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U.S. Department of Agriculture/ARS Children's Nutrition Research Center and Texas Children's Hospital, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030
* To whom correspondence should be addressed. E-mail: sabrams{at}bcm.edu.
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ABSTRACT |
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Introduction |
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We have recently published the results of a blinded, controlled trial into the effects of a mixture of inulin-type fructan5 (ITF) on calcium absorption and bone mineral mass accumulation in young adolescents (3). We found a significant benefit to calcium absorption after both 8 and 52 wk compared with placebo controls. However, not all subjects who received the ITF responded with an increase in calcium absorption. In particular, we found that about two-thirds of subjects who received the ITF responded with an increase in calcium absorption >3%. This result was similar to our previous studies in this age group (4,5). In this article, we consider further this aspect of the response to ITF and the implications of these findings for dietary and nutritional guidance.
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Methods |
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Written informed consent was obtained from a parent or legal guardian for each subject; written assent was obtained from all of the study subjects. The Institutional Review Board of Baylor College of Medicine and Affiliated Hospitals approved this protocol.
Within 8 wk of the screening visit described above, subjects were admitted for 24 h to the General Clinical Research Center of Texas Children's Hospital in Houston. During this stay, measurements of calcium absorption and bone mineralization were carried out.
At the end of this baseline study, subjects were randomized, in a double-blinded fashion, and stratified by gender to 1 of 2 carbohydrate supplement groups: either 8 g/d of an ITF, the Synergy (Orafti N.V., Tienen, Belgium), or maltodextrin as placebo. Subjects were instructed to mix the carbohydrate supplement with 180–240 mL of calcium-fortified orange juice and to drink it with breakfast daily for 12 mo. To provide some dietary variation, subjects were also allowed to use milk to mix the carbohydrate supplement. Dietary recalls and discussions with families demonstrated that all subjects primarily used orange juice, and this accounted for over 95% of total study days.
After 8 wk of receiving the carbohydrate supplement to which they had been randomized, subjects returned for a calcium absorption study. Twelve months after the initial baseline study, they returned for a follow-up visit in which measurements of calcium absorption and bone mineral content (BMC) were performed.
Stable isotope studies were performed as previously described (4–6). Most subjects received a breakfast that contained approximately one-third of their daily intake of calcium (including the tracer-containing juice). Toward the end of breakfast, subjects were given 20 µg of 46Ca that had been mixed with 240 mL of calcium-fortified orange juice. Whole-body BMC was determined using a Hologic QDR-4500A dual-energy x-ray (DXA) absorptiometer scanning in the fan-beam mode.
Comparisons of responders and nonresponders were made using a generalized linear model (ANOVA). Analysis also included those who did not receive the ITF with post-hoc paired analysis performed when the initial differences were significant (P < 0.05). Gender, ethnicity, and Tanner stage at enrollment were included as covariates in all models; other covariates depended on the specific analysis being carried out. Analyses were performed using SPSS 13.0 for Windows (SPSS). All data are presented as the mean ± SEM, and values are considered significant when P < 0.05.
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Results |
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65–75 mg/d in responders. We further considered whether a response in calcium absorption at 8 wk (as previously defined by an increase in calcium absorption from baseline of >3.0%) was predictive of a benefit to bone mineral accretion over the entire year. In this case, using ethnicity, Tanner stage, and gender as covariates, we found that responders at 8 wk had a significantly greater increment in whole-body BMC over the entire year (n = 31 responders and 16 nonresponders because DXA data were not available for 1 responder). The net difference in whole-body BMC accumulation was 47.9 ± 23 g/y (P = 0.04). Calculating the net difference in daily calcium accretion to the skeleton based on the DXA data demonstrated that responders had a greater daily calcium accretion (retention) compared with nonresponders and those who did not receive Synergy 1 (Table 2).
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Discussion |
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30 mg of additional daily calcium accretion to the skeleton, which was equivalent to 11 g of calcium for each year of pubertal growth. In this analysis, we found that an increase in calcium absorption at 8 wk predicted a substantial benefit in both short-term calcium absorption compared with placebo or to nonresponders and long-term whole-body bone mineral accumulation. From the values derived from DXA results, it can be calculated that 15 g of additional calcium would be added to the skeleton each year in responders compared with nonresponders. This amount of calcium is about approximately equal to 10–15% of the annual rate of skeletal calcium accretion. The magnitude of this change may be a result of the definition of response used. However, the finding that our definition of response at 8 wk was associated with longer-term advantages in bone mineralization compared with subjects who did not respond to ITF lends support to this general type of definition. With this analysis we confirm that a short-term marker of ITF response is associated with a longer-term change in a physiological important parameter (whole-body BMC).
Although the primary analysis of placebo vs. all subjects who received the Synergy remains the principal outcome of the study, this newer analysis of responders is a reasonable approach to consider as well. Multiple investigations into the effect of ITF on calcium absorption (4–6) have identified populations of both responders and nonresponders. Response may be affected by genetics, usual inulin intake, other aspects of diet, and/or unidentified factors including compliance with the intervention or diet. It is reasonable to consider the relative ITF benefit and how it might relate to other potential interventions. There are no dietary or other interventions in children or adolescents other than increasing calcium intake that have been shown to have this magnitude of long-term effect (1). Data regarding vitamin D supplementation are minimal at this point in young adolescents (9). The net benefit in retained calcium of 65 mg/d, if one assumes a retention fraction of 25% (dietary calcium source) or 20% (if given as a pill supplement), would require a dietary increase in calcium intake or calcium supplement of 250–320 mg/d.
It is advocated that young adolescents achieve an intake of calcium at the current AI of 1300 mg/d. However, calcium intakes of 900 mg/d, as seen in our study, are consistent with population data for adolescent girls in the United States and many other countries. Only a very small percentage of adolescent girls achieve intakes of 1300 mg/d (1,2). The effect of ITF to increase calcium absorption by an amount similar to what might occur with an increase in calcium intake of 250–320 mg/d would be the equivalent of moving the 50th percentile calcium intake in this population close to the 80th percentile of usual intakes for girls (1).
This magnitude of effect may not be maintained over a long period of time, but this may also be true for the use of dietary and other supplemental forms of calcium. A significant benefit to Synergy is maintained during the crucial pubertal bone growth peak. Thus, multiple strategies can and should be advocated to enhance the achievement of peak bone mass including both enhancement of calcium intake and calcium absorptive efficiency. As further understanding of the underlying mechanism determining response or nonresponse to interventions such as ITF is achieved, these strategies and their public health role will become more apparent.
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FOOTNOTES |
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2 Sources of Financial Support: This work is a publication of the U.S. Department of Agriculture/Agricultural Research Service (ARS) Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine and Texas Children's Hospital, Houston, TX. This project has been funded in part with federal funds from the U.S. Department of Agriculture/ARS under Cooperative Agreement number 58-6250-6-001, the NIH, NCRR General Clinical Research for Children Grant number RR00188, NIH AR43708 and NIDDK P30 DK56338. Orange juice used in the study was provided by The Coca-Cola Company, Houston, TX, and the inulin-type fructan by Orafti, N.V., Tienen, Belgium. Contents of this publication do not necessarily reflect the views or policies of the U.S. Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government.
3 Author disclosures: S. A. Abrams, I. J. Griffin, and K. M. Hawthorne, no conflicts of interest.
4 Abbreviations used: AI, adequate intake; BMC, bone mineral content; DXA, dual-energy x-ray absorptiometry; ITF, inulin-type fructan.
5 In these proceedings, the term inulin-type fructan shall be applied as a generic term to cover all ß–(2
1) linear fructans. In any other circumstances that justify the identification of the oligomers vs. the polymers, the terms oligofructose and/or inulin or eventually long-chain or high-molecular-weight inulin will be used, respectively. Even though the oligomers obtained by partial hydrolysis of inulin or by enzymatic synthesis have a slightly different DPav (4 and 3.6, respectively), the term oligofructose shall be used to identify both. Synergy will be used to identify the 30/70 mixture (wt:wt) of oligofructose and inulin HP otherwise named oligofructose-enriched inulin.
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LITERATURE CITED |
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1. Standing Committee on the Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board, Institute of Medicine. Dietary reference intakes for calcium, magnesium, phosphorus, vitamin D, and fluoride. Washington, DC: National Academy Press; 1997.
2. Greer FR, Krebs NF. Optimizing bone health and calcium intakes of infants, children and adolescents. Pediatrics. 2006;117:578–85.
3. Abrams SA, Griffin IJ, Hawthorne KM, Liang L, Gunn SK, Darlington G, Ellis KJ. A combination of prebiotic short-and long-chain inulin-type fructans enhances calcium absorption and bone mineralization in young adolescents. Am J Clin Nutr. 2005;82:471–6.
4. Griffin IJ, Davila PM, Abrams SA. Non-digestible oligosaccharides and calcium absorption in girls with adequate calcium intakes. Br J Nutr. 2002;87: Suppl 2:S187–91.[Medline]
5. Griffin IJ, Hicks PMD, Heaney RP, Abrams SA. Enriched chicory inulin increases calcium absorption mainly in girls with lower calcium absorption. Nutr Res. 2003;23:901–9.
6. Abrams SA. Using stable isotopes to assess mineral absorption and utilization by children. Am J Clin Nutr. 1999;70:955–64.
7. Heaney RP, Abrams SA. Improved estimation of the calcium content of total digestive secretions. J Clin Endocrinol Metab. 2004;89:1193–5.
8. Abrams SA, Griffin IJ, Hicks PD, Gunn SK. Pubertal girls only partially adapt to low dietary calcium intakes. J Bone Miner Res. 2004;19:759–63.[Medline]
9. Viljakainen HT, Natri AM, Karkkainen M, Huttunen MM, Palssa A, Jakobsen J, Cashman KD, Molgaard C, Lamberg-Allardt C. A positive dose-response effect of vitamin D supplementation on site-specific bone mineral augmentation in adolescent girls: a double-blinded randomized placebo-controlled 1-year intervention. J Bone Miner Res. 2006;21:836–44.[Medline]
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