J Korean Med Sci.  2017 Oct;32(10):1633-1641. 10.3346/jkms.2017.32.10.1633.

The Role of Overweight and Obesity on Bone Health in Korean Adolescents with a Focus on Lean and Fat Mass

• Kim HY
• Jung HW
• Hong H
• Kim JH
• Shin CH
• Yang SW
• Lee YA

• KMID: 2400435
• DOI: http://doi.org/10.3346/jkms.2017.32.10.1633

Abstract

As the associations between pediatric overweight/obesity and bone health remain controversial, we investigated the effects of overweight/obesity as well as lean mass (LM) and fat mass (FM) on bone parameters in adolescents. Bone parameters were evaluated using dual-energy X-ray absorptiometry (DXA) data of 982 adolescents (aged 12-19 years) from the Korea National Health and Nutrition Examination Survey (2009-2010). Z-scores for LM, FM, bone mass, bone mineral density (BMD), and bone mineral apparent density (BMAD) using Korean pediatric reference values were used for analysis. Adolescents with overweight/obesity had significantly higher bone mass and density of the total-body-less-head (TBLH), lumbar spine, and femur neck than underweight or normal-weight adolescents (P < 0.001) after adjusting for vitamin D deficiency, calcium intake, and insulin resistance in both sexes. LM was positively associated with bone parameters at all skeletal sites in both sexes (P < 0.001). FM was negatively related to TBLH BMD in boys (P = 0.018) but was positively associated to BMD and BMAD of the lumbar spine and femur neck in girls. In conclusion, overweight/obesity and LM play a positive role in bone health in adolescents. The effect of FM on bone parameters is sex- and site-specific.

Keyword

Pediatric Obesity; Body Composition; Bone Density; Adolescent; Korea

MeSH Terms

Absorptiometry, Photon
Adolescent*
Body Composition
Bone Density
Calcium
Female
Femur Neck
Humans
Insulin Resistance
Korea
Miners
Nutrition Surveys
Obesity*
Overweight*
Pediatric Obesity
Reference Values
Spine
Thinness
Vitamin D Deficiency
Calcium

Figure

• 

  Fig. 1 Flowchart of the study population. KNHANES = Korea National Health and Nutrition Examination Survey, DXA = dual-energy X-ray absorptiometry.

• 

  Fig. 2 Comparison of body composition and bone density among the underweight, normal-weight, and overweight/obesity groups in males. BMC = bone mineral content, BMD = bone mineral density, BMAD = bone mineral apparent density. *P < 0.01. † P < 0.001.

• 

  Fig. 3 Comparison of body composition and bone density among the underweight, normal-weight, and overweight/obesity groups in females. BMC = bone mineral content, BMD = bone mineral density, BMAD = bone mineral apparent density. *P < 0.01. † P < 0.001.

Reference

1. Korea Centers for Disease Control and Prevention. Korean youth's risk behavior web-based survey 2016 [Internet]. accessed on 11 January 2017. Available at http://yhs.cdc.go.kr.

2. Maggioli C, Stagi S. Bone modeling, remodeling, and skeletal health in children and adolescents: mineral accrual, assessment and treatment. Ann Pediatr Endocrinol Metab. 2017; 22:1–5.

3. El Hage R, Jacob C, Moussa E, Benhamou CL, Jaffré C. Total body, lumbar spine and hip bone mineral density in overweight adolescent girls: decreased or increased? J Bone Miner Metab. 2009; 27:629–633.

4. Ivuskans A, Lätt E, Mäestu J, Saar M, Purge P, Maasalu K, Jürimäe T, Jürimäe J. Bone mineral density in 11–13-year-old boys: relative importance of the weight status and body composition factors. Rheumatol Int. 2013; 33:1681–1687.

5. Hasanoğlu A, Bideci A, Cinaz P, Tümer L, Unal S. Bone mineral density in childhood obesity. J Pediatr Endocrinol Metab. 2000; 13:307–311.

6. El Hage R, Moussa E, El Hage Z, Theunynck D, Jacob C. Influence of age and morphological characteristics on whole body, lumbar spine, femoral neck and 1/3 radius bone mineral apparent density in a group of Lebanese adolescent boys. J Bone Miner Metab. 2011; 29:477–483.

7. Sioen I, Lust E, De Henauw S, Moreno LA, Jiménez-Pavón D. Associations between body composition and bone health in children and adolescents: a systematic review. Calcif Tissue Int. 2016; 99:557–577.

8. Lee YA, Kim HY, Hong H, Kim JY, Kwon HJ, Shin CH, Yang SW. Risk factors for low vitamin D status in Korean adolescents: the Korea National Health and Nutrition Examination Survey (KNHANES) 2008–2009. Public Health Nutr. 2014; 17:764–771.

9. do Prado WL, de Piano A, Lazaretti-Castro M, de Mello MT, Stella SG, Tufik S, do Nascimento CM, Oyama LM, Lofrano MC, Tock L, et al. Relationship between bone mineral density, leptin and insulin concentration in Brazilian obese adolescents. J Bone Miner Metab. 2009; 27:613–619.

10. Crabtree NJ, Arabi A, Bachrach LK, Fewtrell M, El-Hajj Fuleihan G, Kecskemethy HH, Jaworski M, Gordon CM; International Society for Clinical Densitometry. Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD Pediatric Official Positions. J Clin Densitom. 2014; 17:225–242.

11. Jones G, Ma D, Cameron F. Bone density interpretation and relevance in Caucasian children aged 9–17 years of age: insights from a population-based fracture study. J Clin Densitom. 2006; 9:202–209.

12. Kang MJ, Hong HS, Chung SJ, Lee YA, Shin CH, Yang SW. Body composition and bone density reference data for Korean children, adolescents, and young adults according to age and sex: results of the 2009–2010 Korean National Health and Nutrition Examination Survey (KNHANES). J Bone Miner Metab. 2016; 34:429–439.

13. Moon JS, Lee SY, Nam CM, Choi JM, Choe BK, Seo JW, Oh K, Jang MJ, Hwang SS, Yoo MH, et al. 2007 Korean National Growth Charts: review of developmental process and an outlook. Korean J Pediatr. 2008; 51:1–25.

14. Mei Z, Grummer-Strawn LM, Pietrobelli A, Goulding A, Goran MI, Dietz WH. Validity of body mass index compared with other body-composition screening indexes for the assessment of body fatness in children and adolescents. Am J Clin Nutr. 2002; 75:978–985.

15. Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, Murad MH, Weaver CM. Endocrine Society. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2011; 96:1911–1930.

16. Ryoo E. Adolescent nutrition: what do pediatricians do? Korean J Pediatr. 2011; 54:287–291.

17. U.S. Department of Health and Human Services. Physical activity guidelines for Americans [Internet]. accessed on 1 June 2016. Available at http://www.health.gov/paguidelines/guidelines.

18. Katzman DK, Bachrach LK, Carter DR, Marcus R. Clinical and anthropometric correlates of bone mineral acquisition in healthy adolescent girls. J Clin Endocrinol Metab. 1991; 73:1332–1339.

19. Leonard MB, Shults J, Wilson BA, Tershakovec AM, Zemel BS. Obesity during childhood and adolescence augments bone mass and bone dimensions. Am J Clin Nutr. 2004; 80:514–523.

20. Ellis KJ, Shypailo RJ, Wong WW, Abrams SA. Bone mineral mass in overweight and obese children: diminished or enhanced? Acta Diabetol. 2003; 40:Suppl 1. S274–S277.

21. Goulding A, Taylor RW, Jones IE, McAuley KA, Manning PJ, Williams SM. Overweight and obese children have low bone mass and area for their weight. Int J Obes Relat Metab Disord. 2000; 24:627–632.

22. Manzoni P, Brambilla P, Pietrobelli A, Beccaria L, Bianchessi A, Mora S, Chiumello G. Influence of body composition on bone mineral content in children and adolescents. Am J Clin Nutr. 1996; 64:603–607.

23. Frost HM. The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner. 1987; 2:73–85.

24. Thomas T, Gori F, Khosla S, Jensen MD, Burguera B, Riggs BL. Leptin acts on human marrow stromal cells to enhance differentiation to osteoblasts and to inhibit differentiation to adipocytes. Endocrinology. 1999; 140:1630–1638.

25. Rhie YJ, Lee KH, Chung SC, Kim HS, Kim DH. Effects of body composition, leptin, and adiponectin on bone mineral density in prepubertal girls. J Korean Med Sci. 2010; 25:1187–1190.

26. Pietrobelli A, Faith MS, Wang J, Brambilla P, Chiumello G, Heymsfield SB. Association of lean tissue and fat mass with bone mineral content in children and adolescents. Obes Res. 2002; 10:56–60.

27. Gracia-Marco L, Ortega FB, Jiménez-Pavón D, Rodríguez G, Castillo MJ, Vicente-Rodríguez G, Moreno LA. Adiposity and bone health in Spanish adolescents. The HELENA study. Osteoporos Int. 2012; 23:937–947.

28. Rauch F, Bailey DA, Baxter-Jones A, Mirwald R, Faulkner R. The ‘muscle-bone unit’ during the pubertal growth spurt. Bone. 2004; 34:771–775.

29. Vaitkeviciute D, Lätt E, Mäestu J, Jürimäe T, Saar M, Purge P, Maasalu K, Jürimäe J. Physical activity and bone mineral accrual in boys with different body mass parameters during puberty: a longitudinal study. PLoS One. 2014; 9:e107759.

30. El Hage RP, Courteix D, Benhamou CL, Jacob C, Jaffré C. Relative importance of lean and fat mass on bone mineral density in a group of adolescent girls and boys. Eur J Appl Physiol. 2009; 105:759–764.

31. Shin D, Kim S, Kim KH, Park SM. Importance of fat mass and lean mass on bone health in men: the Fourth Korean National Health and Nutrition Examination Survey (KNHANES IV). Osteoporos Int. 2014; 25:467–474.

32. Farr JN, Amin S, LeBrasseur NK, Atkinson EJ, Achenbach SJ, McCready LK, Joseph Melton L 3rd, Khosla S. Body composition during childhood and adolescence: relations to bone strength and microstructure. J Clin Endocrinol Metab. 2014; 99:4641–4648.

33. Mosca LN, da Silva VN, Goldberg TB. Does excess weight interfere with bone mass accumulation during adolescence? Nutrients. 2013; 5:2047–2061.

34. Geer EB, Shen W. Gender differences in insulin resistance, body composition, and energy balance. Gend Med. 2009; 6:Suppl 1. 60–75.

35. Wang Q, Alén M, Nicholson PH, Halleen JM, Alatalo SL, Ohlsson C, Suominen H, Cheng S. Differential effects of sex hormones on peri- and endocortical bone surfaces in pubertal girls. J Clin Endocrinol Metab. 2006; 91:277–282.

36. Roodman GD. Role of cytokines in the regulation of bone resorption. Calcif Tissue Int. 1993; 53:Suppl 1. S94–S98.

37. Fulzele K, Riddle RC, DiGirolamo DJ, Cao X, Wan C, Chen D, Faugere MC, Aja S, Hussain MA, Brüning JC, et al. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell. 2010; 142:309–319.

38. Pramojanee SN, Phimphilai M, Kumphune S, Chattipakorn N, Chattipakorn SC. Decreased jaw bone density and osteoblastic insulin signaling in a model of obesity. J Dent Res. 2013; 92:560–565.

39. Adams JE, Engelke K, Zemel BS, Ward KA; International Society of Clinical Densitometry. Quantitative computer tomography in children and adolescents: the 2013 ISCD Pediatric Official Positions. J Clin Densitom. 2014; 17:258–274.

40. Clark EM, Ness AR, Bishop NJ, Tobias JH. Association between bone mass and fractures in children: a prospective cohort study. J Bone Miner Res. 2006; 21:1489–1495.