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Erschienen in: Calcified Tissue International 5/2017

14.07.2017 | Original Research

Obese Versus Normal-Weight Late-Adolescent Females have Inferior Trabecular Bone Microarchitecture: A Pilot Case-Control Study

verfasst von: Joseph M. Kindler, Norman K. Pollock, Hannah L. Ross, Christopher M. Modlesky, Harshvardhan Singh, Emma M. Laing, Richard D. Lewis

Erschienen in: Calcified Tissue International | Ausgabe 5/2017

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Abstract

Though still a topic of debate, the position that skeletal health is compromised with obesity has received support in the pediatric and adult literature. The limited data relating specifically to trabecular bone microarchitecture, however, have been relatively inconsistent. The aim of this pilot cross-sectional case-control study was to compare trabecular bone microarchitecture between obese (OB) and normal-weight (NW) late-adolescent females. A secondary aim was to compare diaphyseal cortical bone outcomes between these two groups. Twenty-four non-Hispanic white females, ages 18–19 years, were recruited into OB (n = 12) or NW (n = 12) groups based on pre-specified criteria for percent body fat (≥32 vs. <30, respectively), body mass index (>90th vs. 20th–79th, respectively), and waist circumference (≥90th vs. 25th–75th, respectively). Participants were also individually matched on age, height, and oral contraceptive use. Using magnetic resonance imaging, trabecular bone microarchitecture was assessed at the distal radius and proximal tibia metaphysis, and cortical bone architecture was assessed at the mid-radius and mid-tibia diaphysis. OB versus NW had lower apparent trabecular thickness (radius and tibia), higher apparent trabecular separation (radius), and lower apparent bone volume to total volume (radius; all P < 0.050). Some differences in radius and tibia trabecular bone microarchitecture were retained after adjusting for insulin resistance or age at menarche. Mid-radius and mid-tibia cortical bone volume and estimated strength were lower in the OB compared to NW after adjusting for fat-free soft tissue mass (all P < 0.050). These trabecular and cortical bone deficits might contribute to the increased fracture risk in obese youth.
Literatur
1.
Zurück zum Zitat Cheng S, Volgyi E, Tylavsky FA, Lyytikainen A, Tormakangas T, Xu L, Cheng SM, Kroger H, Alen M, Kujala UM (2009) Trait-specific tracking and determinants of body composition: a 7-year follow-up study of pubertal growth in girls. BMC Med 7:5CrossRefPubMedPubMedCentral Cheng S, Volgyi E, Tylavsky FA, Lyytikainen A, Tormakangas T, Xu L, Cheng SM, Kroger H, Alen M, Kujala UM (2009) Trait-specific tracking and determinants of body composition: a 7-year follow-up study of pubertal growth in girls. BMC Med 7:5CrossRefPubMedPubMedCentral
2.
Zurück zum Zitat Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C (2000) Peak Bone Mass. Osteoporos Int 11:985–1009CrossRefPubMed Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C (2000) Peak Bone Mass. Osteoporos Int 11:985–1009CrossRefPubMed
3.
Zurück zum Zitat Nishiyama KK, Macdonald HM, Moore SA, Fung T, Boyd SK, McKay HA (2012) Cortical porosity is higher in boys compared with girls at the distal radius and distal tibia during pubertal growth: an HR-pQCT study. J Bone Miner Res 27(2):273–282CrossRefPubMed Nishiyama KK, Macdonald HM, Moore SA, Fung T, Boyd SK, McKay HA (2012) Cortical porosity is higher in boys compared with girls at the distal radius and distal tibia during pubertal growth: an HR-pQCT study. J Bone Miner Res 27(2):273–282CrossRefPubMed
4.
Zurück zum Zitat Kessler J, Koebnick C, Smith N, Adams A (2013) Childhood obesity is associated with increased risk of most lower extremity fractures. Clin Orthop Relat Res 471(4):1199–1207CrossRefPubMed Kessler J, Koebnick C, Smith N, Adams A (2013) Childhood obesity is associated with increased risk of most lower extremity fractures. Clin Orthop Relat Res 471(4):1199–1207CrossRefPubMed
5.
Zurück zum Zitat Taylor ED, Theim KR, Mirch MC, Ghorbani S, Tanofsky-Kraff M, Adler-Wailes DC, Brady S, Reynolds JC, Calis KA, Yanovski JA (2006) Orthopedic complications of overweight in children and adolescents. Pediatrics 117(6):2167–2174CrossRefPubMedPubMedCentral Taylor ED, Theim KR, Mirch MC, Ghorbani S, Tanofsky-Kraff M, Adler-Wailes DC, Brady S, Reynolds JC, Calis KA, Yanovski JA (2006) Orthopedic complications of overweight in children and adolescents. Pediatrics 117(6):2167–2174CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat Duncan MJ, Stanley M (2012) Functional movement is negatively associated with weight status and positively associated with physical activity in british primary school children. J Obes 2012:697563CrossRefPubMedPubMedCentral Duncan MJ, Stanley M (2012) Functional movement is negatively associated with weight status and positively associated with physical activity in british primary school children. J Obes 2012:697563CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Pollock NK, Laing EM, Baile CA, Hamrick MW, Hall DB, Lewis RD (2007) Is adiposity advantageous for bone strength? A peripheral quantitative computed tomography study in late adolescent females. Am J Clin Nutr 86(5):1530–1538PubMed Pollock NK, Laing EM, Baile CA, Hamrick MW, Hall DB, Lewis RD (2007) Is adiposity advantageous for bone strength? A peripheral quantitative computed tomography study in late adolescent females. Am J Clin Nutr 86(5):1530–1538PubMed
8.
Zurück zum Zitat Pollock NK, Laing EM, Hamrick MW, Baile CA, Hall DB, Lewis RD (2011) Bone and fat relationships in postadolescent black females: a pQCT study. Osteoporos Int 22(2):655–665CrossRefPubMed Pollock NK, Laing EM, Hamrick MW, Baile CA, Hall DB, Lewis RD (2011) Bone and fat relationships in postadolescent black females: a pQCT study. Osteoporos Int 22(2):655–665CrossRefPubMed
9.
Zurück zum Zitat 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(1):106–114CrossRefPubMed 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(1):106–114CrossRefPubMed
10.
Zurück zum Zitat Evans AL, Paggiosi MA, Eastell R, Walsh JS (2015) Bone density, microstructure and strength in obese and normal weight men and women in younger and older adulthood. J Bone Miner Res 30(5):920–928CrossRefPubMed Evans AL, Paggiosi MA, Eastell R, Walsh JS (2015) Bone density, microstructure and strength in obese and normal weight men and women in younger and older adulthood. J Bone Miner Res 30(5):920–928CrossRefPubMed
11.
Zurück zum Zitat Sornay-Rendu E, Boutroy S, Vilayphiou N, Claustrat B, Chapurlat RD (2013) In obese postmenopausal women, bone microarchitecture and strength are not commensurate to greater body weight: the Os des Femmes de Lyon (OFELY) study. J Bone Miner Res 28(7):1679–1687CrossRefPubMed Sornay-Rendu E, Boutroy S, Vilayphiou N, Claustrat B, Chapurlat RD (2013) In obese postmenopausal women, bone microarchitecture and strength are not commensurate to greater body weight: the Os des Femmes de Lyon (OFELY) study. J Bone Miner Res 28(7):1679–1687CrossRefPubMed
12.
Zurück zum Zitat 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(2):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(2):594–602CrossRefPubMed
13.
Zurück zum Zitat Farr JN, Amin S, LeBrasseur NK, Atkinson EJ, Achenbach SJ, McCready LK, Joseph Melton III L, Khosla S (2014) Body composition during childhood and adolescence: relations to bone strength and microstructure. J Clin Endocrinol Metab 99(12):4641–4648CrossRefPubMedPubMedCentral Farr JN, Amin S, LeBrasseur NK, Atkinson EJ, Achenbach SJ, McCready LK, Joseph Melton III L, Khosla S (2014) Body composition during childhood and adolescence: relations to bone strength and microstructure. J Clin Endocrinol Metab 99(12):4641–4648CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Hoy CL, Macdonald HM, McKay HA (2013) How does bone quality differ between healthy-weight and overweight adolescents and young adults? Clin Orthop Relat Res 471(4):1214–1225CrossRefPubMed Hoy CL, Macdonald HM, McKay HA (2013) How does bone quality differ between healthy-weight and overweight adolescents and young adults? Clin Orthop Relat Res 471(4):1214–1225CrossRefPubMed
15.
Zurück zum Zitat Jackowski SA, Faulkner RA, Farthing JP, Kontulainen SA, Beck TJ, Baxter-Jones AD (2009) Peak lean tissue mass accrual precedes changes in bone strength indices at the proximal femur during the pubertal growth spurt. Bone 44(6):1186–1190CrossRefPubMed Jackowski SA, Faulkner RA, Farthing JP, Kontulainen SA, Beck TJ, Baxter-Jones AD (2009) Peak lean tissue mass accrual precedes changes in bone strength indices at the proximal femur during the pubertal growth spurt. Bone 44(6):1186–1190CrossRefPubMed
16.
Zurück zum Zitat Kindler JM, Lewis RD, Hamrick MW (2015) Skeletal muscle and pediatric bone development. Curr Opin Endocrinol Diabetes Obes 22(6):467–474CrossRefPubMed Kindler JM, Lewis RD, Hamrick MW (2015) Skeletal muscle and pediatric bone development. Curr Opin Endocrinol Diabetes Obes 22(6):467–474CrossRefPubMed
17.
Zurück zum Zitat Leonard MB, Zemel BS, Wrotniak BH, Klieger SB, Shults J, Stallings VA, Stettler N (2015) Tibia and radius bone geometry and volumetric density in obese compared to non-obese adolescents. Bone 73:69–76CrossRefPubMed Leonard MB, Zemel BS, Wrotniak BH, Klieger SB, Shults J, Stallings VA, Stettler N (2015) Tibia and radius bone geometry and volumetric density in obese compared to non-obese adolescents. Bone 73:69–76CrossRefPubMed
18.
Zurück zum Zitat Adams AL, Kessler JI, Deramerian K, Smith N, Black MH, Porter AH, Jacobsen SJ, Koebnick C (2013) Associations between childhood obesity and upper and lower extremity injuries. Inj Prev 19(3):191–197CrossRefPubMed Adams AL, Kessler JI, Deramerian K, Smith N, Black MH, Porter AH, Jacobsen SJ, Koebnick C (2013) Associations between childhood obesity and upper and lower extremity injuries. Inj Prev 19(3):191–197CrossRefPubMed
19.
Zurück zum Zitat Fernandez JR, Redden DT, Pietrobelli A, Allison DB (2004) Waist circumference percentiles in nationally representative samples of African-American, European-American, and Mexican-American children and adolescents. J Pediatr 145(4):439–444CrossRefPubMed Fernandez JR, Redden DT, Pietrobelli A, Allison DB (2004) Waist circumference percentiles in nationally representative samples of African-American, European-American, and Mexican-American children and adolescents. J Pediatr 145(4):439–444CrossRefPubMed
20.
Zurück zum Zitat Anthropometry Procedures Manual, National Health and Nutrition Examination Survey (NHANES), 2007 Anthropometry Procedures Manual, National Health and Nutrition Examination Survey (NHANES), 2007
21.
Zurück zum Zitat Kindler JM, Ross HL, Laing EM, Modlesky CM, Pollock NK, Baile CA, Lewis RD (2015) Load-specific physical activity scores are related to tibia bone architecture. Int J Sport Nutr Exerc Metab 25(2):136–144CrossRefPubMed Kindler JM, Ross HL, Laing EM, Modlesky CM, Pollock NK, Baile CA, Lewis RD (2015) Load-specific physical activity scores are related to tibia bone architecture. Int J Sport Nutr Exerc Metab 25(2):136–144CrossRefPubMed
22.
Zurück zum Zitat Weeks BK, Beck BR (2008) The BPAQ: a bone-specific physical activity assessment instrument. Osteoporos Int 19(11):1567–1577CrossRefPubMed Weeks BK, Beck BR (2008) The BPAQ: a bone-specific physical activity assessment instrument. Osteoporos Int 19(11):1567–1577CrossRefPubMed
23.
Zurück zum Zitat Levy JC, Matthews DR, Hermans MP (1998) Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care 21(12):2191–2192CrossRefPubMed Levy JC, Matthews DR, Hermans MP (1998) Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care 21(12):2191–2192CrossRefPubMed
24.
Zurück zum Zitat Modlesky CM, Subramanian P, Miller F (2008) Underdeveloped trabecular bone microarchitecture is detected in children with cerebral palsy using high-resolution magnetic resonance imaging. Osteoporos Int 19(2):169–176CrossRefPubMed Modlesky CM, Subramanian P, Miller F (2008) Underdeveloped trabecular bone microarchitecture is detected in children with cerebral palsy using high-resolution magnetic resonance imaging. Osteoporos Int 19(2):169–176CrossRefPubMed
25.
Zurück zum Zitat Majumdar S, Genant HK, Grampp S, Newitt DC, Truong VH, Lin JC, Mathur A (1997) Correlation of trabecular bone structure with age, bone mineral density, and osteoporotic status: in vivo studies in the distal radius using high resolution magnetic resonance imaging. J Bone Miner Res 12(1):111–118CrossRefPubMed Majumdar S, Genant HK, Grampp S, Newitt DC, Truong VH, Lin JC, Mathur A (1997) Correlation of trabecular bone structure with age, bone mineral density, and osteoporotic status: in vivo studies in the distal radius using high resolution magnetic resonance imaging. J Bone Miner Res 12(1):111–118CrossRefPubMed
26.
Zurück zum Zitat Modlesky CM, Majumdar S, Dudley GA (2008) Trabecular bone microarchitecture in female collegiate gymnasts. Osteoporos Int 19(7):1011–1018CrossRefPubMed Modlesky CM, Majumdar S, Dudley GA (2008) Trabecular bone microarchitecture in female collegiate gymnasts. Osteoporos Int 19(7):1011–1018CrossRefPubMed
27.
Zurück zum Zitat Johnson DL, Miller F, Subramanian P, Modlesky CM (2009) Adipose tissue infiltration of skeletal muscle in children with cerebral palsy. J Pediatr 154(5):715–720CrossRefPubMed Johnson DL, Miller F, Subramanian P, Modlesky CM (2009) Adipose tissue infiltration of skeletal muscle in children with cerebral palsy. J Pediatr 154(5):715–720CrossRefPubMed
28.
Zurück zum Zitat Modlesky CM, Kanoff SA, Johnson DL, Subramanian P, Miller F (2009) Evaluation of the femoral midshaft in children with cerebral palsy using magnetic resonance imaging. Osteoporos Int 20(4):609–615CrossRefPubMed Modlesky CM, Kanoff SA, Johnson DL, Subramanian P, Miller F (2009) Evaluation of the femoral midshaft in children with cerebral palsy using magnetic resonance imaging. Osteoporos Int 20(4):609–615CrossRefPubMed
29.
Zurück zum Zitat Suckling J, Sigmundsson T, Greenwood K, Bullmore ET (1999) A modified fuzzy clustering algorithm for operator independent brain tissue classification of dual echo MR images. Magn Reson Imaging 17(7):1065–1076CrossRefPubMed Suckling J, Sigmundsson T, Greenwood K, Bullmore ET (1999) A modified fuzzy clustering algorithm for operator independent brain tissue classification of dual echo MR images. Magn Reson Imaging 17(7):1065–1076CrossRefPubMed
30.
Zurück zum Zitat Turner CH, Burr DB (2001) Experimental techniques for bone mechanics. CRC Press, Boca RatonCrossRef Turner CH, Burr DB (2001) Experimental techniques for bone mechanics. CRC Press, Boca RatonCrossRef
31.
Zurück zum Zitat Glass NA, Torner JC, Letuchy EM, Burns TL, Janz KF, Eichenberger Gilmore JM, Schlechte JA, Levy SM (2016) The relationship between greater prepubertal adiposity, subsequent age of maturation, and bone strength during adolescence. J Bone Miner Res 31(7):1455–1465CrossRefPubMedPubMedCentral Glass NA, Torner JC, Letuchy EM, Burns TL, Janz KF, Eichenberger Gilmore JM, Schlechte JA, Levy SM (2016) The relationship between greater prepubertal adiposity, subsequent age of maturation, and bone strength during adolescence. J Bone Miner Res 31(7):1455–1465CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Ducher G, Bass SL, Naughton GA, Eser P, Telford RD, Daly RM (2009) Overweight children have a greater proportion of fat mass relative to muscle mass in the upper limbs than in the lower limbs: implications for bone strength at the distal forearm. Am J Clin Nutr 90(4):1104–1111CrossRefPubMed Ducher G, Bass SL, Naughton GA, Eser P, Telford RD, Daly RM (2009) Overweight children have a greater proportion of fat mass relative to muscle mass in the upper limbs than in the lower limbs: implications for bone strength at the distal forearm. Am J Clin Nutr 90(4):1104–1111CrossRefPubMed
33.
Zurück zum Zitat Farr JN, Dimitri P (2017) The impact of fat and obesity on bone microarchitecture and strength in children. Calcif Tissue Int 100(5):500–513CrossRefPubMed Farr JN, Dimitri P (2017) The impact of fat and obesity on bone microarchitecture and strength in children. Calcif Tissue Int 100(5):500–513CrossRefPubMed
34.
Zurück zum Zitat 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(6):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(6):2562–2572CrossRefPubMedPubMedCentral
35.
Zurück zum Zitat Tchernof A, Despres JP (2013) Pathophysiology of human visceral obesity: an update. Physiol Rev 93(1):359–404CrossRefPubMed Tchernof A, Despres JP (2013) Pathophysiology of human visceral obesity: an update. Physiol Rev 93(1):359–404CrossRefPubMed
36.
Zurück zum Zitat Sayers A, Lawlor DA, Sattar N, Tobias JH (2012) The association between insulin levels and cortical bone: findings from a cross-sectional analysis of pQCT parameters in adolescents. J Bone Miner Res 27(3):610–618CrossRefPubMed Sayers A, Lawlor DA, Sattar N, Tobias JH (2012) The association between insulin levels and cortical bone: findings from a cross-sectional analysis of pQCT parameters in adolescents. J Bone Miner Res 27(3):610–618CrossRefPubMed
37.
Zurück zum Zitat Breen ME, Laing EM, Hall DB, Hausman DB, Taylor RG, Isales CM, Ding KH, Pollock NK, Hamrick MW, Baile CA, Lewis RD (2011) 25-hydroxyvitamin D, insulin-like growth factor-I, and bone mineral accrual during growth. J Clin Endocrinol Metab 96(1):E89–E98CrossRefPubMed Breen ME, Laing EM, Hall DB, Hausman DB, Taylor RG, Isales CM, Ding KH, Pollock NK, Hamrick MW, Baile CA, Lewis RD (2011) 25-hydroxyvitamin D, insulin-like growth factor-I, and bone mineral accrual during growth. J Clin Endocrinol Metab 96(1):E89–E98CrossRefPubMed
38.
Zurück zum Zitat Xu L, Wang Q, Wang Q, Lyytikainen A, Mikkola T, Volgyi E, Cheng S, Wiklund P, Munukka E, Nicholson P, Alen M, Cheng S (2011) Concerted actions of insulin-like growth factor 1, testosterone, and estradiol on peripubertal bone growth: a 7-year longitudinal study. J Bone Miner Res 26(9):2204–2211CrossRefPubMed Xu L, Wang Q, Wang Q, Lyytikainen A, Mikkola T, Volgyi E, Cheng S, Wiklund P, Munukka E, Nicholson P, Alen M, Cheng S (2011) Concerted actions of insulin-like growth factor 1, testosterone, and estradiol on peripubertal bone growth: a 7-year longitudinal study. J Bone Miner Res 26(9):2204–2211CrossRefPubMed
39.
Zurück zum Zitat Entingh-Pearsall A, Kahn CR (2004) Differential roles of the insulin and insulin-like growth factor-I (IGF-I) receptors in response to insulin and IGF-I. J Biol Chem 279(36):38016–38024CrossRefPubMed Entingh-Pearsall A, Kahn CR (2004) Differential roles of the insulin and insulin-like growth factor-I (IGF-I) receptors in response to insulin and IGF-I. J Biol Chem 279(36):38016–38024CrossRefPubMed
40.
Zurück zum Zitat Duan C, Ren H, Gao S (2010) Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: roles in skeletal muscle growth and differentiation. Gen Comp Endocrinol 167(3):344–351CrossRefPubMed Duan C, Ren H, Gao S (2010) Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: roles in skeletal muscle growth and differentiation. Gen Comp Endocrinol 167(3):344–351CrossRefPubMed
41.
Zurück zum Zitat Kindler JM, Pollock NK, Laing EM, Oshri A, Jenkins NT, Isales CM, Hamrick MW, Ding KH, Hausman DB, McCabe GP, Martin BR, Hill Gallant KM, Warden SJ, Weaver CM, Peacock M, Lewis RD (2017) Insulin Resistance and the IGF-I-Cortical Bone Relationship in Children Ages 9-13 Years. J Bone Miner Res. doi:10.1002/jbmr.3132 PubMed Kindler JM, Pollock NK, Laing EM, Oshri A, Jenkins NT, Isales CM, Hamrick MW, Ding KH, Hausman DB, McCabe GP, Martin BR, Hill Gallant KM, Warden SJ, Weaver CM, Peacock M, Lewis RD (2017) Insulin Resistance and the IGF-I-Cortical Bone Relationship in Children Ages 9-13 Years. J Bone Miner Res. doi:10.​1002/​jbmr.​3132 PubMed
42.
Zurück zum Zitat Kindler JM, Pollock NK, Laing EM, Jenkins NT, Oshri A, Isales C, Hamrick M, Lewis RD (2016) Insulin resistance negatively influences the muscle-dependent IGF-I-bone mass relationship in pre-menarcheal girls. J Clin Endocrinol Metab 101(1):199–205CrossRefPubMed Kindler JM, Pollock NK, Laing EM, Jenkins NT, Oshri A, Isales C, Hamrick M, Lewis RD (2016) Insulin resistance negatively influences the muscle-dependent IGF-I-bone mass relationship in pre-menarcheal girls. J Clin Endocrinol Metab 101(1):199–205CrossRefPubMed
43.
Zurück zum Zitat Yakar S, Canalis E, Sun H, Mejia W, Kawashima Y, Nasser P, Courtland HW, Williams V, Bouxsein M, Rosen C, Jepsen KJ (2009) Serum IGF-1 determines skeletal strength by regulating subperiosteal expansion and trait interactions. J Bone Miner Res 24(8):1481–1492CrossRefPubMedPubMedCentral Yakar S, Canalis E, Sun H, Mejia W, Kawashima Y, Nasser P, Courtland HW, Williams V, Bouxsein M, Rosen C, Jepsen KJ (2009) Serum IGF-1 determines skeletal strength by regulating subperiosteal expansion and trait interactions. J Bone Miner Res 24(8):1481–1492CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Hamrick MW, McNeil PL, Patterson SL (2010) Role of muscle-derived growth factors in bone formation. J Musculoskelet Neuronal Interact 10(1):64–70PubMedPubMedCentral Hamrick MW, McNeil PL, Patterson SL (2010) Role of muscle-derived growth factors in bone formation. J Musculoskelet Neuronal Interact 10(1):64–70PubMedPubMedCentral
45.
Zurück zum Zitat Kirmani S, Christen D, van Lenthe GH, Fischer PR, Bouxsein ML, McCready LK, Melton LJ 3rd, Riggs BL, Amin S, Muller R, Khosla S (2009) Bone structure at the distal radius during adolescent growth. J Bone Miner Res 24(6):1033–1042CrossRefPubMed Kirmani S, Christen D, van Lenthe GH, Fischer PR, Bouxsein ML, McCready LK, Melton LJ 3rd, Riggs BL, Amin S, Muller R, Khosla S (2009) Bone structure at the distal radius during adolescent growth. J Bone Miner Res 24(6):1033–1042CrossRefPubMed
46.
Zurück zum Zitat Cooper C, Dennison EM, Leufkens HG, Bishop N, van Staa TP (2004) Epidemiology of childhood fractures in Britain: a study using the general practice research database. J Bone Miner Res 19(12):1976–1981CrossRefPubMed Cooper C, Dennison EM, Leufkens HG, Bishop N, van Staa TP (2004) Epidemiology of childhood fractures in Britain: a study using the general practice research database. J Bone Miner Res 19(12):1976–1981CrossRefPubMed
Metadaten
Titel
Obese Versus Normal-Weight Late-Adolescent Females have Inferior Trabecular Bone Microarchitecture: A Pilot Case-Control Study
verfasst von
Joseph M. Kindler
Norman K. Pollock
Hannah L. Ross
Christopher M. Modlesky
Harshvardhan Singh
Emma M. Laing
Richard D. Lewis
Publikationsdatum
14.07.2017
Verlag
Springer US
Erschienen in
Calcified Tissue International / Ausgabe 5/2017
Print ISSN: 0171-967X
Elektronische ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-017-0303-2

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