During childhood and adolescence it is clear that the mechanical component of physical activity effects adap- tations in the growing skeleton. The increases in bone mass (BMD) are relatively modest, between 1 and 5%, but may be manifested by geometric adaptations that 90 x 4
360 x 1 BLC
* ** * ** ** ** * * ** * * * *
* * * 200
150 100 50 0 –50
–100 0 5 10 15 20 25 30 35
Slice number (from proximal end) in 1 mm increments
% Difference (R versus L) in Imin
Fig. 19.2. When daily loading was divided into 4 bouts of 90 cycles per day, instead of a single bout of 360 cycles, ulnas showed significantly greater increases in the geometric property responsible for resistance to bending (CSMI). The graph illus- trates the difference between loaded and unloaded limbs (%) for the CSMI of loaded animals, age‐matched controls (AMC), and baseline controls (BLC). Source: [40]. Reproduced with permis- sion from Elsevier.
Bending load
Torsional load
Original
X-section Adapted
X-section
Tissue adaptation
F F
CSMI
J
Fig. 19.3. The aim of skeletal adaptation is not to increase bone mass per se, but to improve resistance to increased loads efficiently. Increased strength is therefore achieved without jeopardizing lightness. Modeling on appropriate bone surfaces improves the biomechanical determinants for enhanced bend- ing or torsional strength (CSMI), or polar moment of inertia (J), respectively. These changes improve bending and torsional strength, disproportionately to the change in BMC or BMD, and hence can be misinterpreted by DXA. Source: [1]. Reproduced with permission from Springer.
144 Mechanical Loading and the Developing Skeleton
augment bone strength by a significantly greater degree.
It is practically impossible to prove that the adaptations of childhood prevent osteoporotic fracture in old age.
Confounding variables associated with retrospective studies, such as self‐selection for physique, reduce the certainty that a given activity created long‐lasting skeletal protection. But a small number of studies have now traversed childhood and followed adolescents into adulthood. Early studies of this phenomenon suggested that the gains in bone mass from childhood training were lost in adulthood [52,53]. Some of these studies were cross‐sectional, or started relatively late in adolescence, when it is harder to control for confounding variables such as maturity. Longitudinal studies from childhood, through adolescence, report a sustained effect on BMC accrual up to 14 years after training, or cessation of a physical activity intervention [41,54,55] (Fig. 19.4). In addition physically active children achieve greater bone mass (BMC) during adolescence than their sedentary peers [20,22], and their higher BMC is maintained into adulthood [56].
Retention of childhood bone mass into adulthood may be modest but preservation of skeletal architecture and geometry, underlying bone strength, could be more sig- nificant. The distinction between preservation of bone mass or architecture is elegantly illustrated by lifelong preservation of adapted bone structure after short‐term exercise in rapidly growing rodents [57]. Forearm training started at 5 weeks of age, with a short 7‐week exercise program, following which animals were limited to cage activity for up to 92 weeks (2 years of age, equivalent to senescence for rodents). Increases in bone mass induced by exercise (aBMD and BMC) were not retained into adulthood but there was long‐term preservation of bone structural changes, which was manifested in superior strength and fatigue life in the trained
animals [57]. Similar retention of exercise‐induced struc- tural adaptation from childhood has been observed following cessation of gymnastics [55] and racquet sports in male and female tennis players who had started train- ing during childhood (about 10 years of age) [58,59]. Up to 3 years after retirement a greater bone mass was retained at the age of 30, modeled into an architecture that pro- vided greater indices of bone strength, such as cortical area and CSMI. These data support the argument that physical activity during childhood can effect structural adaptations in the skeleton that persist well into adult- hood. The greater strength afforded by these structural changes could reduce the risk of fracture in adults, more than that predicted by bone mass alone.
CONCLUSION
Compared to adults, the skeleton of children and adoles- cents is capable of greater structural adaptations in response to the mechanical stimulus of physical activity.
The evidence is persuasive that the peripubertal period is more advantageous to effect adaptive responses. To grow healthy bones, physical activity should not consist of static or isometric exercises, but should incorporate repetitive cyclical loads that include a range of strain magnitudes and directions, such as running and jumping.
Because only a few cycles of loading are required to elicit an adaptive response, distributed bouts of loading that incorporate rest periods are more osteogenic than single sessions of long duration. These parameters of loading have been translated into feasible public health interven- tions that have achieved improved bone mass and strength in children and adolescents. Those architectural adaptations can persist into adulthood and be translated into a lower risk of fracture.
REFERENCES
1. Forwood MR. Mechanical effects on the skeleton: are there clinical implications? Osteoporos Int. 2001;12:77–83.
2. Heinonen A, Sievänen H, Kannus P, et al. High‐impact exercise and bones of growing girls: a 9‐month controlled trial. Osteoporos Int. 2000;11:1010–17.
3. Forwood MR, Burr DB. Physical activity and bone mass:
exercises in futility? Bone Miner. 1993;21:89–112.
4. Jarvinen TL, Pajamaki I, Sievanen H, et al. Femoral neck response to exercise and subsequent deconditioning in young and adult rats. J Bone Miner Res. 2003;18:1292–9.
5. Rantalainen T, Weeks BK, Nogueira RC, et al. Effects of bone‐specific physical activity, gender and maturity on tibial cross‐sectional bone material distribution: a cross‐
sectional pQCT comparison of children and young adults aged 5‐29 years. Bone 2015;72:101–8.
6. Rubin CT, Bain SD, McLeod KJ. Suppression of the osteo- genic response in the aging skeleton. Calcif Tissue Int.
1992;50:306–13.
Change in hip BMC (%) from controls 0
2.0 4.0
48 60 72
0 12 36
Months following training
80
Fig. 19.4. Results of a school‐based jumping intervention for 7 months in children aged ~8 years [41]. At the end of the 7‐month program (0 months), hip BMC was significantly greater than controls (3.6%). When followed for up to 8 years of detrain- ing, the exercise group retained greater hip BMC (1.4%) after controlling for baseline age and change in height, weight, and sports participation [54]. Source: adapted from [41,54].
7. Turner CH, Takano Y, Owan I. Aging changes mechani- cal loading thresholds for bone formation in rats. J Bone Miner Res. 1995;10:1544–9.
8. Kannus P, Haapasalo H, Sankelo M, et al. Effect of start- ing age of physical activity on bone mass in the domi- nant arm of tennis and squash players. Ann Intern Med.
1995;123:27–31.
9. Kontulainen S, Sievanen H, Kannus P, et al. Effect of long‐term impact‐loading on mass, size, and estimated strength of humerus and radius of female racquet‐sports players: a peripheral quantitative computed tomography study between young and old starters and controls.
J Bone Miner Res. 2002;17:2281–9.
10. Ferrari S, Rizzoli R, Slosman D, et al. Familial resem- blance for bone mineral mass is expressed before puberty.
J Clin Endocrinol Metab. 1998;83:358–61.
11. Hui SL, Slemenda CW, Johnston CC. The contribution of bone loss to post menopausal osteoporosis. Osteoporos Int. 1990;1:30–4.
12. Faulkner RA, Bailey DA. Osteoporosis: a pediatric concern? In: Daly RM, Petit MA (eds) Optimizing one Mass and Strength: The Role of hysical Activity and Nutrition During Growth. Vol. 51, Medicine and Sport Science. Karger, 2007, pp. 1–12.
13. Bachrach LK, Hastie T, Wang M‐C, et al. Bone mineral acquisition in healthy Asian, Hispanic, Black and Caucasian youth: A longitudinal study. J Clin Endocrinol Metab. 1999;84:4702–12.
14. Faulkner RA, Bailey DA, Drinkwater DT, et al. Bone densitometry in Canadian children 8‐17 years of age.
Calcif Tissue Int. 1996;59:344–51.
15. Recker EE, Davies KM, Hinders SM, et al. Bone gain in young adult women. JAMA 1992;268:2403–8.
16. Baxter‐Jones ADG, Faulkner RA, Forwood MR, et al.
Bone mineral accrual from 8 to 30 years of age: An esti- mation of peak bone mass. J Bone Miner Res. 2011;26:
1729–39.
17. Arlot M, Sornay‐Rendu E, Garnero P, et al. Apparent pre‐
and postmenopausal bone loss evaluated by DXA at dif- ferent skeletal sites in women: The OFELY cohort. J Bone Miner Res. 1997;12:683–90.
18. Macdonald HM, Kontulainen SA, Khan KM, et al. Is a school‐based physical activity intervention effective for increasing tibial bone strength in boys and girls? J Bone Miner Res. 2007;22:434–46.
19. Sundberg M, Gardsell P, Johnell O, et al. Peripubertal moderate exercise increases bone mass in boys but not in girls: a population‐based intervention study. Osteoporos Int. 2001;12:230–8.
20. Bailey DA, McKay HA, Mirwald RL, et al. A six‐year longitudinal study of the relationship of physical activity to bone mineral accrual in growing children: the univer- sity of Saskatchewan bone mineral accrual study. J Bone Miner Res. 1999;14:1672–9.
21. Bradney M, Pearce G, Naughton G, et al. Moderate exercise during growth in prepubertal boys: changes in bone mass, size, volumetric density, and bone strength:
a controlled prospective study. J Bone Miner Res.
1998;13:1814–21.
22. Forwood MR, Baxter‐Jones AD, Beck TJ, et al. Physical activity and strength of the proximal femur during the adolescent growth spurt: a longitudinal analysis. Bone.
2006;38:576–83.
23. Kannus P, Haapasalo H, Sankelo M, et al. Effect of start- ing age of physical activity on bone mass in the domi- nant arm of tennis and squash players. Ann Intern Med.
1995;123:27–31.
24. MacDonald HM, Kontulainen S, Petit M, et al. Does a novel school‐based physical activity model benefit fem- oral neck bone strength in pre‐ and early pubertal chil- dren? Osteoporos Int. 2008;9:1445–56.
25. Mackelvie KJ, McKay HA, Khan KM, et al. A school‐
based exercise intervention augments bone mineral accrual in early pubertal girls. J Pediatr. 2001;139:
501–8.
26. MacKelvie KJ, Petit MA, Khan KM, et al. Bone mass and structure are enhanced following a 2‐year randomized controlled trial of exercise in prepubertal boys. Bone.
2004;34:755–64.
27. Petit MA, McKay HA, MacKelvie KJ, et al. 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. 2002;17:363–72.
28. Damien E, Price JS, Lanyon LE. Mechanical strain stim- ulates osteoblast proliferation through the estrogen receptor in males as well as females. J Bone Miner Res.
2000;15:2169–77.
29. Zaman G, Jessop HL, Muzylak M, et al. Osteocytes use estrogen receptor alpha to respond to strain but their ERalpha content is regulated by estrogen. J Bone Miner Res. 2006;21:1297–306.
30. Hert J, Liskova M, Landa J. Reaction of bone to mechani- cal stimuli. 1. Continuous and intermittent loading of tibia in rabbit. Folia Morphol (Praha). 1971;19:290–300.
31. Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am. 1984;66:
397–402.
32. Turner CH, Owan I, Takano Y. Mechanotransduction in bone: role of strain rate. Am J Physiol 1995;269:
E438–42.
33. Robling AG, Duijvelaar KM, Geevers JV, et al.
Modulation of appositional and longitudinal bone growth in the rat ulna by applied static and dynamic force. Bone. 2001;29:105–13.
34. Turner C, Forwood M, Rho J, et al. Mechanical Loading Thresholds for Lamellar and Woven Bone Formation. J Bone Miner Res. 1994;9:87–97.
35. O’Connor JA, Lanyon LE, MacFie H. The influence of strain rate on adaptive bone remodelling. J Biomech.
1982;15:767–81.
36. Turner CH, Forwood MR, Otter MW. Mechanotransduction in bone: do bone cells act as sensors of fluid flow? Faseb J.
1994;8:875–8.
37. Rubin CT, Lanyon LE. Kappa Delta Award paper.
Osteoregulatory nature of mechanical stimuli: function as a determinant for adaptive remodeling in bone.
J Orthop Res. 1987;5:300–10.
146 Mechanical Loading and the Developing Skeleton 38. Rubin CT, Lanyon LE. Regulation of bone mass by
mechanical strain magnitude. Calcif Tissue Int.
1985;37:411–17.
39. 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;15:1596–602.
40. Robling AG, Hinant FM, Burr DB, et al. Improved bone structure and strength after long‐term mechanical load- ing is greatest if loading is separated into short bouts.
J Bone Miner Res. 2002;17:1545–54.
41. Fuchs RK, Bauer JJ, Snow CM. Jumping improves hip and lumbar spine bone mass in prepubescent children:
a randomized controlled trial. J Bone Miner Res.
2001;16:148–56.
42. McKay HA, MacLean L, Petit M, et al. “Bounce at the Bell”: a novel program of short bouts of exercise improves proximal femur bone mass in early pubertal children. Br J Sports Med. 2005;39:521–6.
43. Linden C, Ahlborg HG, Besjakov J, et al. A school cur- riculum‐based exercise program increases bone mineral accrual and bone size in prepubertal girls: two‐year data from the pediatric osteoporosis prevention (POP) study.
J Bone Miner Res. 2006;21:829–35.
44. Weeks BK, Young CM, Beck BR. Eight months of regular in‐school jumping improves indices of bone strength in adolescent boys and girls: the POWER PE study. J Bone Miner Res. 2008;23:1002–11.
45. Faulkner RA, Forwood MR, Beck TJ, et al. Strength indices of the proximal femur and shaft in prepubertal female gymnasts. Med Sci Sports Exerc. 2003;35:513–8.
46. Erlandson MC, Kontulainen SA, Chilibeck PD, et al.Bone mineral accrual in 4‐ to 10‐year‐old precom- petitive, recreational gymnasts: a 4‐year longitudinal study. J Bone Miner Res. 2011;26:1313–20.
47. Turner CH, Robling AG. Designing exercise regimens to increase bone strength. Exerc Sport Sci Rev. 2003;31:
45–50.
48. MacKelvie KJ, McKay HA, Petit MA, et al. Bone mineral response to a 7‐month randomized controlled, school‐
based jumping intervention in 121 prepubertal boys:
associations with ethnicity and body mass index. J Bone Miner Res. 2002;17:834–44.
49. Prentice A, Parsons TJ, Cole TJ. Uncritical use of bone mineral density in absorptiometry may lead to size‐
related artifacts in the identification of bone mineral determinants. Am J Clin Nutr. 1994;60:837–2.
50. Daly RM, Saxon L, Turner CH, et al. The relationship between muscle size and bone geometry during growth and in response to exercise. Bone. 2004;34:281–7.
51. Macdonald HM, Cooper DM, McKay HA. Anterior‐pos- terior bending strength at the tibial shaft increases with physical activity in boys: evidence for non‐uniform geo- metric adaptation. Osteoporos Int. 2009;20:61–70.
52. Karlsson MK, Linden C, Karlsson C, et al. Exercise dur- ing growth and bone mineral density and fractures in old age. Lancet. 2000;355:469–70.
53. Nordström A, Olsson T, Nordström P. Bone gained from physical activity and lost through detraining: a longitu- dinal study in young males. Osteoporos Int. 2004;16:
835–41.
54. Gunter K, Baxter‐Jones AD, Mirwald RL, et al. Impact exercise increases BMC during growth: an 8‐year longi- tudinal study. J Bone Miner Res. 2008;23:986–93.
55. Erlandson MC, Kontulainen SA, Chilibeck PD, et al.
2012 Higher premenarcheal bone mass in elite gymnasts is maintained into young adulthood after long‐term retirement from sport: a 14‐year follow‐up. J Bone Miner Res. 2012;27:104–10.
56. Jackowski SA, Kontulainen SA, Cooper DM, et al.
Adolescent physical activity and bone strength at the proximal femur in adulthood. Med Sci Sports Exerc.
2014;46:736–44.
57. Warden SJ, Fuchs RK, Castillo AB, et al.Exercise when young provides lifelong benefits to bone structure and strength. J Bone Miner Res. 2007;22:251–9.
58. Haapasalo H, Kontulainen S, Sievanen H, et al. 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;27:351–7.
59. Kontulainen S, Kannus P, Haapasalo H, et al. Good main- tenance of exercise‐induced bone gain with decreased training of female tennis and squash players: a prospec- tive 5‐year follow‐up study of young and old starters and controls. J Bone Miner Res. 2001;16:195–201.
147
Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism, Ninth Edition. Edited by John P. Bilezikian.
© 2019 American Society for Bone and Mineral Research. Published 2019 by John Wiley & Sons, Inc.
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