Abstract
The aim of this 3-year prospective study was to examine changes in bone mineral characteristics during pubertal maturation in boys with different BMI values at the beginning of puberty and with different BMI increments during puberty. 26 boys with overweight and obesity (OWB) and 29 normal weight boys (NWB) were studied yearly for 3 years from the age of 11 years to measure the changes in different bone mineral characteristics. The OWB group was further divided into two subgroups according to extensive or non-extensive BMI increment during 3-year period. OWB had higher (P < 0.01) baseline total body (TB) bone mineral density (BMD), TB bone mineral content (BMC), TB BMC for height, lumbar spine (LS) BMD, and LS BMC compared to NWB. Throughout the study period, OWB gained more TB BMD (P = 0.0001), TB BMC (P = 0.0048), TB BMC for height (P = 0.0124), LS BMD (P = 0.0029), and LS BMC (P = 0.0022) compared to NWB. Also during the study period, TB BMD (P = 0.0065), TB BMC (P = 0.0141), TB BMC for height (P = 0.0199), LS BMD (P = 0.0066), LS apparent volumetric BMD (BMAD) (P = 0.0075), and LS BMC (P = 0.017) increased significantly less in those OWB whose BMI increased more extensively. Extensive BMI gain is associated with lower increments in bone mineral characteristics in boys with overweight and obesity. Unfavorable increment in total body fat mass and percentage during pubertal years could be one reason for that.
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Rizzoli R, Bianchi ML, Garabédian M, McKay HA, Moreno LA (2010) Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone 46(2):294–305. doi:10.1016/j.bone.2009.10.0
Baxter-Jones AD, Burrows M, Bachrach LK, Lloyd T, Petit M, Macdonald H, Mirwald RL, Bailey D, McKay H (2010) International longitudinal pediatric reference standards for bone mineral content. Bone 46(1):208–216. doi:10.1016/j.bone.2009.10.017
Vaitkeviciute D, Lätt E, Mäestu J, Jürimäe T, Saar M, Purge P, Maasalu K, Jürimäe J (2014) Physical activity and bone mineral accrual in boys with different body mass parameters during puberty: a longitudinal study. PLoS ONE 9(10):e107759. doi:10.1371/journal.pone.0107759
Mosca LN, da Silva VN, Goldberg TB (2013) Does excess weight interfere with bone mass accumulation during adolescence? Nutrients 5(6):2047–2061. doi:10.3390/nu5062047
El Hage R (2012) Geometric indices of hip bone strength in obese, overweight, and normal-weight adolescent boys. Osteoporos Int 23(5):1593–1600. doi:10.1007/s00198-011-1754-3
Dimitri P, Bishop N, Walsh JS, Eastell R (2012) Obesity is risk factor for fracture in children but is protective against fracture in adults: a paradox. Bone 50(2):457–466. doi:10.1016/j.bone.2011.05.011
Ivuskans A, Lätt E, Mäestu J, Saar M, Purge P, Maasalu K, Jürimäe T, Jürimäe J (2013) Bone mineral density in 11-13-year-old boys: relative importance of the weight status and body composition factors. Rheumatol Int 33(7):1681–1687. doi:10.1007/s00296-012-2612-0
Fintini D, Brufani C, Grossi A, Ubertini G, Fiori R, Pecorelli L, Calzolari A, Cappa M (2011) Gender differences in bone mineral density in obese children during pubertal development. J Endocrinol Invest 34(4):e86–e91. doi:10.3275/7265
Mosca LN, Goldberg TB, da Silva VN, sa Silva CC, Kurokawa CS, Bisi Rizzo AC, Corrente JE (2014) Excess body fat negatively affects bone mass in adolescents. Nutrition 30(7–8):847–852. doi:10.1016/j.nut.2013.12.003
Pollock NK (2015) Childhood obesity, bone development, and cardiometabolic risk factors. Mol Cell Endocrinol 410:52–63. doi:10.1016/j.mce.2015.03.016.
Parm AL, Jürimäe J, Saar M, Pärna K, Tillmann V, Maasalu K, Neissaar I, Jürimäe T (2011) Plasma adipocytokine and ghrelin levels in relation to bone mineral density in prepubertal rhythmic gymnasts. J Bone Miner Metab 29(6):717–724. doi:10.1007/s00774-011-0272-x
Sioen I, Lust E, De Henauw S, Moreno LA, Jiménez-Pavón D (2016) Associations between body composition and bone health in children and adolescents: a systematic review. Calcif Tissue Int 99(6):557–577. doi:10.1007/s00223-016-0183-x
Mengel E, Tillmann V, Remmel L, Kool P, Purge P, Lätt E, Jürimäe J (2017) Changes in inflammatory markers in Estonian pubertal boys with different BMI values and increments: a 3-year follow-up study. Obesity 25(3):600–607. doi:10.1002/oby.21756
Eesti KMI kõverad (Estonian BMI charts). http://kliinikum.ee/lastekliinik/eesti-kmi-koverad. Accessed 21 Dec 2016.
Matsudo SMM, Matsudo VKR (1994) Self-assessment and physician assessment of sexual maturation in Brazilian boys and girls: concordance and reproducibility. Am J Hum Biol 6(4):451–455. doi:10.1002/ajhb.1310060406
Utsal L, Tillmann V, Zilmer M, Mäestu J, Purge P, Jürimäe J, Saar M, Lätt E, Maasalu K, Jürimäe T (2012) Elevated serum IL-6, IL-8, MCP-1, CRP, and IFN-γ levels in 10- to 11-year-old boys with increased BMI. Horm Res Paediatr 78(1):31–39. doi:10.1159/000339831
Rääsk T, Konstabel K, Mäestu J, Lätt E, Jürimäe T, Jürimäe J (2015) Tracking of physical activity in pubertal boys with different BMI over two-year period. J Sports Sci 33(16):1649–1657. doi:10.1080/02640414.2015.1012097
Lätt E, Mäestu J, Ortega FB, Rääsk T, Jürimäe T, Jürimäe J (2015) Vigorous physical activity rather than sedentary behaviour predicts overweight and obesity in pubertal boys: a 2-year follow-up study. Scand J Public Health 43(3):276–282. doi:10.1177/1403494815569867
Greulich WW, Pyle SI (1959) Radiographic atlas of skeletal development of hand and wrist, 2nd edn. Stanford University Press, Stanford.
Katzman DK, Bachrach LK, Carter DR, Marcus R (1991) Clinical and anthropometric correlates of bone mineral acquisition in healthy adolescent girls. J Clin Endocrinol Metab 73(6):1332–1339. doi:10.1210/jcem-73-6-1332
Bachrach LK, Hastie T, Wang MC, Narasimhan B, Marcus B (1999) Bone mineral acquisition in healthy Asian, Hispanic, black, and Caucasian youth: a longitudinal study. J Clin Endocrinol Metab 84:4702–4712
Rocher E, Chappard C, Jaffre C, Benhamou CL, Courteix D (2008) Bone mineral density in prepubertal obese and control children: relation to body weight, lean mass, and fat mass. J Bone Miner Metab 26(1):73–78
De Leonibus C, Marcovecchio ML, Chiavaroli V, de Giorgis T, Chiarelli F, Mohn A (2013) Timing of puberty and physical growth in obese children: a longitudinal study in boys and girls. Pediatr Obes 9(4):292–299. doi:10.1111/j.2047-6310.2013.00176.x.
Baxter-Jones ADG, Faulkner RA, Forwood M, Mirwald RL, Bailey DA (2011) Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res 26(8):1729–1739. doi:10.1002/jbmr.412
Ripka WL, Modesto JD, Ulbricht L, Gewehr PM (2016) Obesity impact evaluated from fat percentage in bone mineral density of male adolescents. PLoS One 11(9):e0163470. doi:10.1371/journal.pone.0163470
Mihalopoulos NL, Holubkov R, Young P, Dai S, Labarthe DR (2010) Expected changes in clinical measures of adiposity during puberty. J Adolesc Health 47(4):360–366. doi:10.1016/j.jadohealth.2010.03.019
Pollock NK, Bernard PJ, Gutin B, Davis CL, Zhu H, Dong Y (2011) Adolescent obesity, bone mass, and cardiometabolic risk factors. J Pediatr 158(5):727–734. doi:10.1016/j.jpeds.2010.11.052
Iwaniec UT, Turner RT (2016) Influence of body weight on bone mass, architecture and turnover. J Endocrinol 230(3):R115–R130. doi:10.1530/JOE-16-0089
Binkovitz LA, Henwood MJ, Sparke P (2008) Pediatric DXA: technique, interpretation and clinical applications. Pediatr Radiol 38(Suppl 2):S227–S239. doi:10.1007/s00247-008-0808-y
Author Contributions
E. Mengel (guarantor) participated in statistical analysis of the data, interpreted the data, prepared the first draft of the manuscript, and revised and finalized the manuscript. V. Tillmann participated in the interpretation of the data, and drafted and revised the manuscript. L. Remmel, P. Purge, and E. Lätt contributed to the experimental work and data collection. P. Kool was responsible for statistical analysis of the data. J. Jürimäe participated in the interpretation of the data, drafted and revised the manuscript, and supervised all work. All authors revised the paper critically for intellectual content and approved the final manuscript as submitted.
Funding
This study was supported by Estonian Ministry of Education and Science grant IUT 20–58.
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Eva Mengel, Vallo Tillmann, Liina Remmel, Pille Kool, Priit Purge, Evelin Lätt, and Jaak Jürimäe declare that they have no conflict of interest.
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The study was approved by the Research Ethics Committee of the University of Tartu, Tartu, Estonia. Informed consent was obtained from all individual participants included in the study.
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Mengel, E., Tillmann, V., Remmel, L. et al. Extensive BMI Gain in Puberty is Associated with Lower Increments in Bone Mineral Density in Estonian Boys with Overweight and Obesity: A 3-Year Longitudinal Study. Calcif Tissue Int 101, 174–181 (2017). https://doi.org/10.1007/s00223-017-0273-4
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DOI: https://doi.org/10.1007/s00223-017-0273-4