Skip to main content

Advertisement

SpringerLink
Log in

Serum interferon gamma concentration is associated with bone mineral density in overweight boys

  • Original Article
  • Published:
Journal of Endocrinological Investigation Aims and scope Submit manuscript

Abstract

Childhood obesity has recently been linked to low-grade inflammation. Overweight children have slightly different processes of bone accumulation than normal weight children. The possible links between inflammation and bone accumulation have not previously been assessed in overweight children.

Aims

An exploratory study to assess whether common inflammatory markers are associated with the development of obesity and bone accumulation in childhood.

Methods

Thirteen different inflammatory markers in serum were measured in 38 boys with BMI >85th centile (overweight) and 38 boys with normal BMI (normal weight), aged 10–11 years. Total body (TB) and lumbar spine (LS) bone mineral density (BMD), bone mineral content (BMC) were measured by DXA. TB BMC for height, TB and LS bone mineral apparent density (BMAD) were calculated.

Results

Overweight boys had higher mean TB and LS BMD, TB BMC and TB BMC for height, but lower mean TB BMAD (all p < 0.05) than normal weight boys. Serum interferon gamma (IFNγ) concentration was significantly (p < 0.05) correlated with TB BMD (r = 0.36), TB BMC (r = 0.38) and TB BMC for height (r = 0.53) in the broader overweight group (n = 38). In obese boys (BMI > 95 centile, n = 36) IFNγ was correlated with LS BMD (r = 0.38).

Conclusion

The positive correlation between serum INFγ concentration and BMD suggests that the inflammatory process, already involved in the early stage of obesity, may also affect bone accumulation. Further studies are needed to clarify the role of INFγ as a possible link between adipose tissue and bone health.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. 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 26:73–78

    Article  PubMed  Google Scholar 

  2. Weiss R, Dziura J, Burgert TS et al (2004) Obesity and the metabolic syndrome in children and adolescents. N Engl J Med 350:2362–2374

    Article  CAS  PubMed  Google Scholar 

  3. Dimitri P, Bishop N, Walsh JS, Eastell R (2012) Obesity is a risk factor for fracture in children but is protective against fracture in adults: a paradox. Bone 50:457–466

    Article  CAS  PubMed  Google Scholar 

  4. Clark EM, Ness AR, Tobias JH, the Avon longitudinal study of parents and children study team (2006) Adipose tissue stimulates bone growth in prepubertal children. J Clin Endocrinol Metab 91:2534–2541

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Dimitri P, Wales JK, Bishop N (2010) Fat and bone in children: differential effects of obesity on bone size and mass according to fracture history. Am Soc Bone Miner Res 25:527–536

    Article  Google Scholar 

  6. Ackerman A, Thornton JC, Wang J, Pierson RN Jr, Horlick M (2006) Sex difference in the effect of puberty on the relationship between fat mass and bone mass in 926 healthy subjects, 6 to 18 years old. Obesity 14:819–825

    Article  PubMed  Google Scholar 

  7. Wey HE, Binkley TL, Beare TM, Wey CL, Specker BL (2011) Cross-sectional versus longitudinal associations of lean and fat mass with pQCT bone outcomes in children. J Clin Endocrinol Metab 96:106–114

    Article  CAS  PubMed  Google Scholar 

  8. Cole ZA, Harvey NC, Kim M et al (2012) Increased fat mass is associated with increased bone size but reduced volumetric density in prepubertal children. Bone 50:462–467

    Article  Google Scholar 

  9. Pollock NK, Bernard PJ, Wenger K et al (2010) Lower bone mass in prepubertal overweight children with prediabetes. J Bone Miner Res 25:2760–2769

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  11. Wang Q, Alén M, Nicholson P et al (2007) Weight-bearing, muscle loading and bone mineral accrual in pubertal girls—a 2-year longitudinal study. Bone 40:1196–1202

    Article  PubMed  Google Scholar 

  12. Hong X, Arguelles LM, Liu X et al (2010) Percent fat mass is inversely associated with bone mass and hip geometry in rural Chinese adolescents. J Bone Miner Res 25:1544–1554

    Article  PubMed  Google Scholar 

  13. El Hage R, Moussa E, Jacob C (2010) Bone mineral content and density in obese, overweight, and normal-weighted sedentary adolescent girls. J Adoles Health 47:591–595

    Article  Google Scholar 

  14. El Hage R, El Hage Z, Jacob C, Moussa E, Theunynck D, Baddoura R (2011) Bone mineral content and density in overweight and control adolescent boys. J Clin Densitom 14:122–128

    Article  PubMed  Google Scholar 

  15. Goulding A, Taylor RW, Jones IE et al (2000) Overweight and obese children have low bone mass and area for their weight. Int J Obes 24:627–632

    Article  CAS  Google Scholar 

  16. Mobley SL, Ha E, Landoll JD et al (2005) Children with bone fragility fractures have reduced bone mineral areal density at the forearm and hip and higher percent body fat. J Bone Miner Res 20(Suppl 1):S34

    Google Scholar 

  17. Utsal L, Tillmann V, Zilmer M et al (2012) Elevated serum IL-6, IL-8, MCP-1, CRP and IFNγ levels in 10- to 11-year-old boys with increased BMI. Horm Res Paediatr 78:31–39

    Article  CAS  PubMed  Google Scholar 

  18. Barbour KE, Boudreau R, Danielson ME et al (2012) Inflammatory markers and the risk of hip fracture: the women’s health initiative. J Bone Miner Res 27:1167–1176

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Ding C, Parameswaran V, Udayan R, Burgess J, Jones G (2008) Circulating levels of inflammatory markers predict change in bone mineral density and resorption in older adults: a longitudinal study. J Clin Endocrinol Metab 93:1952–1958

    Article  CAS  PubMed  Google Scholar 

  20. Hanks LJ, Casazza K, Alvarez JA, Fernandez JR (2010) Does fat fuel the fire: independent and interactive effects of genetic, physiological, and environmental factors on variations in fat deposition and distribution across populations. J Pediatr Endocrinol Metab 23:1233–1244

    PubMed Central  PubMed  Google Scholar 

  21. Nakamura K, Saito T, Kobayashi R et al (2011) C-reactive protein predicts incident fracture in community-dwelling elderly Japanese women: the Muramatsu study. Osteoporos Int 22:2145–2150

    Article  CAS  PubMed  Google Scholar 

  22. Tanner J (1962) Growth at adolescence, 2nd edn. Blackwell, Oxford, pp 121–130

    Google Scholar 

  23. 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 6:451–455

    Article  Google Scholar 

  24. Lätt E, Jürimäe J, Haljaste K, Cicchella A, Purge P, Jürimäe T (2009) Longitudinal development of physical and performance parameters during biological maturation of young male swimmers. Percept Motor Skills 108:297–307

    Article  PubMed  Google Scholar 

  25. Pomerants T, Tillmann V, Karelson K, Jürimäe J, Jürimäe T (2006) Ghrelin response to acute aerobic exercise in boys at different stages of puberty. Horm Metab Res 38:752–757

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  28. Bass S, Delmas PD, Pearce G, Hendrich E, Tabensky A, Seeman E (1999) The differing tempo of growth in bone size, mass, and density in girls is region specific. J Clin Invest 104:795–804

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Duque G, Huang DC, Dion N et al (2011) Interferon-γ plays a role in bone formation in vivo and rescues osteoporosis in ovariectomized mice. J Bone Min Res 26:1472–1483

    Article  CAS  Google Scholar 

  30. Gao Y, Grassi F, Ryan MR et al (2007) IFN-gamma stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation. J Clin Invest 117:122–132

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Breuil V, Ticchioni M, Testa J et al (2010) Immune changes in post-menopausal osteoporosis: the Immunos study. Osteoporos Int 21:805–814

    Article  CAS  PubMed  Google Scholar 

  32. Trebble TM, Stroud MA, Wootton SA et al (2005) High-dose fish oil and antioxidants in Crohn’s disease and the response of bone turnover: a randomised controlled trial. Brit J Nutr 94:253–261

    Article  CAS  PubMed  Google Scholar 

  33. Sasaki H, Hou L, Belani A et al (2000) IL-10, but not IL-4, suppresses infection-stimulated bone resorption in vivo. J Immunol 165:3626–3630

    CAS  PubMed  Google Scholar 

  34. Owens JM, Gallagher AC, Chambers TJ (1996) IL-10 modulates formation of osteoclasts in murine hemopoietic cultures. J Immunol 157:936–940

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was partly supported by the Estonian Ministry of Education grants TKKSP 0489 and GKKSP 9168.

Conflict of interest

The authors L. Utsal, V. Tillmann, M. Zilmer, J. Mäestu, P. Purge, M. Saar, E. Lätt, T. Jürimäe, K. Maasalu, and J. Jürimäe declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Faculty of Exercise and Sport Sciences, University of Tartu, 50090, Tartu, Estonia

    L. Utsal, J. Mäestu, P. Purge, M. Saar, E. Lätt, T. Jürimäe & J. Jürimäe

  2. Department of Paediatrics, Faculty of Medicine, University of Tartu, 50090, Tartu, Estonia

    V. Tillmann

  3. Department of Biochemistry, Faculty of Medicine, Centre of Excellence for Translational Medicine, University of Tartu, 50090, Tartu, Estonia

    M. Zilmer

  4. Department of Traumatology and Orthopaedics, Faculty of Medicine, University of Tartu, 50090, Tartu, Estonia

    K. Maasalu

Authors
  1. L. Utsal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. Tillmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Zilmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Mäestu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. Purge
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Saar
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. E. Lätt
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. T. Jürimäe
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. K. Maasalu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. J. Jürimäe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Utsal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Utsal, L., Tillmann, V., Zilmer, M. et al. Serum interferon gamma concentration is associated with bone mineral density in overweight boys. J Endocrinol Invest 37, 175–180 (2014). https://doi.org/10.1007/s40618-013-0029-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40618-013-0029-6

Keywords

Search

Navigation