Time-course of exercise and its association with 12-month bone changes

Riikka Ahola, Raija Korpelainen, Aki Vainionpää, Juhani Leppäluoto, Timo Jämsä, Riikka Ahola, Raija Korpelainen, Aki Vainionpää, Juhani Leppäluoto, Timo Jämsä

Abstract

Background: Exercise has been shown to have positive effects on bone density and strength. However, knowledge of the time-course of exercise and bone changes is scarce due to lack of methods to quantify and qualify daily physical activity in long-term. The aim was to evaluate the association between exercise intensity at 3, 6 and 12 month intervals and 12-month changes in upper femur areal bone mineral density (aBMD) and mid-femur geometry in healthy premenopausal women.

Methods: Physical activity was continuously assessed with a waist-worn accelerometer in 35 healthy women (35-40 years) participating in progressive high-impact training. To describe exercise intensity, individual average daily numbers of impacts were calculated at five acceleration levels (range 0.3-9.2 g) during time intervals of 0-3, 0-6, and 0-12 months. Proximal femur aBMD was measured with dual x-ray absorptiometry and mid-femur geometry was evaluated with quantitative computed tomography at the baseline and after 12 months. Physical activity data were correlated with yearly changes in bone density and geometry, and adjusted for confounding factors and impacts at later months of the trial using multivariate analysis.

Results: Femoral neck aBMD changes were significantly correlated with 6 and 12 months' impact activity at high intensity levels (> 3.9 g, r being up to 0.42). Trochanteric aBMD changes were associated even with first three months of exercise exceeding 1.1 g (r = 0.39-0.59, p < 0.05). Similarly, mid-femoral cortical bone geometry changes were related to even first three months' activity (r = 0.38-0.52, p < 0.05). In multivariate analysis, 0-3 months' activity did not correlate with bone change at any site after adjusting for impacts at later months. Instead, 0-6 months' impacts were significant correlates of 12-month changes in femoral neck and trochanter aBMD, mid-femur bone circumference and cortical bone attenuation even after adjustment. No significant correlations were found at the proximal or distal tibia.

Conclusion: The number of high acceleration impacts during 6 months of training was positively associated with 12-month bone changes at the femoral neck, trochanter and mid-femur. These results can be utilized when designing feasible training programs to prevent bone loss in premenopausal women.

Trial registration: Clinical trials.gov NCT00697957.

Figures

Figure 1
Figure 1
Correlation between daily number of high impacts at 0-6 months and 12-month trochanter aBMD change. A scatter plot between 0-6 month average daily numbers of impacts at 5.4-9.2 g and trochanteric BMD %-change. N = 34 (DXA data was missing from one subject). r = 0.54, p < 0.01.
Figure 2
Figure 2
Correlation between impact exercise at different time intervals and 12-month aBMD changes in proximal femur. Pearson's correlation coefficients (r) between the impact exercise at different acceleration levels in 0-3, 0-6 and 0-12 months, and yearly aBMD changes A) in the femoral neck, and B) trochanter. N = 34 (DXA data was missing from one subject), g = acceleration of gravity (9.81 m·s-2), * p < 0.05, ** p < 0.01 after Benjamini-Hochberg corrections, (*) the association did not remain significant after adjustment for impacts at later months in multivariate analysis.

References

    1. Barry DW, Kohrt WM. Exercise and the preservation of bone health. J Cardiopulm Rehabil Prev. 2008;28(3):153–162.
    1. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy. Osteoporosis prevention, diagnosis, and therapy. JAMA. 2001;285(6):785–795. doi: 10.1001/jama.285.6.785.
    1. Sievänen H, Kannus P. Physical activity reduces the risk of fragility fracture. PLoS Med. 2007;4(6):e222. doi: 10.1371/journal.pmed.0040222.
    1. Heinonen A, Kannus P, Sievänen H, Oja P, Pasanen M, Rinne M, Uusi-Rasi K, Vuori I. Randomised controlled trial of effect of high-impact exercise on selected risk factors for osteoporotic fractures. Lancet. 1996;348(9038):1343–1347. doi: 10.1016/S0140-6736(96)04214-6.
    1. Turner CH. Three rules for bone adaptation to mechanical stimuli. Bone. 1998;23(5):399–407. doi: 10.1016/S8756-3282(98)00118-5.
    1. Khan K, McKay H, Kannus P, Bailey D, Wark J, Bennell K. Physical activity and bone health. Campaign, IL, Human Kinetics; 2001. pp. 129–142.
    1. Wallace BA, Cumming RG. Systematic review of randomized trials of the effect of exercise on bone mass in pre- and postmenopausal women. Calcif Tissue Int. 2000;67(1):10–18. doi: 10.1007/s00223001089.
    1. Wolff I, van Croonenborg JJ, Kemper HC, Kostense PJ, Twisk JW. The effect of exercise training programs on bone mass: a meta-analysis of published controlled trials in pre- and postmenopausal women. Osteoporos Int. 1999;9(1):1–12. doi: 10.1007/s001980050109.
    1. Vainionpää A, Korpelainen R, Leppäluoto J, Jämsä T. Effects of high-impact exercise on bone mineral density: A randomized controlled trial in premenopausal women. Osteoporos Int. 2005;16(2):191–197. doi: 10.1007/s00198-004-1659-5.
    1. Vainionpää A, Korpelainen R, Sievänen H, Vihriälä E, Leppäluoto J, Jämsä T. Effect of impact exercise and its intensity on bone geometry at weight-bearing tibia and femur. Bone. 2007;40(3):604–611. doi: 10.1016/j.bone.2006.10.005.
    1. Vainionpää A, Korpelainen R, Vihriälä E, Rinta-Paavola A, Leppäluoto J, Jämsä T. Intensity of exercise is associated with bone density change in premenopausal women. Osteoporos Int. 2006;17(3):455–463. doi: 10.1007/s00198-005-0005-x.
    1. Heikkinen R, Vihriälä E, Vainionpää A, Korpelainen R, Jämsä T. Acceleration slope of exercise-induced impacts is a determinant of changes in bone density. J Biomech. 2007;40(13):2967–2974. doi: 10.1016/j.jbiomech.2007.02.003.
    1. Chen KY, Bassett DR Jr. The technology of accelerometry-based activity monitors: current and future. Med Sci Sports Exerc. 2005;37(11 Suppl):S490–500. doi: 10.1249/01.mss.0000185571.49104.82.
    1. Janz KF, Rao S, Baumann HJ, Schultz JL. Measuring children's vertical ground reaction forces with accelerometry during walking, running, and jumping: The Iowa bone development study. Pediatr Exerc Sci. 2003;15(1):34–43.
    1. Janz KF. Physical activity in epidemiology: moving from questionnaire to objective measurement. Br J Sports Med. 2006;40:191–192. doi: 10.1136/bjsm.2005.023036.
    1. Jämsä T, Vainionpää A, Korpelainen R, Vihriälä E, Leppäluoto J. Effect of daily physical activity on proximal femur. Clin Biomech. 2006;21(1):1–7. doi: 10.1016/j.clinbiomech.2005.10.003.
    1. Vihriälä E, Saarimaa R, Myllylä R, Jämsä T. A device for long term monitoring of impact loading on the hip. Mol Quant Acoust. 2003;24:211–224.
    1. Vihriälä E, Oksa J, Karkulehto J, Korpelainen R, Myllylä R, Jämsä T. Reliability of an accelerometer in the assessment of body movements. Technol Health Care. 2004;12:122–124.
    1. Korpelainen R, Keinänen-Kiukaanniemi S, Heikkinen J, Väänänen K, Korpelainen J. Effect of impact exercise on bone mineral density in elderly women with low BMD: a population-based randomized controlled 30-month intervention. Osteoporos Int. 2006;17(1):109–118. doi: 10.1007/s00198-005-1924-2.
    1. Jämsä T, Parviainen O, Salmela I, Pulkkinen P. Assessment of lower limb cross-sectional geometry using CT image analysis. Technol Health Care. 2004;12:111–113.
    1. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate - a Practical and Powerful Approach to Multiple Testing. J R Statist Soc B. 1995;57(1):289–300.
    1. Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann of Statist. 2001;29(4):1165–1188. doi: 10.1214/aos/1013699998.
    1. Bassey EJ, Ramsdale SJ. Increase in femoral bone density in young women following high-impact exercise. Osteoporos Int. 1994;4(2):72–75. doi: 10.1007/BF01623226.
    1. Bassey EJ, Rothwell MC, Littlewood JJ, Pye DW. Pre- and postmenopausal women have different bone mineral density responses to the same high-impact exercise. J Bone Miner Res. 1998;13(12):1805–1813. doi: 10.1359/jbmr.1998.13.12.1805.
    1. Kato T, Terashima T, Yamashita T, Hatanaka Y, Honda A, Umemura Y. Effect of low-repetition jump training on bone mineral density in young women. J Appl Physiol. 2006;100(3):839–843. doi: 10.1152/japplphysiol.00666.2005.
    1. Guadalupe-Grau A, Perez-Gomez J, Olmedillas H, Chavarren J, Dorado C, Santana A, Serrano-Sanchez JA, Calbet JA. Strength training combined with plyometric jumps in adults: sex differences in fat-bone axis adaptations. J Appl Physiol. 2009;106(4):1100–1111. doi: 10.1152/japplphysiol.91469.2008.
    1. Lohman T, Going S, Pamenter R, Hall M, Boyden T, Houtkooper L, Ritenbaugh C, Bare L, Hill A, Aickin M. Effects of resistance training on regional and total bone mineral density in premenopausal women: a randomized prospective study. J Bone Miner Res. 1995;10(7):1015–1024.
    1. Winters KM, Snow CM. Detraining reverses positive effects of exercise on the musculoskeletal system in premenopausal women. J Bone Miner Res. 2000;15(12):2495–2503. doi: 10.1359/jbmr.2000.15.12.2495.
    1. Heinonen A, Kannus P, Sievänen H, Pasanen M, Oja P, Vuori I. Good maintenance of high-impact activity-induced bone gain by voluntary, unsupervised exercises: An 8-month follow-up of a randomized controlled trial. J Bone Miner Res. 1999;14(1):125–128. doi: 10.1359/jbmr.1999.14.1.125.
    1. Winters-Stone KM, Snow CM. Site-specific response of bone to exercise in premenopausal women. Bone. 2006;39(6):1203–1209. doi: 10.1016/j.bone.2006.06.005.
    1. Friedlander AL, Genant HK, Sadowsky S, Byl NN, Gluer CC. A two-year program of aerobics and weight training enhances bone mineral density of young women. J Bone Miner Res. 1995;10(4):574–585.
    1. Karagiannis A, Papakitsou E, Dretakis K, Galanos A, Megas P, Lambiris E, Lyritis GP. Mortality rates of patients with a hip fracture in a southwestern district of Greece: ten-year follow-up with reference to the type of fracture. Calcif Tissue Int. 2006;78(2):72–77. doi: 10.1007/s00223-005-0169-6.
    1. Keene GS, Parker MJ, Pryor GA. Mortality and morbidity after hip fractures. BMJ. 1993;307(6914):1248–1250. doi: 10.1136/bmj.307.6914.1248.
    1. Lauretani F, Bandinelli S, Griswold ME, Maggio M, Semba R, Guralnik JM, Ferrucci L. Longitudinal changes in BMD and bone geometry in a population-based study. J Bone Miner Res. 2008;23(3):400–408. doi: 10.1359/jbmr.071103.
    1. Vondracek SF, Hansen LB, McDermott MT. Osteoporosis risk in premenopausal women. Pharmacotherapy. 2009;29(3):305–317. doi: 10.1592/phco.29.3.305.
    1. Ammann P, Rizzoli R. Bone strength and its determinants. Osteoporos Int. 2003;14(Suppl 3):S13–18.
    1. Heinonen A, Sievänen H, Kannus P, Oja P, Vuori I. Site-specific skeletal response to long-term weight training seems to be attributable to principal loading modality: a pQCT study of female weightlifters. Calcif Tissue Int. 2002;70(6):469–474. doi: 10.1007/s00223-001-1019-9.
    1. Nikander R, Sievänen H, Uusi-Rasi K, Heinonen A, Kannus P. Loading modalities and bone structures at nonweight-bearing upper extremity and weight-bearing lower extremity: a pQCT study of adult female athletes. Bone. 2006;39(4):886–894. doi: 10.1016/j.bone.2006.04.005.
    1. Nikander R, Sievänen H, Heinonen A, Karstila T, Kannus P. Load-specific differences in the structure of femoral neck and tibia between world-class moguls skiers and slalom skiers. Scand J Med Sci Sports. 2008;18(2):145–153.
    1. Haapasalo H, Kontulainen S, Sievänen H, Kannus P, Järvinen M, Vuori I. Exercise-induced bone gain is due to enlargement in bone size without a change in volumetric bone density: a peripheral quantitative computed tomography study of the upper arms of male tennis players. Bone. 2000;27(3):351–357. doi: 10.1016/S8756-3282(00)00331-8.
    1. Carter DR, Meulen MC Van Der, Beaupre GS. Mechanical factors in bone growth and development. Bone. 1996;18(1 Suppl):5S–10S. doi: 10.1016/8756-3282(95)00373-8.
    1. Turner CH, Robling AG. Designing exercise regimens to increase bone strength. Exerc Sport Sci Rev. 2003;31(1):45–50. doi: 10.1097/00003677-200301000-00009.
    1. Seeman E. The periosteum--a surface for all seasons. Osteoporos Int. 2007;18(2):123–128. doi: 10.1007/s00198-006-0296-6.
    1. Adami S, Gatti D, Braga V, Bianchini D, Rossini M. Site-specific effects of strength training on bone structure and geometry of ultradistal radius in postmenopausal women. J Bone Miner Res. 1999;14(1):120–124. doi: 10.1359/jbmr.1999.14.1.120.
    1. Hsieh YF, Robling AG, Ambrosius WT, Burr DB, Turner CH. Mechanical loading of diaphyseal bone in vivo: the strain threshold for an osteogenic response varies with location. J Bone Miner Res. 2001;16(12):2291–2297. doi: 10.1359/jbmr.2001.16.12.2291.
    1. Skerry TM. One mechanostat or many? Modifications of the site-specific response of bone to mechanical loading by nature and nurture. J Musculoskelet Neuronal Interact. 2006;6(2):122–127.
    1. Turner CH. Toward a mathematical description of bone biology: The principle of cellular accommodation. Calcif Tissue Int. 1999;65:466–471. doi: 10.1007/s002239900734.
    1. Lanyon LE. Using functional loading to influence bone mass and architecture: objectives, mechanisms, and relationship with estrogen of the mechanically adaptive process in bone. Bone. 1996;18(1 Suppl):37S–43S. doi: 10.1016/8756-3282(95)00378-9.
    1. Judex S, Gross TS, Zernicke RF. Strain gradients correlate with sites of exercise-induced bone-forming surfaces in the adult skeleton. J Bone Miner Res. 1997;12(10):1737–1745. doi: 10.1359/jbmr.1997.12.10.1737.
    1. Sievänen H. A physical model for dual-energy X-ray absorptiometry--derived bone mineral density. Invest Radiol. 2000;35(5):325–330. doi: 10.1097/00004424-200005000-00007.
    1. Bolotin HH, Sievänen H. Inaccuracies inherent in dual-energy X-ray absorptiometry in vivo bone mineral density can seriously mislead diagnostic/prognostic interpretations of patient-specific bone fragility. J Bone Miner Res. 2001;16(5):799–805. doi: 10.1359/jbmr.2001.16.5.799.
    1. Cullen DM, Smith RT, Akhter MP. Time course for bone formation with long-term external mechanical loading. J Appl Physiol. 2000;88(6):1943–1948.
    1. Vainionpää A, Korpelainen R, Väänänen HK, Haapalahti J, Jämsä T, Leppäluoto J. Effect of impact exercise on bone metabolism. Osteoporos Int. 2009;20(10):1725–1733. doi: 10.1007/s00198-009-0881-6.

Source: PubMed

Sponsorer och medarbetare

Medicinska tillstånd

Läkemedelsinterventioner

3
Prenumerera