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Published in: Osteoporosis International 5/2019

01-05-2019 | Original Article

The muscle-bone unit in adolescent swimmers

Authors: A. Gomez-Bruton, A. Gonzalez-Aguero, A. Matute-Llorente, G. Lozano-Berges, A. Gomez-Cabello, L.A. Moreno, J.A. Casajus, G. Vicente-Rodríguez

Published in: Osteoporosis International | Issue 5/2019

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Abstract

Summary

Most researchers adjust bone by lean mass when comparing swimmers with controls. This adjustment is done under the assumption that lean affects bone similarly in both groups. Nonetheless, we found that the muscle-bone association is uncoupled in swimmers, and consequently, researchers should avoid this adjustment when evaluating swimmers’ bone.

Introduction

To examine the functional and structural muscle-bone unit in adolescent swimmers.

Methods

Sixty-five swimmers (34 girls/31 boys) and 119 controls (51 girls/68 boys) participated in the study. Muscle cross-sectional area (MCSA), bone mineral content (BMC), and polar strength-strain index (SSIPOL) were measured in the non-dominant radius by peripheral quantitative computed tomography (pQCT). Subtotal BMC and lean mass were evaluated with dual-energy X-ray absorptiometry (DXA). Handgrip and isometric knee extension (IKE) tests were performed to determine muscle force. The effect of MCSA, lean and force on SSIPOL, and BMC were tested, and the functional and structural muscle-bone ratios of swimmers and controls were compared.

Results

Both muscle size (MCSA and lean) and muscle force (handgrip and IKE) influenced BMC and SSIPOL in swimmers and controls similarly. Swimmers presented normal MCSA and lean values for their height, but when compared with controls, swimmers presented a higher amount of lean and MCSA for the same BMC or SSIPOL (structural muscle-bone unit). For the functional muscle-bone unit, different results were found for the lower and upper limbs, as no differences were found for the upper limbs, while for the lower limbs, swimmers presented higher muscle force for the same amount of BMC.

Conclusions

The contradictory results regarding BMC in swimmers found in previous studies could partly be explained with the findings of the present study that reinforce the idea that swimming is not an effective sport to practice regarding bone mass and that the muscle-bone unit is different in swimmers than in controls.
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Literature
1.
go back to reference Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, O’Karma M, Wallace TC, Zemel BS (2016) The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int 27:1281–1386CrossRefPubMedPubMedCentral Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, O’Karma M, Wallace TC, Zemel BS (2016) The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int 27:1281–1386CrossRefPubMedPubMedCentral
2.
4.
go back to reference Burr DB (1997) Muscle strength, bone mass, and age-related bone loss. J Bone Miner Res 12:1547–1551CrossRefPubMed Burr DB (1997) Muscle strength, bone mass, and age-related bone loss. J Bone Miner Res 12:1547–1551CrossRefPubMed
7.
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
8.
go back to reference Anliker E, Toigo M (2012) Functional assessment of the muscle-bone unit in the lower leg. J Musculoskelet Neuronal Interact 12:46–55PubMed Anliker E, Toigo M (2012) Functional assessment of the muscle-bone unit in the lower leg. J Musculoskelet Neuronal Interact 12:46–55PubMed
9.
go back to reference Ireland A, Maden-Wilkinson T, McPhee J et al (2012) Upper limb muscle-bone asymmetries and bone adaptation in elite youth tennis players. Med Sci Sports Exerc 45:1749–1758CrossRef Ireland A, Maden-Wilkinson T, McPhee J et al (2012) Upper limb muscle-bone asymmetries and bone adaptation in elite youth tennis players. Med Sci Sports Exerc 45:1749–1758CrossRef
10.
go back to reference Calbet JA, Moysi JS, Dorado C, Rodriguez LP (1998) Bone mineral content and density in professional tennis players. Calcif Tissue Int 62:491–496CrossRefPubMed Calbet JA, Moysi JS, Dorado C, Rodriguez LP (1998) Bone mineral content and density in professional tennis players. Calcif Tissue Int 62:491–496CrossRefPubMed
11.
go back to reference Schoenau E (2005) The “functional muscle-bone unit”: a two-step diagnostic algorithm in pediatric bone disease. Pediatr Nephrol 20:356–359CrossRefPubMed Schoenau E (2005) The “functional muscle-bone unit”: a two-step diagnostic algorithm in pediatric bone disease. Pediatr Nephrol 20:356–359CrossRefPubMed
12.
go back to reference Gomez-Bruton A, Gonzalez-Aguero A, Gomez-Cabello A et al (2015) Bone structure of adolescent swimmers; a peripheral quantitative computed tomography (pQCT) study. J Sci Med Sport 19:707–712CrossRefPubMed Gomez-Bruton A, Gonzalez-Aguero A, Gomez-Cabello A et al (2015) Bone structure of adolescent swimmers; a peripheral quantitative computed tomography (pQCT) study. J Sci Med Sport 19:707–712CrossRefPubMed
15.
go back to reference Tanner JM, Whitehouse RH, Takaishi M (1966) Standards from birth to maturity for height, weight, height velocity, and weight velocity: British children, 1965. II. Arch Dis Child 41:613–635CrossRefPubMedPubMedCentral Tanner JM, Whitehouse RH, Takaishi M (1966) Standards from birth to maturity for height, weight, height velocity, and weight velocity: British children, 1965. II. Arch Dis Child 41:613–635CrossRefPubMedPubMedCentral
16.
go back to reference Leone M, Comtois AS (2007) Validity and reliability of self-assessment of sexual maturity in elite adolescent athletes. J Sport Med Phys Fit 47:361–365 Leone M, Comtois AS (2007) Validity and reliability of self-assessment of sexual maturity in elite adolescent athletes. J Sport Med Phys Fit 47:361–365
17.
go back to reference Marfell-Jones M, Olds T, Stewart A, Carter L (2006) International standards for anthropometric assessment. International Society for the Advancement of Kinanthropometry (ISAK), Potchefstroom Marfell-Jones M, Olds T, Stewart A, Carter L (2006) International standards for anthropometric assessment. International Society for the Advancement of Kinanthropometry (ISAK), Potchefstroom
18.
go back to reference Ruiz JR, Espana-Romero V, Ortega FB et al (2006) Hand span influences optimal grip span in male and female teenagers. J Hand Surg Am 31:1367–1372CrossRefPubMed Ruiz JR, Espana-Romero V, Ortega FB et al (2006) Hand span influences optimal grip span in male and female teenagers. J Hand Surg Am 31:1367–1372CrossRefPubMed
19.
go back to reference Gomez-Bruton A, González-Agüero A, Casajus JA, Vicente-Rodríguez G (2014) Swimming training repercussion on metabolic and structural bone development. Benefits of the incorporation of whole body vibration or pilometric training. The RENACIMIENTO project. Nutr Hosp 30:399–409PubMed Gomez-Bruton A, González-Agüero A, Casajus JA, Vicente-Rodríguez G (2014) Swimming training repercussion on metabolic and structural bone development. Benefits of the incorporation of whole body vibration or pilometric training. The RENACIMIENTO project. Nutr Hosp 30:399–409PubMed
20.
go back to reference Schiessl H, Ferretti JL, Tysarczyk-Niemeyer G, Willnecker J (1996) Noninvasive bone strength index as analysed by peripheral quantitative computed tomography (pQCT). In: Schoenau E (ed) Paediatric osteology: new developments in diagnostics and therapy. Elsevier, Amsterdam, The Netherlands, pp 141–146 Schiessl H, Ferretti JL, Tysarczyk-Niemeyer G, Willnecker J (1996) Noninvasive bone strength index as analysed by peripheral quantitative computed tomography (pQCT). In: Schoenau E (ed) Paediatric osteology: new developments in diagnostics and therapy. Elsevier, Amsterdam, The Netherlands, pp 141–146
21.
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
22.
go back to reference Jurimae J, Cicchella A, Tillmann V et al (2009) Effect of pubertal development and physical activity on plasma ghrelin concentration in boys. J Endocrinol Investig 32:18–22CrossRef Jurimae J, Cicchella A, Tillmann V et al (2009) Effect of pubertal development and physical activity on plasma ghrelin concentration in boys. J Endocrinol Investig 32:18–22CrossRef
23.
go back to reference Ferry B, Lespessailles E, Rochcongar P, Duclos M, Courteix D (2013) Bone health during late adolescence: effects of an 8-month training program on bone geometry in female athletes. Jt Bone Spine 80:57–63CrossRef Ferry B, Lespessailles E, Rochcongar P, Duclos M, Courteix D (2013) Bone health during late adolescence: effects of an 8-month training program on bone geometry in female athletes. Jt Bone Spine 80:57–63CrossRef
26.
go back to reference Burt LA, Greene DA, Ducher G, Naughton GA (2013) Skeletal adaptations associated with pre-pubertal gymnastics participation as determined by DXA and pQCT: a systematic review and meta-analysis. J Sci Med Sport 16:231–239CrossRefPubMed Burt LA, Greene DA, Ducher G, Naughton GA (2013) Skeletal adaptations associated with pre-pubertal gymnastics participation as determined by DXA and pQCT: a systematic review and meta-analysis. J Sci Med Sport 16:231–239CrossRefPubMed
27.
go back to reference Tenforde AS, Fredericson M (2011) Influence of sports participation on bone health in the young athlete: a review of the literature. PM&R 3:861–867CrossRef Tenforde AS, Fredericson M (2011) Influence of sports participation on bone health in the young athlete: a review of the literature. PM&R 3:861–867CrossRef
28.
go back to reference Guadalupe-Grau A, Fuentes T, Guerra B, Calbet JA (2009) Exercise and bone mass in adults. Sports Med 39:439–468CrossRefPubMed Guadalupe-Grau A, Fuentes T, Guerra B, Calbet JA (2009) Exercise and bone mass in adults. Sports Med 39:439–468CrossRefPubMed
29.
go back to reference Meakin LB, Price JS, Lanyon LE (2014) The contribution of experimental in vivo models to understanding the mechanisms of adaptation to mechanical loading in bone. Front Endocrinol 5:154CrossRef Meakin LB, Price JS, Lanyon LE (2014) The contribution of experimental in vivo models to understanding the mechanisms of adaptation to mechanical loading in bone. Front Endocrinol 5:154CrossRef
30.
go back to reference Robling AG, Burr DB, Turner CH (2000) Partitioning a daily mechanical stimulus into discrete loading bouts improves the osteogenic response to loading. J Bone Miner Res 15:1596–1602CrossRefPubMed Robling AG, Burr DB, Turner CH (2000) Partitioning a daily mechanical stimulus into discrete loading bouts improves the osteogenic response to loading. J Bone Miner Res 15:1596–1602CrossRefPubMed
31.
go back to reference Hawkins SA, Schroeder ET, Wiswell RA et al (1999) Eccentric muscle action increases site-specific osteogenic response. Med Sci Sports Exerc 31:1287–1292CrossRefPubMed Hawkins SA, Schroeder ET, Wiswell RA et al (1999) Eccentric muscle action increases site-specific osteogenic response. Med Sci Sports Exerc 31:1287–1292CrossRefPubMed
Metadata
Title
The muscle-bone unit in adolescent swimmers
Authors
A. Gomez-Bruton
A. Gonzalez-Aguero
A. Matute-Llorente
G. Lozano-Berges
A. Gomez-Cabello
L.A. Moreno
J.A. Casajus
G. Vicente-Rodríguez
Publication date
01-05-2019
Publisher
Springer London
Published in
Osteoporosis International / Issue 5/2019
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-019-04857-3

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