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http://dx.doi.org/10.5307/JBE.2015.40.1.078

Review of Ca Metabolic Studies and a Model for Optimizing Gastrointestinal Ca Absorption and Peak Bone Mass in Adolescents  

Park, Jong-Tae (Department of Food Science and Technology, Chungnam National University)
Cho, Byoung-Kwan (Department of Biosystems Machinery Engineering, Chungnam National University)
Lee, Wang-Hee (Department of Biosystems Machinery Engineering, Chungnam National University)
Publication Information
Journal of Biosystems Engineering / v.40, no.1, 2015 , pp. 78-88 More about this Journal
Abstract
Purpose: The objective of this study is to review researches regarding factors that potentially affect adolescent calcium (Ca) metabolism, and to suggest a potential modeling approach for optimizing gastrointestinal Ca absorption and peak bone mass. Background: Optimal gastrointestinal Ca absorption is a key to maximizing peak bone mass in adolescents. Urine Ca excretion in adolescents rises only after bone accretion is saturated, indicating that higher intestinal Ca absorption and bone retention is necessary to ensure maximum bone accretion. Hence, maximizing peak bone mass is possible by controlling the factors influencing gastrointestinal Ca absorption and bone accretion. However, a mechanism that explains the unique adolescent Ca metabolism has not yet been elucidated. Review: Dietary factors that enhance gastrointestinal Ca absorption may increase the available Ca pool usable for bone accretion, and a specific hormone may direct optimal Ca utilization to maximize peak bone mass. IGF-1 is an endocrine hormone whose levels peak during adolescence and increase fractional Ca absorption and bone Ca accretion. Prebiotics, generally obtained from dietary sources, have been reported to exert a beneficial effect on Ca absorption via microbiota activity. We selected and reviewed three candidates that could be used to propose a comprehensive Ca metabolic model for optimal Ca absorption and peak bone mass in adolescents. Modeling: Modeling has been used to investigate Ca metabolism and its regulators. Herein, we reviewed previous Ca modeling studies. Based on this review, we proposed a method for developing a comprehensive model that includes regulatory effectors of IGF-1 and prebiotics.
Keywords
Calcium metabolism; Dietary protein; IGF-1; Mathematical modeling; Prebiotics;
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1 Abraham, A. K., D. E. Mager, X. Gao, M. Li, D. R. Healy and T. S. Maurer. 2009. Mechanism-based pharmacokinetic/pharmacodynamic model of parathyroid hormonecalcium homeostasis in rats and humans. The Journal of pharmacology and experimental therapeutics 330: 169-78.   DOI
2 Awumey, E. M and R. D. Bukoski. 2006. Cellular functions and fluxes of calcium. In: Calcium in Human Health, eds. C.M. Weaver and R.P. Heaney, pp. 13-5. Totowa, USA: Humana Press.
3 Bik, E. M., P. B. Eckburg, S. R. Gill, K. E. Nelson, E. A. Purdom, F. Francois, G. Perez-Perez, M. J. Blaser and D. A. Relman. 2006. Molecular analysis of the bacterial microbiota in the human stomach. Proceedings of the National Academy of Sciences of the United States of America 103:732-7.
4 Bouhnik, Y., L. Raskine, G. Simoneau, E. Vicaut, C. Neut, B. Flourie, F. Brouns and F. R. Bornet. 2004. The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: a double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study. American Journal of Clinical Nutrition 80:1658-64.   DOI
5 Bourrin, S., P. Ammann, J. P. Bonjour and R. Rizzoli. 2000. Dietary protein restriction lowers plasma insulin-like growth factor I (IGF-I), impairs cortical bone formation, and induces osteoblastic resistance to IGF-I in adult female rats. Endocrinology 141:3149-55.   DOI
6 Braun, M., B. R. Martin, M. Kern, G. P. McCabe, M. Peacock, Z. Jiang and C. M. Weaver. 2006. Calcium retention in adolescent boys on a range of controlled calcium intakes. American Journal of Clinical Nutrition 84:414-8.
7 Braun, M., C. Palacios, K. Wigertz, L. A. Jackman, R. J. Bryant, L. D. McCabe, B. R. Martin, G. P. McCabe, M. Peacock and C.M. Weaver. 2007. Racial differences in skeletal calcium retention in adolescent girls with varied controlled calcium intakes. American Journal of Clinical Nutrition 85:1657-63.   DOI
8 Bronner, F., D. Pansu and W. D. Stein. 1986. An analysis of intestinal calcium transport across the rat intestine. American Journal of Physiology 250:G561-9.
9 Bryant, R. J., M. E. Wastney, B. R. Martin, O. Wood, G. P. McCabe, M. Morshidi, D. L. Smith, M. Peacock and C. M. Weaver. 2003. Racial differences in bone turnover and calcium metabolism in adolescent females. Journal of Clinical Endocrinology and Metabolism 88:1043-7.   DOI
10 Budek, A. Z., C. Hoppe, K. F. Michaelsen, S. Bugel and C. Molgaard. 2007. Associations of total, dairy, and meat protein with markers for bone turnover in healthy, prepubertal boys. Journal of Nutrition 137:930-4.   DOI
11 Cadogan, J., R. Eastell, N. Jones and M. E. Barker. 1997. Milk intake and bone mineral acquisition in adolescent girls: randomised, controlled intervention trial. British Medical Journal 315:1255-60.   DOI
12 Chonan, O and M. Watanuki. 1995. Effect of galactooligosaccharides on calcium absorption in rats. Journal of Nutritional Science and Vitaminology (Tokyo) 41: 95-104.   DOI
13 Chonan, O and M. Watanuki. 1996. The effect of 6'-galactooligosaccharides on bone mineralization of rats adapted to different levels of dietary calcium. International Journal for Vitamin and Nutrition Research 66:244-9.
14 Chonan, O., K. Matsumoto and M. Watanuki. 1995. Effect of galactooligosaccharides on calcium absorption and preventing bone loss in ovariectomized rats. Bioscience, Biotechnology, and Biochemistry 59:236-9.   DOI
15 Chonan, O., R. Takahashi and M. Watanuki. 2001. Role of activity of gastrointestinal microflora in absorption of calcium and magnesium in rats fed beta1-4 linked galactooligosaccharides. Bioscience, Biotechnology, and Biochemistry 65:1872-5.   DOI
16 Dawson-Hughes, B and S. S. Harris. 2002. Calcium intake influences the association of protein intake with rates of bone loss in elderly men and women. American Journal of Clinical Nutrition 75:773-9.   DOI
17 Doty, S. E and R. C. Seagrave. 2000. Human water, sodium, and calcium regulation during space flight and exercise. Acta Astronautica 46:591-604.   DOI
18 Engelmann, D. T., T. L. Sie, H. H. Draper and R. R. Bell. 1975. Effect of a high protein intake on calcium metabolism in the rat. Journal of Nutrition 105:475-83.   DOI
19 Egert, M., A. A. de Graaf, H. Smidt, W. M. de Vos and K. Venema. 2006. Beyond diversity: functional microbiomics of the human colon. Trends in Microbiology 14:86-91.   DOI
20 El-Samad, H., J. P. Goff and M. Khammash. 2002. Calcium homeostasis and parturient hypocalcemia: an integral feedback perspective. Journal of Theoretical Biology 214:17-29.   DOI
21 Fatayerji, D., E. B. Mawer and R. Eastell. 2000. The role of insulin-like growth factor I in age-related changes in calcium homeostasis in men. Journal of Clinical Endocrinology and Metabolism 85:4657-62.
22 Fenton, T. R., M. Eliasziw, A. W. Lyon, S. C. Tough and D. A. Hanley. 2008. Meta-analysis of the quantity of calcium excretion associated with the net acid excretion of the modern diet under the acid-ash diet hypothesis. American Journal of Clinical Nutrition 88:1159-66.   DOI
23 Galvanin, F., S. Macchietto and F. Bezzo. 2007. Model-based design of parallel experiments. Industrial & Engineering Chemistry Research 46:871-82.   DOI
24 Heaney, R. P., S. Abrams, B. Dawson-Hughes, A. Looker, R. Marcus, V. Matkovic and C. M. Weaver. 2000. Peak bone mass. Osteoporosis International 11:985-1009.
25 Heaney, R. P., D. A. McCarron, B. Dawson-Hughes, S. Oparil, S. L. Berga, J. S. Stern, S. I. Barr and C. J. Rosen. 1999. Dietary changes favorably affect bone remodeling in older adults. Journal of the American Dietetic Association 99:1228-33.   DOI   ScienceOn
26 Jackman, L. A., S. S. Millane, B. R. Martin, O. B. Wood, G. P. McCabe, M. Peacock and C. M. Weaver. 1997. Calcium retention in relation to calcium intake and postmenarcheal age in adolescent females. American Journal of Clinical Nutrition 66:327-33.   DOI
27 Hill, K. M., M. Braun, M. Kern, B. R. Martin, J. W. Navalta, D. A. Sedlock, L. McCabe, G. P. McCabe, M. Peacock and C. M. Weaver. 2008. Predictors of calcium retention in adolescent boys. Journal of Clinical Endocrinology and Metabolism 93:4743-8.   DOI
28 Hunt, J. R., L. K. Johnson and Z. K. Fariba Roughead. 2009. Dietary protein and calcium interact to influence calcium retention: a controlled feeding study. American Journal of Clinical Nutrition 89:1357-65.   DOI
29 Hurwitz, S., S. Fishman and H. Talpaz, H. 1987. Calcium dynamics: a model system approach. Journal of Nutrition 117:791-6.   DOI
30 Kerstetter, J. E., K. O. O'Brien, D. M. Caseria, D. E. Wall and K. L. Insogna. 2005. The impact of dietary protein on calcium absorption and kinetic measures of bone turnover in women. Journal of Clinical Endocrinology and Metabolism 90:26-31.   DOI
31 Kleerebezem, M and E. E. Vaughan. 2009. Probiotic and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annual Review of Microbiology 63:269-90.   DOI
32 Lee, W. H and B. K. Cho. 2012. Review on application of biosystem modeling: introducing 3 model-based approaches in studying Ca metabolism. Journal of Biosystems Engineering 37:258-64.   DOI
33 Lee, W. H and B. K. Cho. 2013. Mechanistic modeling in biosystem engineering: a review on mechanistic models of calcium metabolism. Food Engineering Progress 17:48-54.
34 Matkovic, V and J.Z. Ilich. 1993. Calcium requirements for growth: are current recommendations adequate? Nutrition reviews 51:171-80.
35 Lee, W. H., M. Wastney, G. Jackson, B. Martin and C. Weaver. 2011. Interpretation of 41Ca data using compartmental modeling in post-menopausal women. Analytical and Bioanalytical Chemistry 399:1613-22.   DOI
36 Margulies, M., M. Egholm, W. E. Altman, S. Attiya, J. S. Bader, L. A. Bemben, J. Berka, M. S. Braverman, Y. J. Chen, Z. Chen, S. B. Dewell, L. Du, J. M. Fierro, X. V. Gomes, B. C. Godwin, W. He, S. Helgesen, C. H. Ho, G. P. Irzyk, S. C. Jando, M. L. Alenquer, T. P. Jarvie, K. B. Jirage, J. B. Kim, J. R. Knight, J. R. Lanza, J. H. Leamon, S. M. Lefkowitz, M. Lei, J. Li, K. L. Lohman, H. Lu, V. B. Makhijani, K. E. McDade, M. P. McKenna, E. W. Myers, E. Nickerson, J. R. Nobile, R. Plant, B. P. Puc, M. T. Ronan, G. T. Roth, G. J. Sarkis, J. F. Simons, J. W. Simpson, M. Srinivasan, K. R. Tartaro, A. Tomasz, K. A. Vogt, G. A. Volkmer, S. H. Wang, Y. Wang, M. P. Weiner, P. Yu, R. F. Begley and J. M. Rothberg. 2005. Genome sequencing in microfabricated high- density picolitre reactors. Nature 437:376-80.   DOI
37 Martin, B. R., M. M. Braun, K. Wigertz, R. Bryant, Y. Zhao, W. Lee, A. Kempa-Steczko and C. M. Weaver. 2010. Fructo-oligosaccharides and calcium absorption and retention in adolescent girls. American Journal of Clinical Nutrition 29:382-6.   DOI
38 Matkovic, V., D. Fontana, C. Tominac, P. Goel and C. H. Chesnut III. 1990. Factors that influence peak bone mass formation: a study of calcium balance and the inheritance of bone mass in adolescent females. American Journal of Clinical Nutrition 52:878-88.   DOI
39 Mitchell, M. L., R. J. Hermos, A. Schoepfer and J. M. Orson. 1990. Reference ranges for insulin-like growth factor-1 in healthy children and adolescents, determined with filter-paper blood specimens. Clinical Chemistry 36: 2138-9.
40 Nesbitt, T and M. K. Drezner. 1993. Insulin-like growth factor-I regulation of renal 25-hydroxyvitamin D-1-hydroxylase activity. Endocrinology 132:133-8.   DOI
41 Perez-Conesa, D., G. Lopez and G. Ros. 2007. Effects of probiotic, prebiotic and synbiotic follow-up infant formulas on large intestine morphology and bone mineralisation in rats. Journal of the Science of Food and Agriculture 87:1059-68.   DOI
42 Park, C. Y., K. M. Hill, A. E. Elble, B. R. Martin, L. A. DiMeglio, M. Peacock, G. P. McCabe and C. M. Weaver. 2010. Daily supplementation with 25 mu g cholecalciferol does not Increase calcium absorption or skeletal retention in adolescent girls with low serum 25-hydroxyvitamin D. Journal of Nutrition 140:2139-44.   DOI
43 Perault-Staub, A. M., P. Tracqui and J. F. Staub. 1992. Modelling of in vivo calcium metabolism. I. Optimal cooperation between constant and rhythmic behaviours. Acta Biotheoretica 40:95-102.   DOI
44 Peterson, M. C and M. M. Riggs. 2010. A physiologically based mathematical model of integrated calcium homeostasis and bone remodeling. Bone 46:49-63.   DOI
45 Raposo, J. F., L. G. Sobrinho and H. G. Ferreira. 2002. A minimal mathematical model of calcium homeostasis. Journal of Clinical Endocrinology and Metabolism 87:4330-40.   DOI
46 Raschka, L and H. Daniel. 2005. Mechanisms underlying the effects of inulin-type fructans on calcium absorption in the large intestine of rats. Bone 37:728-35.   DOI
47 Rastall, R. A., G. R. Gibson, H. S. Gill, F. Guarner, T. R. Klaenhammer, B. Pot, G. Reid, I. R. Rowland and M. E. Sanders. 2005. Modulation of the microbial ecology of the human colon by probiotics, prebiotics and synbiotics to enhance human health: an overview of enabling science and potential applications. FEMS Microbiology Ecology 52:145-52.   DOI
48 Schurch, M. A., R. Rizzoli, D. Slosman, L. Vadas, P. Vergnaud and J. P. Bonjour. 1998. Protein supplements increase serum insulin-like growth factor-I levels and attenuate proximal femur bone loss in patients with recent hip fracture. A randomized, double-blind, placebo-controlled trial. Annals of Internal Medicine 128:801-9.   DOI
49 Russo, A., L. Holmquist and A. Elixhauser, 2009. U.S. Hospitalizations Involving Osteoporosis and Injury, 2006. Agency for Healthcar Research and Quality. Available at: http://www.silverbook.org.
50 Scheppach, W., P. Bartram, A. Richter, F. Richter, H. Liepold, G. Dusel, G. Hofstetter, J. Ruthlein and H. Kasper. 1992. Effect of short-chain fatty acids on the human colonic mucosa in vitro. Journal of Parenteral and Enteral Nutrition 16:43-8.   DOI
51 Sheikh, M. S., L. R. Schiller and J. S. Fordtran. 1990. In vivo intestinal absorption of calcium in humans. Mineral and electrolyte metabolism 16:130-46.
52 Shrestha, R. P., C. V. Hollot, S. R. Chipkin, C. P. Schmitt and Y. Chait. 2010. A mathematical model of parathyroid hormone response to acute changes in plasma ionized calcium concentration in humans. Mathematical Biosciences 226:46-57.   DOI
53 Slavin, J. 2013. Fiber and prebiotics: Mechanisms and health benefits. Nutrients 5:1417-35.   DOI
54 Spence, L. A., E. R. Lipscomb, J. Cadogan, B. Martin, M. E. Wastney, M. Peacock and C. M. Weaver. 2005. The effect of soy protein and soy isoflavones on calcium metabolism in postmenopausal women: a randomized crossover study. American Journal of Clinical Nutrition 81:916-22.   DOI
55 Tracqui, P., J. F. Staub and A. M. Perault-Staub. 1992. Modelling of in vivo calcium metabolism. II. Minimal structure or maximum dynamic diversity: the interplay of biological constraints. Acta Biotheoretica 40:103-11.   DOI
56 Wastney, M. E., J. Ng, D. Smith, B. R. Martin, M. Peacock and C. M. Weaver. 1996. Differences in calcium kinetics between adolescent girls and young women. American Journal of Physiology 271:R208-16.
57 Vatanparast, H., D. A. Bailey, A. D. Baxter-Jones and S. J. Whiting. 2007. The effects of dietary protein on bone mineral mass in young adults may be modulated by adolescent calcium intake. Journal of Nutrition 137: 2674-9.   DOI
58 Wastney, M. E., Y. Zhao and S. M. Smith. 2005. Modelling human calcium dynamics as a mechanism for exploring changes in calcium homeostasis during space flight. In: Mathematical Modelling in Nutrition and Toxicology, eds. J. Hargrove and C. Berdanier, pp. 157-70. Athens, GA, USA: Mathematical Biology Press, Athens.
59 Wastney, M. E., B. H. Patterson, O. A. Linares, P. C. Greif and R. C. Boston. 1999. Investigating Biological Systems Using Modeling: Strategies and Software. San Diego: Academic Press.
60 Weaver, C. M., B. R. Martin, J. A. Story, I. Hutchinson and L. Sanders. 2010. Novel fibers increase bone calcium content and strength beyond efficiency of large intestine fermentation. Journal of Agricultural and Food Chemistry 58:8952-7.   DOI
61 Weaver, C. M., B. R. Martin, K. L. Plawecki, M. Peacock, O. B. Wood, D. L. Smith and M. E. Wastney. 1995. Differences in calcium metabolism between adolescent and adult females. American Journal of Clinical Nutrition 61:577-81.   DOI
62 Weaver, C. M., M. Peacock, B. R. Martin, G. P. McCabe, J. Zhao, D. L. Smith and M. E. Wastney. 1997. Quantification of biochemical markers of bone turnover by kinetic measures of bone formation and resorption in young healthy females. Journal of Bone and Mineral Research 12:1714-20.   DOI
63 Wigertz, K., C. Palacios, L. A. Jackman, B. R. Martin, L. D. McCabe, G. P. McCabe, M. Peacock, J. H. Pratt and C. M. Weaver. 2005. Racial differences in calcium retention in response to dietary salt in adolescent girls. American Journal of Clinical Nutrition 81:845-50.   DOI
64 Weaver, C. M., B. R. Martin, C. H. Nakatsu, A. P. Armstrong, A. Clavijo, L. D. McCabe, G. P. McCabe, S. Duignan, M. H. C. Schoterman and E. G. van den Heuvel. 2011. Galactooligosaccharides improve mineral absorption and bone properties in growing rats through gut fermentation. Journal of Agricultural and Food Chemistry 59:6501-10.   DOI
65 Whisner, C. M., B. R. Martin, C. H. Nakatsu, G. P. McCabe, L. D. McCabe, M. Peacock and C. M. Weaver. 2014. Soluble maize fibre affects short-term calcium absorption in adolescent boys and girls: a randomised controlled trial using dual stable isotopic tracers. British Journal of Nutrition 112:446-56.   DOI
66 Whisner, C. M., B. R. Martin, M. H. Schoterman, C. H. Nakatsu, L. D. McCabe, G. P. McCabe, M. E. Wastney, E. G. van den Heuvel and C. M. Weaver. 2013. Galactooligosaccharides increase calcium absorption and gut bifidobacteria in young girls: a double-blind crossover trial. British Journal of Nutrition 110:1292-303.   DOI
67 Wright, N. M., N. Papadea, B. Wentz, B. Hollis, S. Willi and N. H. Bell. 1997. Increased serum 1,25-dihydroxyvitamin D after growth hormone administration is not parathyroid hormone-mediated. Calcified Tissue International 61: 101-3.   DOI
68 Wu, L., B. R. Martin, M. M. Braun, M. E. Wastney, G. P. McCabe, L. D. McCabe, L. A. DiMeglio, M. Peacock and C. M. Weaver. 2010. Calcium requirements and metabolism in Chinese-American boys and girls. Journal of Bone and Mineral Research 25:1842-9.   DOI
69 Yakar, S., H. W. Courtland and D. Clemmons. 2010. IGF-1 and bone: New discoveries from mouse models. Journal of Bone and Mineral Research 25:2267-76.   DOI
70 Yakar, S and C. J. Rosen. 2003. From mouse to man: redefining the role of insulin-like growth factor-I in the acquisition of bone mass. Experimental Biology and Medicine (Maywood) 228:245-52.   DOI
71 Zhang, Q., M. E. Wastney, C. J. Rosen, W. G. Beamer and C. M. Weaver. 2011. Insulin-like growth factor-1 increases bone calcium accumulation only during rapid growth in female rats. Journal of Nutrition 141:2010-6.   DOI
72 Zhang, Q., G. Ma, H. Greenfield, K. Zhu, X. Du, L. H. Foo, X. Hu and D. R. Fraser. 2010. The association between dietary protein intake and bone mass accretion in pubertal girls with low calcium intakes. British Journal of Nutrition 103:714-23.   DOI   ScienceOn