Skip to main content
Erschienen in: Osteoporosis International 1/2011

01.01.2011 | Original Article

The muscle–bone unit of peripheral and central skeletal sites in children and young adults

verfasst von: R. L. Ashby, J. E. Adams, S. A. Roberts, M. Z. Mughal, K. A. Ward

Erschienen in: Osteoporosis International | Ausgabe 1/2011

Einloggen, um Zugang zu erhalten

Abstract

Summary

Changes and gender differences in the muscle bone unit at different skeletal sites were investigated during pubertal development. Females accrued greater BMC in relation to muscle compared to males; these gender differences were greater after adjustment for height and regional fat mass.

Purpose

To describe changes and gender differences in the muscle–bone unit at different skeletal sites during pubertal development.

Methods

Four hundred forty-two children aged 5–18 years were studied. Measurements of bone mineral content (BMC), lean mass (LM) and fat mass of the whole body (WB), legs, arms and lumbar spine were obtained from dual-energy X-ray absorptiometry. Peripheral quantitative computed tomography was used to measure BMC of the radius diaphysis and cross-sectional muscle area (CSMA) of the mid-forearm. These measurements were used to describe differences between, and within, genders at each pubertal stage in BMC accrual relative to muscle, both before and after adjustment for height, regional fat and muscle at central and peripheral skeletal sites.

Results

In males, there were significant increases in adjusted WB and leg BMC at the end of pubertal development. Unadjusted and adjusted lumbar spine BMC increased at the onset of, and at the end, of puberty. Radius BMC increased at most pubertal stages. In females, there were increases in unadjusted and adjusted whole body BMC at late puberty, in leg BMC at the onset of puberty and at pubertal stage four. Unadjusted arm BMC increased at most pubertal stages; however, after adjustment, an increase occurred at pubertal stage four. Both adjusted and unadjusted lumbar spine BMC increased at pubertal stage four. Unadjusted radius BMC increased at most pubertal stages. Females had greater BMC at all skeletal sites, compared to males, except at the radius, where adjusted BMC was greater in males at pubertal stage four.

Conclusions

Males and females accrue more BMC in relation to lean mass at multiple skeletal sites as puberty proceeds. Females accrue more BMC in relation to lean mass, in comparison to males, at most skeletal sites.
Fußnoten
1
Regional fat mass refers to fat mass of either the whole body, arms or legs. Therefore, whole-body BMC and lumbar spine BMC were adjusted for whole-body fat mass, arm and radius BMC for arm fat mass and leg BMC for leg fat mass.
 
Literatur
1.
Zurück zum Zitat Parfitt AM (1994) The two faces of growth: benefits and risks to bone integrity. Osteoporos Int 4:382–398CrossRefPubMed Parfitt AM (1994) The two faces of growth: benefits and risks to bone integrity. Osteoporos Int 4:382–398CrossRefPubMed
2.
Zurück zum Zitat Parfitt AM, Travers R, Rauch F, Glorieux FH (2000) Structural and cellular changes during bone growth in healthy children. Bone 27:487–494CrossRefPubMed Parfitt AM, Travers R, Rauch F, Glorieux FH (2000) Structural and cellular changes during bone growth in healthy children. Bone 27:487–494CrossRefPubMed
3.
Zurück zum Zitat 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 104:795–804CrossRefPubMed 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 104:795–804CrossRefPubMed
4.
Zurück zum Zitat Bradney M, Karlsson MK, Duan Y, Stuckey S, Bass S, Seeman E (2000) Heterogeneity in the growth of the axial and appendicular skeleton in boys: Implications for the pathogenesis of bone fragility in men. J Bone Miner Res 15:1871–1878CrossRefPubMed Bradney M, Karlsson MK, Duan Y, Stuckey S, Bass S, Seeman E (2000) Heterogeneity in the growth of the axial and appendicular skeleton in boys: Implications for the pathogenesis of bone fragility in men. J Bone Miner Res 15:1871–1878CrossRefPubMed
5.
Zurück zum Zitat Lian JB, Stein GS, Canalis E, Gehron Robey P, Boskey AL (1999) Bone formation: osteoblast lineage cells, growth factors, matrix proteins and the mineralization process. In: Favus MJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism Lippincott. Williams and Wilkins, Philadelphia, pp 14–29 Lian JB, Stein GS, Canalis E, Gehron Robey P, Boskey AL (1999) Bone formation: osteoblast lineage cells, growth factors, matrix proteins and the mineralization process. In: Favus MJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism Lippincott. Williams and Wilkins, Philadelphia, pp 14–29
6.
Zurück zum Zitat Mundy GR, Chen D, Oyajobi BO (2003) Bone remodeling. In: Favus MJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism Lippincott. Williams and Wilkins, Philadelphia, pp 46–58 Mundy GR, Chen D, Oyajobi BO (2003) Bone remodeling. In: Favus MJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism Lippincott. Williams and Wilkins, Philadelphia, pp 46–58
7.
Zurück zum Zitat Crabtree NJ, Kibirige MS, Fordham JN, Banks LM, Muntoni F, Chinn D, Boivin CM, Shaw NJ (2004) The relationship between lean body mass and bone mineral content in paediatric health and disease. Bone 35:965–972CrossRefPubMed Crabtree NJ, Kibirige MS, Fordham JN, Banks LM, Muntoni F, Chinn D, Boivin CM, Shaw NJ (2004) The relationship between lean body mass and bone mineral content in paediatric health and disease. Bone 35:965–972CrossRefPubMed
8.
Zurück zum Zitat Hogler W, Briody J, Woodhead HJ, Chan A, Cowell CT (2003) Importance of lean mass in the interpretation of total body densitometry in children and adolescents. J Pediatr 143:81–88CrossRefPubMed Hogler W, Briody J, Woodhead HJ, Chan A, Cowell CT (2003) Importance of lean mass in the interpretation of total body densitometry in children and adolescents. J Pediatr 143:81–88CrossRefPubMed
9.
Zurück zum Zitat Rauch F, Bailey DA, Baxter-Jones A, Mirwald R, Faulkner R (2004) The ‘muscle–bone unit’ during the pubertal growth spurt. Bone 34:771–775CrossRefPubMed Rauch F, Bailey DA, Baxter-Jones A, Mirwald R, Faulkner R (2004) The ‘muscle–bone unit’ during the pubertal growth spurt. Bone 34:771–775CrossRefPubMed
10.
Zurück zum Zitat Schoenau E, Neu CM, Beck B, Manz F, Rauch F (2002) Bone mineral content per muscle cross-sectional area as an index of the functional muscle–bone unit. J Bone Miner Res 17:1095–1101CrossRefPubMed Schoenau E, Neu CM, Beck B, Manz F, Rauch F (2002) Bone mineral content per muscle cross-sectional area as an index of the functional muscle–bone unit. J Bone Miner Res 17:1095–1101CrossRefPubMed
11.
Zurück zum Zitat Macdonald HM, Kontulainen SA, MacKelvie-O’Brien KJ, Petit MA, Janssen P, Khan KM, McKay HA (2005) Maturity- and sex-related changes in tibial bone geometry, strength and bone-muscle strength indices during growth: a 20-month pQCT study. Bone 36:1003–1011CrossRefPubMed Macdonald HM, Kontulainen SA, MacKelvie-O’Brien KJ, Petit MA, Janssen P, Khan KM, McKay HA (2005) Maturity- and sex-related changes in tibial bone geometry, strength and bone-muscle strength indices during growth: a 20-month pQCT study. Bone 36:1003–1011CrossRefPubMed
12.
Zurück zum Zitat Pludowski P, Matusik H, Olszaniecka M, Lebiedowski M, Lorenc RS (2005) Reference values for the indicators of skeletal and muscular status of healthy Polish children. J Clin Densitom 8:164–177CrossRefPubMed Pludowski P, Matusik H, Olszaniecka M, Lebiedowski M, Lorenc RS (2005) Reference values for the indicators of skeletal and muscular status of healthy Polish children. J Clin Densitom 8:164–177CrossRefPubMed
13.
14.
Zurück zum Zitat Frost HM (2003) Bone’s mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 275:1081–1101CrossRefPubMed Frost HM (2003) Bone’s mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 275:1081–1101CrossRefPubMed
15.
Zurück zum Zitat Frost HM, Schoenau E (2000) The “muscle–bone unit” in children and adolescents: a 2000 overview. J Pediatr Endocrinol Metab 13:571–590PubMed Frost HM, Schoenau E (2000) The “muscle–bone unit” in children and adolescents: a 2000 overview. J Pediatr Endocrinol Metab 13:571–590PubMed
16.
Zurück zum Zitat Schiessl H, Frost HM, Jee WS (1998) Estrogen and bone–muscle strength and mass relationships. Bone 22:1–6CrossRefPubMed Schiessl H, Frost HM, Jee WS (1998) Estrogen and bone–muscle strength and mass relationships. Bone 22:1–6CrossRefPubMed
17.
Zurück zum Zitat Ferretti JL, Capozza RF, Cointry GR, Garcia SL, Plotkin H, Alvarez Filgueira ML, Zanchetta JR (1998) Gender-related differences in the relationship between densitometric values of whole-body bone mineral content and lean body mass in humans between 2 and 87 years of age. Bone 22:683–690CrossRefPubMed Ferretti JL, Capozza RF, Cointry GR, Garcia SL, Plotkin H, Alvarez Filgueira ML, Zanchetta JR (1998) Gender-related differences in the relationship between densitometric values of whole-body bone mineral content and lean body mass in humans between 2 and 87 years of age. Bone 22:683–690CrossRefPubMed
18.
Zurück zum Zitat 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 85:1095–1098CrossRefPubMed 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 85:1095–1098CrossRefPubMed
19.
Zurück zum Zitat Tothill P, Hannan WJ (2002) Bone mineral and soft tissue measurements by dual-energy X-ray absorptiometry during growth. Bone 31:492–496CrossRefPubMed Tothill P, Hannan WJ (2002) Bone mineral and soft tissue measurements by dual-energy X-ray absorptiometry during growth. Bone 31:492–496CrossRefPubMed
20.
Zurück zum Zitat Clark EM, Ness AR, Tobias JH (2006) Adipose tissue stimulates bone growth in prepubertal children. J Clin Endocrinol Metab 91:2534–2541CrossRefPubMed Clark EM, Ness AR, Tobias JH (2006) Adipose tissue stimulates bone growth in prepubertal children. J Clin Endocrinol Metab 91:2534–2541CrossRefPubMed
21.
Zurück zum Zitat 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 92:143–147CrossRefPubMed 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 92:143–147CrossRefPubMed
22.
Zurück zum Zitat Weiler HA, Janzen L, Green K, Grabowski J, Seshia MM, Yuen KC (2000) Percent body fat and bone mass in healthy Canadian females 10 to 19 years of age. Bone 27:203–207CrossRefPubMed Weiler HA, Janzen L, Green K, Grabowski J, Seshia MM, Yuen KC (2000) Percent body fat and bone mass in healthy Canadian females 10 to 19 years of age. Bone 27:203–207CrossRefPubMed
23.
Zurück zum Zitat 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 (Silver Spring) 14:819–825CrossRef 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 (Silver Spring) 14:819–825CrossRef
24.
Zurück zum Zitat Ashby RL, Ward KA, Roberts SA, Edwards L, Mughal MZ, Adams JE (2009) A reference database for the Stratec XCT-2000 peripheral quantitative computed tomography (pQCT) scanner in healthy children and young adults aged 6–19 years. Osteoporos Int 20:1337–1346CrossRefPubMed Ashby RL, Ward KA, Roberts SA, Edwards L, Mughal MZ, Adams JE (2009) A reference database for the Stratec XCT-2000 peripheral quantitative computed tomography (pQCT) scanner in healthy children and young adults aged 6–19 years. Osteoporos Int 20:1337–1346CrossRefPubMed
25.
Zurück zum Zitat Ward KA, Ashby RL, Roberts SA, Adams JE, Zulf Mughal M (2007) UK reference data for the Hologic QDR Discovery dual-energy x ray absorptiometry scanner in healthy children and young adults aged 6–17 years. Arch Dis Child 92:53–59CrossRefPubMed Ward KA, Ashby RL, Roberts SA, Adams JE, Zulf Mughal M (2007) UK reference data for the Hologic QDR Discovery dual-energy x ray absorptiometry scanner in healthy children and young adults aged 6–17 years. Arch Dis Child 92:53–59CrossRefPubMed
26.
Zurück zum Zitat Duke PM, Litt IF, Gross RT (1980) Adolescents’ self-assessment of sexual maturation. Pediatrics 66:918–920PubMed Duke PM, Litt IF, Gross RT (1980) Adolescents’ self-assessment of sexual maturation. Pediatrics 66:918–920PubMed
27.
Zurück zum Zitat Tanner JM (1969) Growth at adolescence: with a general consideration of the effects of hereditary and environmental factors upon growth and maturation from birth to maturity. Blackwell, Oxford Tanner JM (1969) Growth at adolescence: with a general consideration of the effects of hereditary and environmental factors upon growth and maturation from birth to maturity. Blackwell, Oxford
29.
Zurück zum Zitat National Osteoporosis Society (2004) A practical guide to bone densitometry in children. Camerton, Bath, UK National Osteoporosis Society (2004) A practical guide to bone densitometry in children. Camerton, Bath, UK
30.
Zurück zum Zitat Thomas SR, Kalkwarf HJ, Buckley DD, Heubi JE (2005) Effective dose of dual-energy X-ray absorptiometry scans in children as a function of age. J Clin Densitom 8:415–422CrossRefPubMed Thomas SR, Kalkwarf HJ, Buckley DD, Heubi JE (2005) Effective dose of dual-energy X-ray absorptiometry scans in children as a function of age. J Clin Densitom 8:415–422CrossRefPubMed
31.
Zurück zum Zitat Watson SJ, Jones AL, Oatway WB, Hughes JS (2005) Ionising radiation exposure of the UK population: 2005 review. In. Health Protection Agency Centre for Radiation, Chemical and Environmental Hazards Radiation Protection Division, Chilton, Didcot, Oxfordshire, UK. Watson SJ, Jones AL, Oatway WB, Hughes JS (2005) Ionising radiation exposure of the UK population: 2005 review. In. Health Protection Agency Centre for Radiation, Chemical and Environmental Hazards Radiation Protection Division, Chilton, Didcot, Oxfordshire, UK.
32.
Zurück zum Zitat Landau S, Everitt B (2004) A handbook of statistical analyses using SPSS. Chapman & Hall/CRC, Boca Raton, Florida Landau S, Everitt B (2004) A handbook of statistical analyses using SPSS. Chapman & Hall/CRC, Boca Raton, Florida
33.
Zurück zum Zitat Lunt M, Felsenberg D, Reeve J, Benevolenskaya L, Cannata J, Dequeker J, Dodenhof C, Falch JA, Masaryk P, Pols HA, Poor G, Reid DM, Scheidt-Nave C, Weber K, Varlow J, Kanis JA, O’Neill TW, Silman AJ (1997) Bone density variation and its effects on risk of vertebral deformity in men and women studied in thirteen European centers: the EVOS Study. J Bone Miner Res 12:1883–1894CrossRefPubMed Lunt M, Felsenberg D, Reeve J, Benevolenskaya L, Cannata J, Dequeker J, Dodenhof C, Falch JA, Masaryk P, Pols HA, Poor G, Reid DM, Scheidt-Nave C, Weber K, Varlow J, Kanis JA, O’Neill TW, Silman AJ (1997) Bone density variation and its effects on risk of vertebral deformity in men and women studied in thirteen European centers: the EVOS Study. J Bone Miner Res 12:1883–1894CrossRefPubMed
34.
Zurück zum Zitat Ismail AA, Pye SR, Cockerill WC, Lunt M, Silman AJ, Reeve J, Banzer D, Benevolenskaya LI, Bhalla A, Bruges Armas J, Cannata JB, Cooper C, Delmas PD, Dequeker J, Dilsen G, Falch JA, Felsch B, Felsenberg D, Finn JD, Gennari C, Hoszowski K, Jajic I, Janott J, Johnell O, Kanis JA, Kragl G, Lopez Vaz A, Lorenc R, Lyritis G, Marchand F, Masaryk P, Matthis C, Miazgowski T, Naves-Diaz M, Pols HA, Poor G, Rapado A, Raspe HH, Reid DM, Reisinger W, Scheidt-Nave C, Stepan J, Todd C, Weber K, Woolf AD, O’Neill TW (2002) Incidence of limb fracture across Europe: results from the European Prospective Osteoporosis Study (EPOS). Osteoporos Int 13:565–571CrossRefPubMed Ismail AA, Pye SR, Cockerill WC, Lunt M, Silman AJ, Reeve J, Banzer D, Benevolenskaya LI, Bhalla A, Bruges Armas J, Cannata JB, Cooper C, Delmas PD, Dequeker J, Dilsen G, Falch JA, Felsch B, Felsenberg D, Finn JD, Gennari C, Hoszowski K, Jajic I, Janott J, Johnell O, Kanis JA, Kragl G, Lopez Vaz A, Lorenc R, Lyritis G, Marchand F, Masaryk P, Matthis C, Miazgowski T, Naves-Diaz M, Pols HA, Poor G, Rapado A, Raspe HH, Reid DM, Reisinger W, Scheidt-Nave C, Stepan J, Todd C, Weber K, Woolf AD, O’Neill TW (2002) Incidence of limb fracture across Europe: results from the European Prospective Osteoporosis Study (EPOS). Osteoporos Int 13:565–571CrossRefPubMed
35.
Zurück zum Zitat Forwood MR, Bailey DA, Beck TJ, Mirwald RL, Baxter-Jones AD, Uusi-Rasi K (2004) Sexual dimorphism of the femoral neck during the adolescent growth spurt: a structural analysis. Bone 35:973–981CrossRefPubMed Forwood MR, Bailey DA, Beck TJ, Mirwald RL, Baxter-Jones AD, Uusi-Rasi K (2004) Sexual dimorphism of the femoral neck during the adolescent growth spurt: a structural analysis. Bone 35:973–981CrossRefPubMed
36.
Zurück zum Zitat Iuliano-Burns S, Mirwald RL, Bailey DA (2001) Timing and magnitude of peak height velocity and peak tissue velocities for early, average, and late maturing boys and girls. Am J Hum Biol 13:1–8CrossRefPubMed Iuliano-Burns S, Mirwald RL, Bailey DA (2001) Timing and magnitude of peak height velocity and peak tissue velocities for early, average, and late maturing boys and girls. Am J Hum Biol 13:1–8CrossRefPubMed
37.
Zurück zum Zitat Neu CM, Rauch F, Rittweger J, Manz F, Schoenau E (2002) Influence of puberty on muscle development at the forearm. Am J Physiol Endocrinol Metab 283:E103–107PubMed Neu CM, Rauch F, Rittweger J, Manz F, Schoenau E (2002) Influence of puberty on muscle development at the forearm. Am J Physiol Endocrinol Metab 283:E103–107PubMed
38.
Zurück zum Zitat Rauch F (2005) Bone growth in length and width: the yin and yang of bone stability. J Musculoskelet Neuronal Interact 5:194–201PubMed Rauch F (2005) Bone growth in length and width: the yin and yang of bone stability. J Musculoskelet Neuronal Interact 5:194–201PubMed
39.
Zurück zum Zitat Rauch F, Schoenau E (2001) The developing bone: slave or master of its cells and molecules? Pediatr Res 50:309–314CrossRefPubMed Rauch F, Schoenau E (2001) The developing bone: slave or master of its cells and molecules? Pediatr Res 50:309–314CrossRefPubMed
40.
Zurück zum Zitat Frost HM (1987) The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner 2:73–85PubMed Frost HM (1987) The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner 2:73–85PubMed
41.
Zurück zum Zitat van der Meulen MC, Ashford MW Jr, Kiratli BJ, Bachrach LK, Carter DR (1996) Determinants of femoral geometry and structure during adolescent growth. J Orthop Res 14:22–29CrossRefPubMed van der Meulen MC, Ashford MW Jr, Kiratli BJ, Bachrach LK, Carter DR (1996) Determinants of femoral geometry and structure during adolescent growth. J Orthop Res 14:22–29CrossRefPubMed
42.
Zurück zum Zitat Zanchetta JR, Plotkin H, Alvarez Filgueira ML (1995) Bone mass in children: normative values for the 2–20-year-old population. Bone 16:393S–399SPubMed Zanchetta JR, Plotkin H, Alvarez Filgueira ML (1995) Bone mass in children: normative values for the 2–20-year-old population. Bone 16:393S–399SPubMed
43.
Zurück zum Zitat van der Sluis IM, de Ridder MA, Boot AM, Krenning EP, de Muinck Keizer-Schrama SM (2002) Reference data for bone density and body composition measured with dual energy X-ray absorptiometry in white children and young adults. Arch Dis Child 87:341–347CrossRefPubMed van der Sluis IM, de Ridder MA, Boot AM, Krenning EP, de Muinck Keizer-Schrama SM (2002) Reference data for bone density and body composition measured with dual energy X-ray absorptiometry in white children and young adults. Arch Dis Child 87:341–347CrossRefPubMed
44.
Zurück zum Zitat 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 86:613–618CrossRefPubMed 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 86:613–618CrossRefPubMed
45.
Zurück zum Zitat 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 12:538–547CrossRefPubMed 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 12:538–547CrossRefPubMed
46.
Zurück zum Zitat Molgaard C, Michaelsen KF (1998) Changes in body composition during growth in healthy school-age children. Appl Radiat Isot 49:577–579CrossRefPubMed Molgaard C, Michaelsen KF (1998) Changes in body composition during growth in healthy school-age children. Appl Radiat Isot 49:577–579CrossRefPubMed
47.
Zurück zum Zitat Maynard LM, Guo SS, Chumlea WC, Roche AF, Wisemandle WA, Zeller CM, Towne B, Siervogel RM (1998) Total-body and regional bone mineral content and areal bone mineral density in children aged 8–18 y: the Fels Longitudinal Study. Am J Clin Nutr 68:1111–1117PubMed Maynard LM, Guo SS, Chumlea WC, Roche AF, Wisemandle WA, Zeller CM, Towne B, Siervogel RM (1998) Total-body and regional bone mineral content and areal bone mineral density in children aged 8–18 y: the Fels Longitudinal Study. Am J Clin Nutr 68:1111–1117PubMed
48.
Zurück zum Zitat Magarey AM, Boulton TJ, Chatterton BE, Schultz C, Nordin BE, Cockington RA (1999) Bone growth from 11 to 17 years: relationship to growth, gender and changes with pubertal status including timing of menarche. Acta Paediatr 88:139–146CrossRefPubMed Magarey AM, Boulton TJ, Chatterton BE, Schultz C, Nordin BE, Cockington RA (1999) Bone growth from 11 to 17 years: relationship to growth, gender and changes with pubertal status including timing of menarche. Acta Paediatr 88:139–146CrossRefPubMed
49.
Zurück zum Zitat Landin L, Nilsson BE (1981) Forearm bone mineral content in children. Normative data Acta Paediatr Scand 70:919–923CrossRef Landin L, Nilsson BE (1981) Forearm bone mineral content in children. Normative data Acta Paediatr Scand 70:919–923CrossRef
50.
Zurück zum Zitat Faulkner RA, Bailey DA, Drinkwater DT, McKay HA, Arnold C, Wilkinson AA (1996) Bone densitometry in Canadian children 8–17 years of age. Calcif Tissue Int 59:344–351CrossRef Faulkner RA, Bailey DA, Drinkwater DT, McKay HA, Arnold C, Wilkinson AA (1996) Bone densitometry in Canadian children 8–17 years of age. Calcif Tissue Int 59:344–351CrossRef
51.
Zurück zum Zitat Baxter-Jones AD, Mirwald RL, McKay HA, Bailey DA (2003) A longitudinal analysis of sex differences in bone mineral accrual in healthy 8–19-year-old boys and girls. Ann Hum Biol 30:160–175CrossRefPubMed Baxter-Jones AD, Mirwald RL, McKay HA, Bailey DA (2003) A longitudinal analysis of sex differences in bone mineral accrual in healthy 8–19-year-old boys and girls. Ann Hum Biol 30:160–175CrossRefPubMed
52.
Zurück zum Zitat van Coeverden SC, Netelenbos JC, de Ridder CM, Roos JC, Popp-Snijders C, Delemarre-van de Waal HA (2002) Bone metabolism markers and bone mass in healthy pubertal boys and girls. Clin Endocrinol (Oxf) 57:107–116CrossRef van Coeverden SC, Netelenbos JC, de Ridder CM, Roos JC, Popp-Snijders C, Delemarre-van de Waal HA (2002) Bone metabolism markers and bone mass in healthy pubertal boys and girls. Clin Endocrinol (Oxf) 57:107–116CrossRef
53.
Zurück zum Zitat Wang Q, Alen M, Nicholson PH, Halleen JM, Alatalo SL, Ohlsson C, Suominen H, Cheng S (2006) Differential effects of sex hormones on peri- and endocortical bone surfaces in pubertal girls. J Clin Endocrinol Metab 91:277–282CrossRefPubMed Wang Q, Alen M, Nicholson PH, Halleen JM, Alatalo SL, Ohlsson C, Suominen H, Cheng S (2006) Differential effects of sex hormones on peri- and endocortical bone surfaces in pubertal girls. J Clin Endocrinol Metab 91:277–282CrossRefPubMed
54.
Zurück zum Zitat Frost HM (1999) On the estrogen–bone relationship and postmenopausal bone loss: A new model. J Bone Miner Res 14:1473–1477CrossRefPubMed Frost HM (1999) On the estrogen–bone relationship and postmenopausal bone loss: A new model. J Bone Miner Res 14:1473–1477CrossRefPubMed
55.
Zurück zum Zitat Libanati C, Baylink DJ, Lois-Wenzel E, Srinvasan N, Mohan S (1999) Studies on the potential mediators of skeletal changes occurring during puberty in girls. J Clin Endocrinol Metab 84:2807–2814CrossRefPubMed Libanati C, Baylink DJ, Lois-Wenzel E, Srinvasan N, Mohan S (1999) Studies on the potential mediators of skeletal changes occurring during puberty in girls. J Clin Endocrinol Metab 84:2807–2814CrossRefPubMed
56.
Zurück zum Zitat Wang Q, Alen M, Nicholson P, Lyytikainen A, Suuriniemi M, Helkala E, Suominen H, Cheng S (2005) Growth patterns at distal radius and tibial shaft in pubertal girls: a 2-year longitudinal study. J Bone Miner Res 20:954–961CrossRefPubMed Wang Q, Alen M, Nicholson P, Lyytikainen A, Suuriniemi M, Helkala E, Suominen H, Cheng S (2005) Growth patterns at distal radius and tibial shaft in pubertal girls: a 2-year longitudinal study. J Bone Miner Res 20:954–961CrossRefPubMed
57.
Zurück zum Zitat Hogler W, Blimkie CJ, Cowell CT, Kemp AF, Briody J, Wiebe P, Farpour-Lambert N, Duncan CS, Woodhead HJ (2003) A comparison of bone geometry and cortical density at the mid-femur between prepuberty and young adulthood using magnetic resonance imaging. Bone 33:771–778CrossRefPubMed Hogler W, Blimkie CJ, Cowell CT, Kemp AF, Briody J, Wiebe P, Farpour-Lambert N, Duncan CS, Woodhead HJ (2003) A comparison of bone geometry and cortical density at the mid-femur between prepuberty and young adulthood using magnetic resonance imaging. Bone 33:771–778CrossRefPubMed
58.
Zurück zum Zitat Bechtold S, Rauch F, Noelle V, Donhauser S, Neu CM, Schoenau E, Schwarz HP (2001) Musculoskeletal analyses of the forearm in young women with Turner syndrome: a study using peripheral quantitative computed tomography. J Clin Endocrinol Metab 86:5819–5823CrossRefPubMed Bechtold S, Rauch F, Noelle V, Donhauser S, Neu CM, Schoenau E, Schwarz HP (2001) Musculoskeletal analyses of the forearm in young women with Turner syndrome: a study using peripheral quantitative computed tomography. J Clin Endocrinol Metab 86:5819–5823CrossRefPubMed
59.
Zurück zum Zitat Parfitt AM (2004) The attainment of peak bone mass: what is the relationship between muscle growth and bone growth? Bone 34:767–770CrossRefPubMed Parfitt AM (2004) The attainment of peak bone mass: what is the relationship between muscle growth and bone growth? Bone 34:767–770CrossRefPubMed
60.
Zurück zum Zitat Seeman E, Hopper JL, Young NR, Formica C, Goss P, Tsalamandris C (1996) Do genetic factors explain associations between muscle strength, lean mass, and bone density? A twin study. Am J Physiol 270:E320–327PubMed Seeman E, Hopper JL, Young NR, Formica C, Goss P, Tsalamandris C (1996) Do genetic factors explain associations between muscle strength, lean mass, and bone density? A twin study. Am J Physiol 270:E320–327PubMed
61.
Zurück zum Zitat Ferretti JL, Cointry GR, Capozza RF (2002) Noninvasive analysis of bone mass, structure and strength. In: An YH (ed) Orthopaedic issues in osteoporosis. CRC, Florida, pp 145–167 Ferretti JL, Cointry GR, Capozza RF (2002) Noninvasive analysis of bone mass, structure and strength. In: An YH (ed) Orthopaedic issues in osteoporosis. CRC, Florida, pp 145–167
Metadaten
Titel
The muscle–bone unit of peripheral and central skeletal sites in children and young adults
verfasst von
R. L. Ashby
J. E. Adams
S. A. Roberts
M. Z. Mughal
K. A. Ward
Publikationsdatum
01.01.2011
Verlag
Springer-Verlag
Erschienen in
Osteoporosis International / Ausgabe 1/2011
Print ISSN: 0937-941X
Elektronische ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-010-1216-3

Weitere Artikel der Ausgabe 1/2011

Osteoporosis International 1/2011 Zur Ausgabe

Arthropedia

Grundlagenwissen der Arthroskopie und Gelenkchirurgie. Erweitert durch Fallbeispiele, Videos und Abbildungen. 
» Jetzt entdecken

Update Orthopädie und Unfallchirurgie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.