Swimming and peak bone mineral density: A systematic review and meta-analysis

References

• Ammann, P., & Rizzoli, R. (2003). Bone strength and its determinants. Osteoporosis International, Suppl 14, S13–18. doi:10.1007/s00198-002-1345-4
   Web of Science ®Google Scholar
• Begg, C. B., & Mazumdar, M. (1994). Operating characteristics of a rank correlation test for publication bias. Biometrics, 50(4), 1088–1101. doi:10.2307/2533446
   PubMed Web of Science ®Google Scholar
• Bischoff-Ferrari, H. A., Dietrich, T., Orav, E. J., & Dawson-Hughes, B. (2004). Positive association between 25-hydroxy vitamin D levels and bone mineral density: A population-based study of younger and older adults. The American Journal of Medicine, 116(9), 634–639. doi:10.1016/j.amjmed.2003.12.029
   PubMed Web of Science ®Google Scholar
• Bonjour, J. P., Chevalley, T., Ferrari, S., & Rizzoli, R. (2009). The importance and relevance of peak bone mass in the prevalence of osteoporosis. Salud Publica de Mexico, 51 Suppl 1, S5–17.
   PubMed Web of Science ®Google Scholar
• Borenstein, M., Hedges, L. V., Higgins, J P. T., & Rothstein, H. R. (2009). Introduction to meta-analysis. Cornwall: Wiley.
   Google Scholar
• Burge, R., Dawson-Hughes, B., Solomon, D. H., Wong, J. B., King, A., & Tosteson, A. (2007). Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025. Journal of Bone and Mineral Research, 22(3), 465–475. doi:10.1359/jbmr.061113
   PubMed Web of Science ®Google Scholar
• Carbuhn, A. F., Fernandez, T. E., Bragg, A. F., Green, J. S., & Crouse, S. F. (2010). Sport and training influence bone and body composition in women collegiate athletes. Journal of Strength and Conditioning Research, 24(7), 1710–1717. doi:10.1519/JSC.0b013e3181d09eb3
   PubMed Web of Science ®Google Scholar
• Cauley, J. A. (2011). Defining ethnic and racial differences in osteoporosis and fragility fractures. Clinical Orthopaedics and Related Research, 469(7), 1891–1899. doi:10.1007/s11999-011-1863-5
   PubMed Web of Science ®Google Scholar
• Chase, N. L., Sui, X., & Blair, S. N. (2008). Comparison of the health aspects of swimming with other types of physical activity and sedentary lifestyle habits. International Journal Aquat Researcher Education, 2, 151–161.
   Google Scholar
• Cooper, H., & Lv, H. (1994). The handbook of research synthesis. New York: Russell sage foundation.
   Google Scholar
• Creighton, D. L., Morgan, A. L., Boardley, D., & Gunnar Brolinson, P. (2001). Weight-bearing exercise and markers of bone turnover in female athletes. Journal of Applied Physiology, 90(2), 565–570.
   PubMed Web of Science ®Google Scholar
• Cuijpers, P., Geraedts, A. S., Van Oppen, P., Andersson, G., Markowitz, J. C., & Van Straten, A. (2008). Interpersonal psychotherapy for depression: A meta-analysis. American Journal of Psychiatry, 168(6), 581–592. doi:10.1176/appi.ajp.2010.10101411
   Web of Science ®Google Scholar
• Duan, Y., Turner, C. H., Kim, B.-T., & Seeman, E. (2001). Sexual dimorphism in vertebral fragility is more the result of gender differences in age-related bone gain than bone loss. Journal of Bone and Mineral Research, 16(12), 2267–2275. doi:10.1359/jbmr.2001.16.12.2267
   PubMed Web of Science ®Google Scholar
• Duval, S., & Tweedie, R. (2000). Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics, 56(2), 455–463. doi:10.1111/j.0006-341X.2000.00455.x
   PubMed Web of Science ®Google Scholar
• Egger, M., Davey Smith, G., Schneider, M., & Minder, C. (1997). Bias in meta-analysis detected by a simple, graphical test. Bmj, 315(7109), 629–634. doi:10.1136/bmj.315.7109.629
   PubMed Web of Science ®Google Scholar
• Emslander, H. C., Sinaki, M., Muhs, J. M., Chao, E. Y. S., Wahner, H. W., & Bryant, S. C. (1998). Bone mass and muscle strength in female college athletes (runners and swimmers). Mayo Clinic Proceedings, 73(12), 1151–1160. doi:10.4065/73.12.1151
   PubMed Web of Science ®Google Scholar
• Fehling, P. C., Alekel, L., Clasey, J., Rector, A., & Stillman, R. J. (1995). A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone, 17(3), 205–210. doi:10.1016/8756-3282(95)00171-9
   PubMed Web of Science ®Google Scholar
• Gomez-Bruton, A., Gonzalez-Aguero, A., Gomez-Cabello, A., Casajus, J. A., & Vicente-Rodriguez, G. (2013). Is bone tissue really affected by swimming? A systematic review. Plos One, 8(8), e70119. doi:10.1371/journal.pone.0070119
   PubMed Web of Science ®Google Scholar
• Gómez-Bruton, A., González-Agüero, A., Gómez-Cabello, A., Matute-Llorente, A., Casajús, J. A., & Vicente-Rodríguez, G. (2016). Swimming and bone: Is low bone mass due to hypogravity alone or does other physical activity influence it? Osteoporosis International, 27(5), 1785–1793. doi:10.1007/s00198-015-3448-8
   PubMed Web of Science ®Google Scholar
• Gomez-Bruton, A., Matute-Llorente, A., Gonzalez-Aguero, A., Casajus, J., & Vicente-Rodríguez, G. (2017). Plyometric exercise and bone health in children and adolescents: a systematic review. World Journal of Pediatrics. doi: 10.1007/s12519-016-0076-0
   PubMed Web of Science ®Google Scholar
• Gomez-Bruton, A., Montero-Marin, J., Gonzalez-Aguero, A., Garcia-Campayo, J., Moreno, L. A., & Casajus, J. A. (2015). The effect of swimming during childhood and adolescence on bone mineral density: A systematic review and meta-analysis. Sports Medicine (Auckland, N.Z.), 46(3), 365–379. doi:10.1007/s40279-015-0427-3
   Web of Science ®Google Scholar
• González-Agüero, A., Vicente-Rodríguez, G., Moreno, L. A., & Casajús, J. A. (2011). Bone mass in male and female children and adolescents with Down syndrome. Osteoporosis International, 22(7), 2151–2157. doi:10.1007/s00198-010-1443-7
   PubMed Web of Science ®Google Scholar
• Gracia-Marco, L., Moreno, L. A., Ortega, F. B., León, F., Sioen, I., & Kafatos, A. (2011). Levels of physical activity that predict optimal bone mass in adolescents: The HELENA study. American Journal of Preventive Medicine, 40(6), 599–607. doi:10.1016/j.amepre.2011.03.001
   PubMed Web of Science ®Google Scholar
• Guadalupe-Grau, A., Fuentes, T., Guerra, B., & Calbet, J. A. (2009). Exercise and bone mass in adults. Sports Medicine, 39(6), 439–468. doi:10.2165/00007256-200939060-00002
   PubMed Web of Science ®Google Scholar
• Guggenbuhl, P. (2009). Osteoporosis in males and females: Is there really a difference? Joint Bone Spine, 76(6), 595–601. doi:10.1016/j.jbspin.2009.10.001
   PubMed Web of Science ®Google Scholar
• Harvey, N., Dennison, E., & Cooper, C. (2013). The epidemiology of osteoporotic fractures. In C. J. Rosen (Ed.), Primer on the metabolic bone diseases and disorders of mineral metabolism (8th ed.). Ames: John Wiley & Sons, Inc. doi:10.1002/9781118453926.ch40
   Google Scholar
• Heaney, R. P., Abrams, S., Dawson-Hughes, B., Looker, A., Marcus, R., & Matkovic, V. (2000). Peak bone mass. Osteoporosis International, 11(12), 985–1009. doi:10.1007/s001980070020
   PubMed Web of Science ®Google Scholar
• Hedges, L. V., & Olkin, I. (1985). Statistical methods for meta analysis. Florida: Academic Press.
   Google Scholar
• Heinrich, C. H., Going, S. B., Pamenter, R. W., Perry, C. D., Boyden, T. W., & Lohman, T. G. (1990). Bone mineral content of cyclically menstruating female resistance and endurance trained athletes. Medicine & Science in Sports & Exercise, 22(5), 558–563. doi:10.1249/00005768-199010000-00003
   PubMed Web of Science ®Google Scholar
• Hernandez, C. J., Beaupre, G. S., & Carter, D. (2003). A theoretical analysis of the relative influences of peak BMD, age-related bone loss and menopause on the development of osteoporosis. Osteoporosis International, 14(10), 843–847. doi:10.1007/s00198-003-1454-8
   PubMed Web of Science ®Google Scholar
• Higgins, J. P., Altman, D. G., Gotzsche, P. C., Juni, P., Moher, D., & Oxman, A. D. (2011). The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. Bmj, 343, d5928. doi:10.1136/bmj.d5928
   PubMed Web of Science ®Google Scholar
• Higgins, J. P., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003). Measuring inconsistency in meta-analyses. Bmj, 327(7414), 557–560. doi:10.1136/bmj.327.7414.557
   PubMed Web of Science ®Google Scholar
• Hind, K., & Burrows, M. (2007). Weight-bearing exercise and bone mineral accrual in children and adolescents: A review of controlled trials. Bone, 40(1), 14–27. doi:10.1016/j.bone.2006.07.006
   PubMed Web of Science ®Google Scholar
• Hind, K., Gannon, L., Whatley, E., Cooke, C., & Truscott, J. (2012). Bone cross-sectional geometry in male runners, gymnasts, swimmers and non-athletic controls: A hip-structural analysis study. European Journal of Applied Physiology, 112(2), 535–541. doi:10.1007/s00421-011-2008-y
   PubMed Web of Science ®Google Scholar
• Hinton, P. S., Nigh, P., & Thyfault, J. (2015). Effectiveness of resistance training or jumping-exercise to increase bone mineral density in men with low bone mass: A 12-month randomized, clinical trial. Bone, 79, 203–212. doi:10.1016/j.bone.2015.06.008
   PubMed Web of Science ®Google Scholar
• Holick, M. F., Siris, E. S., Binkley, N., Beard, M. K., Khan, A., & Katzer, J. T. (2005). Prevalence of vitamin D inadequacy among postmenopausal North American women receiving osteoporosis therapy. The Journal of Clinical Endocrinology & Metabolism, 90(6), 3215–3224. doi:10.1210/jc.2004-2364
   PubMed Web of Science ®Google Scholar
• Johansson, C., Black, D., Johnell, O., Odén, A., & Mellström, D. (1998). Bone mineral density is a predictor of survival. Calcified Tissue International, 63(3), 190–196. doi:10.1007/s002239900513
   PubMed Web of Science ®Google Scholar
• Johnell, O., Kanis, J. A., Oden, A., Johansson, H., De Laet, C., & Delmas, P. (2005). Predictive value of BMD for hip and other fractures. Journal of Bone and Mineral Research, 20(7), 1185–1194. doi:10.1359/JBMR.050304
   PubMed Web of Science ®Google Scholar
• Kanemura, H., Hatakeyama, K., Sano, F., Yagasaki, H., Sugita, K., & Aihara, M. (2016). Effect of sunlight exposure on bone mineral density in children with severe disability. Neuropediatrics, 47(4), 233–237. doi:10.1055/s-00000041
   PubMed Web of Science ®Google Scholar
• Kemper, H. C., Twisk, J. W., Van Mechelen, W., Post, G. B., Roos, J. C., & Lips, P. (2000). A fifteen-year longitudinal study in young adults on the relation of physical activity and fitness with the development of the bone mass: The Amsterdam Growth and Health Longitudinal Study. Bone, 27(6), 847–853. doi:10.1016/S8756-3282(00)00397-5
   PubMed Web of Science ®Google Scholar
• Lee, E. J., Long, K. A., Risser, W. L., Poindexter, H. B. W., Gibbons, W. E., & Goldzieher, J. (1995). Variations in bone status of contralateral and regional sites in young athletic women. Medicine & Science in Sports & Exercise, 27(10), 1354–1361. doi:10.1249/00005768-199510000-00002
   PubMed Web of Science ®Google Scholar
• Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P. C., & Ioannidis, J. P. (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. Journal of Clinical Epidemiology, 62(10), e1–34. doi:10.1016/j.jclinepi.2009.06.006
   PubMed Web of Science ®Google Scholar
• Mackey, D. C., Lui, L. Y., Cawthon, P. M., Bauer, D. C., Nevitt, M. C., & Cauley, J. A. (2007). High-trauma fractures and low bone mineral density in older women and men. Jama, 298(20), 2381–2388. doi:10.1001/jama.298.20.2381
   PubMed Web of Science ®Google Scholar
• Magkos, F., Kavouras, S. A., Yannakoulia, M., Karipidou, M., Sidossi, S., & Sidossis, L. S. (2007). The bone response to non-weight-bearing exercise is sport-, site-, and sex-specific. Clinical Journal of Sport Medicine, 17(2), 123–128. doi:10.1097/JSM.0b013e318032129d
   PubMed Web of Science ®Google Scholar
• Magkos, F., Yannakoulia, M., Kavouras, S. A., & Sidossis, L. S. (2007). The type and intensity of exercise have independent and additive effects on bone mineral density. International Journal of Sports Medicine, 28(9), 773–779. doi:10.1055/s-2007-964979
   PubMed Web of Science ®Google Scholar
• Maimoun, L., Lumbroso, S., Manetta, J., Paris, F., Leroux, J. L., & Sultan, C. (2003). Testosterone is significantly reduced in endurance athletes without impact on bone mineral density. Hormone Research, 59(6), 285–292.
   PubMedGoogle Scholar
• Maïmoun, L., Mariano-Goulart, D., Couret, I., Manetta, J., Peruchon, E., & Micallef, J. P. (2004). Effects of physical activities that induce moderate external loading on bone metabolism in male athletes. Journal of Sports Sciences, 22(9), 875–883. doi:10.1080/02640410410001716698
   PubMed Web of Science ®Google Scholar
• Matkovic, V., Jelic, T., Wardlaw, G. M., Ilich, J. Z., Goel, P. K., & Wright, J. K. (1994). Timing of peak bone mass in Caucasian females and its implication for the prevention of osteoporosis. Inference from a cross-sectional model. The Journal of Clinical Investigation, 93(2), 799–808. doi:10.1172/JCI117034
   PubMed Web of Science ®Google Scholar
• Matsumoto, T., Nakagawa, S., Nishida, S., & Hirota, R. (1997). Bone density and bone metabolic markers in active collegiate athletes: Findings in long-distance runners, judoists, and swimmers. International Journal of Sports Medicine, 28(6), 408–412. doi:10.1055/s-2007-972656
   Google Scholar
• Morel, J., Combe, B., Francisco, J., & Bernard, J. (2001). Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporosis International, 12(2), 152–157. doi:10.1007/s001980170148
   PubMed Web of Science ®Google Scholar
• Morgan, A., & Weiss Jarrett, J. (2011). Markers of bone turnover across a competitive season in female athletes: A preliminary investigation. The Journal of Sports Medicine and Physical Fitness, 51(3), 515–524.
   PubMed Web of Science ®Google Scholar
• Mouratidou, T., Vicente-Rodriguez, G., Gracia-Marco, L., Huybrechts, I., Sioen, I., & Widhalm, K. (2013). Associations of dietary calcium, vitamin D, milk intakes, and 25-hydroxyvitamin D with bone mass in Spanish adolescents: The HELENA study. Journal of Clinical Densitometry, 16(1), 110–117. doi:10.1016/j.jocd.2012.07.008
   PubMed Web of Science ®Google Scholar
• Mudd, L. M., Fornetti, W., & Pivarnik, J. M. (2007). Bone mineral density in collegiate female athletes: Comparisons among sports. Journal of Athletic Training, 42(3), 403–408.
   PubMed Web of Science ®Google Scholar
• NIH. (2014). Quality assessment tool for observational cohort and cross-sectional studies. National Heart, Lung, and Blood Institute.
   Google Scholar
• Oja, P., Titze, S., Kokko, S., Kujala, U. M., Heinonen, A., & Kelly, P. (2015). Health benefits of different sport disciplines for adults: Systematic review of observational and intervention studies with meta-analysis. British Journal of Sports Medicine, 49(7), 434–440. doi:10.1136/bjsports-2014-093885
   PubMed Web of Science ®Google Scholar
• Olmedillas, H., González-Agüero, A., Moreno, L. A., Casajus, J. A., & Vicente-Rodríguez, G. (2012). Cycling and bone health: A systematic review. BMC Medicine, 10(1), 168. doi:10.1186/1741-7015-10-168
   PubMed Web of Science ®Google Scholar
• Peacock, M., Turner, C. H., Econs, M. J., & Foroud, T. (2002). Genetics of osteoporosis. Endocrine Reviews, 23(3), 303–326. doi:10.1210/edrv.23.3.0464
   PubMed Web of Science ®Google Scholar
• Risser, W. L., Lee, E. J., LeBlanc, A., Poindexter, H. B., Risser, J. M., & Schneider, V. (1990). Bone density in eumenorrheic female college athletes. Medicine & Science in Sports & Exercise, 22(5), 570–574. doi:10.1249/00005768-199010000-00005
   PubMed Web of Science ®Google Scholar
• Sadat-Ali, M., Al-Turki, A. H., Al-Ali, H. A., Al Elq, F. A., & Al-Mulhim, F. (2011). Influence of vitamin D levels on bone mineral density and osteoporosis. Annals of Saudi Medicine, 31(6), 602–608. doi:10.4103/0256-4947.87097
   PubMed Web of Science ®Google Scholar
• Taaffe, D. R., & Marcus, R. (1999). Regional and total body bone mineral density in elite collegiate male swimmers. The Journal of Sports Medicine and Physical Fitness, 39(2), 154–159.
   PubMed Web of Science ®Google Scholar
• Taaffe, D. R., Robinson, T. L., Snow, C. M., & Marcus, R. (1997). High-impact exercise promotes bone gain in well-trained female athletes. Journal of Bone and Mineral Research, 12(2), 255–260. doi:10.1359/jbmr.1997.12.2.255
   PubMed Web of Science ®Google Scholar
• Taaffe, D. R., Snow-Harter, C., Connolly, D. A., Robinson, T. L., Brown, M. D., & Marcus, R. (1995). Differential effects of swimming versus weight-bearing activity on bone mineral status of eumenorrheic athletes. Journal of Bone and Mineral Research, 10(4), 586–593. doi:10.1002/jbmr.5650100411
   PubMed Web of Science ®Google Scholar
• Tan, V. P., Macdonald, H. M., Kim, S., Nettlefold, L., Gabel, L., & Ashe, M. C. (2014). Influence of physical activity on bone strength in children and adolescents: A systematic review and narrative synthesis. Journal of Bone and Mineral Research, 29(10), 2161–2181. doi:10.1002/jbmr.2254
   PubMed Web of Science ®Google Scholar
• Tenforde, A. S., & Fredericson, M. (2011). Influence of sports participation on bone health in the young athlete: A review of the literature. Pm&R, 3(9), 861–867. doi:10.1016/j.pmrj.2011.05.019
   Web of Science ®Google Scholar
• Valimaki, M. J., Karkkainen, M., Lamberg-Allardt, C., Laitinen, K., Alhava, E., & Heikkinen, J. (1994). Exercise, smoking, and calcium intake during adolescence and early adulthood as determinants of peak bone mass. Cardiovascular Risk in Young Finns Study Group. Bmj, 309(6949), 230–235. doi:10.1136/bmj.309.6949.230
   PubMed Web of Science ®Google Scholar
• Valtuena, J., Gracia-Marco, L., Vicente-Rodriguez, G., Gonzalez-Gross, M., Huybrechts, I., & Rey-Lopez, J. P. (2012). Vitamin D status and physical activity interact to improve bone mass in adolescents. The HELENA Study. Osteoporosis International, 23(8), 2227–2237. doi:10.1007/s00198-011-1884-7
   PubMed Web of Science ®Google Scholar
• Velez, N. F., Zhang, A., Stone, B., Perera, S., Miller, M., & Greenspan, S. L. (2008). The effect of moderate impact exercise on skeletal integrity in master athletes. Osteoporosis International, 19(10), 1457–1464. doi:10.1007/s00198-008-0590-6
   PubMed Web of Science ®Google Scholar
• Vicente-Rodriguez, G. (2006). How does exercise affect bone development during growth? Sports Medicine, 36(7), 561–569. doi:10.2165/00007256-200636070-00002
   PubMed Web of Science ®Google Scholar
• Weeks, B. K., & Beck, B. R. (2008). The BPAQ: A bone-specific physical activity assessment instrument. Osteoporosis International, 19(11), 1567–1577. doi:10.1007/s00198-008-0606-2
   PubMed Web of Science ®Google Scholar
• Yeum, K.-J., Song, B. C., & Joo, N.-S. (2016). Impact of geographic location on vitamin D status and bone mineral density. International Journal of Environmental Research and Public Health, 13(2), 184. doi:10.3390/ijerph13020184
   PubMed Web of Science ®Google Scholar