The relationship between metabolic syndrome and bone mineral density in adolescents: analysis of the National Health and Nutrition Examination Survey
-
Chun-Ming Ma
Abstract
Objectives
The purpose of this study was to observe the relationship between metabolic syndrome (MetS) and height (Ht) adjusted Z-scores for areal bone mineral density (aBMD) in adolescents.
Methods
A retrospective study was conducted on the United States adolescents aged 12–17 years. Data were extracted from the National Health and Nutrition Examination Survey (NHANES) 2011–2012, 2013–2014 and 2015–2016 cycles. Ht adjusted Z-scores for aBMD were calculated.
Results
A total of 969 adolescents (493 boys and 476 girls), aged 14.5 ± 1.7 years were enrolled in this study. After control for age, gender, race, 25-hydroxyvitamin D [25(OH)D], and lean body mass index (LBMI) Z-score, adolescents with MetS had significantly lower levels of total body (less head) aBMD Ht-Z-adjusted Z-score than adolescents with one, two components of MetS and without component of MetS (p<0.05) and significantly lower levels of lumbar spine aBMD Ht-Z-adjusted Z-score than adolescents with one component of MetS and without component of MetS (p<0.05). There were significantly negative associations between total body (less head) aBMD Ht-Z-adjusted Z-score and waist circumference (WC) (β=−0.027, p<0.001, R2=0.057) and homeostasis model assessment insulin resistance (HOMA-IR) (β=−0.225, p<0.001, R2=0.016). There were significantly negative associations between lumbar spine aBMD Ht-Z-adjusted Z-score and WC (β=−0.039, p<0.001, R2=0.058) and HOMA-IR (β=−0.251, p<0.001, R2=0.008).
Conclusions
The present study demonstrates that MetS may have a negative effect on bone mineral density in adolescents. Abdominal obesity and insulin resistance play a major role on the decline of aBMD in adolescents.
-
Research funding: None declared.
-
Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
-
Competing interests: Authors state no conflict of interest.
-
Informed consent: Informed consent was obtained from all individuals included in this study.
-
Ethical approval: The local Institutional Review Board deemed the study exempt from review.
References
1. Eckel, RH, Grundy, SM, Zimmet, PZ. The metabolic syndrome. Lancet 2005;365:1415–28. https://doi.org/10.1016/s0140-6736(05)66378-7.Search in Google Scholar
2. Friend, A, Craig, L, Turner, S. The prevalence of metabolic syndrome in children: a systematic review of the literature. Metab Syndr Relat Disord 2013;11:71–80. https://doi.org/10.1089/met.2012.0122.Search in Google Scholar PubMed
3. Koskinen, J, Magnussen, CG, Sinaiko, A, Woo, J, Urbina, E, Jacobs, DRJr., et al.. Childhood age and associations between childhood metabolic syndrome and adult risk for metabolic syndrome, type 2 diabetes mellitus and carotid intima media thickness: the international childhood cardiovascular cohort consortium. J Am Heart Assoc 2017;6:e005632. https://doi.org/10.1161/jaha.117.005632.Search in Google Scholar
4. Yang, Y, Wu, F, Winzenberg, T, Jones, G. Tracking of areal bone mineral density from age eight to young adulthood and factors associated with deviation from tracking: a 17-year prospective cohort study. J Bone Miner Res 2018;33:832–9. https://doi.org/10.1002/jbmr.3361.Search in Google Scholar PubMed
5. Foley, S, Quinn, S, Jones, G. Tracking of bone mass from childhood to adolescence and factors that predict deviation from tracking. Bone 2009;44:752–7. https://doi.org/10.1016/j.bone.2008.11.009.Search in Google Scholar PubMed
6. da Silva, VN, Fiorelli, LN, da Silva, CC, Kurokawa, CS, Goldberg, TB. Do metabolic syndrome and its components have an impact on bone mineral density in adolescents? Nutr Metab 2017;14:1. https://doi.org/10.1186/s12986-016-0156-0.Search in Google Scholar PubMed PubMed Central
7. Nobrega da Silva, V, Goldberg, TB, Mosca, LN, Bisi Rizzo Ada, C, Teixeira Ados, S, Corrente, JE. Metabolic syndrome reduces bone mineral density in overweight adolescents. Bone 2014;66:1–7. https://doi.org/10.1016/j.bone.2014.05.011.Search in Google Scholar PubMed
8. Ubago-Guisado, E, Gracia-Marco, L, Medrano, M, Cadenas-Sanchez, C, Arenaza, L, Migueles, JH, et al.. Differences in areal bone mineral density between metabolically healthy and unhealthy overweight/obese children: the role of physical activity and cardiorespiratory fitness. Pediatr Res 2020;87:1219–25. https://doi.org/10.1038/s41390-019-0708-x.Search in Google Scholar PubMed
9. Pollock, NK, Bernard, PJ, Gutin, B, Davis, CL, Zhu, H, Dong, Y. Adolescent obesity, bone mass, and cardiometabolic risk factors. J Pediatr 2011;158:727–34. https://doi.org/10.1016/j.jpeds.2010.11.052.Search in Google Scholar PubMed PubMed Central
10. Matthews, DR, Hosker, JP, Rudenski, AS, Naylor, BA, Treacher, DF, Turner, RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28:412–9. https://doi.org/10.1007/bf00280883.Search in Google Scholar
11. Ford, ES, Li, C, Cook, S, Choi, HK. Serum concentrations of uric acid and the metabolic syndrome among US children and adolescents. Circulation 2007;115:2526–32. https://doi.org/10.1161/circulationaha.106.657627.Search in Google Scholar PubMed
12. Li, C, Ford, ES, Mokdad, AH, Cook, S. Recent trends in waist circumference and waist-height ratio among US children and adolescents. Pediatrics 2006;118:e1390–8. https://doi.org/10.1542/peds.2006-1062.Search in Google Scholar PubMed
13. National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents. The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 2004;114:555–76.10.1542/peds.114.S2.555Search in Google Scholar
14. American Diabetes, A. 2. Classification and diagnosis of diabetes: standards of medical care in diabetes-2019. Diabetes Care 2019;42:S13–28. https://doi.org/10.2337/dc19-s002.Search in Google Scholar
15. Zemel, BS, Kalkwarf, HJ, Gilsanz, V, Lappe, JM, Oberfield, S, Shepherd, JA, et al.. Revised reference curves for bone mineral content and areal bone mineral density according to age and sex for black and non-black children: results of the bone mineral density in childhood study. J Clin Endocrinol Metab 2011;96:3160–9. https://doi.org/10.1210/jc.2011-1111.Search in Google Scholar PubMed PubMed Central
16. Weber, DR, Moore, RH, Leonard, MB, Zemel, BS. Fat and lean BMI reference curves in children and adolescents and their utility in identifying excess adiposity compared with BMI and percentage body fat. Am J Clin Nutr 2013;98:49–56. https://doi.org/10.3945/ajcn.112.053611.Search in Google Scholar PubMed PubMed Central
17. Jeddi, M, Dabbaghmanesh, MH, Ranjbar Omrani, G, Ayatollahi, SM, Bagheri, Z, Bakhshayeshkaram, M. Relative importance of lean and fat mass on bone mineral density in Iranian children and adolescents. Int J Endocrinol Metabol 2015;13:e25542. https://doi.org/10.5812/ijem.25542v2.Search in Google Scholar PubMed PubMed Central
18. Guo, B, Wu, Q, Gong, J, Xiao, Z, Tang, Y, Shang, J, et al.. Relationships between the lean mass index and bone mass and reference values of muscular status in healthy Chinese children and adolescents. Int J Endocrinol Metabol 2016;34:703–13. https://doi.org/10.1007/s00774-015-0725-8.Search in Google Scholar PubMed
19. Nobrega da Silva, V, Goldberg, TBL, Silva, CC, Kurokawa, CS, Fiorelli, LNM, Rizzo, A, et al.. Impact of metabolic syndrome and its components on bone remodeling in adolescents. PLoS One 2021;16:e0253892. https://doi.org/10.1371/journal.pone.0253892.Search in Google Scholar PubMed PubMed Central
20. Zemel, BS, Leonard, MB, Kelly, A, Lappe, JM, Gilsanz, V, Oberfield, S, et al.. Height adjustment in assessing dual energy x-ray absorptiometry measurements of bone mass and density in children. J Clin Endocrinol Metab 2010;95:1265–73. https://doi.org/10.1210/jc.2009-2057.Search in Google Scholar PubMed PubMed Central
21. Crabtree, NJ, Arabi, A, Bachrach, LK, Fewtrell, M, El-Hajj Fuleihan, G, Kecskemethy, HH, et al.. Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD Pediatric Official Positions. J Clin Densitom 2014;17:225–42. https://doi.org/10.1016/j.jocd.2014.01.003.Search in Google Scholar PubMed
22. Koo, HC, Lim, GP, Kaur, S, Chan, KQ, Chan, KE, Chung, C, et al.. Bone health and its positive relationships with body composition in Malaysian schoolchildren: findings from a cross-sectional study. Children 2021;8. https://doi.org/10.3390/children8070569.Search in Google Scholar PubMed PubMed Central
23. Ferrer, FS, Castell, EC, Marco, FC, Ruiz, MJ, Rico, JAQ, Roca, APN. Influence of weight status on bone mineral content measured by DXA in children. BMC Pediatr 2021;21:185. https://doi.org/10.1186/s12887-021-02665-5.Search in Google Scholar PubMed PubMed Central
24. Kindler, JM, Lobene, AJ, Vogel, KA, Martin, BR, McCabe, LD, Peacock, M, et al.. Adiposity, insulin resistance, and bone mass in children and adolescents. J Clin Endocrinol Metab 2019;104:892–9. https://doi.org/10.1210/jc.2018-00353.Search in Google Scholar PubMed
25. Hua, Y, Fang, J, Yao, X, Zhu, Z. Can waist circumference be a predictor of bone mineral density independent of BMI in middle-aged adults? Endocr Connect 2021;10:1307–14. https://doi.org/10.1530/ec-21-0352.Search in Google Scholar
26. Kim, MH, Song, SW, Kim, KS. Abdominal obesity is associated with lower bone mineral density in non-weight-bearing site in Korean men. Am J Men’s Health 2019;13:1557988318813499. https://doi.org/10.1177/1557988318813499.Search in Google Scholar PubMed PubMed Central
27. Harrington, DM, Staiano, AE, Broyles, ST, Gupta, AK, Katzmarzyk, PT. Waist circumference measurement site does not affect relationships with visceral adiposity and cardiometabolic risk factors in children. Pediatr Obes 2013;8:199–206. https://doi.org/10.1111/j.2047-6310.2012.00106.x.Search in Google Scholar PubMed PubMed Central
28. Bruckert, E. [Abdominal obesity: a health threat]. Presse Med 2008;37:1407–14. https://doi.org/10.1016/j.lpm.2008.01.021.Search in Google Scholar PubMed
29. Ma, C, Tonks, KT, Center, JR, Samocha-Bonet, D, Greenfield, JR. Complex interplay among adiposity, insulin resistance and bone health. Clin Obes 2018;8:131–9. https://doi.org/10.1111/cob.12240.Search in Google Scholar PubMed
30. Bilinski, WJ, Szternel, L, Siodmiak, J, Krintus, M, Paradowski, PT, Domagalski, K, et al.. Effect of fasting hyperglycemia and insulin resistance on bone turnover markers in children aged 9-11 years. J Diabetes Complicat 2021;35:108000. https://doi.org/10.1016/j.jdiacomp.2021.108000.Search in Google Scholar PubMed
31. Xiao, P, Hou, DQ, Gao, AY, Zhu, ZX, Yu, ZC, Lin, NX, et al.. [The association between blood lipids and calcaneus bone mineral density in children and adolescents aged 6–16 years in Beijing]. Zhonghua Yufang Yixue Zazhi 2019;53:196–201.Search in Google Scholar
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/jpem-2022-0087).
© 2022 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Original Articles
- The effects of topical iodine containing antiseptics on thyroidal status and early neurodevelopment of preterm infants
- Effect of COVID-19 pandemic on presentation and referral patterns of newly diagnosed children with type 1 diabetes in a developing country
- Influence of the SARS-CoV-2 pandemic on paediatric patients with type 1 diabetes mellitus after one year of follow-up
- Combined diagnostic value of insulin-like growth factor-1, insulin-like growth factor binding protein-3, and baseline luteinizing hormone levels for central precocious puberty in girls
- Differences in the proportion of Croatian adolescents with abnormal individual metabolic syndrome components adjusted to gender and different criterion for individual metabolic syndrome component
- Low HDL-C is a non-fasting marker of insulin resistance in children
- Impact of COVID-19 lockdown on idiopathic central precocious puberty – experience from an Indian centre
- The relationship between metabolic syndrome and bone mineral density in adolescents: analysis of the National Health and Nutrition Examination Survey
- Long-term follow-up of alkaptonuria patients: single center experience
- Local aromatase excess with recruitment of unusual promoters of CYP19A1 gene in prepubertal patients with gynecomastia
- Urinary phthalate concentrations are associated with total fat mass in Thai children
- Clinical profile and aetiologies of delayed puberty: a 15 years’ experience from a tertiary centre in Sudan
- Case Reports
- Congenital generalized lipodystrophy type 4 due to a novel PTRF/CAVIN1 pathogenic variant in a child: effects of metreleptin substitution
- Prepubertal and pubertal gonadal morphology, expression of cell lineage markers and hormonal evaluation in two 46,XY siblings with 17β-hydroxysteroid dehydrogenase 3 deficiency
- Pleomorphism of the HPG axis with NR0B1 gene mutation — a case report of longitudinal follow-up of a proband with central precocious puberty
- Successful treatment of severe hypertriglyceridemia with icosapent ethyl in a case of congenital generalized lipodystrophy type 4
Articles in the same Issue
- Frontmatter
- Original Articles
- The effects of topical iodine containing antiseptics on thyroidal status and early neurodevelopment of preterm infants
- Effect of COVID-19 pandemic on presentation and referral patterns of newly diagnosed children with type 1 diabetes in a developing country
- Influence of the SARS-CoV-2 pandemic on paediatric patients with type 1 diabetes mellitus after one year of follow-up
- Combined diagnostic value of insulin-like growth factor-1, insulin-like growth factor binding protein-3, and baseline luteinizing hormone levels for central precocious puberty in girls
- Differences in the proportion of Croatian adolescents with abnormal individual metabolic syndrome components adjusted to gender and different criterion for individual metabolic syndrome component
- Low HDL-C is a non-fasting marker of insulin resistance in children
- Impact of COVID-19 lockdown on idiopathic central precocious puberty – experience from an Indian centre
- The relationship between metabolic syndrome and bone mineral density in adolescents: analysis of the National Health and Nutrition Examination Survey
- Long-term follow-up of alkaptonuria patients: single center experience
- Local aromatase excess with recruitment of unusual promoters of CYP19A1 gene in prepubertal patients with gynecomastia
- Urinary phthalate concentrations are associated with total fat mass in Thai children
- Clinical profile and aetiologies of delayed puberty: a 15 years’ experience from a tertiary centre in Sudan
- Case Reports
- Congenital generalized lipodystrophy type 4 due to a novel PTRF/CAVIN1 pathogenic variant in a child: effects of metreleptin substitution
- Prepubertal and pubertal gonadal morphology, expression of cell lineage markers and hormonal evaluation in two 46,XY siblings with 17β-hydroxysteroid dehydrogenase 3 deficiency
- Pleomorphism of the HPG axis with NR0B1 gene mutation — a case report of longitudinal follow-up of a proband with central precocious puberty
- Successful treatment of severe hypertriglyceridemia with icosapent ethyl in a case of congenital generalized lipodystrophy type 4
