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Published in: Archives of Osteoporosis 1/2023

01-12-2023 | Obesity | Original Article

The relationship between obesity and bone mineral density in children and adolescents: analysis of the National Health and Nutrition Examination Survey

Authors: Chun-Ming Ma, Na Lu, Meng-Meng Zhang, Fan-Shuo Kong, Qiang Lu, Fu-Zai Yin, Xu Zhang, Rui Wang

Published in: Archives of Osteoporosis | Issue 1/2023

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Abstract

Summary

Childhood and puberty are important period for the skeleton grows. Fat mass, especially visceral adipose tissue, was negatively correlated with areal bone mineral density in children and adolescents. The present study suggests that fat mass, especially visceral adipose tissue, has a slightly negative association with bone development in children and adolescents.

Purpose

This study observed the relationship between fat mass and distribution, and areal bone mineral density (aBMD) in children and adolescents.

Methods

A retrospective study was conducted on US children and adolescents aged 8–19 years. Whole body (less head) aBMD was evaluated. Height (Ht) adjusted Z-scores for aBMD were calculated.

Results

After controlling for age, gender, race, and lean body mass index (LBMI) Z-score, there were significant negative associations between fat mass index (FMI) Z-score and aBMD Ht-Z-adjusted Z-score (β =  − 0.272, P < 0.001, R2 = 0.033). In the linear regression models with aBMD Ht-Z-adjusted Z-score as the dependent variable, the regression coefficients of android fat mass were − 0.241 (P < 0.05, R2 = 0.002), − 0.473 (P < 0.001, R2 = 0.036), and − 0.474 (P < 0.001, R2 = 0.038) for healthy weight, overweight, and obesity group, respectively. The regression coefficients of visceral adipose tissue (VAT) mass were − 0.218 (P > 0.05, R2 = 0.001), − 2.025 (P < 0.001, R2 = 0.044), and − 1.826 (P < 0.001, R2 = 0.039), and the regression coefficients of subcutaneous adipose tissue (SAT) mass were − 0.467 (P < 0.001, R2 = 0.004), − 0.339 (P < 0.01, R2 = 0.024), and − 0.347 (P < 0.001, R2 = 0.018) for healthy weight, overweight, and obesity group, respectively.

Conclusions

The present study suggests that fat mass has a slightly negative association with bone development in children and adolescents. Trunk fat accumulation, especially visceral adipose tissue, was correlated with the lower level of aBMD. This association was obvious in overweight and obese children.
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Literature
1.
go back to reference Sarafrazi N, Wambogo EA, Shepherd JA (2021) Osteoporosis or low bone mass in older adults: United States, 2017-2018. NCHS Data Brief 405:1–8 Sarafrazi N, Wambogo EA, Shepherd JA (2021) Osteoporosis or low bone mass in older adults: United States, 2017-2018. NCHS Data Brief 405:1–8
2.
go back to reference Barrett-Connor E, Siris ES, Wehren LE, Miller PD, Abbott TA, Berger ML, Santora AC, Sherwood LM (2005) Osteoporosis and fracture risk in women of different ethnic groups. J bone miner res : off j Am Soc Bone Miner Res 20:185–194CrossRef Barrett-Connor E, Siris ES, Wehren LE, Miller PD, Abbott TA, Berger ML, Santora AC, Sherwood LM (2005) Osteoporosis and fracture risk in women of different ethnic groups. J bone miner res : off j Am Soc Bone Miner Res 20:185–194CrossRef
3.
go back to reference Bliuc D, Nguyen ND, Milch VE, Nguyen TV, Eisman JA, Center JR (2009) Mortality risk associated with low-trauma osteoporotic fracture and subsequent fracture in men and women. JAMA 301:513–521CrossRefPubMed Bliuc D, Nguyen ND, Milch VE, Nguyen TV, Eisman JA, Center JR (2009) Mortality risk associated with low-trauma osteoporotic fracture and subsequent fracture in men and women. JAMA 301:513–521CrossRefPubMed
4.
go back to reference Clynes MA, Harvey NC, Curtis EM, Fuggle NR, Dennison EM, Cooper C (2020) The epidemiology of osteoporosis. Br Med Bull 133:105–117PubMed Clynes MA, Harvey NC, Curtis EM, Fuggle NR, Dennison EM, Cooper C (2020) The epidemiology of osteoporosis. Br Med Bull 133:105–117PubMed
5.
go back to reference Yang Y, Wu F, Winzenberg T, Jones G (2018) 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 : off j Am Soc Bone Miner Res 33:832–839CrossRef Yang Y, Wu F, Winzenberg T, Jones G (2018) 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 : off j Am Soc Bone Miner Res 33:832–839CrossRef
6.
go back to reference Foley S, Quinn S, Jones G (2009) Tracking of bone mass from childhood to adolescence and factors that predict deviation from tracking. Bone 44:752–757CrossRefPubMed Foley S, Quinn S, Jones G (2009) Tracking of bone mass from childhood to adolescence and factors that predict deviation from tracking. Bone 44:752–757CrossRefPubMed
8.
go back to reference van Leeuwen J, Koes BW, Paulis WD, van Middelkoop M (2017) Differences in bone mineral density between normal-weight children and children with overweight and obesity: a systematic review and meta-analysis. Obes Rev 18:526–546CrossRefPubMed van Leeuwen J, Koes BW, Paulis WD, van Middelkoop M (2017) Differences in bone mineral density between normal-weight children and children with overweight and obesity: a systematic review and meta-analysis. Obes Rev 18:526–546CrossRefPubMed
9.
go back to reference Zhu K, Hunter M, James A, Lim EM, Walsh JP (2015) Associations between body mass index, lean and fat body mass and bone mineral density in middle-aged Australians: the Busselton Healthy Ageing Study. Bone 74:146–152CrossRefPubMed Zhu K, Hunter M, James A, Lim EM, Walsh JP (2015) Associations between body mass index, lean and fat body mass and bone mineral density in middle-aged Australians: the Busselton Healthy Ageing Study. Bone 74:146–152CrossRefPubMed
10.
go back to reference Jeddi M, Dabbaghmanesh MH, Ranjbar Omrani G, Ayatollahi SM, Bagheri Z, Bakhshayeshkaram M (2015) Relative importance of lean and fat mass on bone mineral density in Iranian children and adolescents. Int J Endocrinol Metab 13:e25542CrossRefPubMedPubMedCentral Jeddi M, Dabbaghmanesh MH, Ranjbar Omrani G, Ayatollahi SM, Bagheri Z, Bakhshayeshkaram M (2015) Relative importance of lean and fat mass on bone mineral density in Iranian children and adolescents. Int J Endocrinol Metab 13:e25542CrossRefPubMedPubMedCentral
12.
go back to reference Junior IF, Cardoso JR, Christofaro DG, Codogno JS, de Moraes AC, Fernandes RA (2013) The relationship between visceral fat thickness and bone mineral density in sedentary obese children and adolescents. BMC Pediatr 13:37CrossRefPubMedPubMedCentral Junior IF, Cardoso JR, Christofaro DG, Codogno JS, de Moraes AC, Fernandes RA (2013) The relationship between visceral fat thickness and bone mineral density in sedentary obese children and adolescents. BMC Pediatr 13:37CrossRefPubMedPubMedCentral
13.
go back to reference Liang J, Chen Y, Zhang J, Ma B, Hu Y, Liu Y, Lin S, Zhang Z, Song Y (2020) Associations of weight-adjusted body fat and fat distribution with bone mineral density in Chinese children aged 6-10 Years. Int J Environ Res Public Health 17(5):1763. https://doi.org/10.3390/ijerph17051763 Liang J, Chen Y, Zhang J, Ma B, Hu Y, Liu Y, Lin S, Zhang Z, Song Y (2020) Associations of weight-adjusted body fat and fat distribution with bone mineral density in Chinese children aged 6-10 Years. Int J Environ Res Public Health 17(5):1763. https://​doi.​org/​10.​3390/​ijerph17051763
14.
go back to reference Kindler JM, Kelly A, Khoury PR, Levitt Katz LE, Urbina EM, Zemel BS (2020) Bone mass and density in youth with type 2 diabetes, obesity, and healthy weight. Diabetes Care 43:2544–2552CrossRefPubMedPubMedCentral Kindler JM, Kelly A, Khoury PR, Levitt Katz LE, Urbina EM, Zemel BS (2020) Bone mass and density in youth with type 2 diabetes, obesity, and healthy weight. Diabetes Care 43:2544–2552CrossRefPubMedPubMedCentral
15.
go back to reference Barlow SE, Expert C (2007) Expert committee recommendations regarding the prevention, assessment, and treatment of child and adolescent overweight and obesity: summary report. Pediatr 120(Suppl 4):S164–S192CrossRef Barlow SE, Expert C (2007) Expert committee recommendations regarding the prevention, assessment, and treatment of child and adolescent overweight and obesity: summary report. Pediatr 120(Suppl 4):S164–S192CrossRef
16.
go back to reference Zemel BS, Kalkwarf HJ, Gilsanz V, Lappe JM, Oberfield S, Shepherd JA, Frederick MM, Huang X, Lu M, Mahboubi S, Hangartner T, Winer KK (2011) 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 96:3160–3169CrossRefPubMedPubMedCentral Zemel BS, Kalkwarf HJ, Gilsanz V, Lappe JM, Oberfield S, Shepherd JA, Frederick MM, Huang X, Lu M, Mahboubi S, Hangartner T, Winer KK (2011) 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 96:3160–3169CrossRefPubMedPubMedCentral
17.
go back to reference Weber DR, Moore RH, Leonard MB, Zemel BS (2013) 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 98:49–56CrossRefPubMedPubMedCentral Weber DR, Moore RH, Leonard MB, Zemel BS (2013) 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 98:49–56CrossRefPubMedPubMedCentral
18.
go back to reference Gordon CM, Bachrach LK, Carpenter TO, Crabtree N, El-Hajj Fuleihan G, Kutilek S, Lorenc RS, Tosi LL, Ward KA, Ward LM, Kalkwarf HJ (2008) Dual energy X-ray absorptiometry interpretation and reporting in children and adolescents: the 2007 ISCD Pediatric Official Positions. J clin densitom : off j Int Soc Clin Densitom 11:43–58CrossRef Gordon CM, Bachrach LK, Carpenter TO, Crabtree N, El-Hajj Fuleihan G, Kutilek S, Lorenc RS, Tosi LL, Ward KA, Ward LM, Kalkwarf HJ (2008) Dual energy X-ray absorptiometry interpretation and reporting in children and adolescents: the 2007 ISCD Pediatric Official Positions. J clin densitom : off j Int Soc Clin Densitom 11:43–58CrossRef
19.
go back to reference Guo B, Wu Q, Gong J, Xiao Z, Tang Y, Shang J, Cheng Y, Xu H (2016) Relationships between the lean mass index and bone mass and reference values of muscular status in healthy Chinese children and adolescents. J Bone Miner Metab 34:703–713CrossRefPubMed Guo B, Wu Q, Gong J, Xiao Z, Tang Y, Shang J, Cheng Y, Xu H (2016) Relationships between the lean mass index and bone mass and reference values of muscular status in healthy Chinese children and adolescents. J Bone Miner Metab 34:703–713CrossRefPubMed
20.
go back to reference Cohen A, Dempster DW, Recker RR, Lappe JM, Zhou H, Zwahlen A, Muller R, Zhao B, Guo X, Lang T, Saeed I, Liu XS, Guo XE, Cremers S, Rosen CJ, Stein EM, Nickolas TL, McMahon DJ, Young P, Shane E (2013) Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. J Clin Endocrinol Metab 98:2562–2572CrossRefPubMedPubMedCentral Cohen A, Dempster DW, Recker RR, Lappe JM, Zhou H, Zwahlen A, Muller R, Zhao B, Guo X, Lang T, Saeed I, Liu XS, Guo XE, Cremers S, Rosen CJ, Stein EM, Nickolas TL, McMahon DJ, Young P, Shane E (2013) Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. J Clin Endocrinol Metab 98:2562–2572CrossRefPubMedPubMedCentral
21.
go back to reference Kim H, Lee SH, Kim BJ, Koh JM (2017) Association between obesity and femoral neck strength according to age, sex, and fat distribution. Osteoporos int : j established as result of cooperation between the Eur Found Osteoporos Natl Osteoporos Found USA 28:2137–2146CrossRef Kim H, Lee SH, Kim BJ, Koh JM (2017) Association between obesity and femoral neck strength according to age, sex, and fat distribution. Osteoporos int : j established as result of cooperation between the Eur Found Osteoporos Natl Osteoporos Found USA 28:2137–2146CrossRef
22.
go back to reference Li HB, Hou DQ, Liu JT, Gao AY, Zhu ZX, Yu ZC, Lin NX (2019) Chang SY and Mi [The association between body fat distribution and calcaneal bone mineral density in children and adolescents aged 6–16 years in Beijing]. J Zhonghua Yu Fang Yi Xue Za Zhi 53:191–195 Li HB, Hou DQ, Liu JT, Gao AY, Zhu ZX, Yu ZC, Lin NX (2019) Chang SY and Mi [The association between body fat distribution and calcaneal bone mineral density in children and adolescents aged 6–16 years in Beijing]. J Zhonghua Yu Fang Yi Xue Za Zhi 53:191–195
23.
go back to reference Koo HC, Lim GP, Kaur S, Chan KQ, Chan KE, Chung C, Wong M, Danaselvam U (2021) Bone health and its positive relationships with body composition in Malaysian schoolchildren: findings from a cross-sectional study. Child (Basel) 8(7):569. https://doi.org/10.3390/children8070569 Koo HC, Lim GP, Kaur S, Chan KQ, Chan KE, Chung C, Wong M, Danaselvam U (2021) Bone health and its positive relationships with body composition in Malaysian schoolchildren: findings from a cross-sectional study. Child (Basel) 8(7):569. https://​doi.​org/​10.​3390/​children8070569
24.
go back to reference Pollock NK, Bernard PJ, Wenger K, Misra S, Gower BA, Allison JD, Zhu H, Davis CL (2010) Lower bone mass in prepubertal overweight children with prediabetes. J bone miner res : off j Am Soc Bone Miner Res 25:2760–2769CrossRef Pollock NK, Bernard PJ, Wenger K, Misra S, Gower BA, Allison JD, Zhu H, Davis CL (2010) Lower bone mass in prepubertal overweight children with prediabetes. J bone miner res : off j Am Soc Bone Miner Res 25:2760–2769CrossRef
25.
go back to reference Afghani A, Goran MI (2009) The interrelationships between abdominal adiposity, leptin and bone mineral content in overweight Latino children. Horm Res 72:82–87PubMedPubMedCentral Afghani A, Goran MI (2009) The interrelationships between abdominal adiposity, leptin and bone mineral content in overweight Latino children. Horm Res 72:82–87PubMedPubMedCentral
27.
go back to reference Ma C, Tonks KT, Center JR, Samocha-Bonet D, Greenfield JR (2018) Complex interplay among adiposity, insulin resistance and bone health. Clin Obes 8:131–139CrossRefPubMed Ma C, Tonks KT, Center JR, Samocha-Bonet D, Greenfield JR (2018) Complex interplay among adiposity, insulin resistance and bone health. Clin Obes 8:131–139CrossRefPubMed
28.
go back to reference Fuglsang-Nielsen R, Rakvaag E, Vestergaard P, Hartmann B, Holst JJ, Hermansen K, Gregersen S, Starup-Linde J (2020) Consumption of nutrients and insulin resistance suppress markers of bone turnover in subjects with abdominal obesity. Bone 133:115230CrossRefPubMed Fuglsang-Nielsen R, Rakvaag E, Vestergaard P, Hartmann B, Holst JJ, Hermansen K, Gregersen S, Starup-Linde J (2020) Consumption of nutrients and insulin resistance suppress markers of bone turnover in subjects with abdominal obesity. Bone 133:115230CrossRefPubMed
29.
go back to reference Tonks KT, White CP, Center JR, Samocha-Bonet D, Greenfield JR (2017) Bone turnover is suppressed in insulin resistance, independent of adiposity. J Clin Endocrinol Metab 102:1112–1121CrossRefPubMed Tonks KT, White CP, Center JR, Samocha-Bonet D, Greenfield JR (2017) Bone turnover is suppressed in insulin resistance, independent of adiposity. J Clin Endocrinol Metab 102:1112–1121CrossRefPubMed
30.
go back to reference Bilinski WJ, Szternel L, Siodmiak J, Krintus M, Paradowski PT, Domagalski K, Sypniewska G (2021) Effect of fasting hyperglycemia and insulin resistance on bone turnover markers in children aged 9–11 years. J Diabetes Complicat 35:108000CrossRef Bilinski WJ, Szternel L, Siodmiak J, Krintus M, Paradowski PT, Domagalski K, Sypniewska G (2021) Effect of fasting hyperglycemia and insulin resistance on bone turnover markers in children aged 9–11 years. J Diabetes Complicat 35:108000CrossRef
31.
go back to reference Kindler JM, Lobene AJ, Vogel KA, Martin BR, McCabe LD, Peacock M, Warden SJ, McCabe GP, Weaver CM (2019) Adiposity, insulin resistance, and bone mass in children and adolescents. J Clin Endocrinol Metab 104:892–899CrossRefPubMed Kindler JM, Lobene AJ, Vogel KA, Martin BR, McCabe LD, Peacock M, Warden SJ, McCabe GP, Weaver CM (2019) Adiposity, insulin resistance, and bone mass in children and adolescents. J Clin Endocrinol Metab 104:892–899CrossRefPubMed
32.
go back to reference Gil-Cosano JJ, Gracia-Marco L, Ubago-Guisado E, Labayen I, Adelantado-Renau M, Cadenas-Sanchez C, Mora-Gonzalez J, Plaza-Florido A, Aguilera CM, Gomez-Vida J, Maldonado J, Jurimae J, Ortega FB (2020) Inflammatory markers and bone mass in children with overweight/obesity: the role of muscular fitness. Pediatr Res 87:42–47CrossRefPubMed Gil-Cosano JJ, Gracia-Marco L, Ubago-Guisado E, Labayen I, Adelantado-Renau M, Cadenas-Sanchez C, Mora-Gonzalez J, Plaza-Florido A, Aguilera CM, Gomez-Vida J, Maldonado J, Jurimae J, Ortega FB (2020) Inflammatory markers and bone mass in children with overweight/obesity: the role of muscular fitness. Pediatr Res 87:42–47CrossRefPubMed
33.
go back to reference Yao Z, Xing L, Qin C, Schwarz EM, Boyce BF (2008) Osteoclast precursor interaction with bone matrix induces osteoclast formation directly by an interleukin-1-mediated autocrine mechanism. J Biol Chem 283:9917–9924CrossRefPubMedPubMedCentral Yao Z, Xing L, Qin C, Schwarz EM, Boyce BF (2008) Osteoclast precursor interaction with bone matrix induces osteoclast formation directly by an interleukin-1-mediated autocrine mechanism. J Biol Chem 283:9917–9924CrossRefPubMedPubMedCentral
34.
go back to reference Yokota K, Sato K, Miyazaki T, Kitaura H, Kayama H, Miyoshi F, Araki Y, Akiyama Y, Takeda K, Mimura T (2014) Combination of tumor necrosis factor alpha and interleukin-6 induces mouse osteoclast-like cells with bone resorption activity both in vitro and in vivo. Arthritis Rheumatol 66:121–129CrossRefPubMed Yokota K, Sato K, Miyazaki T, Kitaura H, Kayama H, Miyoshi F, Araki Y, Akiyama Y, Takeda K, Mimura T (2014) Combination of tumor necrosis factor alpha and interleukin-6 induces mouse osteoclast-like cells with bone resorption activity both in vitro and in vivo. Arthritis Rheumatol 66:121–129CrossRefPubMed
35.
go back to reference Dimitri P, Jacques RM, Paggiosi M, King D, Walsh J, Taylor ZA, Frangi AF, Bishop N, Eastell R (2015) Leptin may play a role in bone microstructural alterations in obese children. J Clin Endocrinol Metab 100:594–602CrossRefPubMed Dimitri P, Jacques RM, Paggiosi M, King D, Walsh J, Taylor ZA, Frangi AF, Bishop N, Eastell R (2015) Leptin may play a role in bone microstructural alterations in obese children. J Clin Endocrinol Metab 100:594–602CrossRefPubMed
36.
go back to reference Zemel BS, Leonard MB, Kelly A, Lappe JM, Gilsanz V, Oberfield S, Mahboubi S, Shepherd JA, Hangartner TN, Frederick MM, Winer KK, Kalkwarf HJ (2010) Height adjustment in assessing dual energy x-ray absorptiometry measurements of bone mass and density in children. J Clin Endocrinol Metab 95:1265–1273CrossRefPubMedPubMedCentral Zemel BS, Leonard MB, Kelly A, Lappe JM, Gilsanz V, Oberfield S, Mahboubi S, Shepherd JA, Hangartner TN, Frederick MM, Winer KK, Kalkwarf HJ (2010) Height adjustment in assessing dual energy x-ray absorptiometry measurements of bone mass and density in children. J Clin Endocrinol Metab 95:1265–1273CrossRefPubMedPubMedCentral
37.
go back to reference Crabtree NJ, Arabi A, Bachrach LK, Fewtrell M, El-Hajj Fuleihan G, Kecskemethy HH, Jaworski M, Gordon CM, International Society for Clinical D (2014) Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD Pediatric Official Positions. J clin densitom : off j Int Soc Clin Densitom 17:225–42CrossRef Crabtree NJ, Arabi A, Bachrach LK, Fewtrell M, El-Hajj Fuleihan G, Kecskemethy HH, Jaworski M, Gordon CM, International Society for Clinical D (2014) Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD Pediatric Official Positions. J clin densitom : off j Int Soc Clin Densitom 17:225–42CrossRef
Metadata
Title
The relationship between obesity and bone mineral density in children and adolescents: analysis of the National Health and Nutrition Examination Survey
Authors
Chun-Ming Ma
Na Lu
Meng-Meng Zhang
Fan-Shuo Kong
Qiang Lu
Fu-Zai Yin
Xu Zhang
Rui Wang
Publication date
01-12-2023
Publisher
Springer London
Published in
Archives of Osteoporosis / Issue 1/2023
Print ISSN: 1862-3522
Electronic ISSN: 1862-3514
DOI
https://doi.org/10.1007/s11657-022-01208-4

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