SpringerLink
Log in

Bone Tissue Responsiveness To Mechanical Loading—Possible Long-Term Implications of Swimming on Bone Health and Bone Development

  • Nutrition, Exercise and Lifestyle (S Shapses and R Daly, Section Editors)
  • Published:
Current Osteoporosis Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

To revisit the bone tissue mechanotransduction mechanisms behind the bone tissue response to mechanical loading and, within this context, explore the possible negative influence of regular swimming practice on bone health, particularly during the growth and development period.

Recent Findings

Bone is a dynamic tissue, responsive to mechanical loading and unloading, being these adaptative responses more intense during the growth and development period. Cross-sectional studies usually report a lower bone mass in swimmers compared to athletes engaged in weigh-bearing sports. However, studies with animal models show contradictory findings about the effect of swimming on bone health, highlighting the need for longitudinal studies.

Summary

Due to its microgravity characteristics, swimming seems to impair bone mass, but mostly at the lower limbs. It is unkown if there is a causal relationship between swimming and low BMD or if other confounding factors, such as a natural selection whithin the sport, are the cause.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data Availability

Not applicable.

Code Availability

Not applicable.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Langdahl B, Ferrari S, Dempster DW. Bone modeling and remodeling: potential as therapeutic targets for the treatment of osteoporosis. Ther Adv Musculoskelet Dis. 2016;8(6):225–35. https://doi.org/10.1177/1759720x16670154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bonewald LF. Osteocytes as dynamic multifunctional cells. Ann N Y Acad Sci. 2007;1116(1):281–90. https://doi.org/10.1196/annals.1402.018.

    Article  CAS  PubMed  Google Scholar 

  3. Bonewald LF. Mechanosensation and transduction in osteocytes. Bonekey Osteovision. 2006;3(10):7–15. https://doi.org/10.1138/20060233.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Qin L, Liu W, Cao H, **ao G. Molecular mechanosensors in osteocytes. Bone Res. 2020;8(8):23. https://doi.org/10.1038/s41413-020-0099-y. This review reports important evidence about the osteocytes’ role in bone mechanosensation and mechanotransduction.

  5. Hung CT, Allen FD, Pollack SR, Brighton CT. Intracellular Ca2+ stores and extracellular Ca2+ are required in the real-time Ca2+ response of bone cells experiencing fluid flow. J Biomech. 1996;29(11):1411–7. https://doi.org/10.1016/0021-9290(96)84536-2.

    Article  CAS  PubMed  Google Scholar 

  6. Robling AG, Turner CH. Mechanical signaling for bone modeling and remodeling. Crit Rev Eukaryot Gene Expr. 2009;19(4):319–38. https://doi.org/10.1615/critreveukargeneexpr.v19.i4.50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Klein-Nulend J, van Oers RFM, Bakker AD, Bacabac RG. Nitric oxide signaling in mechanical adaptation of bone. Osteoporos Int. 2014;25(5):1427–37. https://doi.org/10.1007/s00198-013-2590-4.

    Article  CAS  PubMed  Google Scholar 

  8. Cheng B, Kato Y, Zhao S, Luo J, Sprague E, Bonewald LF, Jiang JX. PGE(2) is essential for gap junction-mediated intercellular communication between osteocyte-like MLO-Y4 cells in response to mechanical strain. Endocrinology. 2001;142(8):3464–73. https://doi.org/10.1210/endo.142.8.8338.

    Article  CAS  PubMed  Google Scholar 

  9. Bonewald LF, Johnson ML. Osteocytes, mechanosensing and Wnt signaling. Bone. 2008;42(4):606–15. https://doi.org/10.1016/j.bone.2007.12.224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Lin C, Jiang X, Dai Z, Guo X, Weng T, Wang J, Li Y, Feng G, Gao X, He L. Sclerostin mediates bone response to mechanical unloading through antagonizing Wnt/beta-catenin signaling. J Bone Miner Res. 2009;24(10):1651–61. https://doi.org/10.1359/jbmr.090411.

    Article  CAS  PubMed  Google Scholar 

  11. Gaudio A, Pennisi P, Bratengeier C, Torrisi V, Lindner B, Mangiafico RA, Pulvirenti I, Hawa G, Tringali G, Fiore CE. Increased sclerostin serum levels associated with bone formation and resorption markers in patients with immobilization-induced bone loss. J Clin Endocrinol Metab. 2010;95(5):2248–53. https://doi.org/10.1210/jc.2010-0067.

    Article  CAS  PubMed  Google Scholar 

  12. Spatz JM, Fields EE, Yu EW, Divieti Pajevic P, Bouxsein ML, Sibonga JD, et al. Serum sclerostin increases in healthy adult men during bed rest. J Clin Endocrinol Metab. 2012;97(9):E1736–40. https://doi.org/10.1210/jc.2012-1579.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Smith SM, Heer M, Shackelford LC, Sibonga JD, Spatz J, Pietrzyk RA, Hudson EK, Zwart SR. Bone metabolism and renal stone risk during International Space Station missions. Bone. 2015;81:712–20. https://doi.org/10.1016/j.bone.2015.10.002.

    Article  CAS  PubMed  Google Scholar 

  14. Razi H, Birkhold AI, Weinkamer R, Duda GN, Willie BM, Checa S. Aging leads to a dysregulation in mechanically driven bone formation and resorption. J Bone Miner Res. 2015;30(10):1864–73. https://doi.org/10.1002/jbmr.2528.

    Article  PubMed  Google Scholar 

  15. Baxter-Jones AD, Faulkner RA, Forwood MR, Mirwald RL, Bailey DA. Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res. 2011;26(8):1729–39. https://doi.org/10.1002/jbmr.412.

    Article  PubMed  Google Scholar 

  16. Forwood MR. Mechanical loading and the develo** skeleton. Primer Metab Bone Dis Disord Miner Metab. 2018;25:141–6. https://doi.org/10.1002/9781119266594.ch19

  17. Faienza MF, Lassandro G, Chiarito M, Valente F, Ciaccia L, Giordano P. How physical activity across the lifespan can reduce the impact of bone ageing: a literature review. Int J Environ Res Public Health. 2020;17(6):1862. https://doi.org/10.3390/ijerph17061862. This literature review provides evidence about the importance of physical activity as a nonpharmacological therapy for prevent bone aging.

  18. Gomez-Bruton A, Montero-Marin J, Gonzalez-Aguero A, Gomez-Cabello A, Garcia-Campayo J, Moreno LA, et al. Swimming and peak bone mineral density: a systematic review and meta-analysis. J Sports Sci. 2017;36(4):365–77. https://doi.org/10.1080/02640414.2017.1307440.

    Article  PubMed  Google Scholar 

  19. Brooke-Wavell K, Skelton DA, Barker KL, Clark EM, De Biase S, Arnold S, et al. Strong, steady and straight: UK consensus statement on physical activity and exercise for osteoporosis. Br J Sports Med. 2022;56(15):837–46. https://doi.org/10.1136/bjsports-2021-104634.

    Article  PubMed  Google Scholar 

  20. Bellver M, Del Rio L, Jovell E, Drobnic F, Trilla A. Bone mineral density and bone mineral content among female elite athletes. Bone. 2019;127:393–400. https://doi.org/10.1016/j.bone.2019.06.030. This study evidence that swimmers can display lower BMD compared with athletes of different weight-bearing sports.

  21. Valente-Dos-Santos J, Tavares OM, Duarte JP, Sousa ESPM, Rama LM, Casanova JM, et al. Total and regional bone mineral and tissue composition in female adolescent athletes: comparison between volleyball players and swimmers. BMC Pediatr. 2018;18(1):212. https://doi.org/10.1186/s12887-018-1182-z.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Courteix D, Lespessailles E, Peres SL, Obert P, Germain P, Benhamou CL. Effect of physical training on bone mineral density in prepubertal girls: a comparative study between impact-loading and non-impact-loading sports. Osteoporos Int. 1998;8(2):152–8. https://doi.org/10.1007/bf02672512.

    Article  CAS  PubMed  Google Scholar 

  23. Creighton DL, Morgan AL, Boardley D, Brolinson PG. Weight-bearing exercise and markers of bone turnover in female athletes. J Appl Physiol. 2001;90(2):565–70. https://doi.org/10.1152/jappl.2001.90.2.565.

    Article  CAS  PubMed  Google Scholar 

  24. Fehling PC, Alekel L, Clasey J, Rector A, Stillman RJ. A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone. 1995;17(3):205–10. https://doi.org/10.1016/8756-3282(95)00171-9.

    Article  CAS  PubMed  Google Scholar 

  25. Silva CC, Goldberg TB, Teixeira AS, Dalmas JC. The impact of different types of physical activity on total and regional bone mineral density in young brazilian athletes. J Sports Sci. 2011;29(3):227–34. https://doi.org/10.1080/02640414.2010.529456.

    Article  PubMed  Google Scholar 

  26. Gomez-Bruton A, Montero-Marin J, Gonzalez-Aguero A, Garcia-Campayo J, Moreno LA, Casajus JA, et al. The effect of swimming during childhood and adolescence on bone mineral density: a systematic review and meta-analysis. Sports Med. 2015;46:365–79. https://doi.org/10.1007/s40279-015-0427-3.

    Article  Google Scholar 

  27. Magkos F, Yannakoulia M, Kavouras SA, Sidossis LS. The type and intensity of exercise have independent and additive effects on bone mineral density. Int J Sports Med. 2007;28(9):773–9. https://doi.org/10.1055/s-2007-964979.

    Article  CAS  PubMed  Google Scholar 

  28. Ju YI, Sone T, Ohnaru K, Tanaka K, Fukunaga M. Effect of swimming exercise on three-dimensional trabecular bone microarchitecture in ovariectomized rats. J Appl Physiol. 2015;119(9):990–7. https://doi.org/10.1152/japplphysiol.00147.2015.

    Article  CAS  PubMed  Google Scholar 

  29. Turner CH. Three rules for bone adaptation to mechanical stimuli. Bone. 1998;23(5):399–407. https://doi.org/10.1016/S8756-3282(98)00118-5.

    Article  CAS  PubMed  Google Scholar 

  30. Portier H, Benaitreau D, Pallu S. Does physical exercise always improve bone quality in rats? Life (Basel). 2020;10(10). https://doi.org/10.3390/life10100217. This review compares the effect of different exercises protocols in rats and demonstrates that swimming, the only non-weight bearing activity, is related to a higher bone negative effect.

  31. Harding AT, Beck BR. Exercise, osteoporosis, and bone geometry. Sports (Basel). 2017;5(2):29. https://doi.org/10.3390/sports5020029.

    Article  PubMed  Google Scholar 

  32. Robling AG, Burr DB, Turner CH. Partitioning a daily mechanical stimulus into discrete loading bouts improves the osteogenic response to loading. J Bone Miner Res. 2000;15(8):1596–602. https://doi.org/10.1359/jbmr.2000.15.8.1596.

    Article  CAS  PubMed  Google Scholar 

  33. Gardinier JD. The diminishing returns of mechanical loading and potential mechanisms that desensitize osteocytes. Curr Osteoporos Rep. 2021;19(4):436–43. https://doi.org/10.1007/s11914-021-00693-9.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Weidauer L, Minett M, Negus C, Binkley T, Vukovich M, Wey H, Specker B. Odd-impact loading results in increased cortical area and moments of inertia in collegiate athletes. Eur J Appl Physiol. 2014;114(7):1429–38. https://doi.org/10.1007/s00421-014-2870-5.

    Article  PubMed  Google Scholar 

  35. Gómez-Bruton A, Gónzalez-Agüero A, Gómez-Cabello A, Casajús JA, Vicente-Rodríguez G. Is bone tissue really affected by swimming? A systematic review. PLoS ONE. 2013;8(8):e70119. https://doi.org/10.1371/journal.pone.0070119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Olmedillas H, González-Agüero A, Moreno LA, Casajus JA, Vicente-Rodríguez G. Cycling and bone health: a systematic review. BMC Med. 2012;10(1):168. https://doi.org/10.1186/1741-7015-10-168.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Carbuhn AF, Fernandez TE, Bragg AF, Green JS, Crouse SF. Sport and training influence bone and body composition in women collegiate athletes. J Strength Cond Res. 2010;24(7):1710–7. https://doi.org/10.1519/JSC.0b013e3181d09eb3.

    Article  PubMed  Google Scholar 

  38. Duncan CS, Blimkie CJ, Cowell CT, Burke ST, Briody JN, Howman-Giles R. Bone mineral density in adolescent female athletes: relationship to exercise type and muscle strength. Med Sci Sports Exerc. 2002;34(2):286–94. https://doi.org/10.1097/00005768-200202000-00017.

    Article  PubMed  Google Scholar 

  39. Magkos F, Kavouras SA, Yannakoulia M, Karipidou M, Sidossi S, Sidossis LS. The bone response to non-weight-bearing exercise is sport-, site-, and sex-specific. Clin J Sport Med. 2007;17(2):123–8. https://doi.org/10.1097/JSM.0b013e318032129d.

    Article  PubMed  Google Scholar 

  40. Czeczelewski J, Dlugolecka B, Czeczelewska E, Raczynska B. Intakes of selected nutrients, bone mineralisation and density of adolescent female swimmers over a three-year period. Biol Sport. 2013;30(1):17–20. https://doi.org/10.5604/20831862.1029816.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Ferry B, Lespessailles E, Rochcongar P, Duclos M, Courteix D. Bone health during late adolescence: effects of an 8-month training program on bone geometry in female athletes. Joint Bone Spine. 2013;80(1):57–63. https://doi.org/10.1016/j.jbspin.2012.01.006.

    Article  PubMed  Google Scholar 

  42. Gomez-Bruton A, Gonzalez-Aguero A, Gomez-Cabello A, Matute-Llorente A, Casajus JA, Vicente-Rodriguez G. The effects of swimming training on bone tissue in adolescence. Scand J Med Sci Sports. 2014;25(6):589–602. https://doi.org/10.1111/sms.12378.

    Article  Google Scholar 

  43. Kang YS, Kim SH, Kim JC. Effects of swimming exercise on high-fat diet-induced low bone mineral density and trabecular bone microstructure in rats. J Exerc Nutr Biochem. 2017;21(2):48-55. https://doi.org/10.20463/jenb.2016.0063.

  44. Abrahin O, Rodrigues RP, Marçal AC, Alves EA, Figueiredo RC, Sousa EC. Swimming and cycling do not cause positive effects on bone mineral density: a systematic review. Rev Bras Reumatol. 2016;56(4):345–51. https://doi.org/10.1016/j.rbr.2015.09.010.

    Article  Google Scholar 

  45. Huang T-H, Hsieh SS, Liu S-H, Chang F-L, Lin S-C, Yang R-S. Swimming training increases the post-yield energy of bone in young male rats. Calcif Tissue Int. 2010;86(2):142–53. https://doi.org/10.1007/s00223-009-9320-0.

    Article  CAS  PubMed  Google Scholar 

  46. Bourrin S, Ghaemmaghami F, Vico L, Chappard D, Gharib C, Alexandre C. Effect of a five-week swimming program on rat bone: a histomorphometric study. Calcif Tissue Int. 1992;51(2):137–42. https://doi.org/10.1007/BF00298502.

    Article  CAS  PubMed  Google Scholar 

  47. Papageorgiou M, Dolan E, Elliott-Sale KJ, Sale C. Reduced energy availability: implications for bone health in physically active populations. Eur J Nutr. 2018;57(3):847–59. https://doi.org/10.1007/s00394-017-1498-8.

    Article  PubMed  Google Scholar 

  48. Ju YI, Sone T. Effects of different types of mechanical loading on trabecular bone microarchitecture in rats. J Bone Metab. 2021;28(4):253-65. https://doi.org/10.11005/jbm.2021.28.4.253. This review updates current evidence regarding major adaptations in bone microarchitecture in small animals, supporting that different types of loading can lead to different microarchitecture adaptations.

  49. Tan VP, Macdonald HM, Kim S, Nettlefold L, Gabel L, Ashe MC, et al. Influence of physical activity on bone strength in children and adolescents: a systematic review and narrative synthesis. J Bone Miner Res. 2014;29(10):2161–81. https://doi.org/10.1002/jbmr.2254.

    Article  PubMed  Google Scholar 

  50. Nikander R, Sievänen H, Heinonen A, Daly RM, Uusi-Rasi K, Kannus P. Targeted exercise against osteoporosis: a systematic review and meta-analysis for optimising bone strength throughout life. BMC Med Educ. 2010;8(47). https://doi.org/10.1186/1741-7015-8-47.

  51. Hervás G, Ruiz-Litago F, Irazusta J, Irazusta A, Sanz B, Gil-Goikouria J, Fraile-Bermudez AB, Pérez-Rodrigo C, Zarrazquin I. Bone health and its relationship with impact loading and the continuity of physical activity throughout school periods. Int J Environ Res Public Health. 2019;16(16):2834. https://doi.org/10.3390/ijerph16162834. This study provides evidence about the importance of high impact physical activity to improve bone stiffness.

  52. Fuchs RK, Bauer JJ, Snow CM. Jum** improves hip and lumbar spine bone mass in prepubescent children: a randomized controlled trial. J Bone Miner Res. 2001;16(1):148–56. https://doi.org/10.1359/jbmr.2001.16.1.148.

    Article  CAS  PubMed  Google Scholar 

  53. Yan C, Moshage SG, Kersh ME. Play during growth: the effect of sports on bone adaptation. Curr Osteoporos Rep. 2020;18(6):684–95. https://doi.org/10.1007/s11914-020-00632-0. This study is an interesting review regarding how bone adapts to mechano-stimulation of different types of sports during growth.

  54. Vicente-Rodríguez G. How does exercise affect bone development during growth? Sports Med. 2006;36(7):561–9. https://doi.org/10.2165/00007256-200636070-00002.

    Article  PubMed  Google Scholar 

  55. Bradbury P, Wu H, Choi JU, Rowan AE, Zhang H, Poole K, Lauko J, Chou J. Modeling the Impact of microgravity at the cellular level: implications for human disease. Front Cell Dev Biol. 2020;8:96. https://doi.org/10.3389/fcell.2020.00096. This review updates evidence related with mechanotransduction and bone physiology under microgravity environment.

  56. Vico L, Hargens A. Skeletal changes during and after spaceflight. Nat Rev Rheumatol. 2018;14(4):229–45. https://doi.org/10.1038/nrrheum.2018.37.

    Article  PubMed  Google Scholar 

  57. Falcai MJ, Zamarioli A, Okubo R, de Paula FJ, Volpon JB. The osteogenic effects of swimming, jum**, and vibration on the protection of bone quality from disuse bone loss. Scand J Med Sci Sports. 2015;25(3):390–7. https://doi.org/10.1111/sms.12240.

    Article  CAS  PubMed  Google Scholar 

  58. Leblanc AD, Schneider VS, Evans HJ, Engelbretson DA, Krebs JM. Bone mineral loss and recovery after 17 weeks of bed rest. J Bone Miner Res. 1990;5(8):843–50. https://doi.org/10.1002/jbmr.5650050807.

    Article  CAS  PubMed  Google Scholar 

  59. Beller G, Belavý DL, Sun L, Armbrecht G, Alexandre C, Felsenberg D. WISE-2005: bed-rest induced changes in bone mineral density in women during 60 days simulated microgravity. Bone. 2011;49(4):858–66. https://doi.org/10.1016/j.bone.2011.06.021.

    Article  PubMed  Google Scholar 

  60. Armbrecht G, Belavý DL, Backström M, Beller G, Alexandre C, Rizzoli R, Felsenberg D. Trabecular and cortical bone density and architecture in women after 60 days of bed rest using high-resolution pQCT: WISE 2005. J Bone Miner Res. 2011;26(10):2399–410. https://doi.org/10.1002/jbmr.482.

    Article  PubMed  Google Scholar 

  61. Sibonga JD, Evans HJ, Sung HG, Spector ER, Lang TF, Oganov VS, Bakulin AV, Shackelford LC, LeBlanc AD. Recovery of spaceflight-induced bone loss: bone mineral density after long-duration missions as fitted with an exponential function. Bone. 2007;41(6):973–8. https://doi.org/10.1016/j.bone.2007.08.022.

    Article  CAS  PubMed  Google Scholar 

  62. Orwoll ES, Adler RA, Amin S, Binkley N, Lewiecki EM, Petak SM, Shapses SA, Sinaki M, Watts NB, Sibonga JD. Skeletal health in long-duration astronauts: nature, assessment, and management recommendations from the NASA Bone Summit. J Bone Miner Res. 2013;28(6):1243–55. https://doi.org/10.1002/jbmr.1948.

    Article  PubMed  Google Scholar 

  63. LeBlanc A, Schneider V, Shackelford L, West S, Oganov V, Bakulin A, et al. Bone mineral and lean tissue loss after long duration space flight. J Musculoskelet Nueronal Interact. 2000;1(2):157–60.

    CAS  Google Scholar 

  64. Smith SM, Heer MA, Shackelford LC, Sibonga JD, Ploutz-Snyder L, Zwart SR. Benefits for bone from resistance exercise and nutrition in long-duration spaceflight: evidence from biochemistry and densitometry. J Bone Miner Res. 2012;27(9):1896–906. https://doi.org/10.1002/jbmr.1647.

    Article  CAS  PubMed  Google Scholar 

  65. Sibonga J, Matsumoto T, Jones J, Shapiro J, Lang T, Shackelford L, Smith SM, Young M, Keyak J, Kohri K, Ohshima H, Spector E, LeBlanc A. Resistive exercise in astronauts on prolonged spaceflights provides partial protection against spaceflight-induced bone loss. Bone. 2019;128:112037. https://doi.org/10.1016/j.bone.2019.07.013.

    Article  CAS  PubMed  Google Scholar 

  66. Midura RJ, Dillman CJ, Grabiner MD. Low amplitude, high frequency strains imposed by electrically stimulated skeletal muscle retards the development of osteopenia in the tibiae of hindlimb suspended rats. Med Eng Phys. 2005;27(4):285–93. https://doi.org/10.1016/j.medengphy.2004.12.014.

    Article  PubMed  Google Scholar 

  67. Vickerton P, Jarvis JC, Gallagher JA, Akhtar R, Sutherland H, Jeffery N. Morphological and histological adaptation of muscle and bone to loading induced by repetitive activation of muscle. Proc R Soc B. 2014;281(1788):20140786. https://doi.org/10.1098/rspb.2014.0786.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Robling AG. Is bone's response to mechanical signals dominated by muscle forces? Med Sci Sports Exerc. 2009;41(11):2044–9. https://doi.org/10.1249/MSS.0b013e3181a8c702.

    Article  PubMed  PubMed Central  Google Scholar 

  69. LeBlanc AD, Schneider VS, Evans HJ, Pientok C, Rowe R, Spector E. Regional changes in muscle mass following 17 weeks of bed rest. J Appl Physiol. 1992;73(5):2172–8. https://doi.org/10.1152/jappl.1992.73.5.2172.

    Article  CAS  PubMed  Google Scholar 

  70. Gordon CM, Zemel BS, Wren TA, Leonard MB, Bachrach LK, Rauch F, Gilsanz V, Rosen CJ, Winer KK. The determinants of peak bone mass. J Pediatr. 2016;180:261–9. https://doi.org/10.1016/j.jpeds.2016.09.056.

    Article  PubMed  Google Scholar 

  71. Ramos E, Frontera WR, Llopart A, Feliciano D. Muscle strength and hormonal levels in adolescents: gender related differences. Int J Sports Med. 1998;19(08):526–31.

    Article  CAS  PubMed  Google Scholar 

  72. Zhu X, Zheng H. Factors influencing peak bone mass gain. Front Med. 2021;15(1):53–69. https://doi.org/10.1007/s11684-020-0748-y. This review updates available information about the peak bone mass and its determinants, such as the importance of the physical activity practice during the bone growth and development period.

  73. Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, O’Karma M, Wallace TC, Zemel BS. The National Osteoporosis Foundation's position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int. 2016;27(4):1281–386. https://doi.org/10.1007/s00198-015-3440-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Rizzoli R, Bianchi ML, Garabédian M, McKay HA, Moreno LA. Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone. 2010;46(2):294–305. https://doi.org/10.1016/j.bone.2009.10.005.

    Article  PubMed  Google Scholar 

  75. Faulkner RA, Bailey DA. Osteoporosis: a pediatric concern? J Sports Sci Med. 2007;51:1–12. https://doi.org/10.1159/000102993.

    Article  Google Scholar 

  76. Xue S, Kemal O, Lu M, Lix LM, Leslie WD, Yang S. Age at attainment of peak bone mineral density and its associated factors: The National Health and Nutrition Examination Survey 2005-2014. Bone. 2020;131:115163. https://doi.org/10.1016/j.bone.2019.115163.

    Article  PubMed  Google Scholar 

  77. Boot AM, de Ridder MA, van der Sluis IM, van Slobbe I, Krenning EP, Keizer-Schrama SM. Peak bone mineral density, lean body mass and fractures. Bone. 2010;46(2):336–41. https://doi.org/10.1016/j.bone.2009.10.003.

    Article  PubMed  Google Scholar 

  78. Bonjour JP, Chevalley T. Pubertal timing, bone acquisition, and risk of fracture throughout life. Endocr Rev. 2014;35(5):820–47. https://doi.org/10.1210/er.2014-1007.

    Article  CAS  PubMed  Google Scholar 

  79. Karlsson MK, Rosengren BE. Exercise and peak bone mass. Curr Osteoporos Rep. 2020;18(3):285–90. https://doi.org/10.1007/s11914-020-00588-1.

    Article  PubMed  PubMed Central  Google Scholar 

  80. McCormack SE, Cousminer DL, Chesi A, Mitchell JA, Roy SM, Kalkwarf HJ, Lappe JM, Gilsanz V, Oberfield SE, Shepherd JA, Winer KK, Kelly A, Grant SFA, Zemel BS. Association between linear growth and bone accrual in a diverse cohort of children and adolescents. JAMA Pediatr Sci Child Adolesc Health. 2017;171(9):e171769. https://doi.org/10.1001/jamapediatrics.2017.1769.

    Article  Google Scholar 

  81. Callewaert F, Venken K, Kopchick JJ, Torcasio A, van Lenthe GH, Boonen S, Vanderschueren D. Sexual dimorphism in cortical bone size and strength but not density is determined by independent and time-specific actions of sex steroids and IGF-1: evidence from pubertal mouse models. J Bone Miner Res. 2010;25(3):617–26. https://doi.org/10.1359/jbmr.090828.

    Article  CAS  PubMed  Google Scholar 

  82. Turner CH, Robling AG. Designing exercise regimens to increase bone strength. Exerc Sport Sci Rev. 2003;31(1):45–50.

    Article  PubMed  Google Scholar 

  83. Maggiano IS, Maggiano CM, Tiesler VG, Chi-Keb JR, Stout SD. Drifting diaphyses: asymmetry in diametric growth and adaptation along the humeral and femoral length. Anat Rec (Hoboken). 2015;298(10):1689–99. https://doi.org/10.1002/ar.23201.

    Article  PubMed  Google Scholar 

  84. Isojima T, Sims NA. Cortical bone development, maintenance and porosity: genetic alterations in humans and mice influencing chondrocytes, osteoclasts, osteoblasts and osteocytes. Cell Mol Life Sci. 2021;78(15):5755–73. https://doi.org/10.1007/s00018-021-03884-w.

    Article  CAS  PubMed  Google Scholar 

  85. Khosla S, Riggs BL, Atkinson EJ, Oberg AL, McDaniel LJ, Holets M, Peterson JM, Melton LJ 3rd. Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res. 2006;21(1):124–31. https://doi.org/10.1359/jbmr.050916.

  86. Riggs BL, Melton Iii LJ 3rd, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, et al. Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J Bone Miner Res 2004;19(12):1945-1954. https://doi.org/10.1359/jbmr.040916.

  87. McVeigh JA, Howie EK, Zhu K, Walsh JP, Straker L. Organized sport participation from childhood to adolescence is associated with bone mass in young adults from the Raine Study. J Bone Miner Res. 2019;34(1):67–74. https://doi.org/10.1002/jbmr.3583.

    Article  CAS  PubMed  Google Scholar 

  88. Gabel L, Macdonald HM, Nettlefold L, McKay HA. Physical activity, sedentary time, and bone strength from childhood to early adulthood: a mixed longitudinal HR-pQCT study. J Bone Miner Res. 2017;32(7):1525–36. https://doi.org/10.1002/jbmr.3115.

    Article  CAS  PubMed  Google Scholar 

  89. Palaiothodorou D, Antoniou T, Vagenas G. Bone asymmetries in the limbs of children tennis players: testing the combined effects of age, sex, training time, and maturity status. J Sports Sci. 2020;38(20):2298–306. https://doi.org/10.1080/02640414.2020.1779490.

    Article  PubMed  Google Scholar 

  90. Warden SJ, Mantila Roosa SM, Kersh ME, Hurd AL, Fleisig GS, Pandy MG, Fuchs RK. Physical activity when young provides lifelong benefits to cortical bone size and strength in men. Proc Natl Acad Sci. 2014;111(14):5337–42. https://doi.org/10.1073/pnas.1321605111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Nilsson M, Ohlsson C, Mellström D, Lorentzon M. Previous sport activity during childhood and adolescence is associated with increased cortical bone size in young adult men. J Bone Miner Res. 2009;24(1):125–33. https://doi.org/10.1359/jbmr.080909.

    Article  PubMed  Google Scholar 

  92. Warden SJ, Fuchs RK, Castillo AB, Nelson IR, Turner CH. Exercise when young provides lifelong benefits to bone structure and strength. J Bone Miner Res. 2007;22(2):251–9. https://doi.org/10.1359/jbmr.061107.

    Article  PubMed  Google Scholar 

  93. Emslander HC, Sinaki M, Muhs JM, Chao EY, Wahner HW, Bryant SC, et al. Bone mass and muscle strength in female college athletes (runners and swimmers). Mayo Clin Proc. 1998;73(12):1151–60. https://doi.org/10.4065/73.12.1151.

    Article  CAS  PubMed  Google Scholar 

  94. Min SK, Oh T, Kim SH, Cho J, Chung HY, Park DH, et al. Position statement: exercise guidelines to increase peak bone mass in adolescents. J Bone Metab. 2019;26(4):225-39. https://doi.org/10.11005/jbm.2019.26.4.225. This position statement updates the guidelines to increase the peak bone mass in adolescents and includes osteogenic exercises performance in their daily physical activities’ recommendations.

  95. Gomez-Bruton A, Gonzalez-Aguero A, Matute-Llorente A, Lozano-Berges G, Gomez-Cabello A, Moreno LA, Casajus JA, Vicente-Rodríguez G. The muscle-bone unit in adolescent swimmers. Osteoporos Int. 2019;30(5):1079–88. https://doi.org/10.1007/s00198-019-04857-3.

    Article  CAS  PubMed  Google Scholar 

  96. Gómez-Bruton A, González-Agüero A, Gómez-Cabello A, Matute-Llorente A, Casajús JA, Vicente-Rodríguez G. Swimming and bone: is low bone mass due to hypogravity alone or does other physical activity influence it? Osteoporos Int. 2016;27(5):1785–93. https://doi.org/10.1007/s00198-015-3448-8.

    Article  PubMed  Google Scholar 

  97. Lee EJ, Long KA, Risser WL, Poindexter HB, Gibbons WE, Goldzieher J. Variations in bone status of contralateral and regional sites in young athletic women. Med Sci Sports Exerc. 1995;27(10):1354–61.

    Article  CAS  PubMed  Google Scholar 

  98. Derman O, Cinemre A, Kanbur N, Dogan M, Kilic M, Karaduman E. Effect of swimming on bone metabolism in adolescents. Turk J Pediatr. 2008;50(2):149–54.

    PubMed  Google Scholar 

  99. Taaffe DR, Snow-Harter C, Connolly DA, Robinson TL, Brown MD, Marcus R. Differential effects of swimming versus weight-bearing activity on bone mineral status of eumenorrheic athletes. J Bone Miner Res. 1995;10(4):586–93. https://doi.org/10.1002/jbmr.5650100411.

    Article  CAS  PubMed  Google Scholar 

  100. Agostinete RR, Duarte JP, Valente-Dos-Santos J, Coelho ESMJ, Tavares OM, Conde JM, et al. Bone tissue, blood lipids and inflammatory profiles in adolescent male athletes from sports contrasting in mechanical load. PLoS ONE. 2017;12(6):1–18. https://doi.org/10.1371/journal.pone.0180357.

    Article  CAS  Google Scholar 

  101. Gruodyte R, Jurimae J, Saar M, Jurimae T. The relationships among bone health, insulin-like growth factor-1 and sex hormones in adolescent female athletes. J Bone Miner Metab. 2010;28(3):306–13. https://doi.org/10.1007/s00774-009-0130-2.

    Article  CAS  PubMed  Google Scholar 

  102. Agostinete RR, Maillane-Vanegas S, Lynch KR, Turi-Lynch B, Coelho ESMJ, Campos EZ, et al. The impact of training load on bone mineral density of adolescent swimmers: a structural equation modeling approach. Pediatr Exerc Sci. 2017;29(4):520–8. https://doi.org/10.1123/pes.2017-0008.

    Article  PubMed  Google Scholar 

  103. Vantorre J, Seifert L, Fernandes RJ, Vilas-Boas JP, Chollet D. Kinematical profiling of the front crawl start. Int J Sports Med. 2010;31(1):16–21. https://doi.org/10.1055/s-0029-1241208.

    Article  CAS  PubMed  Google Scholar 

  104. Chainok P, Machado L, de Jesus K, Abraldes JA, Borgonovo-Santos M, Fernandes RJ, Vilas-Boas JP. Backstroke to breaststroke turning performance in age-group swimmers: hydrodynamic characteristics and pull-out strategy. Int J Environ Res Public Health. 2021;18(1858):1–10. https://doi.org/10.3390/ijerph18041858.

    Article  Google Scholar 

  105. Figueiredo P, Rouard A, Vilas-Boas JP, Fernandes RJ. Upper- and lower-limb muscular fatigue during the 200-m front crawl. Appl Physiol Nutr Metab. 2013;38(7):716–24. https://doi.org/10.1139/apnm-2012-0263.

    Article  CAS  PubMed  Google Scholar 

  106. Hart NH, Nimphius S, Rantalainen T, Ireland A, Siafarikas A, Newton RU. Mechanical basis of bone strength: Influence of bone material, bone structure and muscle action. J Musculoskelet Neuronal Interact. 2017;17(3):114–39.

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Maillane-Vanegas S, Agostinete RR, Lynch KR, Ito IH, Luiz-de-Marco R, Rodrigues-Junior MA, Turi-Lynch BC, Fernandes RA. Bone mineral density and sports participation. J Clin Densitom. 2020;23(2):294–302. https://doi.org/10.1016/j.jocd.2018.05.041.

    Article  PubMed  Google Scholar 

  108. Vlachopoulos D, Barker AR, Ubago-Guisado E, Ortega FB, Krustrup P, Metcalf B, Castro Pinero J, Ruiz JR, Knapp KM, Williams CA, Moreno LA, Gracia-Marco L. The effect of 12-month participation in osteogenic and non-osteogenic sports on bone development in adolescent male athletes. The PRO-BONE study. J Sci Med Sport. 2018;21(4):404–9. https://doi.org/10.1016/j.jsams.2017.08.018.

    Article  PubMed  Google Scholar 

  109. Maimoun L, Coste O, Philibert P, Briot K, Mura T, Galtier F, et al. Peripubertal female athletes in high-impact sports show improved bone mass acquisition and bone geometry. Metabolism. 2013;62(8):1088–98. https://doi.org/10.1016/j.metabol.2012.11.010.

    Article  CAS  PubMed  Google Scholar 

  110. Dias Quiterio AL, Carnero EA, Baptista FM, Sardinha LB. Skeletal mass in adolescent male athletes and nonathletes: relationships with high-impact sports. J Strength Cond Res. 2011;25(12):3439–47.

    Article  PubMed  Google Scholar 

  111. Vlachopoulos D, Barker AR, Williams CA, SA AR, Knapp KM, Metcalf BS, et al. The impact of sport participation on bone mass and geometry in male adolescents. Med Sci Sports Exerc. 2017;49(2):317–26. https://doi.org/10.1249/mss.0000000000001091.

    Article  PubMed  Google Scholar 

  112. Agostinete RR, Lynch KR, Gobbo LA, Lima MC, Ito IH, Luiz-de-Marco R, et al. Basketball affects bone mineral density accrual in boys more than swimming and other impact sports: 9-mo follow-up. J Clin Densitom. 2016;19(3):375–81. https://doi.org/10.1016/j.jocd.2016.04.006.

    Article  PubMed  Google Scholar 

  113. Ribeiro-Dos-Santos MR, Lynch KR, Agostinete RR, Maillane-Vanegas S, Turi-Lynch B, Ito IH, et al. Prolonged practice of swimming is negatively related to bone mineral density gains in adolescents. J Bone Metab. 2016;23(3):149-55. https://doi.org/10.11005/jbm.2016.23.3.149.

  114. Maimoun L, Coste O, Philibert P, Briot K, Mura T, Galtier F, et al. Testosterone secretion in elite adolescent swimmers does not modify bone mass acquisition: a 1-year follow-up study. Fertil Steril. 2013;99(1):270–8. https://doi.org/10.1016/j.fertnstert.2012.08.020.

    Article  CAS  PubMed  Google Scholar 

  115. Pezhman L, Sheikhzadeh Hesari F, Ghiasi R, Alipour MR. The impact of forced swimming on expression of RANKL and OPG in a type 2 diabetes mellitus rat model. Arch Physiol Biochem. 2019;125(3):195–200. https://doi.org/10.1080/13813455.2018.1446178.

    Article  CAS  PubMed  Google Scholar 

  116. Snyder A, Zierath JR, Hawley JA, Sleeper MD, Craig BW. The effects of exercise mode, swimming vs. running, upon bone growth in the rapidly growing female rat. Mech Ageing Dev. 1992;66(1):59–69. https://doi.org/10.1016/0047-6374(92)90073-M.

    Article  CAS  PubMed  Google Scholar 

  117. Gomes GJ, Carlo RJD, Silva MFD, Cunha D, Silva ED, Silva KAD, et al. Swimming training potentiates the recovery of femoral neck strength in young diabetic rats under insulin therapy. Clinics. 2019;74:e829. https://doi.org/10.6061/clinics/2019/e829.

    Article  PubMed  Google Scholar 

  118. Swissa-Sivan A, Azoury R, Statter M, Leichter I, Nyska A, Nyska M, Menczel J, Samueloff S. The effect of swimming on bone modeling and composition in young adult rats. Calcif Tissue Int. 1990;47(3):173–7. https://doi.org/10.1007/BF02555984.

    Article  CAS  PubMed  Google Scholar 

  119. Ju Y-I, Sone T, Ohnaru K, Tanaka K, Yamaguchi H, Fukunaga M. Effects of different types of jump impact on trabecular bone mass and microarchitecture in growing rats. PLoS ONE. 2014;9(9):e107953. https://doi.org/10.1371/journal.pone.0107953.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Ju YI, Sone T, Ohnaru K, Choi HJ, Choi KA, Fukunaga M. Jump exercise during hindlimb unloading protect against the deterioration of trabecular bone microarchitecture in growing young rats. Springerplus. 2013;2(1):35. https://doi.org/10.1186/2193-1801-2-35.

    Article  PubMed  PubMed Central  Google Scholar 

  121. Hemmatian H, Bakker AD, Klein-Nulend J, van Lenthe GH. Alterations in osteocyte lacunar morphology affect local bone tissue strains. J Mech Behav Biomed Mater. 2021;123:104730. https://doi.org/10.1016/j.jmbbm.2021.104730.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The authors perform their research activity at the Research Center in Physical Activity, Health and Leisure (CIAFEL), Faculty of Sport, University of Porto (FADEUP) which is funded by Fundação Para a Ciência e Tecnologia (FCT) grant UIDB/00617/2020 and at the Laboratory for Integrative and Translational Research in Population Health (ITR) which is funded by FCT grant LA/P/0064/2020. The author’s work is currently supported by FCT grant PTDC/SAU-DES/4113/2020.

Author information

Authors and Affiliations

  1. Research Centre in Physical Activity, Health and Leisure (CIAFEL), Faculty of Sport, University of Porto (FADE/UP), 4200-450, Porto, Portugal

    Andréa Bezerra, Laura Freitas, Leonardo Maciel & Hélder Fonseca

  2. Laboratory for Integrative and Translational Research in Population Health (ITR), 4050-600, Porto, Portugal

    Andréa Bezerra, Laura Freitas, Leonardo Maciel & Hélder Fonseca

  3. Department of Physiotherapy, Federal University of Sergipe, Campus Lagarto, Lagarto, Brazil

    Leonardo Maciel

Authors
  1. Andréa Bezerra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leonardo Maciel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hélder Fonseca
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, H.F. and A.B.; investigation, A.B., L.F. and L.M.; resources, H.F.; writing—original draft preparation, A.B., L.F. and L.M.; writing—review and editing, A.B. and H.F.; supervision, H.F.; funding acquisition, H.F. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Andréa Bezerra.

Ethics declarations

Conflict of Interest

The authors declare no conflict of interest.

Humans and Animal Rights

All reported studies/experiments with human or animal subjects performed by the author have been previously published and complied with all applicable ethical standards (including the Helsinki Declaration and its amendments, institutional/national research committee standards, and international/national/institutional guidelines).

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Nutrition, Exercise and Lifestyle

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bezerra, A., Freitas, L., Maciel, L. et al. Bone Tissue Responsiveness To Mechanical Loading—Possible Long-Term Implications of Swimming on Bone Health and Bone Development. Curr Osteoporos Rep 20, 453–468 (2022). https://doi.org/10.1007/s11914-022-00758-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11914-022-00758-3

Keywords

Search

Navigation