Abstract
This study evaluates the effect of three calcium levels in the diet (normal, moderate, and severe calcium depletion) on bone metabolism of male Wistar rats during their growth period. Bone mineral density (BMD) and femur length were determined in vivo during the growth stage using a single X-ray transmission system. The apparent calcium absorption was calculated in the rat adolescent and adulthood stages. At the end of the experiment, calcium concentrations in serum and urine were analyzed. The bones were evaluated postmortem to corroborate in vivo analyses. Microstructural properties of cortical and trabecular tissues of femurs bones were assessed using scanning electron microscopy. Bone mineral contents (Mg, Ca, P, and K) were quantified by inductively coupled plasma. Severe calcium depletion in the diets in the development stage affects the bone quality parameters such as bone mineral density and mineral content. Moreover, it was found thinner cortical and trabecular bone areas. Additionally, it was found that severe calcium depletion increased the apparent absorption of calcium as a defense mechanism, but with the decrease of the BMD peak, and the thickness of cortical bone as well as trabecular bone porosity. The severe calcium depletion increased the efficiency of apparent absorption calcium as a defense mechanism, but, even so, decreases the BMD peak as well as the thickness of cortical bone and trabecular bone porosity.
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Hunt JR, Hunt CD, Zito CA, Idso JP, Johnson LK (2008) Calcium requirements of growing rats based on bone mass, structure, or biomechanical strength are similar. The J Nutr 138:1462–1468. https://doi.org/10.1093/jn/138.8.1462
Ito S, Ishida H, Uenishi K, Murakami K, Sasaki S (2011) The relationship between habitual dietary phosphorus and calcium intake, and bone mineral density in young Japanese women: a cross-sectional study. Asia Pac J Clin Nutr 20:411–717
Viguet-Carrin SV, Hoppler M, Membrez SF, Vuichoud J, Vigo M, Offord EA, Ammann P (2014) Peak bone strength is influenced by calcium intake in growing rats. Bone 68:85–91. https://doi.org/10.1016/j.bone.2014.07.029
Buchowski MS, Semenya J, Johnson AO (2002) Dietary calcium intake in lactose maldigesting intolerant and tolerant African-American women. J Amer Coll Nutr 21(1):47–54. https://doi.org/10.1080/07315724.2002.10719193
Aguilera-Barreiro MDA, Rivera-Márquez JA, Trujillo-Arriaga HM, Tamayo-Orozco JA, Barreira-Mercado E, Rodríguez-García ME (2013) Intake of dehydrated nopal (Opuntia ficus índica) improves bone mineral density and calciuria in adult Mexican women. Food Nutr Res 57(1):19106–19115
Calvo MS, Uribarri J (2013) Public health impact of dietary phosphorus excess on bone and cardiovascular health in the general population. Am J Clin Nutr 1:6–15
Takeda E, Yamamoto H, Yamanaka-Okumura H, Taketani Y (2012) Dietary phosphorus in bone health and quality of life. Nutr Rev 70:311–321
Anderson JJ (1996) Calcium, phosphorous and human bone development. J Nutr 126(4):1153S–1158S
Koshihara M, Mayuzama R, Uehara M, Susuky K (2004) Effect of dietary calcium: phosphorus ratio on bone mineralization and intestinal calcium absorption in ovariectomized rats. Biofactors 22(1-4):39–42
Peterson CA, Eurell JAC, Erdman JW (1995) Alterations in calcium intake on peak bone mass in the female rats. J Bone Miner Res 10(1):81–95
Wachter WJ, Krischak GD, Mentzel M, Sarkar MR, Ebinger T, Hinzl L, Claes L, Augat P (2002) Correlation of bone mineral density with strength and microstructural parameters structural parameters of cortical bone in vitro. Bone 3(1):90–95
Pineda-Gomez P, Hernandez-Becerra E, Rojas-Molina I, Rosales-Rivera A, Rodriguez-Garcia ME (2019) The effect of calcium deficiency on bone properties in growing rats. Curr Nutr & Food Sci 15(5):1–5. https://doi.org/10.2174/1573401314666180919142102
Reeves PG, Nielsen FH, Fahey JGC (1993) AIN-93 purified diets for laboratory rodents, final report of the American Institute of Nutrition ad hoc writing committee on reformulation of the AIN-76A rodent diet. J Nutr 123:1939–1951
Hernández-Becerra E, Gutiérrez-Cortez E, Del Real A, Rojas-Molina A, Rodriguez-Garcia ME, Rubio E, Quintero-Garcia M, Rojas-Molina JI (2017) Bone mineral density, mechanical, microstructural properties and mineral content of the femur in growing rats fed with Opuntia ficus indica as calcium source in diet. Nutrients 9(2):108–125. https://doi.org/10.3390/nu9020108
Miyazato S, Nakagawa C, Kishimoto Y, Tagami H, Hara H (2010) Promotive effects of resistant maltodextrin on apparent absorption of calcium, magnesium, iron and zinc in rats. Eur J Nutr 49(3):165–171
Hernández-Becerra E, Mendoza-Avilez M, Jiménez-Mendoza M, Gutiérrez-Cortez E, Rodriguez-Garcia ME, Rojas-Molina I (2019) Effect of Nopal (Opuntia ficus indica) consumption at different maturity stages as an only calcium source on bone mineral metabolism in growing rats. J. Biol Trace Elem Res:1–9. https://doi.org/10.1007/s12011-019-01752-0
Jimenez-Mendoza D, Espinosa-Arbelaez DG, Giraldo-Betancur AL, Hernandez-Urbiola MI, Vargas-Vazquez D, Rodriguez-Garcia ME (2011) Single X-ray transmission system for bone mineral density determination. The Rev Sci Instr 82(12):125105–125111
Kim C, Park D (2013) The effect of restriction of dietary calcium on trabecular and cortical bone mineral density in the rats. J Exer Nutr Biochemy 17(4):123–131
Takakura I, Creasy DM, Yokoi R, Terashimaa Y, Onozato T, Maruyama Y, Chino T, Tahara T, Tamura T, Kuroda J, Kusama H (2013) Effects of male sexual maturity of reproductive endpoints relevant to DART studies in Wistar Hannover rats. J Toxicol 39(2):269–279
Sengupta P (2013) The laboratory rat: Relating its age with human’s. Int J Prev Med 4:624–630
Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M (2013) Mechanisms regulating skeletal muscle growth and atrophy. The FEBS J 280(17):4294–4314. https://doi.org/10.1111/febs.12253
Tamaki T, Uchiyama S (1995) Absolute and relative growth of rat skeletal muscle. Physiol Behav 57(5):913–919
Gallagher JC, Riggs BL, Eisman J, Hamstra A, Arnaud SB, DeLuca HF (1979) Intestinal calcium absorption and serum vitamin D metabolites in normal subjects and osteoporotic patients: effect of age and dietary calcium. The J Clin Invest 64:729–736
Bronner F (2003) Mechanisms of intestinal calcium absorption. J Cell Biochem 88(2):387–393
Mehrotra M, Gupta KS, Kumar K, Awassthi K, Dubey M, Pandey MC, Godbole M (2006) Calcium deficiency-induced secondary hyperparathyroidism and osteopenia are rapidly reversible with calcium supplementation in growing rabbit pups. Br J Nutr 95:582–590. https://doi.org/10.1079/BJN20051656
Londoño-Restrepo SM, Ramírez-Gutiérrez CF, Del Real A, Rubio-Rosas E, Rodríguez-García ME (2016) Study of bovine hydroxyapatite obtained by calcination at low heating rates and cooled in furnace air. J Mat Scien 51:4431–4441. https://doi.org/10.1007/s10853-016-9755-4
Creedon AFA, Cashman K (1999) The effect of moderately and severely restricted dietary magnesium intakes on bone composition and bone metabolism in the rat. The Brit J Nutr 82(1):63–71. https://doi.org/10.1017/S0007114599001130
Gruber HE, Rude RK, Wei L, Fausto A, Mills BG, Norton HJ (2003) Magnesium deficiency: effect on bone mineral density in the mouse appendicular skeleton. BMC Musculoskelet Disord 3:4–7
Acknowledgments
Ezequiel Hernández Becerra wishes to thank Consejo Nacional de Ciencia y Tecnología (CONACYT, México) for his Postdoctoral position at CFATA-UNAM-Juriquilla. We want to thank M. en I.Q Alicia del Real for the SEM and Mayté Juárez Meneses (Investigación Aplicada, Centro Universitario de Vinculación-BUAP) for their technical support.
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This project was supported by PAPIIT-UNAM project number IN112317.
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All procedures performed in studies involving animals were in accordance with the ethical standards of Mexican current regulation (NOM-062-ZOO-1999).
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Hernández-Becerra, E., Jímenez-Mendoza, D., Mutis-Gonzalez, N. et al. Calcium Deficiency in Diet Decreases the Magnesium Content in Bone and Affects Femur Physicochemical Properties in Growing Rats. Biol Trace Elem Res 197, 224–232 (2020). https://doi.org/10.1007/s12011-019-01989-9
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DOI: https://doi.org/10.1007/s12011-019-01989-9