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Horm Metab Res 2019; 51(01): 42-46
DOI: 10.1055/a-0755-2799
Endocrine Care
© Georg Thieme Verlag KG Stuttgart · New York

The Relationship Between Bone Mineral Density and Type 2 Diabetes in Obese Children and Adolescents at the Time of Initial Diagnosis

Hae Sang Lee
1   Department of Pediatrics, Ajou University School of Medicine, Ajou University Hospital, Suwon, Korea
,
Jong Seo Yoon
1   Department of Pediatrics, Ajou University School of Medicine, Ajou University Hospital, Suwon, Korea
,
Kyu Jung Park
1   Department of Pediatrics, Ajou University School of Medicine, Ajou University Hospital, Suwon, Korea
,
Jung Sub Lim
2   Department of Pediatrics, Korea Cancer Center Hospital, Seoul, Korea
,
Jin Soon Hwang
1   Department of Pediatrics, Ajou University School of Medicine, Ajou University Hospital, Suwon, Korea
› Author Affiliations
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Publication History

received 11 April 2018

accepted 02 October 2018

Publication Date:
19 October 2018 (online)

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Abstract

Long-term effects of type 2 diabetes mellitus (T2D) on bone health remain unclear. The objective of this study was to assess the possible association of bone mineral density (BMD) at multiple sites with T2D after correcting for several potential confounders such as age, sex, Tanner stage, and BMI known to affect BMD in adolescents with newly developed T2D. In this cross-sectional study, 17 children and adolescents with T2D and 59 age, sex, and BMI-matched controls were included. All subjects underwent dual-energy X-ray absorptiometry to measure regional and whole-body composition with Lunar Prodigy at the time of initial diagnosis. A BMD Z-score was calculated using data from healthy Korean children and adolescents after adjusting for height-for-age. The mean age of all subjects was 12.9±2.4 years (range, 8.3–18.3 years). BMDht Z-scores for lumbar spine and total body after adjusted for age, sex, BMI SDS, and Tanner stage were not significantly different between patients and controls. However, BMDht Z-scores for femur neck and bone mineral apparent density (BMAD) Z-scores of lumbar spine were significantly lower in T2D patients than those in healthy controls. HOMA-IR or HbA1c was not associated with BMDht Z-scores at multiple sites. BMDht Z-scores at multiple sites except femur neck in adolescents with newly developed T2D were similar to those in obese controls after adjustment for potential confounders.

Key words

bone mineral density - type 2 diabetes - diabetic complications
 

  • References

  • 1 Wang Y, Lobstein T. Worldwide trends in childhood overweight and obesity. Int J Pediatr Obes 2006; 1: 11-25
    CrossrefPubMedSearch in Google Scholar
  • 2 Kim HM, Park J, Kim HS, Kim DH, Park SH. Obesity and cardiovascular risk factors in korean children and adolescents aged 10-18 years from the korean national health and nutrition examination survey, 1998 and 2001. Am J Epidemiol 2006; 164: 787-793
    CrossrefPubMedSearch in Google Scholar
  • 3 Leslie WD, Rubin MR, Schwartz AV, Kanis JA. Type 2 diabetes and bone. J Bone Mineral Res 2012; 27: 2231-2237
    CrossrefPubMedSearch in Google Scholar
  • 4 Chobot AP, Haffke A, Polanska J, Halaba ZP, Deja G, Jarosz-Chobot P, Pluskiewicz W. Bone status in adolescents with type 1 diabetes. Diabetologia 2010; 53: 1754-1760
    CrossrefPubMedSearch in Google Scholar
  • 5 Yaturu S, Humphrey S, Landry C, Jain SK. Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med Sci Monitor 2009; 15: Cr5-Cr9
    PubMedSearch in Google Scholar
  • 6 Majima T, Komatsu Y, Yamada T, Koike Y, Shigemoto M, Takagi C, Hatanaka I, Nakao K. Decreased bone mineral density at the distal radius, but not at the lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporos Int 2005; 16: 907-913
    CrossrefPubMedSearch in Google Scholar
  • 7 Dennison EM, Syddall HE, Aihie Sayer A, Craighead S, Phillips DI, Cooper C. Type 2 diabetes mellitus is associated with increased axial bone density in men and women from the Hertfordshire cohort Study: Evidence for an indirect effect of insulin resistance?. Diabetologia 2004; 47: 1963-1968
    CrossrefPubMedSearch in Google Scholar
  • 8 Unwin N, Shaw J, Zimmet P, Alberti KG. Impaired glucose tolerance and impaired fasting glycaemia: The current status on definition and intervention. Diabetic Med 2002; 19: 708-723
    CrossrefPubMedSearch in Google Scholar
  • 9 Lim JS, Hwang JS, Lee JA, Kim DH, Park KD, Cheon GJ, Shin CH, Yang SW. Bone mineral density according to age, bone age, and pubertal stages in korean children and adolescents. J Clin Densitom 2010; 13: 68-76
    CrossrefPubMedSearch in Google Scholar
  • 10 [Anonymous] . Standards of medical care in diabetes–2014. Diabetes Care 2014; 37 (Suppl. 01) S14-S80
    CrossrefPubMedSearch in Google Scholar
  • 11 Moon JS, Lee SY, Nam CM, Choi JM, Choe BK, Seo JW, Oh K, Jang MJ, Hwang SS, Yoo MH, Kim YT, Lee CG. 2007 Korean national growth charts: Review of developmental process and an outlook. Korean J Pediatr 2008; 51: 1-25
    CrossrefPubMedSearch in Google Scholar
  • 12 Wheeler MD. Physical changes of puberty. Endocrinol Metab Clin North Am 1991; 20: 1-14
    CrossrefPubMedSearch in Google Scholar
  • 13 Kroger H, Vainio P, Nieminen J, Kotaniemi A. Comparison of different models for interpreting bone mineral density measurements using DXA and MRI technology. Bone 1995; 17: 157-159
    CrossrefPubMedSearch in Google Scholar
  • 14 Zemel BS, Leonard MB, Kelly A, Lappe JM, Gilsanz V, Oberfield S, Mahboubi S, Shepherd JA, Hangartner TN, Frederick MM, Winer KK, Kalkwarf HJ. Height adjustment in assessing dual energy x-ray absorptiometry measurements of bone mass and density in children. J Clin Endocrinol Metab 2010; 95: 1265-1273
    CrossrefPubMedSearch in Google Scholar
  • 15 Napoli N, Chandran M, Pierroz DD, Abrahamsen B, Schwartz AV, Ferrari SL. Mechanisms of diabetes mellitus-induced bone fragility. Nat Rev Endocrinol 2017; 13: 208-219
    CrossrefPubMedSearch in Google Scholar
  • 16 Ma L, Oei L, Jiang L, Estrada K, Chen H, Wang Z, Yu Q, Zillikens MC, Gao X, Rivadeneira F. Association between bone mineral density and type 2 diabetes mellitus: a meta-analysis of observational studies. Eur J Epidemiol 2012; 27: 319-332
    CrossrefPubMedSearch in Google Scholar
  • 17 Abdulameer SA, Sulaiman SA, Hassali MA, Subramaniam K, Sahib MN. Osteoporosis and type 2 diabetes mellitus: What do we know, and what we can do?. Patient Pref Adher 2012; 6: 435-448
    PubMedSearch in Google Scholar
  • 18 Nakamura M, Inaba M, Yamada S, Ozaki E, Maruo S, Okuno S, Imanishi Y, Kuriyama N, Watanabe Y, Emoto M, Motoyama K. Association of decreased handgrip strength with reduced cortical thickness in japanese female patients with type 2 diabetes mellitus. Sci Rep 2018; 8: 10767
    CrossrefPubMedSearch in Google Scholar
  • 19 Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes–a meta-analysis. Osteoporos Int 2007; 18: 427-444
    CrossrefPubMedSearch in Google Scholar
  • 20 Afghani A, Cruz ML, Goran MI. Impaired glucose tolerance and bone mineral content in overweight latino children with a family history of type 2 diabetes. Diabetes Care 2005; 28: 372-378
    CrossrefPubMedSearch in Google Scholar
  • 21 Shanbhogue VV, Mitchell DM, Rosen CJ, Bouxsein ML. Type 2 diabetes and the skeleton: New insights into sweet bones. Lancet Diabetes Endocrinol 2016; 4: 159-173
    CrossrefPubMedSearch in Google Scholar
  • 22 Ferron M, Wei J, Yoshizawa T, Del Fattore A, DePinho RA, Teti A, Ducy P, Karsenty G. Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 2010; 142: 296-308
    CrossrefPubMedSearch in Google Scholar
  • 23 Jehle PM, Jehle DR, Mohan S, Bohm BO. Serum levels of insulin-like growth factor system components and relationship to bone metabolism in Type 1 and Type 2 diabetes mellitus patients. J Endocrinol 1998; 159: 297-306
    CrossrefPubMedSearch in Google Scholar
  • 24 Abrahamsen B, Rohold A, Henriksen JE, Beck-Nielsen H. Correlations between insulin sensitivity and bone mineral density in non-diabetic men. Diabetic Med 2000; 17: 124-129
    CrossrefPubMedSearch in Google Scholar
  • 25 Arikan S, Tuzcu A, Bahceci M, Ozmen S, Gokalp D. Insulin resistance in type 2 diabetes mellitus may be related to bone mineral density. J Clin Densitom 2012; 15: 186-190
    CrossrefPubMedSearch in Google Scholar
  • 26 Starup-Linde J, Frost M, Vestergaard P, Abrahamsen B. Epidemiology of fractures in diabetes. Calcif Tissue Int 2017; 100: 109-121
    CrossrefPubMedSearch in Google Scholar
  • 27 de II L, van der Klift M, de Laet CE, van Daele PL, Hofman A, Pols HA. Bone mineral density and fracture risk in type-2 diabetes mellitus: The rotterdam study. Osteoporos Int 2005; 16: 1713-1720
    CrossrefPubMedSearch in Google Scholar
  • 28 Petit MA, Paudel ML, Taylor BC, Hughes JM, Strotmeyer ES, Schwartz AV, Cauley JA, Zmuda JM, Hoffman AR, Ensrud KE. Bone mass and strength in older men with type 2 diabetes: The Osteoporotic Fractures in Men Study. J Bone Mineral Res 2010; 25: 285-291
    CrossrefPubMedSearch in Google Scholar
  • 29 Szulc P, Munoz F, Duboeuf F, Marchand F, Delmas PD. Low width of tubular bones is associated with increased risk of fragility fracture in elderly men–the MINOS study. Bone 2006; 38: 595-602
    CrossrefPubMedSearch in Google Scholar
  • 30 Agius R, Galea R, Fava S. Bone mineral density and intervertebral disc height in type 2 diabetes. J Diabetes Complicat 2016; 30: 644-650
    CrossrefPubMedSearch in Google Scholar