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  PubMed  PubMed Central  Google Scholar 

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  PubMed  Google Scholar 

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 

Qin L, Liu W, Cao H, Xiao 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.

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  PubMed  Google Scholar 

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  PubMed  PubMed Central  Google Scholar 

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  PubMed  Google Scholar 

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  PubMed  Google Scholar 

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  PubMed  PubMed Central  Google Scholar 

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  PubMed  Google Scholar 

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  PubMed  Google Scholar 

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  PubMed  PubMed Central  Google Scholar 

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  PubMed  Google Scholar 

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 

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 

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

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.

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 

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  Google Scholar 

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.

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 

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  PubMed  Google Scholar 

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  PubMed  Google Scholar 

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  PubMed  Google Scholar 

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 

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 

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  PubMed  Google Scholar 

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  PubMed  Google Scholar 

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  PubMed  Google Scholar 

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.

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

Article  Google Scholar 

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  PubMed  Google Scholar 

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 

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 

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  PubMed  PubMed Central  Google Scholar 

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 

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 

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 

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 

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  PubMed  PubMed Central  Google Scholar 

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