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Published in: Osteoporosis International 2/2019

01-02-2019 | Original Article

A longitudinal comparison of appendicular bone growth and markers of strength through adolescence in a South African cohort using radiogrammetry and pQCT

Authors: A. Magan, L. K. Micklesfield, L. H. Nyati, S. A. Norris, J. M. Pettifor

Published in: Osteoporosis International | Issue 2/2019

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Abstract

Summary

To compare growth patterns and strength of weight- and non-weight-bearing bones longitudinally. Irrespective of sex and ethnicity, metacarpal growth was similar to that of the non-weight-bearing radius but differed from that of the weight-bearing tibia. Weight- and non-weight-bearing bones have different growth and strength patterns.

Introduction

Functional loading modulates bone size and strength.

Methods

To compare growth patterns and strength of weight- and non-weight-bearing bones longitudinally, we performed manual radiogrammetry of the second metacarpal on hand-wrist radiographs and measured peripheral quantitative computed tomography images of the radius (65%) and tibia (38% and 65%), annually on 372 black and 152 white South African participants (ages 12–20 years). We aligned participants by age from peak metacarpal length velocity. We assessed bone width (BW, mm); cortical thickness (CT, mm); medullary width (MW, mm); stress-strain index (SSI, mm3); and muscle cross-sectional area (MCSA, mm2).

Results

From 12 to 20 years, the associations between metacarpal measures (BW, CT and SSI) and MCSA at the radius (males R2 = 0.33–0.45; females R2 = 0.12–0.20) were stronger than the tibia (males R2 = 0.01–0.11; females R2 = 0.007–0.04). In all groups, radial BW, CT and MW accrual rates were similar to those of the metacarpal, except in white females who had lower radial CT (0.04 mm/year) and greater radial MW (0.06 mm/year) accrual. In all groups, except for CT in white males, tibial BW and CT accrual rates were greater than at the metacarpal. Tibial MW (0.29–0.35 mm/year) increased significantly relative to metacarpal MW (− 0.07 to 0.06 mm/year) in males only. In all groups, except white females, SSI increased in each bone.

Conclusion

Irrespective of sex and ethnicity, metacarpal growth was similar to that of the non-weight-bearing radius but differed from that of the weight-bearing tibia. The local and systemic factors influencing site-specific differences require further investigation.
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Literature
1.
go back to reference Jarvinen TL, Sievanen H, Jokihaara J, Einhorn TA (2005) Revival of bone strength: the bottom line. J Bone Miner Res 20:717–720CrossRefPubMed Jarvinen TL, Sievanen H, Jokihaara J, Einhorn TA (2005) Revival of bone strength: the bottom line. J Bone Miner Res 20:717–720CrossRefPubMed
2.
3.
go back to reference Garn S (1970) The earlier gain and later loss of cortical bone. In: Thomas CC (ed) Nutritional Perspectives. Springfield, IL p 3–120 Garn S (1970) The earlier gain and later loss of cortical bone. In: Thomas CC (ed) Nutritional Perspectives. Springfield, IL p 3–120
4.
go back to reference Kirmani S, Christen D, van Lenthe GH, Fischer PR, Bouxsein ML, McCready LK, Melton LJ III, Riggs BL, Amin S, Müller R, Khosla S (2009) Bone structure at the distal radius during adolescent growth. J Bone Miner Res 24:1033–1042CrossRefPubMed Kirmani S, Christen D, van Lenthe GH, Fischer PR, Bouxsein ML, McCready LK, Melton LJ III, Riggs BL, Amin S, Müller R, Khosla S (2009) Bone structure at the distal radius during adolescent growth. J Bone Miner Res 24:1033–1042CrossRefPubMed
5.
go back to reference Gabel L, Nettlefold L, Brasher PM, Moore SA, Ahamed Y, Macdonald HM, McKay HA (2015) Reexamining the surfaces of bone in boys and girls during adolescent growth: a 12-year mixed longitudinal pQCT study. J Bone Miner Res 30:2158–2167CrossRefPubMedPubMedCentral Gabel L, Nettlefold L, Brasher PM, Moore SA, Ahamed Y, Macdonald HM, McKay HA (2015) Reexamining the surfaces of bone in boys and girls during adolescent growth: a 12-year mixed longitudinal pQCT study. J Bone Miner Res 30:2158–2167CrossRefPubMedPubMedCentral
6.
go back to reference Micklesfield LK, Norris SA, Pettifor JM (2011) Determinants of bone size and strength in 13-year-old south African children: the influence of ethnicity, sex and pubertal maturation. Bone 48:777–785CrossRefPubMed Micklesfield LK, Norris SA, Pettifor JM (2011) Determinants of bone size and strength in 13-year-old south African children: the influence of ethnicity, sex and pubertal maturation. Bone 48:777–785CrossRefPubMed
7.
go back to reference Magan A, Nyati LH, Micklesfield LK, Norris SA, Pettifor JM (2017) Metacarpal growth during adolescence in a longitudinal South African cohort. J Bone Miner Res 32:1926–1934CrossRefPubMed Magan A, Nyati LH, Micklesfield LK, Norris SA, Pettifor JM (2017) Metacarpal growth during adolescence in a longitudinal South African cohort. J Bone Miner Res 32:1926–1934CrossRefPubMed
8.
go back to reference Schoenbuchner SM, Pettifor JM, Norris SA, Micklesfield LK, Prentice A, Ward KA (2017) Ethnic differences in peripheral skeletal development among urban South African adolescents: a ten-year longitudinal pQCT study. J Bone Miner Res 32:2355–2366CrossRefPubMedPubMedCentral Schoenbuchner SM, Pettifor JM, Norris SA, Micklesfield LK, Prentice A, Ward KA (2017) Ethnic differences in peripheral skeletal development among urban South African adolescents: a ten-year longitudinal pQCT study. J Bone Miner Res 32:2355–2366CrossRefPubMedPubMedCentral
9.
go back to reference Meiring RM, Micklesfield LK, McVeigh JA (2016) The effect of loading and ethnicity on annual changes in cortical bone of the radius and tibia in pre-pubertal children. Ann Hum Biol 43:520–526CrossRefPubMed Meiring RM, Micklesfield LK, McVeigh JA (2016) The effect of loading and ethnicity on annual changes in cortical bone of the radius and tibia in pre-pubertal children. Ann Hum Biol 43:520–526CrossRefPubMed
10.
go back to reference Schoenau E, Frost HM (2002) The “muscle-bone unit” in children and adolescents. Calcif Tissue Int 70:405–407CrossRefPubMed Schoenau E, Frost HM (2002) The “muscle-bone unit” in children and adolescents. Calcif Tissue Int 70:405–407CrossRefPubMed
11.
go back to reference Ruff C (2003) Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. Bone 33:317–329CrossRefPubMed Ruff C (2003) Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. Bone 33:317–329CrossRefPubMed
12.
go back to reference Schoenau E (2004) The peak bone mass concept: is it still relevant? Pediatr Nephrol 19:825–831 Schoenau E (2004) The peak bone mass concept: is it still relevant? Pediatr Nephrol 19:825–831
13.
go back to reference 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
14.
go back to reference Pang MY, Ashe MC, Eng JJ (2007) Muscle weakness, spasticity and disuse contribute to demineralization and geometric changes in the radius following chronic stroke. Osteoporos Int 18:1243–1252CrossRefPubMedPubMedCentral Pang MY, Ashe MC, Eng JJ (2007) Muscle weakness, spasticity and disuse contribute to demineralization and geometric changes in the radius following chronic stroke. Osteoporos Int 18:1243–1252CrossRefPubMedPubMedCentral
15.
go back to reference Pang MY, Ashe MC, Eng JJ (2008) Tibial bone geometry in chronic stroke patients: influence of sex, cardiovascular health, and muscle mass. J Bone Miner Res 23:1023–1030CrossRefPubMedPubMedCentral Pang MY, Ashe MC, Eng JJ (2008) Tibial bone geometry in chronic stroke patients: influence of sex, cardiovascular health, and muscle mass. J Bone Miner Res 23:1023–1030CrossRefPubMedPubMedCentral
16.
go back to reference Fox KM, Kimura S, Powell-Threets K, Plato CC (1995) Radial and ulnar cortical thickness of the second metacarpal. J Bone Miner Res 10:1930–1934CrossRefPubMed Fox KM, Kimura S, Powell-Threets K, Plato CC (1995) Radial and ulnar cortical thickness of the second metacarpal. J Bone Miner Res 10:1930–1934CrossRefPubMed
18.
go back to reference Barnett E, Nordin BE (1960) The radiological diagnosis of osteoporosis: a new approach. Clin Radiol 11:166–174CrossRefPubMed Barnett E, Nordin BE (1960) The radiological diagnosis of osteoporosis: a new approach. Clin Radiol 11:166–174CrossRefPubMed
19.
go back to reference Binkley TL, Berry R, Specker BL (2008) Methods for measurement of pediatric bone. Rev Endocr Metab Disord 9:95–106CrossRefPubMed Binkley TL, Berry R, Specker BL (2008) Methods for measurement of pediatric bone. Rev Endocr Metab Disord 9:95–106CrossRefPubMed
20.
go back to reference Kontulainen SA, Johnston JD, Liu D, Leung C, Oxland TR, McKay HA (2008) Strength indices from pQCT imaging predict up to 85% of variance in bone failure properties at tibial epiphysis and diaphysis. J Musculoskelet Neuronal Interact 8:401–409PubMed Kontulainen SA, Johnston JD, Liu D, Leung C, Oxland TR, McKay HA (2008) Strength indices from pQCT imaging predict up to 85% of variance in bone failure properties at tibial epiphysis and diaphysis. J Musculoskelet Neuronal Interact 8:401–409PubMed
21.
go back to reference Richter L, Norris S, Pettifor J, Yach D, Cameron N (2007) Cohort profile: Mandela’s children: the 1990 birth to twenty study in South Africa. Int J Epidemiol 36:504–511CrossRefPubMedPubMedCentral Richter L, Norris S, Pettifor J, Yach D, Cameron N (2007) Cohort profile: Mandela’s children: the 1990 birth to twenty study in South Africa. Int J Epidemiol 36:504–511CrossRefPubMedPubMedCentral
22.
go back to reference May A, Pettifor JM, Norris SA, Ramsay M, Lombard Z (2013) Genetic factors influencing bone mineral content in a black south African population. J Bone Miner Metab 31:708–716CrossRefPubMedPubMedCentral May A, Pettifor JM, Norris SA, Ramsay M, Lombard Z (2013) Genetic factors influencing bone mineral content in a black south African population. J Bone Miner Metab 31:708–716CrossRefPubMedPubMedCentral
24.
go back to reference Tanner JM (2001) Assessment of skeletal maturity and prediction of adult height (TW3 method). W.B. Saunders, London Tanner JM (2001) Assessment of skeletal maturity and prediction of adult height (TW3 method). W.B. Saunders, London
25.
go back to reference Cointry GR, Ferretti JL, Reina PS, Nocciolino LM, Rittweger J, Capozza RF (2014) The pQCT ‘Bone Strength Indices’ (BSIs, SSI). Relative mechanical impact and diagnostic value of the indicators of bone tissue and design quality employed in their calculation in healthy men and pre- and post-menopausal women. J Musculoskelet Neuronal Interact 14:29–40PubMed Cointry GR, Ferretti JL, Reina PS, Nocciolino LM, Rittweger J, Capozza RF (2014) The pQCT ‘Bone Strength Indices’ (BSIs, SSI). Relative mechanical impact and diagnostic value of the indicators of bone tissue and design quality employed in their calculation in healthy men and pre- and post-menopausal women. J Musculoskelet Neuronal Interact 14:29–40PubMed
26.
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 86:613–618CrossRefPubMed 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
27.
go back to reference Eser P, Aeberli D, Widmer J, Moller B, Villiger PM (2011) Abnormal bone geometry at the metacarpal bone shaft of rheumatoid arthritis patients with maintained muscle-bone relationship. Arthritis Care Res 63:383–389CrossRef Eser P, Aeberli D, Widmer J, Moller B, Villiger PM (2011) Abnormal bone geometry at the metacarpal bone shaft of rheumatoid arthritis patients with maintained muscle-bone relationship. Arthritis Care Res 63:383–389CrossRef
28.
go back to reference Zhu K, Briffa K, Smith A, Mountain J, Briggs AM, Lye S, Pennell C, Straker L, Walsh JP (2014) Gender differences in the relationships between lean body mass, fat mass and peak bone mass in young adults. Osteoporos Int 25:1563–1570CrossRefPubMed Zhu K, Briffa K, Smith A, Mountain J, Briggs AM, Lye S, Pennell C, Straker L, Walsh JP (2014) Gender differences in the relationships between lean body mass, fat mass and peak bone mass in young adults. Osteoporos Int 25:1563–1570CrossRefPubMed
29.
go back to reference Nieves JW, Formica C, Ruffing J, Zion M, Garrett P, Lindsay R, Cosman F (2005) Males have larger skeletal size and bone mass than females, despite comparable body size. J Bone Miner Res 20:529–535CrossRefPubMed Nieves JW, Formica C, Ruffing J, Zion M, Garrett P, Lindsay R, Cosman F (2005) Males have larger skeletal size and bone mass than females, despite comparable body size. J Bone Miner Res 20:529–535CrossRefPubMed
30.
go back to reference 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
31.
go back to reference Sumner DR, Andriacchi TP (1996) Adaptation to differential loading: comparison of growth-related changes in cross-sectional properties of the human femur and humerus. Bone 19:121–126CrossRefPubMed Sumner DR, Andriacchi TP (1996) Adaptation to differential loading: comparison of growth-related changes in cross-sectional properties of the human femur and humerus. Bone 19:121–126CrossRefPubMed
32.
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 85:1095–1098CrossRefPubMed 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
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 12:538–547CrossRefPubMed 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
34.
go back to reference 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
35.
go back to reference Bailey DA, Wedge JH, McCulloch RG, Martin AD, Bernhardson SC (1989) Epidemiology of fractures of the distal end of the radius in children as associated with growth. J Bone Joint Surg Am 71:1225–1231CrossRefPubMed Bailey DA, Wedge JH, McCulloch RG, Martin AD, Bernhardson SC (1989) Epidemiology of fractures of the distal end of the radius in children as associated with growth. J Bone Joint Surg Am 71:1225–1231CrossRefPubMed
36.
go back to reference 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 27:273–282CrossRefPubMed 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 27:273–282CrossRefPubMed
37.
go back to reference Turner CH (2002) Biomechanics of bone: determinants of skeletal fragility and bone quality. Osteoporos Int 13:97–104CrossRefPubMed Turner CH (2002) Biomechanics of bone: determinants of skeletal fragility and bone quality. Osteoporos Int 13:97–104CrossRefPubMed
38.
go back to reference Thandrayen K, Norris SA, Pettifor JM (2009) Fracture rates in urban South African children of different ethnic origins: the birth to twenty cohort. Osteoporos Int 20:47–52CrossRefPubMed Thandrayen K, Norris SA, Pettifor JM (2009) Fracture rates in urban South African children of different ethnic origins: the birth to twenty cohort. Osteoporos Int 20:47–52CrossRefPubMed
39.
go back to reference Frisancho AR, Garn SM, Ascoli W (1970) Subperiosteal and endosteal bone apposition during adolescence. Hum Biol 42:639–664PubMed Frisancho AR, Garn SM, Ascoli W (1970) Subperiosteal and endosteal bone apposition during adolescence. Hum Biol 42:639–664PubMed
40.
go back to reference Martin DD, Heckmann C, Jenni OG, Ranke MB, Binder G, Thodberg HH (2011) Metacarpal thickness, width, length and medullary diameter in children—reference curves from the first Zurich longitudinal study. Osteoporos Int 22:1525–1536CrossRefPubMed Martin DD, Heckmann C, Jenni OG, Ranke MB, Binder G, Thodberg HH (2011) Metacarpal thickness, width, length and medullary diameter in children—reference curves from the first Zurich longitudinal study. Osteoporos Int 22:1525–1536CrossRefPubMed
41.
go back to reference Gabel L, Macdonald HM, McKay HA (2017) Sex differences and growth-related adaptations in bone microarchitecture, geometry, density, and strength from childhood to early adulthood: a mixed longitudinal HR-pQCT study. J Bone Miner Res 32:250–263CrossRefPubMed Gabel L, Macdonald HM, McKay HA (2017) Sex differences and growth-related adaptations in bone microarchitecture, geometry, density, and strength from childhood to early adulthood: a mixed longitudinal HR-pQCT study. J Bone Miner Res 32:250–263CrossRefPubMed
42.
go back to reference 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 19:1976–1981CrossRefPubMed 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 19:1976–1981CrossRefPubMed
43.
go back to reference Beck TJ, Ruff CB, Shaffer RA, Betsinger K, Trone DW, Brodine SK (2000) Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors. Bone 27:437–444CrossRefPubMed Beck TJ, Ruff CB, Shaffer RA, Betsinger K, Trone DW, Brodine SK (2000) Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors. Bone 27:437–444CrossRefPubMed
44.
go back to reference Gabel L, Macdonald HM, McKay HA (2016) Reply to: challenges in the acquisition and analysis of bone microstructure during growth. J Bone Miner Res 31:2242–2243CrossRefPubMed Gabel L, Macdonald HM, McKay HA (2016) Reply to: challenges in the acquisition and analysis of bone microstructure during growth. J Bone Miner Res 31:2242–2243CrossRefPubMed
45.
go back to reference Tan VP, Macdonald HM, Kim S, Nettlefold L, Gabel L, Ashe MC, McKay HA (2014) Influence of physical activity on bone strength in children and adolescents: a systematic review and narrative synthesis. J Bone Miner Res 29:2161–2181CrossRefPubMed Tan VP, Macdonald HM, Kim S, Nettlefold L, Gabel L, Ashe MC, McKay HA (2014) Influence of physical activity on bone strength in children and adolescents: a systematic review and narrative synthesis. J Bone Miner Res 29:2161–2181CrossRefPubMed
Metadata
Title
A longitudinal comparison of appendicular bone growth and markers of strength through adolescence in a South African cohort using radiogrammetry and pQCT
Authors
A. Magan
L. K. Micklesfield
L. H. Nyati
S. A. Norris
J. M. Pettifor
Publication date
01-02-2019
Publisher
Springer London
Published in
Osteoporosis International / Issue 2/2019
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-018-4761-9

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