In peripubertal girls, artistic gymnastics improves areal bone mineral density and femoral bone geometry without affecting serum OPG/RANKL levels

Osteoporosis International

Volumn 22, Issue 12, 2011, Pages 3055-3066

  Maimoun L ^a   Coste, O ^a,b   Mariano Goulart, D ^a   Galtier, F ^c,d   Mura, T ^c,d   Philibert, P ^a   Briot, K ^e   Paris, F ^a,f   Sultan, C ^a,f  

^a LAPEYRONIE HOSPITAL   (France)

^b Des Sports et Cohésion Sociale ^*  (France)

^c MONTPELLIER UNIVERSITY HOSPITAL   (France)

^d INSERM   (France)

^e INSERM ^*  (France)

^f HÔPITAL ARNAUD DE VILLENEUVE   (France)

Author keywords

Areal bone mineral density; Bone geometry; Bone mass acquisition; Bone strength; Intensive training; Markers of bone turnover; OPG RANKL system; Peripuberty

Indexed keywords

OSTEOCLAST DIFFERENTIATION FACTOR;

ADIPOSE TISSUE; ADOLESCENT; ARTICLE; ATHLETE; BODY HEIGHT; BODY WEIGHT; BONE DENSITY; BONE REMODELING; BONE TURNOVER; CHILD; CONTROLLED STUDY; DUAL ENERGY X RAY ABSORPTIOMETRY; FEMALE; FEMUR; FEMUR SHAFT; HUMAN; LEISURE; LUMBAR SPINE; MENARCHE; PHYSICAL ACTIVITY; PHYSICAL EDUCATION; PREPUBERTY; PRIORITY JOURNAL; SCHOOL CHILD; SKULL;

ABSORPTIOMETRY, PHOTON; ADOLESCENT; BONE DENSITY; BONE REMODELING; CHILD; CROSS-SECTIONAL STUDIES; FEMALE; FEMUR; GYMNASTICS; HUMANS; LUMBAR VERTEBRAE; OSTEOPROTEGERIN; RADIUS; RANK LIGAND;

EID: 84155165143     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-011-1541-1     Document Type: Article

References (50)

1. OM Rutherford 1999 Is there a role for exercise in the prevention of osteoporotic fractures? Br J Sports Med 33 378 386 10597845 10.1136/bjsm.33.6. 378 1:STN:280:DC%2BD3c%2FmsVOitw%3D%3D
2. KA Witzke CM Snow 2000 Effects of plyometric jump training on bone mass in adolescent girls Med Sci Sports Exerc 32 1051 1057 10862529 10.1097/00005768-200006000-00003 1:STN:280:DC%2BD3M%2FhtFeitQ%3D%3D (Pubitemid 30390266)
3. K Hind M Burrows 2007 Weight-bearing exercise and bone mineral accrual in children and adolescents: a review of controlled trials Bone 40 14 27 16956802 10.1016/j.bone.2006.07.006 1:STN:280:DC%2BD28jhvV2mtw%3D%3D (Pubitemid 44848417)
4. DR Taaffe TL Robinson CM Snow R Marcus 1997 High-impact exercise promotes bone gain in well-trained female athletes J Bone Miner Res 12 255 260 9041058 10.1359/jbmr.1997.12.2.255 1:STN:280:DyaK2s7ptlCltQ%3D%3D (Pubitemid 27086307)
5. D Courteix E Lespessailles SL Peres P Obert P Germain CL Benhamou 1998 Effect of physical training on bone mineral density in prepubertal girls: a comparative study between impact-loading and non-impact-loading sports Osteoporos Int 8 152 158 9666939 10.1007/BF02672512 1:STN:280: DyaK1czjtFGltg%3D%3D (Pubitemid 28230438)
6. S Tournis E Michopoulou IG Fatouros I Paspati M Michalopoulou P Raptou D Leontsini A Avloniti M Krekoukia V Zouvelou A Galanos N Aggelousis A Kambas I Douroudos GP Lyritis K Taxildaris N Pappaioannou 2010 Effect of rhythmic gymnastics on volumetric bone mineral density and bone geometry in premenarcheal female athletes and controls J Clin Endocrinol Metab 95 2755 2762 20375211 10.1210/jc.2009-2382 1:CAS:528:DC%2BC3cXnvVaksLo%3D
7. TJ Beck CB Ruff KE Warden WW Scott Jr GU Rao 1990 Predicting femoral neck strength from bone mineral data. A structural approach Invest Radiol 25 6 18 2298552 10.1097/00004424-199001000-00004 1:STN:280:DyaK3c7ivFKktA%3D%3D (Pubitemid 20040519)
8. R Nikander H Sievanen A Heinonen P Kannus 2005 Femoral neck structure in adult female athletes subjected to different loading modalities J Bone Miner Res 20 520 528 15746998 10.1359/JBMR.041119 (Pubitemid 40293501)
9. RA Faulkner MR Forwood TJ Beck JC Mafukidze K Russell W Wallace 2003 Strength indices of the proximal femur and shaft in prepubertal female gymnasts Med Sci Sports Exerc 35 513 518 12618584 10.1249/01.MSS.0000053724.33480.8B (Pubitemid 36278779)
10. L Maimoun O Coste F Galtier T Mura D Mariano-Goulart F Paris C Sultan 2010 Bone mineral density acquisition in peripubertal female rhythmic gymnasts is directly associated with plasma IGF1/IGF-binding protein 3 ratio Eur J Endocrinol 163 157 164 20423985 10.1530/EJE-10-0315 1:CAS:528: DC%2BC3cXpsFeisrY%3D
11. L Maimoun O Coste A Jaussent D Mariano-Goulart C Sultan F Paris 2010 Bone mass acquisition in female rhythmic gymnasts during puberty: no direct role for leptin Clin Endocrinol (Oxf) 72 604 611 10.1111/j.1365-2265.2009.03718.x 1:CAS:528:DC%2BC3cXlvVKht7o%3D
12. M Herrmann W Herrmann 2004 The assessment of bone metabolism in female elite endurance athletes by biochemical bone markers Clin Chem Lab Med 42 1384 1389 15576300 10.1515/CCLM.2004.258 1:CAS:528:DC%2BD2cXhtFGmtLzJ (Pubitemid 40057826)
13. S Ziegler A Niessner B Richter S Wirth E Billensteiner W Woloszczuk J Slany G Geyer 2005 Endurance running acutely raises plasma osteoprotegerin and lowers plasma receptor activator of nuclear factor kappa B ligand Metabolism 54 935 938 15988704 10.1016/j.metabol.2005.02.009 1:CAS:528:DC%2BD2MXlt1KntLc%3D (Pubitemid 40827211)
14. K Kerschan-Schindl M Thalmann GH Sodeck K Skenderi AL Matalas S Grampp C Ebner P Pietschmann 2009 A 246-km continuous running race causes significant changes in bone metabolism Bone 45 1079 1083 19665602 10.1016/j.bone.2009.07.088 1:CAS:528:DC%2BD1MXhtlGit7fM
15. J Rubin T Murphy MS Nanes X Fan 2000 Mechanical strain inhibits expression of osteoclast differentiation factor by murine stromal cells Am J Physiol Cell Physiol 278 C1126 C1132 10837340 1:CAS:528:DC%2BD3cXks1KnsLk%3D (Pubitemid 30432396)
16. Y Kobayashi F Hashimoto H Miyamoto K Kanaoka Y Miyazaki-Kawashita T Nakashima M Shibata K Kobayashi Y Kato H Sakai 2000 Force-induced osteoclast apoptosis in vivo is accompanied by elevation in transforming growth factor beta and osteoprotegerin expression J Bone Miner Res 15 1924 1934 11028444 10.1359/jbmr.2000.15.10.1924 1:CAS:528:DC%2BD3cXnsVCltbc%3D
17. DL Lacey E Timms HL Tan MJ Kelley CR Dunstan T Burgess R Elliott A Colombero G Elliott S Scully H Hsu J Sullivan N Hawkins E Davy C Capparelli A Eli YX Qian S Kaufman I Sarosi V Shalhoub G Senaldi J Guo J Delaney WJ Boyle 1998 Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation Cell 93 165 176 9568710 10.1016/S0092-8674(00) 81569-X 1:CAS:528:DyaK1cXivVyhtrg%3D (Pubitemid 28180851)
18. LC Hofbauer S Khosla CR Dunstan DL Lacey WJ Boyle BL Riggs 2000 The roles of osteoprotegerin and osteoprotegerin ligand in the paracrine regulation of bone resorption J Bone Miner Res 15 2 12 10646108 10.1359/jbmr.2000.15.1.2 1:CAS:528:DC%2BD3cXmsVygsQ%3D%3D (Pubitemid 30026926)
19. Tanner J (1962) Growth at adolescence. Blackwell, Oxford
20. Greulich WW, Pyle SI (1959) Radiographic Atlas of skeletal development of hand and wrist, 2nd edn. Stanford University Press, Stanford
21. BC Khoo TJ Beck QH Qiao P Parakh L Semanick RL Prince KP Singer RI Price 2005 In vivo short-term precision of hip structure analysis variables in comparison with bone mineral density using paired dual-energy X-ray absorptiometry scans from multi-center clinical trials Bone 37 112 121 15869917 10.1016/j.bone.2005.03.007 (Pubitemid 40848424)
22. HM Frost 1992 The role of changes in mechanical usage set points in the pathogenesis of osteoporosis J Bone Miner Res 7 253 261 1585826 10.1002/jbmr.5650070303 1:STN:280:DyaK383msVWqsA%3D%3D
23. TL Robinson C Snow-Harter DR Taaffe D Gillis J Shaw R Marcus 1995 Gymnasts exhibit higher bone mass than runners despite similar prevalence of amenorrhea and oligomenorrhea J Bone Miner Res 10 26 35 7747628 10.1002/jbmr.5650100107 1:STN:280:DyaK2M3ms1Cksg%3D%3D
24. KL Proctor WC Adams JD Shaffrath MD Van Loan 2002 Upper-limb bone mineral density of female collegiate gymnasts versus controls Med Sci Sports Exerc 34 1830 1835 12439090 10.1097/00005768-200211000-00021 (Pubitemid 35283502)
25. EW Helge IL Kanstrup 2002 Bone density in female elite gymnasts: impact of muscle strength and sex hormones Med Sci Sports Exerc 34 174 180 11782664 10.1097/00005768-200201000-00026 (Pubitemid 34052391)
26. JN Dowthwaite JG DiStefano RJ Ploutz-Snyder JA Kanaley TA Scerpella 2006 Maturity and activity-related differences in bone mineral density: Tanner I vs. II and gymnasts vs. non-gymnasts Bone 39 895 900 16757218 10.1016/j.bone.2006. 04.007 (Pubitemid 44311720)
27. MC Erlandson SA Kontulainen AD Baxter-Jones 2010 Precompetitive and recreational gymnasts have greater bone density, mass, and estimated strength at the distal radius in young childhood Osteoporos Int 22 1 75 84 20458575 10.1007/s00198-010-1263-9
28. EM Laing JA Massoni SM Nickols-Richardson CM Modlesky PJ O'Connor RD Lewis 2002 A prospective study of bone mass and body composition in female adolescent gymnasts J Pediatr 141 211 216 12183716 10.1067/mpd.2002.126599
29. MA Petit HA McKay KJ MacKelvie A Heinonen KM Khan TJ Beck 2002 A randomized school-based jumping intervention confers site and maturity-specific benefits on bone structural properties in girls: a hip structural analysis study J Bone Miner Res 17 363 372 11874228 10.1359/jbmr.2002.17.3.363 1:STN:280:DC%2BD387ksVartw%3D%3D (Pubitemid 34171750)
30. P Szulc F Duboeuf AM Schott P Dargent-Molina PJ Meunier PD Delmas 2006 Structural determinants of hip fracture in elderly women: re-analysis of the data from the EPIDOS study Osteoporos Int 17 231 236 15983728 10.1007/s00198-005-1980-7 1:STN:280:DC%2BD287islWrug%3D%3D (Pubitemid 43053586)
31. KF Janz JM Gilmore SM Levy EM Letuchy TL Burns TJ Beck 2007 Physical activity and femoral neck bone strength during childhood: the Iowa Bone Development Study Bone 41 216 222 17560839 10.1016/j.bone.2007.05.001 (Pubitemid 47001827)
32. G Alwis C Linden S Stenevi-Lundgren HG Ahlborg J Besjakov P Gardsell MK Karlsson 2008 A one-year exercise intervention program in pre-pubertal girls does not influence hip structure BMC Musculoskelet Disord 9 9 18215332 10.1186/1471-2474-9-9 (Pubitemid 351337372)
33. MC Erlandson LB Sherar RL Mirwald N Maffulli AD Baxter-Jones 2008 Growth and maturation of adolescent female gymnasts, swimmers, and tennis players Med Sci Sports Exerc 40 34 42 18182934
34. K Christo R Prabhakaran B Lamparello J Cord KK Miller MA Goldstein N Gupta DB Herzog A Klibanski M Misra 2008 Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects Pediatrics 121 1127 1136 18519482 10.1542/peds.2007-2392
35. T Chevalley JP Bonjour S Ferrari R Rizzoli 2009 Deleterious effect of late menarche on distal tibia microstructure in healthy 20-year-old and premenopausal middle-aged women J Bone Miner Res 24 144 152 19086917 10.1359/jbmr.080815
36. K Hind JG Truscott JA Evans 2006 Low lumbar spine bone mineral density in both male and female endurance runners Bone 39 880 885 16682267 10.1016/j.bone.2006.03.012 1:STN:280:DC%2BD28rjs1yisQ%3D%3D (Pubitemid 44322070)
37. EM Kirchner RD Lewis PJ O'Connor 1995 Bone mineral density and dietary intake of female college gymnasts Med Sci Sports Exerc 27 543 549 7791585 1:STN:280:DyaK2MzhtFOjtA%3D%3D
38. KL Bennell SA Malcolm KM Khan SA Thomas SJ Reid PD Brukner PR Ebeling JD Wark 1997 Bone mass and bone turnover in power athletes, endurance athletes, and controls: a 12-month longitudinal study Bone 20 477 484 9145246 10.1016/S8756-3282(97)00026-4 1:STN:280:DyaK2s3ptVKjsg%3D%3D (Pubitemid 27230453)
39. J Morel B Combe J Francisco J Bernard 2001 Bone mineral density of 704 amateur sportsmen involved in different physical activities Osteoporos Int 12 152 157 11303716 10.1007/s001980170148 1:STN:280:DC%2BD3M3oslalsw%3D%3D (Pubitemid 32244669)
40. L Maimoun O Coste AM Puech E Peruchon A Jaussent F Paris M Rossi C Sultan D Mariano-Goulart 2008 No negative impact of reduced leptin secretion on bone metabolism in male decathletes Eur J Appl Physiol 102 343 351 17943305 10.1007/s00421-007-0592-7 1:CAS:528:DC%2BD2sXhtlyit7jO (Pubitemid 350245959)
41. SM Nickols-Richardson PJ O'Connor SA Shapses RD Lewis 1999 Longitudinal bone mineral density changes in female child artistic gymnasts J Bone Miner Res 14 994 1002 10352109 10.1359/jbmr.1999.14.6.994 1:STN:280:DyaK1M3otVaqtg%3D%3D (Pubitemid 29262895)
42. SC van Coeverden JC Netelenbos CM de Ridder JC Roos C Popp-Snijders HA Delemarre-van de Waal 2002 Bone metabolism markers and bone mass in healthy pubertal boys and girls Clin Endocrinol (Oxf) 57 107 116 10.1046/j.1365-2265. 2002.01573.x (Pubitemid 34785891)
43. Maimoun L, Sultan C (2010) Effects of physical activity on bone remodeling. Metabolism. doi: 10.1016/j.metabol.2010.03.001
44. D Courteix N Rieth T Thomas E Van Praagh CL Benhamou K Collomp E Lespessailles C Jaffre 2007 Preserved bone health in adolescent elite rhythmic gymnasts despite hypoleptinemia Horm Res 68 20 27 17220634 10.1159/000098546 1:CAS:528:DC%2BD2sXmt1Sqtrc%3D (Pubitemid 46878355)
45. A Wasilewska AA Rybi-Szuminska W Zoch-Zwierz 2009 Serum osteoprotegrin (OPG) and receptor activator of nuclear factor kappaB (RANKL) in healthy children and adolescents J Pediatr Endocrinol Metab 22 1099 1104 20333868 10.1515/JPEM.2009.22.12.1099 1:CAS:528:DC%2BC3cXjsFymtrc%3D
46. F Buzi G Maccarinelli B Guaragni F Ruggeri G Radetti A Meini E Mazzolari D Cocchi 2004 Serum osteoprotegerin and receptor activator of nuclear factors kB (RANKL) concentrations in normal children and in children with pubertal precocity, Turner's syndrome and rheumatoid arthritis Clin Endocrinol (Oxf) 60 87 91 10.1111/j.1365-2265.2004.01951.x 1:CAS:528:DC%2BD2cXhslGmtLk%3D (Pubitemid 38183503)
47. J Gajewska J Ambroszkiewicz T Laskowska-Klita 2006 Osteoprotegerin and C-telopeptide of type I collagen in Polish healthy children and adolescents Adv Med Sci 51 269 272 17357324 1:CAS:528:DC%2BD2sXitlaisLc%3D
48. P Szulc LC Hofbauer AE Heufelder S Roth PD Delmas 2001 Osteoprotegerin serum levels in men: correlation with age, estrogen, and testosterone status J Clin Endocrinol Metab 86 3162 3165 11443182 10.1210/jc.86.7.3162 1:CAS:528:DC%2BD3MXlt1Gjt78%3D (Pubitemid 32673481)
49. RM Zebaze A Jones F Welsh M Knackstedt E Seeman 2005 Femoral neck shape and the spatial distribution of its mineral mass varies with its size: clinical and biomechanical implications Bone 37 243 252 15939679 10.1016/j.bone.2005.03. 019 (Pubitemid 40962433)
50. F Rivadeneira MC Zillikens CE De Laet A Hofman AG Uitterlinden TJ Beck HA Pols 2007 Femoral neck BMD is a strong predictor of hip fracture susceptibility in elderly men and women because it detects cortical bone instability: the Rotterdam study J Bone Miner Res 22 1781 1790 17638578 10.1359/jbmr.070712 (Pubitemid 351235145)