oligofructose is a mixture of oligosaccharides composed of fructose units linked together by ß(21) linkages. Part of these molecules are terminated by a glucose. The total number of fructose or glucose units in an oligofructose molecule generally ranges between 2 and 8.

Like other nondigestible oligosaccharides (NDOs), oligofructose resists hydrolysis by human alimentary enzymes (1), but is fermented by colonic microbiota and induces a decrease in the pH of the human culture medium (2). Because of this cecocolonic fermentation, large amounts of short-chain fatty acids (SCFAs) are produced, which may cause a trophic effect on intestinal epithelium as well as on the triacylglycerol- and cholesterol-lowering effects of these NDOs (1). In addition, NDOs have been shown to improve mineral absorption in rats (3–5). In healthy, adult men (mean age: 22 y) a positive effect of 40 g of the NDO inulin daily on apparent calcium absorption was found by using the chemical balance technique (6). The positive effect found in rats (3–5) and humans (6) likely originates predominantly in the colon. Younes et al (7) showed that the large intestine is a major site of calcium absorption when acidic fermentation takes place. Contrary to the results of Coudray et al (6), we did not find an effect of 15 g/d inulin, oligofructose, or galactooligosaccharides on true calcium or iron absorption in adult men (mean age: 23 y) when we used stable-isotope techniques (8). This finding might have resulted because we used a lower NDO concentration than used by Coudray et al. However, 17 g NDO/d also had no effect on apparent calcium absorption in ileostomy subjects (mean age: 54 y) (9).

Therefore, it is also possible that our previous study (8) did not include the colonic component of calcium absorption because calcium absorption was calculated from the enrichment of both isotopes in 24-h urine samples: calcium absorption takes >24 h after isotope administration to be complete (10).

In addition, the stimulating effect of a more plausible dose of oligofructose on mineral absorption could be more pronounced in younger volunteers, whose calcium requirement is larger. Therefore, the aim of the present study was to investigate whether 15 g oligofructose/d stimulates true absorption of calcium in male adolescents aged 14–16 y. A supplement of 15 g NDO/d to the diet is feasible by using NDO-enriched products and raises substantially the total amount of NDOs in the diet (from 4 to 19 g/d) without bringing about symptoms of intolerance because the first symptoms of intolerance (eg, excessive flatus) are expected at intakes >30 g NDO/d (11). True fractional absorption was measured by using the double stable-isotope technique. Colonic calcium absorption was included by extending the collection of urine over 36 h instead of 24 h after isotope administration.

	SUBJECTS AND METHODS

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Subjects
Subjects were recruited through an advertisement in a local newspaper. Twelve healthy boys were selected for the study. On the basis of our experience with adults, we calculated that with 12 subjects a difference of 5% true calcium absorption could be detected with a power of 90%. At the start of the study, the subjects were aged 14–16 y (: 15.3 y) and their body mass index (in kg/m²) was between 16.0 and 20.7 (: 18.4). Normal health was assessed at prestudy screening, which included a medical history, a physical examination, measurements of blood pressure and heart rate, and routine clinical laboratory tests. The study protocol was approved by the TNO external Medical Ethics Committee and all subjects and their parents signed informed consent forms.

Preparation of stable-isotope solutions
The double stable-isotope technique involves the administration of 2 stable isotopes, one orally and one intravenously. Taking the amount administered and the natural abundances of these stable isotopes into account, true fractional calcium absorption can be calculated from the enrichment of both stable isotopes in a urine sample (12). The isotopic labels were obtained from NEDRAY (Bunschoten, Netherlands) in the form of calcium carbonate. The abundances of the different isotopic labels, as determined by inductively coupled plasma mass spectrometry (ICPMS), were as follows: enriched ⁴⁴Ca (3.39% ⁴⁰Ca, 0.06% ⁴²Ca, 0.03% ⁴³Ca, 96.5% ⁴⁴Ca, <0.01% ⁴⁶Ca, and 0.02% ⁴⁸Ca) and enriched ⁴⁸Ca (8.96% ⁴⁰Ca, 0.09% ⁴²Ca, 0.02% ⁴³Ca, 0.24% ⁴⁴Ca, <0.01% ⁴⁶Ca, and 90.69% ⁴⁸Ca). One subject was given calcium enriched in ⁴⁴Ca that was leftover from an earlier experiment, which had the following enrichment: 2.80% ⁴⁰Ca, 0.05% ⁴²Ca, 0.02% ⁴³Ca, 97.1% ⁴⁴Ca, <0.002% ⁴⁶Ca, and 0.03% ⁴⁸Ca. The ⁴⁴Ca carbonate was converted into chloride salt, diluted with deionized water, and then adjusted to a pH of 5. A similar procedure was followed for ⁴⁸Ca carbonate, except that saline was used instead of deionized water (13). After filtration, the solution was distributed into 10-mL injection bottles and sterilized for 25 min.

Study design
The subjects were asked to maintain their normal food intake during the study as best as possible, but to restrict consumption of fiber-rich and oligosaccharide-containing food products. During the two 9-d treatment periods, subjects drank 100 mL orange juice containing 5 g oligofructose or the control treatment (fine-powdered sucrose) 3 times daily (at breakfast, lunch, and dinner). Oligofructose is obtained by partial enzymatic hydrolysis of inulin, which is prepared by hot-water extraction of chicory roots. Because the pure oligosaccharide content of the oligofructose-containing product (Raftilose P95; ORAFTI, Tienen, Belgium) was not 100% (Table 1), the weight of oligofructose was adjusted for a constant intake of 5 g pure oligofructose. Aspartame was added to the oligofructose-containing product to obtain the same sweetness as the control treatment. The treatments were given to the subjects according to a randomized, crossover design. This strictly controlled study was double blind.

For the calcium absorption test, the orange juice containing the study substance was extrinsically labeled with ⁴⁴Ca and given to the subjects with a standard breakfast (with 200 mg Ca) on the 8th day of each treatment period after a 12-h overnight fast. No food or drinks were allowed, except for water, for 4 h after ⁴⁴Ca administration. ⁴⁸Ca was administered intravenously within 30 min after the oral administration of ⁴⁴Ca. Before and after the bolus injection, blood pressure and heart rate were recorded for safety reasons.

The exact quantity of isotopes given by each route, as calculated by weighing the bottles or syringes before and after administration, was 14.0 mg (range: 13.0–15.5 mg) true ⁴⁴Ca and 1.15 mg (range: 1.09–1.16 mg) true ⁴⁸Ca. ⁴⁴Ca:⁴³Ca and ⁴⁸Ca:⁴³Ca values in urine collected before isotope administration (basal urine sample) and over the 36 h after administration were used to compute fractional calcium absorption according to the formula reported by van Dokkum et al (12).

Stable-isotope analysis
⁴⁴Ca:⁴³Ca and ⁴⁸Ca:⁴³Ca in basal and 36-h urine samples were measured by ICPMS (Elan 500; Perkin-Elmer Sciex,, Norwalk, CT). The accuracy of this method was evaluated by analyzing enriched urine samples with our inductively coupled plasma mass spectrometer and a thermal ionization mass spectrometer. Comparable results were found with both methods, as described by Luten et al (15).

All measurements were carried out in isotope-ratio peak hopping mode. ICPMS was operated in the high-resolution mode to provide maximal accuracy. Typical conditions for operations were as follows: plasma power 1.2 kW, reflected power <5 W, coolant argon flow rate 18 L/min, dwell time 20 ms, 1 measurement per peak, 10 repeats per integration, and total measuring time 270 s.

Trichloroacetic acid (3.5%) was added to the urine samples for deproteinization. The calcium was concentrated by precipitation of calcium with saturated ammonium oxalate and dissolution of the formed calcium oxalate into 1.2 mol HCl/L (15). The calcium concentration in the HCl solution was measured by atomic absorption spectrometry and, if necessary, adjusted by dilution to 10 mg Ca/L.

The prepared urine samples taken during each treatment, before and after isotope administration for the same subject, were tested within 1 d. Between each 4 urine samples, one standard solution of 10 mg Ca/L and one blank solution were measured. Mean ⁴⁴Ca:⁴³Ca values of the standard solutions, measured within 1 d, ranged between 15.560% and 15.858% (CV: 0.26–0.77%). Mean ⁴⁸Ca:⁴³Ca values ranged between 1.463% and 1.587% (CV: 0.46–1.75%). All values were adjusted for minor deviations from standard calcium solutions with accepted natural ratios. All samples were measured in duplicate.

Statistics
Statistically, the null hypothesis was that there would be no positive effect of oligofructose consumption on calcium absorption. Because the animal experiments and the study in humans of Coudray et al (6) indicated a positive effect of NDOs on calcium absorption and because our first human study (8) did not indicate a negative effect of oligofructose on mineral absorption, the alternative hypothesis was that there would be a positive effect of 15 g oligofructose/d on calcium absorption. The null hypothesis was to be rejected at the 0.05 level of probability (one sided). Because one sample was lost, the differences in calcium absorption between treatments were evaluated by using the general linear models procedure for an unbalanced analysis of variance (ANOVA) (16). ANOVA was used to be able to include the advantages of a crossover design.

	RESULTS

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All subjects completed the study; however, the 36-h urine sample of subject 12, collected during the treatment with oligofructose, was lost. Compliance, as checked by returned test substances and questionnaires, was good. On day 6 of the first treatment period, 2 subjects forgot to drink their orange juice containing the study substance at dinnertime. Reports of gastrointestinal complaints were no higher after consumption of 15 g oligofructose/d than after the control treatment.

All samples were measured in duplicate. Within-duplicate CVs were 0.30% for ⁴⁴Ca:⁴³Ca and 0.82% for ⁴⁸Ca:⁴³Ca. Because of small amounts of calcium in some basal urine samples, no reliable counts (outside the 95% upper limit of confidence) could be measured by ICPMS. In these cases, the mean basal ratio per treatment period was used. The average basal value for ⁴⁴Ca:⁴³Ca (n = 20) was 15.46% (CV: 0.22%) and for ⁴⁸Ca:⁴³Ca (n = 19) was 1.407% (CV: 1.70%). The average enrichment value (n = 23) was 4.8% (range: 2.9–8.2%) for urinary ⁴⁴Ca:⁴³Ca and 8.8% (range: 5.0–12.5%) for urinary ⁴⁸Ca:⁴³Ca.

Mean basal and enriched ⁴⁴Ca:⁴³Ca and ⁴⁸Ca:⁴³Ca values and the mean percentage enrichment of these ratios by treatment are shown in Table 2. Mean (±SD) calcium absorption during the control treatment was 47.8 ± 16.4% (n = 12) and during the treatment with 15 g oligofructose/d (n = 11) was 60.1 ± 17.2%. Mean and individual changes in calcium absorption are shown in Figure 1. There was an increase in percentage calcium absorption (%) after consumption of oligofructose (mean difference ± SE of the difference: 10.8 ± 5.6; P < 0.05, one sided).

View larger version (17K): [in this window] [in a new window]   FIGURE 1. Individual changes in calcium absorption in male adolescents after consumption of 15 g oligofructose/d or a control substance. The thick black line represents the mean change in calcium absorption (mean difference ± SE of difference = 10.8 ± 5.6; P < 0.05, one sided).

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
An increase in true fractional calcium absorption was found in male adolescents after consumption of oligofructose. In addition, the study in humans by Coudray et al (6) and experiments in rats (3, 4) showed a positive effect of NDOs on apparent calcium absorption. Contrary to these results, we did not find an effect of NDOs on true calcium absorption in an earlier study (8). This might have been because colonic calcium absorption was not considered in that study. Coudray et al's study (6) and most experiments in rats used the chemical balance technique to measure apparent calcium absorption. The advantage of the chemical balance technique is that it measures complete calcium absorption, including that from the colon. Absorption from the colon should be considered when investigating the effect of NDOs on calcium absorption, mainly because the large intestine may represent a major site of calcium absorption when acidic fermentation take place (7), but also because it is hypothesized that SCFAs, produced during fermentation of NDOs, improve calcium absorption through an exchange of intracellular H⁺ for Ca²⁺ in the distal colon (17). Experiments in rats have shown that fermentable oligosaccharides facilitate colorectal (18) and cecal absorption of calcium (3, 19). A disadvantage of the chemical balance technique, however, is that it does not distinguish between unabsorbed and endogenously secreted minerals, so true absorption cannot be determined. This was the main reason for using the double stable-isotope technique in the present study. In addition, we compared the results of the present study with those of our earlier study in humans (8). The measurement of colonic calcium absorption was included by extending the collection of urine from 24 h to 36 h after isotope administration.

One of the oldest approaches developed for the measurement of true fractional calcium absorption is determination of the ratio of isotopes excreted in complete urine collections. This method was used in our work with stable isotopes administered orally in a single meal (8, 12). Use of complete urine collections over a period of time instead of a single urine or blood sample gives better approximations of fractional calcium absorption (20, 21) because intravenously injected isotopes and absorbed orally administered isotopes do not necessarily arrive in the bloodstream at the same time or are metabolized in parallel. Measurement of isotopes in a complete 24-h urine sample largely reflects the ratio of the areas under the plasma disappearance curves for the 2 isotopes (20) and is therefore much less dependent on equal metabolic kinetics of the orally and intravenously administered isotopes. Measurement of calcium absorption, based on 24-h urinary excretion of isotopes, is a proven, valid method; therefore, there is no reason to doubt the validity of the method when urine collection is extended to 36 h to include colonic calcium absorption.

Nevertheless, we cannot exclude the possibility that the metabolic kinetics of calcium absorbed in the colon are different from those of calcium absorbed earlier in the duodenum or ileum or from that of the injected isotope because of the lag time between the entrance of these isotopes in the blood and the existence of a diurnal rhythm in the metabolism of calcium (22, 23). Such a bias would, however, not change the outcome of the present study because such a bias would exist with both treatments.

If the only difference between the earlier and the present study in humans had been the duration of urine collection, we have speculated that most of the enhancement of calcium absorption due to oligofructose takes place in the large intestine. However, there were other differences between the 2 studies: age, the duration of adaptation to oligofructose consumption, and the carrier dose of calcium given at breakfast with the stable isotopes.

Calcium absorption was not correlated with urinary calcium excretion, which is consistent with the results found in white girls and boys (24, 25). Apparently, during the period of bone development, absorbed calcium is largely taken up by the bone tissue so that no relation between absorption and urinary excretion becomes apparent. The oligofructose-induced enhancement of calcium absorption was not reflected by an increase in urinary calcium excretion. Moreover, the enrichment of ⁴⁸Ca:⁴³Ca, and hence the excretion of injected calcium, was not affected by oligofructose. In rats, a positive effect of nondigestible carbohydrates on bone development was found (26–28). Therefore, oligofructose may help to maximize the peak bone mass in boys.

In conclusion, 15 g oligofructose/d increases calcium absorption in adolescent boys. More research is warranted to explore in which part of the intestine the oligofructose-induced enhancement takes place and whether it can improve calcium balance in humans.

	ACKNOWLEDGMENTS

 
We are grateful to P van Aken-Schneyder, I van Assum-van den Ziel, FW Sieling, C Kistemaker, and EJ Brink for technical assistance.

	FOOTNOTES

 
¹ From the TNO Nutrition and Food Research Institute, Department of Physiology, Zeist, Netherlands.

² Supported by the European Union and ORAFTI sa, Tienen, Belgium.

³ Reprints not available. Address correspondence to EGHM van den Heuvel, TNO Nutrition and Food Research Institute, Department of Physiology, PO Box 360, 3700 AJ Zeist, Netherlands. E-mail: vandenheuvel{at}Voeding.TNO.NL.

	REFERENCES

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