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Die Deutsche Zeitschrift für Sportmedizin behandelt die klinische Praxis und deren angrenzende Felder im Sinne translationaler Forschung, die den Einfluss von körperlicher Aktivität, Bewegung, Training und Sport sowie Bewegungsmangel von gesunden Personen und Patienten aller Altersgruppen erforscht. Dies umfasst die Auswirkungen von Prävention, Diagnose, Therapie, Rehabilitation und körperlichem Training sowie das gesamte Feld der Sportmedizin und sportwissenschaftliche, physiologische und biomechanische Forschung.

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100 Jahre Deutsche Sportmedizin
ÜBERSICHT
SPORTS AND EXERCISE ON OSTEOPOROSIS AND FRACTURE RISK

Therapeutic and Prophylactic Effects of Sports and Exercise on Osteoporosis and Fracture Risk

Therapeutische und prophylaktische Effekte von Sport und Training bei Osteoporose und Fraktur Risiko

ZUSAMMENFASSUNG

Osteoporose kann entweder durch reduzierten Knochenaufbau oder erhöhten altersbedingten Knochenabbau verursacht werden. Im Gegensatz zu den Ursachen des Knochenabbaus, die seit längerer Zeit untersucht werden, hat die Forschung nach  Mechanismen  des  Knochenaufbaus  erst  in  den  vergangenen  zehn  Jahren begonnen. Die gängige Lehrmeinung derzeit besagt, dass die Kindheits- und Jugendjahre  entscheidend  für  den  Aufbau  der  Knochendichte  sind.  Desweiteren haben Lebensgewohnheiten, wie z.B. körperliche Aktivität einen entscheidenden Einfluss  auf  die  Knochendichte.  Mechanische  Beanspruchungen  haben  sich  als effektive Reize für den Erhalt und Aufbau der Knochendichte und Knochenstärke  erwiesen.  Knochendichte  sowie  Knochenstärke  können  entscheidend  in  der späten  prä-pubertären  Phase  sowie  auch  in  der  frühen  peri-pubertären  Phase durch körperliches Training verbessert werden. Es gibt Studien die belegen,dass eine Erhöhung der Knochendichte durch mechanische Belastungen während der Wachstumsphasen bei Kindern und Jugendlichen im Alter weitgehend erhalten bleiben, auch bei einem geringeren Umfang körperlicher Aktivität. Untersuchungen zeigen, dass frühere männliche Leistungssportler ein geringeres Frakturrisiko aufweisen im Vergleich zu nicht-Leistungssportlern der gleichen Altersgruppen. Diese Befunde sprechen dafür, dass körperliche Aktivität bei Kindern und Jugendlichen während der Wachstumsphasen empfohlen werden sollte, unter anderem um das Frakturrisiko im Alter zu reduzieren.

Schlüsselwörter: Sportliches  Training,  Knochendichte,  BMD,  Knochenaufbau, Fraktur.

SUMMARY

Osteoporosis and low bone strength in older people may be due to low bone mass accrual  or  elevated  age-related  loss  of  bone  mass.  The  mechanisms  underlying loss of bone mass have long been subjected to research. However, research has only started in the last decade to focus on strategies to increase bone mass.The current opinion is that childhood and adolescence are critical periods for building up bone mineral density. It is also known that life style factors, such as physical activity,  may  influence  the  accrual  of  bone  mineral  density.  Mechanical  loading has been shown to be one of the best stimuli to enhance not only bone mass but also  structural  skeletal  adaptations,  both  independently  contributing  to  bone strength. Exercise prescription also includes a window of opportunity to improve  bone  strength  in  the  late  pre-  and  early  peri-pubertal  period.  There  is  some evidence supporting the notion that gains inbone mass obtained by mechanical loading during growth are maintained at older age despite reduction of physical activity in adulthood. The notion that former male athletes have a lower fracture risk compared to non-athlets of the same age suggests that physical activity during  growth  and  adolescence  should  be  recommended  as  a  feasible  strategy  to reduce the future incidence of fragility fractures.

Key words: Physical activity, bone mass, BMD, bone structure, fractures.

ADAPTIVE RESPONSEOF BONE TO LOADING

Key  features  for  osteogenic  stimuli  include  load  that  is  dynamic, have a high magnitude, a high frequency and unusually distributed strains, where the required mechanical loading necessary to stimulate osteogenesis decreases as the strain magnitude and frequency increases (30). However, the osteogenic response to high magnitude loading becomes saturated after a few loading cycles (28) where after additional loading confers limited benefit (32). But, bone cell mechanosensitivity seems to recover following rest so that separating loading into short bouts with periods of rest in between optimises the  osteogenic  response  (26).  That  is,  the  loading  characteristics associated with an improvement in bone strength are very specific, making the general prescription of exercise for cardiovascular health  or  weight  management  unsuitable  for  skeletal  health.  Studies have also shown that the osteogenic response is maturity and gender dependent (8, 15) so that a stronger response to mechanical stimuli, predominantly occur during growth especially in the pre- or early pubertal period (8, 9, 15, 20). In adulthood, prospective studies have shown that physical activity can reduce age related bone loss or at best produce increments in bone mineral density (BMD) of a few percentage points (4, 12). These benefits are much lower than the ones obtained by physical activity during growth and of questionable biological significance. The reported lower fracture incidence in physically active elderly is therefore probably the result of nonskeletal  effects  such  as  increased  muscle  strength  and  improved neuromuscular function. As the aim of this review was to evaluate exercise as prophylaxis and treatment of osteoporosis and fragility fractures, it focuses on effects of physical activity during growth and if exercise induced skeletal effects are retained at older ages.

PHYSICAL ACTIVITY AND THE SKELETON AT GROWTH

Physical activity enhances bone mineral accrual especially during the first two decades in life and a variety of reports have inferred practice of high impact sports such as tennis, squash, gymnastics and soccer to be associated with higher BMD than expected while practice  of  endurance  sports  such  as  running,  cycling  and  swimming show less promising results (17). For example, young female gymnasts have a 30 to 85% more rapidly increase in BMD than sedentary children (2) and young tennis players display 10- 15% arms side-to-side difference in BMD in comparison with lower than 5% difference in age-matched controls (3, 15). Studies in children have also shown that exercise intervention provided as education classes or exercise additional to regular physical education classes with up to 5 years of follow-up is associated with skeletal benefits but of a lower magnitude than in athletes (6, 9, 20). The interventions have in these studies in general resulted in up to 5% greater increase in BMD at mechanically loaded sites. Such benefits should however not be underestimated as small increase in bone mass can generate a  more  than  two-fold  increase  in  bone  strength  (27).  In  addition, today  we  know  that  these  interventions  can  be  initiated  without an increased rate of childhood fractures (9, 20), an adverse effect that have been reported to follow high level of physical activity, as a result of a higher exposure to trauma (7, 31).

The  prepubertal  skeleton  seems  to  have  the  capacity  to  respond  to  loading  by  adding  more  bone  on  the  periosteal  surface than  would  normally  occur  through  growth-induced  periosteal apposition  (10, 21).  But  studies  also  infer  that  there  is  an  endosteal  apposition  in  pre-pubertal  boys  as  a  response  to  mechanical loading (7, 21). Such a response is less obvious in pre-pubertal girls (3, 34).  Exercise  in  late  puberty  is  therefore  associated  with  bone apposition on the endosteal surface, as shown in female tennis players  (3)  and  the  enlargement  of  bone  size  in  response  to  loading has been reported to increase from pre- to peri-puberty in male but not in female tennis players (3, 21). The effects of physical activity on periosteal apposition (bone size) are also translated to a greater increases in bone strength than an increase in bone mass alone (3, 11, 19). Bone size is for example 10% larger in upper limbs of young pre-pubertal gymnasts than in normo active children (10, 34) as is the arms side-to-side difference in young pre-pubertal tennis players  (3, 21).  But  bone  may  also  be  laid  down  on  the  endosteal surface  so  that  cortical  thickness  increases  and  there  are  reports that infer cortical cross-sectional area to be 5 to 12% greater in the lower  limbs  of  young  runners  and  young  gymnasts  compared  to controls in spite of having the same bone size (34). The endosteal apposition is however less beneficial than a periosteal apposition since the bone resistance to bending increases by the forth power of the radius (29).
The  osteogenic  response  in  the  upper  and  lower  limbs  are site-specific  (13, 34)  and  endosteal  apposition  has  been  found  at the 60- 70% distal humerus but not at the 40- 50% mid humerus in young tennis players (3, 8, 14). There is also a different response to mechanical loading in anterior-posterior compared to the mediallateral direction and in the proximal, mid-diaphysis or distal part of a long bones (3, 8, 11, 13, 14, 27, 34). But increased bone strength could also be derived by redistribution of bone mass to areas submitted to high mechanical strains. Bone strength could thus be increased by changing the shape of the bone without an associated increase in bone mass or bone size, an adaptive model that have been reported in several human studies (14, 22). That is, the effects of mechanical stimuli must be evaluated in a region specific and gender specific fashion in relation to the applied loading histories and loading magnitudes.

ARE BONE MASS BENEFITS GAINED DURING GROWTH PRESERVED WITH CESSATION OF EXERCISE?

Hypothetically it seems less likely that exercise-induced skeletal benefits obtained during growth are maintained into late adulthood as the mechanostat-theory indicates a decrease in bone strength as a response to reduced level of physical activity. Prospective studies infer that there is a larger BMD loss with retirement from exercise so that a BMD benefit of 1.0- 1.5 SD during active career is transferred to a benefit of 0.5- 1.0 SD after 5- 10 years after reduced activity level (2, 23, 33) and a non significant 0.3 standard deviation (SD) lower leg BMD 4- 5 decades after retirement (16) (Figure 1). However, there is now also prospective, controlled study data that infer exercise induced benefits in BMD to be retained also after long term retirement. Male athletes aged 53- 79 years and retired from sports for a mean 30 years still had higher BMD than expected by age (31) (Figure 2). If so, this would hypothetically be transferred to a reduced incidence of fragility fractures.

ARE BONE STRUCTURAL BENEFITS GAINED DURING GROWTH PRESERVED WITH CESSATION OF EXERCISE?

As  the  mature  skeleton  is  thought  to  loose  bone  mass  essentially through remodelling on the endosteal envelope, and to a much lower extent on the periosteal envelope (25), the structural adaptations  obtained  by  physical  activity  during  growth  (8, 9, 20)  may be better preserved (16) than bone mass. This would be of clinical importance as bone structure contributes to the skeletal resistance to  fractures  independently  of  bone  mass  (1).  Haapasalo  et  al.  reported an exercise-associated enlargement in bone size that was maintained  after  retirement  in  former  racket  players  (11),  children  aged  3  to  5  years  that  had  reached  structural  benefits  of  the skeleton by training retained these benefits with cessation of the training program (5) and old retired athletes still had structural benefits  (18).  These  structural  benefits  could  also  hypothetically  be transferred to a lower fracture incidence than expected by age.

IS EXERCISE DURING YOUNGER YEARS FOLLOWED BY REDUCED FRACTURE INCIDENCE AT OLD AGES?

Reduced fracture risk has been reported in retired athletes. The prevalence of fractures in 663 former athletes above age 50 years, and retied from sports for up to 65 years were lower than in 943 age- and gender matched controls, 8.9% in the former athletes versus 12.1% in the controls (24). Additionally, the proportion of subjects with low energy fragility fractures sustained after age 50 years was lower in the former athletes in comparison with the controls, 2.3% versus 4.2%, as well as the proportion of individuals with a distal radius  fracture,  0.8%  versus  2.3%  (Figure  3).  Similar  conclusions have been reported in 400 former male soccer players and 800 controls (18) and there are now also data published that infer among 2075 former male athletes and controls aged 50- 91 years, a lower incidence of both all type of fractures as well as fragility fractures in the former sportsmen (31). But other studies refute the view. One often cited study includes 2622 former female college athletes and 2776 controls now aged 20- 80 years, a trial that reported a similar fraction of former athletes with fractures than controls after retirement, 29% versus 32% (35). However, as this study includes individuals from age 20 years with an extremely short retirement period and  former  recreational  athletes,  there  could  have  been  too  few elderly individuals and too few highly active athletes in the cohort to give a true risk evaluation of osteoporosis related fractures after training during growth.

CONCLUSIONS AND PERSPECTIVE

Childhood  and  adolescence  are  critical  periods  for  the  skeleton. Mechanical loading has then been shown to be one of the best stimuli to enhance not only bone mass but also the structural skeletal adaptations, both contributing to bone strength. Exercise prescription also includes a window of opportunity to improve bone strength in the late pre- and early peri-pubertal period. There are some evidence supporting the notion that skeletal gains obtained by mechanical loading during growth are maintained at older age despite  reduction  of  physical  activity  in  adulthood  in  the  notion that former male athletes have a lower fracture risk than expected by age at least do not oppose the view that physical activity during growth and adolescence should be supported as one feasible strategy to reduce the future incidence of fragility fractures.
The  future  research  should  now  determine:  (i)  the  minimum threshold  of  exercise  during  growth  that  is  necessary  to  obtain  a clinically significant increase in bone strength and (ii) the minimum threshold of exercise during adulthood that is required to maintain the skeletal benefits (gained during growth) and prevent osteoporosis and (iii) in prospective long term studies evaluate if exercise induced benefits in the skeleton with accompanied fracture reduction are retained after cessation of exercise. This is a pivotal area of research that underpins future decisions regarding the role of exercise during growth for improved bone health in the aged individual.

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Korrespondenzadresse:
Magnus Karlsson
Department of Clinical Sciences and Orthopaedics
Skane University Hospital, Lund University
20502 Malmö
Schweden
E-Mail: magnus.karlsson@med.lu.se
 
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