Do metabolic syndrome and its components have an impact on bone mineral density in adolescents?

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Abstract

In recent years, there has been growing concern about the occurrence of metabolic syndrome (MetS) at an early age and its effects on bone mass in adolescents. Adolescence is considered a critical period for bone mass gain. Impaired bone acquisition during this phase can lead to “suboptimal” peak bone mass and increase the risk of osteopenia/osteoporosis and fractures in old age. The objective of this review was to perform a critical analysis of articles that specifically focus on this age group, evaluating the influence of MetS and its components on bone mineral density in adolescents. A possible relationship between this syndrome and bone mass has been demonstrated, but the number of studies addressing this topic in adolescents is small. Despite the scarcity of evidence, the results of those studies show that Metabolic Syndrome is negatively correlated with bone mass and also that some components of MetS are negatively correlated with bone mineral density in adolescents. However, the associations between MetS and bone mass development need to be further explored in the age group corresponding to adolescence. Further good-quality studies are necessary to complement the understanding of this relationship.

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Most cited references 43

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Association between serum osteocalcin and markers of metabolic phenotype.

Daniel Stark, M J Eliades, Anastassios G Pittas … (2009)

Osteocalcin has been reported to contribute to the regulation of glucose tolerance and insulin secretion and sensitivity in experimental animals. Our objective was to examine the association between serum osteocalcin concentration and markers of dysmetabolic phenotype using data from a completed clinical trial in adults age 65 and older [n = 380, mean age 71 yr, body mass index (BMI) 26.9 kg/m(2), 5% with diabetes]. In cross-sectional analyses (baseline data), we estimated the associations of serum osteocalcin and urine N-telopeptide with markers of metabolic phenotype including fasting plasma glucose (FPG) (primary outcome), fasting insulin, insulin sensitivity estimated by homeostasis model assessment for insulin resistance, plasma high-sensitivity C-reactive protein, IL-6, and measures of adiposity (BMI and body fat) (secondary outcomes) after multivariate adjustment for potential confounders. In prospective analysis (placebo arm), we estimated the associations of osteocalcin and N-telopeptide with change in the primary outcome, FPG, over a 3-yr period. In cross-sectional analyses, serum osteocalcin concentration was inversely associated with FPG (P = 0.01), fasting insulin (P = 0.006), homeostasis model assessment for insulin resistance (P = 0.002), high-sensitivity C-reactive protein (P = 0.01), IL-6 (P = 0.02), BMI (P < 0.001), and body fat (P < 0.001). When participants were divided into tertiles by serum osteocalcin, mean FPG was 97.1 vs. 104.8 mg/dl in the highest vs. lowest osteocalcin tertile, respectively (P < 0.01). In prospective analyses, exposure to higher osteocalcin levels during follow-up was associated with a significantly lower rise in FPG at 3 yr. Urine N-telopeptide was not associated with any marker of metabolic phenotype. Serum osteocalcin concentration was inversely associated with blood markers of dysmetabolic phenotype and measures of adiposity. Our findings should be considered hypothesis generating, and they need to be replicated in human studies designed to test the hypothesis that osteocalcin affects metabolism.

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Calcium accretion in girls and boys during puberty: a longitudinal analysis.

D A Bailey, A Martin, H McKay … (2000)

The primary purpose of this study was to estimate the magnitude and variability of peak calcium accretion rates in the skeletons of healthy white adolescents. Total-body bone mineral content (BMC) was measured annually on six occasions by dual-energy X-ray absorptiometry (DXA; Hologic 2000, array mode), a BMC velocity curve was generated for each child by a cubic spline fit, and peak accretion rates were determined. Anthropometric measures were collected every 6 months and a 24-h dietary recall was recorded two to three times per year. Of the 113 boys and 115 girls initially enrolled in the study, 60 boys and 53 girls who had peak height velocity (PHV) and peak BMC velocity values were used in this longitudinal analysis. When the individual BMC velocity curves were aligned on the age of peak bone mineral velocity, the resulting mean peak bone mineral accrual rate was 407 g/year for boys (SD, 92 g/year; range, 226-651 g/year) and 322 g/year for girls (SD, 66 g/year; range, 194-520 g/year). Using 32.2% as the fraction of calcium in bone mineral, as determined by neutron activation analysis (Ellis et al., J Bone Miner Res 1996;11:843-848), these corresponded to peak calcium accretion rates of 359 mg/day for boys (81 mg/day; 199-574 mg/day) and 284 mg/day for girls (58 mg/day; 171-459 mg/day). These longitudinal results are 27-34% higher than our previous cross-sectional analysis in which we reported mean values of 282 mg/day for boys and 212 mg/day for girls (Martin et al., Am J Clin Nutr 1997;66:611-615). Mean age of peak calcium accretion was 14.0 years for the boys (1.0 years; 12.0-15.9 years), and 12.5 years for the girls (0.9 years; 10.5-14.6 years). Dietary calcium intake, determined as the mean of all assessments up to the age of peak accretion was 1140 mg/day (SD, 392 mg/day) for boys and 1113 mg/day (SD, 378 mg/day) for girls. We estimate that 26% of adult calcium is laid down during the 2 adolescent years of peak skeletal growth. This period of rapid growth requires high accretion rates of calcium, achieved in part by increased retention efficiency of dietary calcium.

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Visceral fat is a negative predictor of bone density measures in obese adolescent girls.

Howard J. Rosen, Marcia K. Peck, Melissa Russell … (2010)

Regional fat is increasingly recognized as a determinant of bone mineral density (BMD), an association that may be mediated by adipokines, such as adiponectin and leptin, and inflammatory fat products. Chronic inflammation is deleterious to bone, and visceral adipose tissue (VAT) predicts inflammatory markers such as soluble intercellular adhesion molecule-1 and E-selectin, whereas sc adipose tissue (SAT) and VAT predict IL-6 in adolescents. Our objective was to determine associations of regional fat mass and adipokines with BMD. We hypothesized that girls with greater VAT relative to SAT would have lower bone density mediated by inflammatory cytokines, adiponectin, and leptin. This was a cross-sectional study. The study was conducted at a clinical research center. SUBJECTS included 30 girls (15 obese, 15 normal weight) 12-18 yr old, matched for maturity (bone age), race, and ethnicity. We assessed regional fat (SAT, VAT) using magnetic resonance imaging, total fat, and BMD using dual-energy x-ray absorptiometry. Fasting leptin, adiponectin, IL-6, soluble intercellular adhesion molecule-1, and E-selectin were obtained. Mean body mass index sd score was 3.7 +/- 1.5 in obese subjects and 0.1 +/- 0.4 kg/m(2) in controls. VAT was a negative predictor of spine BMD and bone mineral apparent density, whole-body BMD and bone mineral content/height in obese girls and whole-body BMD and bone mineral content/height for the group as a whole after controlling for SAT, as was the ratio of VAT to SAT. In a regression model that included VAT/SAT, adipokines, and cytokines, E-selectin and adiponectin were negative predictors of BMD and leptin a positive predictor. VAT is an independent inverse determinant of bone density in obesity. This association may be mediated by adipokines and a chronic inflammatory state.

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Author and article information

Contributors

Valéria Nóbrega da Silva: valerianutry@gmail.com

Luciana Nunes Mosca Fiorelli: lunutricionista@yahoo.com.br

Carla Cristiane da Silva: ccsilva@uenp.edu.br

Cilmery Suemi Kurokawa: cskurokawa@gmail.com

Tamara Beres Lederer Goldberg:

ORCID: http://orcid.org/0000-0001-7017-766X

+55-14-3811-6274/3811-6083 , tamara@fmb.unesp.br

Journal

Journal ID (nlm-ta): Nutr Metab (Lond)

Journal ID (iso-abbrev): Nutr Metab (Lond)

Title: Nutrition & Metabolism

Publisher: BioMed Central (London )

ISSN (Electronic): 1743-7075

Publication date (Electronic): 4 January 2017

Publication date PMC-release: 4 January 2017

Publication date Collection: 2017

Volume: 14

Electronic Location Identifier: 1

Affiliations

[1 ]Department of Pediatrics, Discipline of Adolescent Medicine, Postgraduate Program in Gynecology, Obstetrics, and Mastology, Botucatu School of Medicine, UNESP, São Paulo State University, Botucatu, São Paulo Brazil

[2 ]Department of Physical Education, University of North Paraná, Jacarezinho, Paraná Brazil

[3 ]Clinical and Experimental Pediatric Research Center, Department of Pediatrics and Postgraduate Program in Tropical Disease, Botucatu School of Medicine, UNESP, São Paulo State University, Botucatu, São Paulo Brazil

Author information

Tamara Beres Lederer Goldberg http://orcid.org/0000-0001-7017-766X

Article

Publisher ID: 156

DOI: 10.1186/s12986-016-0156-0

PMC ID: 5209875

SO-VID: b2fb1dbd-c168-461d-bddb-54f4c6cb50e7

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Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 18 August 2016

Date accepted : 21 December 2016

Funding

Funded by: FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo)

Award ID: 07/07731-0, 2011/05991-0 and 2015/04040-2

Award Recipient : Valéria Nóbrega da Silva

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ScienceOpen disciplines: Nutrition & Dietetics

Keywords: metabolic syndrome x,abdominal obesity,waist circumference,bone mineral density,hypertriglyceridemia,adolescents

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ScienceOpen disciplines: Nutrition & Dietetics

Keywords: metabolic syndrome x, abdominal obesity, waist circumference, bone mineral density, hypertriglyceridemia, adolescents

Do metabolic syndrome and its components have an impact on bone mineral density in adolescents?

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Most cited references 43

Association between serum osteocalcin and markers of metabolic phenotype.

Calcium accretion in girls and boys during puberty: a longitudinal analysis.

Visceral fat is a negative predictor of bone density measures in obese adolescent girls.

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