Skip to main content
Top
Published in: Calcified Tissue International 6/2008

01-06-2008

Subcutaneous Fat and Body Fat Mass Have Different Effects on Bone Development at the Forearm in Children and Adolescents

Authors: Oliver Fricke, Christof Land, Oliver Semler, Baerbel Tutlewski, Angelika Stabrey, Thomas Remer, Eckhard Schoenau

Published in: Calcified Tissue International | Issue 6/2008

Login to get access

Abstract

The present study investigated whether subcutaneous fat differs in the impact on bone development from fat mass (FM). We analyzed 295 healthy children and adolescents (age 5–19 years, 139 males) for FM by measuring four skinfold thicknesses and for bone development and body composition at the forearm by peripheral quantitative computed tomography in a cross-sectional investigation. Relative cross-sectional fat area (FA) was a surrogate for relative subcutaneous FM at the forearm and was associated positively with percent fat in prepubertal individuals and pubertal females but negatively in pubertal males. Percent FM was associated with trabecular bone mineral density (BMDtrab) in prepubertal individuals (females r = 0.394, males r = 0.242) and pubertal individuals (females r = 0.215, males r = −0.275). Bone mineral count was correlated with percent FM in pubertal males (r = −0.287). FA was correlated with BMDtrab (r = 0.285) and with cortical bone mineral density (BMDcort, r = −0.296) in pubertal females. The ratio FA/FM was negatively correlated with BMDcort (r = −0.299) in pubertal females. Pubertal females with relatively high subcutaneous fat area (high ratio FA/FM) were characterized by lower bone strength (P = 0.047). FM and the relative amount of subcutaneous fat have effects on bone formation and resorption that depend on gender and puberty. Especially in pubertal females, higher levels of subcutaneous fat may decrease bone strength due to increased cortical remodeling.
Literature
2.
go back to reference Reid RI (2008) Relationships between fat and bone. Osteoporos Int 19:595–606 Reid RI (2008) Relationships between fat and bone. Osteoporos Int 19:595–606
4.
go back to reference Fricke O, Schoenau E (2007) The “functional muscle-bone unit”: probing the relevance of mechanical signals for bone development in children and adolescents. Growth Horm IGF Res 17:1–9PubMedCrossRef Fricke O, Schoenau E (2007) The “functional muscle-bone unit”: probing the relevance of mechanical signals for bone development in children and adolescents. Growth Horm IGF Res 17:1–9PubMedCrossRef
5.
go back to reference Takeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, Parker KL, Armstrong D, Ducy P, Karsenty G (2002) Leptin regulates bone formation via the sympathetic nervous system. Cell 111:305–317PubMedCrossRef Takeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, Parker KL, Armstrong D, Ducy P, Karsenty G (2002) Leptin regulates bone formation via the sympathetic nervous system. Cell 111:305–317PubMedCrossRef
6.
go back to reference Elefteriou F, Ahn JD, Takeda S, Starbuck M, Yang X, Liu X, Kondo H, Richards WG, Bannon TW, Noda M, Clement K, Vaisse C, Karsenty G (2005) Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature 434:514–520PubMedCrossRef Elefteriou F, Ahn JD, Takeda S, Starbuck M, Yang X, Liu X, Kondo H, Richards WG, Bannon TW, Noda M, Clement K, Vaisse C, Karsenty G (2005) Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature 434:514–520PubMedCrossRef
7.
go back to reference Jürimäe J, Jürimäe T (2006) Influence of insulin-like growth factor-1 and leptin on bone mineral content in healthy premenopausal women. Exp Biol Med 231:1673–1677 Jürimäe J, Jürimäe T (2006) Influence of insulin-like growth factor-1 and leptin on bone mineral content in healthy premenopausal women. Exp Biol Med 231:1673–1677
8.
go back to reference Oh KW, Lee WY, Rhee EJ, Baek KH, Yoon KH, Kang MI, Yun EJ, Park CY, Ihm SH, Choi MG, Yoo HJ, Park SW (2005) The relationship between serum resistin, leptin, adiponectin, ghrelin levels and bone mineral density in middle-aged men. Clin Endocrinol 63:131–138CrossRef Oh KW, Lee WY, Rhee EJ, Baek KH, Yoon KH, Kang MI, Yun EJ, Park CY, Ihm SH, Choi MG, Yoo HJ, Park SW (2005) The relationship between serum resistin, leptin, adiponectin, ghrelin levels and bone mineral density in middle-aged men. Clin Endocrinol 63:131–138CrossRef
9.
go back to reference Kontogianni MD, Dafni UG, Routsias JG, Skopouli FN (2004) Blood leptin and adiponectin as possible mediators of the relation between fat mass and BMD in perimenopausal women. J Bone Miner Res 19:546–551PubMedCrossRef Kontogianni MD, Dafni UG, Routsias JG, Skopouli FN (2004) Blood leptin and adiponectin as possible mediators of the relation between fat mass and BMD in perimenopausal women. J Bone Miner Res 19:546–551PubMedCrossRef
10.
go back to reference Karsenty G (2006) Convergence between bone and energy homeostases: leptin regulation of bone mass. Cell Metab 4:341–348PubMedCrossRef Karsenty G (2006) Convergence between bone and energy homeostases: leptin regulation of bone mass. Cell Metab 4:341–348PubMedCrossRef
11.
go back to reference Blain H, Vuillemin A, Guillemin F, Durant R, Hanesse B, de Talance N, Doucet B, Jeandel C (2002) Serum leptin level is a predictor of bone mineral density in postmenopausal women. J Clin Endocrinol Metab 87:1030–1035PubMedCrossRef Blain H, Vuillemin A, Guillemin F, Durant R, Hanesse B, de Talance N, Doucet B, Jeandel C (2002) Serum leptin level is a predictor of bone mineral density in postmenopausal women. J Clin Endocrinol Metab 87:1030–1035PubMedCrossRef
12.
go back to reference Pasco JA, Henry MJ, Kotowicz MA, Collier GR, Ball MJ, Ugoni AM, Nicholson GC (2001) Serum leptin levels are associated with bone mass in nonobese women. J Clin Endocrinol Metab 86:1884–1887PubMedCrossRef Pasco JA, Henry MJ, Kotowicz MA, Collier GR, Ball MJ, Ugoni AM, Nicholson GC (2001) Serum leptin levels are associated with bone mass in nonobese women. J Clin Endocrinol Metab 86:1884–1887PubMedCrossRef
13.
go back to reference Yamauchi M, Sugimoto T, Yamaguchi T, Nakaoka D, Kanzawa M, Yano S, Ozuru R, Sugishita T, Chihara K (2001) Plasma leptin concentrations are associated with bone mineral density and the presence of vertebral fractures in postmenopausal women. Clin Endocrinol 55:341–347CrossRef Yamauchi M, Sugimoto T, Yamaguchi T, Nakaoka D, Kanzawa M, Yano S, Ozuru R, Sugishita T, Chihara K (2001) Plasma leptin concentrations are associated with bone mineral density and the presence of vertebral fractures in postmenopausal women. Clin Endocrinol 55:341–347CrossRef
14.
go back to reference Iwamoto I, Douchi T, Kosha S, Murakami M, Fujino T, Nagata Y (2000) Relationships between serum leptin level and regional bone mineral density, bone metabolic markers in healthy women. Acta Obstet Gynecol Scand 79:1060–1064PubMedCrossRef Iwamoto I, Douchi T, Kosha S, Murakami M, Fujino T, Nagata Y (2000) Relationships between serum leptin level and regional bone mineral density, bone metabolic markers in healthy women. Acta Obstet Gynecol Scand 79:1060–1064PubMedCrossRef
15.
go back to reference Goulding A, Taylor RW (1998) Plasma leptin values in relation to bone mass and density and to dynamic biochemical markers of bone resorption and formation in postmenopausal women. Calcif Tissue Int 63:456–458PubMedCrossRef Goulding A, Taylor RW (1998) Plasma leptin values in relation to bone mass and density and to dynamic biochemical markers of bone resorption and formation in postmenopausal women. Calcif Tissue Int 63:456–458PubMedCrossRef
16.
go back to reference Rauch F, Blum WF, Klein K, Allolio B, Schonau E (1998) Does leptin have an effect on bone in adult women? Calcif Tissue Int 63:453–455PubMedCrossRef Rauch F, Blum WF, Klein K, Allolio B, Schonau E (1998) Does leptin have an effect on bone in adult women? Calcif Tissue Int 63:453–455PubMedCrossRef
17.
go back to reference Luo XH, Guo LJ, Xie H, Yuan LQ, Wu XP, Zhou HD, Liao EY (2006) Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res 21:1648–1656PubMedCrossRef Luo XH, Guo LJ, Xie H, Yuan LQ, Wu XP, Zhou HD, Liao EY (2006) Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res 21:1648–1656PubMedCrossRef
18.
go back to reference Høiberg M, Nielsen TL, Wraae K, Abrahamsen B, Hagen C, Andersen M, Brixen K (2007) Population-based reference values for bone mineral density in young men. Osteoporos Int 18:1507–1514PubMedCrossRef Høiberg M, Nielsen TL, Wraae K, Abrahamsen B, Hagen C, Andersen M, Brixen K (2007) Population-based reference values for bone mineral density in young men. Osteoporos Int 18:1507–1514PubMedCrossRef
19.
go back to reference Matsubara M, Maruoka S, Katayose S (2002) Inverse relationship between plasma adiponectin and leptin concentrations in normal-weight and obese women. Eur J Endocrinol 147:173–180PubMedCrossRef Matsubara M, Maruoka S, Katayose S (2002) Inverse relationship between plasma adiponectin and leptin concentrations in normal-weight and obese women. Eur J Endocrinol 147:173–180PubMedCrossRef
20.
go back to reference Park KG, Park KS, Kim MJ, Kim HS, Suh YS, Ahn JD, Park KK, Chang YC, Lee IK (2004) Relationship between serum adiponectin and leptin concentrations and body fat distribution. Diabetes Res Clin Pract 63:135–142PubMedCrossRef Park KG, Park KS, Kim MJ, Kim HS, Suh YS, Ahn JD, Park KK, Chang YC, Lee IK (2004) Relationship between serum adiponectin and leptin concentrations and body fat distribution. Diabetes Res Clin Pract 63:135–142PubMedCrossRef
21.
go back to reference Hanley AJ, Bowden D, Wagenknecht LE, Balasubramanyam A, Langfeld C, Saad MF, Rotter JI, Guo X, Chen YD, Bryer-Ash M, Norris JM, Haffner SM (2007) Associations of adiponectin with body fat distribution and insulin sensitivity in nondiabetic Hispanics and African-Americans. J Clin Endocrinol Metab 92:2665–2671PubMedCrossRef Hanley AJ, Bowden D, Wagenknecht LE, Balasubramanyam A, Langfeld C, Saad MF, Rotter JI, Guo X, Chen YD, Bryer-Ash M, Norris JM, Haffner SM (2007) Associations of adiponectin with body fat distribution and insulin sensitivity in nondiabetic Hispanics and African-Americans. J Clin Endocrinol Metab 92:2665–2671PubMedCrossRef
22.
go back to reference Deurenberg P (1992) The assessment of body composition: use and misuse. In: Annual report of the Nestle Foundation. Nestle, Lausanne, pp 35–72 Deurenberg P (1992) The assessment of body composition: use and misuse. In: Annual report of the Nestle Foundation. Nestle, Lausanne, pp 35–72
23.
go back to reference Forbes GB (1972) Human body composition. Springer Verlag, New York Forbes GB (1972) Human body composition. Springer Verlag, New York
24.
go back to reference Roche AF, Heymsfield SB, Lohman TG (1996) Human body composition. Human Kinetics, Champaign, IL Roche AF, Heymsfield SB, Lohman TG (1996) Human body composition. Human Kinetics, Champaign, IL
25.
go back to reference Norgan NG (1995) The assessment of the body composition of populations. In: Davies PSW, Cole TJ (eds) Body composition techniques in health and disease. Cambridge University Press, Cambridge, pp 195–221 Norgan NG (1995) The assessment of the body composition of populations. In: Davies PSW, Cole TJ (eds) Body composition techniques in health and disease. Cambridge University Press, Cambridge, pp 195–221
26.
go back to reference Schoenau E, Neu CM, Mokov E, Wassmer G, Manz F (2000) Influence of puberty on muscle area and cortical bone area of the forearm in boys and girls. J Clin Endocrinol Metab 85:1095–1098PubMedCrossRef Schoenau E, Neu CM, Mokov E, Wassmer G, Manz F (2000) Influence of puberty on muscle area and cortical bone area of the forearm in boys and girls. J Clin Endocrinol Metab 85:1095–1098PubMedCrossRef
27.
go back to reference Schoenau E, Neu CM, Rauch F, Manz F (2001) The development of bone strength at the proximal radius during childhood and adolescence. J Clin Endocrinol Metab 86:613–618PubMedCrossRef Schoenau E, Neu CM, Rauch F, Manz F (2001) The development of bone strength at the proximal radius during childhood and adolescence. J Clin Endocrinol Metab 86:613–618PubMedCrossRef
28.
go back to reference Tanner J (1962) Growth at adolescence. Blackwell, Oxford Tanner J (1962) Growth at adolescence. Blackwell, Oxford
29.
go back to reference Deurenberg P, Pieters JJ, Hautvast JG (1990) The assessment of the body fat percentage by skinfold thickness measurements in childhood and young adolescence. Br J Nutr 63:293–303PubMedCrossRef Deurenberg P, Pieters JJ, Hautvast JG (1990) The assessment of the body fat percentage by skinfold thickness measurements in childhood and young adolescence. Br J Nutr 63:293–303PubMedCrossRef
30.
go back to reference Fricke O, Sumnik Z, Remer T, Stabrey A, Tutlewski B, Schoenau E (2008) Cross-sectional fat area at the forearm in children and adolescents. Horm Res 69:160–164PubMedCrossRef Fricke O, Sumnik Z, Remer T, Stabrey A, Tutlewski B, Schoenau E (2008) Cross-sectional fat area at the forearm in children and adolescents. Horm Res 69:160–164PubMedCrossRef
31.
go back to reference Schoenau E, Neu CM, Rauch F, Manz F (2002) Gender-specific pubertal changes in volumetric cortical bone mineral density at the proximal radius. Bone 31:110–113PubMedCrossRef Schoenau E, Neu CM, Rauch F, Manz F (2002) Gender-specific pubertal changes in volumetric cortical bone mineral density at the proximal radius. Bone 31:110–113PubMedCrossRef
32.
go back to reference Rauch F, Klein K, Allolio B, Schoenau E (1999) Age at menarche and cortical bone geometry in premenopausal women. Bone 25:69–73PubMedCrossRef Rauch F, Klein K, Allolio B, Schoenau E (1999) Age at menarche and cortical bone geometry in premenopausal women. Bone 25:69–73PubMedCrossRef
33.
go back to reference Neu CM, Rauch F, Manz F, Schoenau E (2001) Modeling of cross-sectional bone size, mass and geometry at the proximal radius: a study of normal bone development using peripheral quantitative computed tomography. Osteoporos Int 12:538–547PubMedCrossRef Neu CM, Rauch F, Manz F, Schoenau E (2001) Modeling of cross-sectional bone size, mass and geometry at the proximal radius: a study of normal bone development using peripheral quantitative computed tomography. Osteoporos Int 12:538–547PubMedCrossRef
34.
go back to reference Alexy U, Remer T, Manz F, Neu CM, Schoenau E (2005) Long-term protein intake and dietary potential renal acid load are associated with bone modeling and remodeling at the proximal radius in healthy children. Am J Clin Nutr 82:1107–1114PubMed Alexy U, Remer T, Manz F, Neu CM, Schoenau E (2005) Long-term protein intake and dietary potential renal acid load are associated with bone modeling and remodeling at the proximal radius in healthy children. Am J Clin Nutr 82:1107–1114PubMed
35.
go back to reference Gluer CC, Blake G, Lu Y, Blunt BA, Jergas M, Genant HK (1995) Accurate assessment of precision errors: how to measure the reproducibility of bone densitometry techniques. Osteoporos Int 5:262–270PubMedCrossRef Gluer CC, Blake G, Lu Y, Blunt BA, Jergas M, Genant HK (1995) Accurate assessment of precision errors: how to measure the reproducibility of bone densitometry techniques. Osteoporos Int 5:262–270PubMedCrossRef
36.
go back to reference Fox KR, Peters DM, Sharpe P, Bell M (2000) Assessment of abdominal fat development in young adolescents using magnetic resonance imaging. Int J Obes Relat Metab Disord 24:1653–1659PubMedCrossRef Fox KR, Peters DM, Sharpe P, Bell M (2000) Assessment of abdominal fat development in young adolescents using magnetic resonance imaging. Int J Obes Relat Metab Disord 24:1653–1659PubMedCrossRef
37.
go back to reference Janicka A, Wren TA, Sanchez MM, Dorey F, Kim PS, Mittelman SD, Gilsanz V (2007) Fat mass is not beneficial to bone in adolescents and young adults. J Clin Endocrinol Metab 92:143–147PubMedCrossRef Janicka A, Wren TA, Sanchez MM, Dorey F, Kim PS, Mittelman SD, Gilsanz V (2007) Fat mass is not beneficial to bone in adolescents and young adults. J Clin Endocrinol Metab 92:143–147PubMedCrossRef
38.
go back to reference Ackerman A, Thornton JC, Wang J, Pierson RN Jr, Horlick M (2006) Sex differences in the effect of puberty on the relationship between fat mass and bone mass in 926 healthy subjects, 6 to 18 years old. Obesity 14:819–825PubMedCrossRef Ackerman A, Thornton JC, Wang J, Pierson RN Jr, Horlick M (2006) Sex differences in the effect of puberty on the relationship between fat mass and bone mass in 926 healthy subjects, 6 to 18 years old. Obesity 14:819–825PubMedCrossRef
39.
go back to reference Garnett SP, Hoegler W, Blades B, Baur LA, Peat JL, Cowell CT (2004) Relation between hormones and body composition, including bone, in prepubertal children. Am J Clin Nutr 80:966–972PubMed Garnett SP, Hoegler W, Blades B, Baur LA, Peat JL, Cowell CT (2004) Relation between hormones and body composition, including bone, in prepubertal children. Am J Clin Nutr 80:966–972PubMed
40.
go back to reference Eastell R (2005) Role of oestrogen in the regulation of bone turnover at the menarche. J Endocrinol 185:223–234PubMedCrossRef Eastell R (2005) Role of oestrogen in the regulation of bone turnover at the menarche. J Endocrinol 185:223–234PubMedCrossRef
41.
go back to reference Hong SC, Yoo SW, Cho GJ, Kim T, Hur JY, Park YK, Lee KW, Kim SH (2007) Correlation between estrogens and serum adipocytokines in premenopausal and postmenopausal women. Menopause 14:835–840 Hong SC, Yoo SW, Cho GJ, Kim T, Hur JY, Park YK, Lee KW, Kim SH (2007) Correlation between estrogens and serum adipocytokines in premenopausal and postmenopausal women. Menopause 14:835–840
42.
go back to reference Aldhahi W, Mun E, Goldfine AB (2004) Portal and peripheral cortisol levels in obese humans. Diabetologia 47:833–836PubMedCrossRef Aldhahi W, Mun E, Goldfine AB (2004) Portal and peripheral cortisol levels in obese humans. Diabetologia 47:833–836PubMedCrossRef
Metadata
Title
Subcutaneous Fat and Body Fat Mass Have Different Effects on Bone Development at the Forearm in Children and Adolescents
Authors
Oliver Fricke
Christof Land
Oliver Semler
Baerbel Tutlewski
Angelika Stabrey
Thomas Remer
Eckhard Schoenau
Publication date
01-06-2008
Publisher
Springer-Verlag
Published in
Calcified Tissue International / Issue 6/2008
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-008-9129-2

Other articles of this Issue 6/2008

Calcified Tissue International 6/2008 Go to the issue