Does Exercise Reduce the Burden of Fractures? a review Magnus Karlsson

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Does cessation of exercise confer residual high BMD after retirement?

There are a few, and only short-term, longitudinal studies evaluating the effect on BMD with cessation of exercise. Michel et al. (1992) reported a decrease of 16% in the BMD of the spine in 9 middle-aged male runners who ceased their running career, compared to no loss in 3 individuals who continued running over a 5-year period. Similarly, 12 women, aged 19-27 years increased the muscle strength in the trained leg by 24% and leg BMD by 2% during 12 months with unilateral leg presses four times a week, but the BMD returned to its pre-training level after no more than three months of detraining (Vuori et al., 1994). No long-term studies evaluating the structural changes in the skeleton with reduction or cessation of exercise exist. Only 3 cross-sectional studies evaluated the BMD effects of cessation of exercise after age 65 years, the age when fragility fractures exponentially increase (Karlsson et al., 1995; 1996; 2000; Khan et al., 1996). Leg BMD was reported 10% higher than age-matched controls in retired male soccer players retired for 5 years, 5% higher in players retired for 16 years, but no higher in players retired for 42 years (Figure 4). The BMD decrease with age was, in the legs 0.33 % /year in the former soccer players compared to 0.21% /year in the controls. A non-significant, residual, higher leg BMD was reported in the legs in the former players aged 70 or more, a significant difference when adjusted for differences in body composition relative to the controls. However, no differences were found in the spine or hip either before or after adjustment for confounders, indicating that after 3 to 5decades of retirement, no residual BMD benefits could be found (Karlsson, et al., 1993a; 1993b; 1995; 1996; 2000; Khan, et al., 1996). Similar data have previously been presented, evaluating both male weight lifters and female ballet dancers (Karlsson, et al., 1993a; 1993b; 1995; 1996)There are problems with cross-sectional studies spanning 7 decades as secular trends in exercise may be present (Karlsson, et al., 2000). Intensity and duration of training in youth were perhaps less vigorous 5 decades ago. However, the duration of activity in the oldest former soccer players was at a level conferring the same high BMD during their active career as the BMD in soccer players active today (Karlsson, et al., 2001).

A lower level of activity may retain some BMD benefits achieved during an active career. The male soccer study supports this when showing a correlation between current activity level and femoral neck BMD (r = ~0.25) (Karlsson, et al., 2000). The notion is also supported in a 4-year longitudinal study of 13 formerly competitive male tennis players in which all players at baseline were Finnish national top level players with an average training frequency of 8 hours exercise/week. No changes were seen in the discrepancies in bone mineral content between the playing and the non-playing arm after the detraining period of 2 years, but the athletes were still playing mean 3 hours/week (Kontulainen et al., 1999). Maybe continued activity, but on a lower level, preserves the exercise-induced, beneficial skeletal effects achieved during growth and adolescence but currently, no data exist suggesting the amount of exercise needed to maintain exercise induced skeletal benefits also after active career.
Does exercise increase muscle size and muscle strength?

Muscle size, muscle strength, neuromuscular fibre recruitment, and balance decrease with advancing age, traits often regarded as surrogate end points for fractures (Hakkinen et al 1995; Lipsitz et al., 1994; Lord and Ward, 1994; Roman et al., 1993; Tracy et al., 1999).

It is unclear whether the age-related decrease in muscle size and strength can cause the age-related decrease in BMD or whether the decrease in these two variables, both predicting fracture, can occur with no causal relationship. Grip strength correlated with BMD in all measured locations in 649 postmenopausal women (Kritz-Silverstein and Barrett-Connor, 1994) and quadriceps strength and femoral neck BMD were correlated in both 109 men and 231 women aged 20-89 years (both r= 0.6) (Hyakutake et al., 1994), similar to the data reported in most studies. Muscle strength has been described as an independent predictor of femoral neck BMD in some (Hyakutake, et al., 1994; Pocock et al., 1989; Snow-Harter et al., 1990) but not all studies (Seeman et al., 1996). It is unclear whether muscle strength partially determines the BMD or whether strength and BMD covariate only due to shared genetic regulation, as large individuals with a large skeleton and a high BMD probably also has a larger muscle volume (Hyakutake, et al., 1994; Kritz-Silverstein and Barrett-Connor, 1994; Pocock, et al., 1989; Snow-Harter, et al., 1990).
Muscle strength seems highly adaptable to exercise also in the elderly and an increase by up to 200% with exercise has been reported in octogenarians. The increase is far greater than the corresponding increase in the muscle volume and BMD. Tracy et al. (1999) reported a 27% increase in quadriceps strength, a 12% increase in quadriceps muscle mass and a 14% increase in muscle quality defined as strength per unit of muscle mass by a 9- week program of resistance exercise for the quadriceps 3 days/ week in 12 men aged 65-75 years. The corresponding increase in 11 women aged 65-73 years was 29%, 12% and 16%, respectively. Lord et al. (1995) verified these findings by reporting 29% increased quadriceps strength, while BMD was unchanged in individuals aged 60-85 years after a 12 month of exercise and Ryan et al. (1998) reported up to 98% increased strength without changes in femoral neck BMD after 16 week training program. A corresponding training program for 21 men aged 61 years conferred a 39% increase in upper body and a 38% increase in lower body strength but also a 3% increase in femoral neck BMD (Ryan et al., 1994). Moreover, decrease in activity level confers rapid changes in muscular strength. Kontulainen et al. (1999) reported that muscle volume measured as differences in forearm circumference between the playing and non-playing arm diminished from 6 to 3% with reduced training level in the course of 2 years and Fiatarone et al. (1990) reported a 32% loss of muscle strength after no more than 4 weeks with no training.
The exercise-induced muscle response is probably of greater significance than the BMD response in the elderly for the reduction of the fracture risk by exercise through improved mobility, speed of movement and ability to prevent or reduce the severity of falls. The specific neuromuscluar mechanisms responsible for the increase in muscle quality with exercise are unknown. Neuromuscular recruitment with increase in motor unit recruitment or discharge rate, increased activation of synergistic muscles, decreased activation of antagonistic muscles and alteration in muscle architecture may all contribute (Fiatarone, et al., 1990; Hakkinen et al., 1998; Hakkinen et al., 1983; Narici et al., 1989; Pyka et al., 1994).

Does exercise reduce the number of falls?

Impaired balance and impaired gait are known risk factors for a future fall (Lipsitz, et al., 1994; Lord and Ward, 1994; Overstall et al., 1978; Tinetti et al., 1986; Wolfson et al., 1986). Among individuals aged 65 years, living in the community, 30% fall in the course of a year and the fall frequency increases with age so that 40% of 80-year old individuals fall at least once a year (Campbell et al., 1989; Tinetti et al., 1988). Observational, cohort studies and case-control studies indicate that a fall precedes more than 90% of hip and forearm fractures, but only 5% of all falls lead to a fracture and fewer than 1% of all falls result in a hip fracture (Greenspan et al., 1994; Grisso, et al., 1991; Hayes et al., 1993; Nevitt et al., 1989; Tinetti, et al., 1988). The fall tendency seems to be a predictor for hip fractures. Cummings et al. (1995), in the prospective SOF study reported that a history of falls conferred an increased risk of hip fracture, where the fracture risk increased by 30% with each fall during the first five registered falls.

Prospective, randomized or unrandomised intervention studies and observational cohort studies consistently indicate that exercise improves balance, co-ordination, muscle strength, reaction time, protective responses during a fall, lean body mass and mobility, all surrogate end-points for fractures (Daly et al., 2000; Fiatarone et al., 1994; Hu and Woollacott, 1994; Meyer, et al., 1993; Nelson, et al., 1994; Nevitt et al., 1991; Nevitt, et al., 1989; Province et al., 1995; Tinetti, et al., 1988). Several observational studies report a reduction in the number of falls with exercise (Graafmans et al., 1996; O'Loughlin et al., 1993; Tinetti et al., 1995; Tinetti, et al., 1988). Hornbrook et al. (1994) reported in 1611 individuals with an intervention program and 1571 controls 65 years and older a reduced the fall frequency by 15% with exercise, Tinetti et al. (1994) in 301 men and women 70 years and older that 35% of the exercisers fell compared to 47% of the controls. Several randomized controlled trails have evaluated the effect of exercise and fall risk. The first longitudinal study who reported exercise to reduce the fall risk was The Frail and Injuries: Cooperative Studies of Interventions Techniques (FICSIT) including 60-75-year old individuals, reported that 10-36 weeks of different training programs reduced the number of falls by 17%. The most advantageous results were reported with 15 weeks of Tai-Chi training, resulting in a 47% reduction in multiple falls during the 4 month period (Wolf et al., 1996). Since this study, four newer randomized controlled trails have supported that exercise reduce the number of falls (Buchner et al., 1997; Campbell et al., 1999a; Campbell et al., 1997; Lehtola et al., 2000) while 4 other randomized controlled trails could not detect a fall reduction with exercise (Campbell et al., 1999b; McMurdo, et al., 1997; Rubenstein et al., 2000; Steinberg et al., 2000). Some studies even imply that the most active individuals are at the same risk of sustaining a fall as the most inactive (Graafmans, et al., 1996; O'Loughlin, et al., 1993; Tinetti, et al., 1995; Tinetti, et al., 1988), probably due to a longer exposure to risk during the activity in the most active elderly. Two recently published reviews concluded that exercise alone does not protect against future falls (Campbell, et al., 1999a; Gillespie et al., 2000). By contrast, Gregg et al. (Gregg, et al., 2000) summarizing 6 randomised studies, presented that exercise do reduce the fall frequency. It seems that the outcome in one population of elderly cannot automatically be extrapolated to another population and it appears as intervention studies directed at nursing home populations with a fall as end point show less promising results. Additional questions arise - what dose, frequency and duration of exercise is necessary to maintain the achieved level of function and does this differ between populations?
Figure legends
Figure 1 Proportion of individuals with fractures among 284 former soccer players now 48-94 years of age and 568 age- and gender- matched controls. Adapted from Karlsson et al. 2000.
Figure 2 The side to side differences in bone mass at the humerus were two to four times higher in female tennis players who had started training before menarche compared with those who started playing up to 15 years after menarche. Bars represent 95% CI’s. Adapted from Kannus et al. 1994.
Figure 3 Bone mineral density (BMD) of the upper part of the skull / the skull, the arms and the legs, in active male soccer players, male weight lifters and female gymnasts expressed as Z scores (number of standard (SD) deviations above or below age predicted mean). Adapted from Karlsson et al. 1996, Karlsson et al. 2000 and Bass et al. 1998 .
Figure 4 Bone mineral density (BMD) of the legs, femoral neck and arms in active and former soccer players expressed as Z scores (number of standard (SD) deviations above or below age predicted mean). Adapted from Karlsson et al. 2000.

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