Scand J Med Sci Sports 2014: 24 (Suppl. 1): 98–104 doi: 10.1111/sms.12239
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Recreational football improves bone mineral density and bone turnover marker profile in elderly men E. W. Helge1, T. R. Andersen1, J. F. Schmidt1,2, N. R. Jørgensen3, T. Hornstrup1, P. Krustrup1,4, J. Bangsbo1 1
Copenhagen Centre for Team Sport and Health, Department of Nutrition, Exercise and Sports, University of Copenhagen, Copenhagen, Denmark, 2Department of Cardiology, Gentofte Hospital, Gentofte, Denmark, 3Research Center for Ageing and Osteoporosis, Departments of Diagnostics and Medicine, Copenhagen University Hospital Glostrup, Glostrup, Denmark, 4Sport and Health Sciences, College of Life and Environmental Sciences, University of Exeter, Exeter, UK Corresponding author: Eva W. Helge, PhD, Department of Nutrition, Exercise and Sports, Section of Integrated Physiology, University of Copenhagen, Nørre Allé 51, Copenhagen N DK-2200, Denmark. Tel: +45 3532 0803, Fax: +45 3532 0870, E-mail: [email protected] Accepted for publication 28 March 2014
This study examined the effect of recreational football and resistance training on bone mineral density (BMD) and bone turnover markers (BTMs) in elderly men. Twenty-six healthy sedentary men (age 68.2 ± 3.2 years) were randomized into three groups: football (F; n = 9) and resistance training (R; n = 9), completing 45–60 min training two to three times weekly, and inactive controls (C; n = 8). Before, after 4 months, and after 12 months, BMD in proximal femur (PF) and whole body (WB) were determined together with plasma osteocalcin (OC), procollagen type-1 amino-terminal propeptide (P1NP), and carboxy-terminal type-1 collagen crosslinks (CTX-1). In F, BMD in PF increased up to 1.8% (P < 0.05) from 0
to 4 months and up to 5.4% (P < 0.001) from 0 to 12 months; WB-BMD remained unchanged. After 4 and 12 months of football, OC was 45% and 46% higher (P < 0.001), and P1NP was 41% and 40% higher (P < 0.001) than at baseline, respectively. After 12 months, CTX-1 showed a main effect of 43% (P < 0.05). In R and C, BMD and BTM remained unchanged. In conclusion, 4 months of recreational football for elderly men had an osteogenic effect, which was further developed after 12 months, whereas resistance training had no effect. The anabolic response may be due to increased bone turnover, especially improved bone formation.
As the amount of physical activity afforded by daily living and work in the Western countries is becoming lesser and the populations are growing older, the prevalence of osteoporosis is increasing, which impose a large health burden on the society and a negative effect on life quality for the individual patients. It is therefore of utmost relevance to examine whether the recommendations of physical activity to increase bone mass and diminish the risk of osteoporosis and bone fractures in elderly people (WHO, 2010) can be improved. Previously, the prevention of osteoporosis has mainly focused upon women, but recently, the attention has also been directed toward the need for a better understanding of osteoporosis prevention in the male population (Madeo et al., 2007) and the role of physical activity. Animal studies have shown that the osteogenic stimulus from mechanical impact is depending on the deformation (strain) of the bones induced by the external forces applied to them. Thus, the larger the strain, the higher the strain rate, and the more differentiated the strain distribution, the larger the osteogenic stimulus (Turner, 1991; Turner & Robling, 2003; Lee & Lanyon, 2004). In accordance with this, it has been reported from
cross-sectional studies that athletes engaged in oddimpact and high-impact sports, which impose large and varied strains on the skeleton, exhibit larger bone mass and bone mineral density (BMD) than age-matched counterparts not engaged in that type of exercise (Fehling et al., 1995; Heinonen et al., 1995; Taaffe et al., 1995; Alfredson et al., 1996; Söderman et al., 2000; Calbet et al., 2001; Helge & Kanstrup, 2002; Nikander et al., 2005; Fredericson et al., 2007; Wilks et al., 2009), but it has been hypothesized that after the attainment of peak bone mass, the augmentation of bone mass due to mechanical impact from exercise would only be sparse. However, intervention studies examining the musculoskeletal health-enhancing effect of recreational football in different middle-aged populations (Krustrup et al., 2009, 2010; Helge et al., 2010; Randers et al., 2010) have reported an osteogenic effect in this age group. In addition to the osteogenic effect of high- and oddimpact exercise, the osteogenic effect of resistance training in elderly people has been studied (Vincent & Braith, 2002; Kohrt et al., 2004; von Stengel et al., 2007; Guadalupe-Grau et al., 2009; Bolam et al., 2013), and it is reported that the loading magnitude (Vincent &
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BMD and bone turnover markers in elderly men Table 1. Baseline characteristics of subjects randomized to football training (F), resistance training (R), or controls (C)
Age (years) Height (cm) Body mass (kg) BMI (kg/m2) VO2max (mL/min/kg)
F (n = 9)
R (n = 9)
C (n = 8)
68.0 ± 4.0 173.3 ± 7.8 77.7 ± 9.4 26.1 ± 3.9 27.5 ± 5.4
69.1 ± 3.1 176.7 ± 9.8 85.8 ± 12.0 27.4 ± 2.8 28.9 ± 5.5
67.4 ± 2.7 179.0 ± 6.2 89.3 ± 12.4 27.9 ± 4.6 30.8 ± 3.3
Values are given as means ± standard deviation. BMI, body mass index; VO2max, maximum oxygen uptake.
Braith, 2002) as well as the movement velocity and power output during the resistance training (von Stengel et al., 2007) are independent predictors of the anabolic bone response. Most studies have included postmenopausal women, and it has been proposed that with a similar training regimen, the bone adaptation is similar in men and women and that common recommendations of physical activity are applicable (Kohrt et al., 2004). However, as hormonal factors influence the bone metabolism, it seems relevant and highly needed to conduct studies on men separately. Thus, the aim of the present study was to examine the osteogenic effect of recreational football compared with resistance training in elderly sedentary men. The intervention lasted 12 months, and the BMD was evaluated by Dual-Energy X-ray Absorptiometry (DXA) scanning; to examine the response in bone turnover, the concentration of plasma bone turnover markers (BTMs) was measured.
intensity were progressively increased. In F, the training consisted of small-sided play on a natural grass pitch: 3 × 15-min play interspersed with 2-min rest periods (week 0–12) and 4 × 15-min play interspersed with 2-min rest periods (week 13–52). To evaluate the exercise intensity of the participants during the football training, HR was measured during most training sessions over the first 4 months of training using Polar Team 2 system chest belts (Polar Oy, Kempele, Finland). These results revealed an average intensity of 82% (range 64–90%) of maximal HR. In R, 5 min of low intensity warm-up was followed by resistance training including five exercises: leg press, seated leg extension, hamstring curl, pull-down, and lateral dumbbell raises. Each set of exercises was separated by 1.5-min rest, and at the end of each training session, 5 min of core training was performed. The individual training loads were set using the “RM” (repetition maximum) notion for resistance training, which is defined as the maximal load an individual is able to lift a given number of times. This means that the higher the number of RM, the lower the absolute load in each repetition. In this way, the training load in each exercise was progressively increased as follows: three sets of 16–20 RM (week 0–4), three sets of 12 RM (week 5–8), three sets of 10 RM (week 9–12), and four sets of 8 RM (week 13–52), and as the training progressed, the participants were encouraged to perform the exercises with maximal speed in the concentric phase. From week 25 onwards, lunges and seated row (both with four sets of 8 RM) were added to the training program. The lunges were performed as standing lunges with dumbbells, and seated row was performed in a cable pull machine. During the 1-year intervention, the attendance rate for F and R was 66% ± 4% (range 61–114 training sessions) and 73% ± 3% (range 77–116 training sessions), respectively. The average number of training sessions per week in F and R were 1.7 ± 0.3 (range 1.2–2.2) and 1.9 ± 0.2 (range 1.4–2.2), respectively. There was no difference between the groups.
Methods
Testing procedures
Participants
To evaluate the osteogenic adaptations induced by the intervention, BMD in the proximal femur (PF) and in whole body (WB) was determined together with the plasma concentration of BTM at baseline and after 4 and 12 months, the participants showed up in the early morning after an overnight fast and without any strenuous exercise during the preceding day or the same morning. BMD in WB and PF (femoral neck, femoral shaft, and total PF) was measured by DXA scanning (iDXA, Lunar Corporation, Madison, WI, USA) according to standard procedures. Before the scanning the participants were asked to use the toilet to empty the bladder. A resting blood sample was drawn from the antecubital vein for later analysis of the plasma concentrations of osteocalcin (OC), procollagen type-1 amino-terminal propeptide (P1NP) and carboxy-terminal type-1 collagen crosslinks (CTX-1), which were evaluated by a fully automated immunoassay system (iSYS, Immunodiagnostic Systems Ltd., Boldon, England) by method of Chemiluminescence. The performance of the assay, expressed as inter-run coefficients of variation, were 9% for P-OC, 10% for P-CTX-1, and 8% for P-PINP.
Thirty-two elderly men responded to recruitment advertisements in local newspapers, seeking non-smoking healthy men without chronic diseases, aged 65–75 years, who had not participated in regular physical activity during the preceding 5 years. After a medical examination, four subjects were excluded due to a history of cardiovascular disease (n = 2), type 2 diabetes mellitus (n = 1), and obstructive lung disease (n = 1) and one never showed up for baseline testing. Twenty-seven of the 32 elderly men, who responded initially, were therefore included in the study and were randomized and stratified by body mass index (BMI) and maximum oxygen uptake (VO2max) into a football group (F), a resistance training group (R), and an inactive control group (C). At the first training session, one subject in F suffered from an Achilles tendon rupture and was excluded from all analyses, and thus the final numbers in the three groups were: F = 9, R = 9, and C = 8; with a total of n = 26. There were no statistical differences in age, height, body mass, BMI, and VO2max between F, R, and C (Table 1). All participants were fully informed of experimental procedures and possible discomfort associated with the study before giving their written informed consent to participate. The study was carried out in accordance with the Declaration of Helsinki and approved by the local ethics committee of the Capital Region of Denmark, H-1-2011-013; ClinicalTrials.gov identifier: NCT01530035.
Training In both F and R supervised training was offered during the total intervention period of 12 months, and the training volume and
Statistical analysis Differences at baseline between F, R, and C, and longitudinal changes within and between groups were tested by two-way repeated measures ANOVA with Holm–Sidak post-hoc testing. Statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS), version 20.0 and SigmaStat, version 3.5. Results are presented as means ± standard error unless otherwise stated.
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Helge et al. Results Plasma BTMs No differences in plasma BTMs between the groups were observed before the intervention period (Fig. 1). (a)
1.0
#
0.8
CTX (ug/L)
0 months 4 months 12 months
BMD
0.6
0.4
0.2
0.0
F
(b)
80 70
#
R
C
#
0 months 4 months 12 months
P1NP (ug/L)
60 50 40 30 20 10 0
F
(c)
40
#
R
0 months 4 months 12 months
#
Osteocalcin (ug/L)
20
10
0
F
R
Prior to the intervention period, BMD in the PF did not differ between F, R, and C, except for the left total PF, which was lower (P < 0.05) in F compared with C (Table 2). A normalization of femoral BMD in relation to body mass (Table 3) revealed no difference in femoral BMD between the groups (0.79 ≤ P ≤ 1.00). Compared with baseline, the absolute BMD values after 4 and 12 months of intervention (Table 2) were changed in F, and the relative increase in BMD corresponded to 1.0% ± 0.5% (P < 0.05) and 2.9% ± 0.7% (P < 0.001), respectively, in the right total PF, and 1.1% ± 0.5% (P < 0.05) and 2.4% ± 0.8% (P < 0.001), respectively, in the left total PF. In the right femoral shaft, BMD after 4 and 12 months was 1.8% ± 0.4% (P < 0.005) and 3.5% ± 0.8% (P < 0.001) increased, respectively. After 12 months, BMD in the right and left femoral neck was increased (P < 0.001) by 3.8% ± 1.2% and 5.4% ± 2.6%, respectively (Fig. 2). For WB and left femoral shaft BMD, no interaction between group and time was observed. Discussion
C
30
C
Fig. 1. Concentration of the plasma bone turnover markers carboxy-terminal type-1 collagen crosslinks (CTX-1) (a), procollagen type-1 amino-terminal propeptide (P1NP) (b) and osteocalcin (c) for elderly men in the football training group (F), the resistance training group (R), and the control group (C) at baseline after 4 months and after 12 months of intervention. #, > 0 months; P < 0.001.
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After 4 and 12 months of football training, plasma OC was 45% ± 12% and 46% ± 11% higher (P < 0.001), respectively, than before the intervention, and plasma P1NP was 41% ± 16% and 40% ± 17% higher (P < 0.001), respectively. Plasma OC and P1NP were higher (P < 0.05) in F than in R and C after 4 and 12 months. For CTX-1, there was no interaction between time and group, but after 12 months, there was a main effect of time at 43% ± 13% (P < 0.05).
This intervention is the first to study the osteogenic effect of recreational football in comparison with resistance training in elderly men. The main findings were that football participation resulted in an augmentation in BMD in the weight bearing appendicular skeleton and a marked increase in bone formation markers, which was not seen after participation in resistance training. In addition, the bone resorption was similar after football and resistance training, which indicates that the osteogenic impact of football is primarily due to an effect on bone formation, which leads to a positive bone balance and an increase in BMD. As the osteogenic stimulus from exercise is mainly depending on the strain rate and magnitude induced by various muscle and ground reaction forces acting upon the bone (Rubin & Lanyon, 1984; Turner & Pavalko, 1998; Kohrt et al., 2009; Robling, 2009), it seems reasonable to hypothesize that an odd-impact physical activity like recreational football, which involves both kind of forces, would have a large osteogenic potential in elderly men. The hypothesis was confirmed by the findings of a profound augmentation in BMD in the left
1.008 ± 0.063 1.018 ± 0.043 1.254 ± 0.059 1.282 ± 0.045 1.083 ± 0.048 1.117 ± 0.041 1.268 ± 0.030 1.015 ± 0.066 1.009 ± 0.045 1.247 ± 0.057 1.283 ± 0.044 1.081 ± 0.046 1.112 ± 0.040 1.262 ± 0.030 1.007 ± 0.065 1.017 ± 0.043 1.243 ± 0.056 1.282 ± 0.043 1.080 ± 0.048 1.121 ± 0.038 1.266 ± 0.031 1.000 ± 0.042 1.006 ± 0.036 1.229 ± 0.056 1.229 ± 0.057 1.066 ± 0.048 1.069 ± 0.048 1.225 ± 0.024 *< C, P < 0.05. † > T0, P < 0.05. ‡ > T0, P < 0.005. § > T0, P < 0.001. ¶ > T4, P < 0.05. **> T4, P < 0.01. †† > T4, P < 0.001. Values are given as means ± standard error.
Femoral neck (FN), right Femoral neck (FN), left Femoral shaft (FS), right Femoral shaft (FS), left Total proximal femur (TPF), right Total proximal femur (TPF), left Whole body (WB)
0.921 ± 0.034§¶ 0.939 ± 0.034§†† 1.156 ± 0.042§** 1.143 ± 0.043 0.982 ± 0.031§†† 0.989 ± 0.031§¶ 1.211 ± 0.036
1.000 ± 0.043 1.010 ± 0.040 1.236 ± 0.059 1.231 ± 0.059 1.070 ± 0.049 1.068 ± 0.048 1.227 ± 0.024 0.893 ± 0.034 0.917 ± 0.032 1.138 ± 0.044‡ 1.133 ± 0.043 0.965 ± 0.032† 0.977 ± 0.031† 1.174 ± 0.035 0.888 ± 0.034 0.893 ± 0.034 1.117 ± 0.042 1.120 ± 0.041 0.955 ± 0.030 0.966 ± 0.030* 1.167 ± 0.035
1.011 ± 0.042 1.015 ± 0.037 1.237 ± 0.057 1.234 ± 0.057 1.070 ± 0.047 1.073 ± 0.046 1.227 ± 0.024
12 months (T12) 4 months (T4) 0 months (T0) 0 months (T0) 12 months (T12) 4 months (T4) 0 months (T0)
4 months (T4)
12 months (T12)
C (n = 6) R (n = 8) F (n = 9) Bone region
Table 2. Bone mineral density (g/cm2) in proximal femur and whole body for a football training (F), resistance training (R) and control (C) group before (T0) as well as after 4 (T4) and 12 (T12) months of intervention
BMD and bone turnover markers in elderly men (5.4%) and the right femoral neck (3.8%) as well as in the left (2.4%) and the right (2.9%) total PF after 12 months of recreational football, which is markedly higher than in other intervention studies examining the skeletal effect of physical activity in elderly men (Vincent & Braith, 2002; Guadalupe-Grau et al., 2009; Bolam et al., 2013). It should be emphasized that the absolute values for femoral BMD was lower in F than in R and C, albeit not significantly different, and that BMD in the left total femur was significantly lower than in C. However, when analyzing the individual responses in F, it was observed that the three subjects that had baseline BMDs above 1.0 had a similar training-induced increase in BMD as the other six subjects and that no correlations were found when correlating the BMD in PF at baseline to the absolute delta values in BMD after 4 and 12 months of football. Thus, it seems as if the marked increase in femoral BMD in F is not due to simple regression to the mean. This notion is supported by a similar finding of no correlation between BTM concentrations at baseline and absolute delta values in BTM in F. All together, this indicates that the increase in femoral BMD in F and the reported differences between the intervention groups were due to the training itself. Already after 4 months of football training in the present study, BMD in left and right total PF was augmented by 1.1% and 1.0%, respectively, which is marginally lower compared with other football interventions from our lab examining the osteogenic effects but in younger age groups and with different methods. Thus, we have found an increase in lower extremity bone mass of 41 g (P < 0.05) after 12 weeks of recreational football with 20- to 40-year-old sedentary men (Krustrup et al., 2009), and an increase in total volumetric BMD in left and right tibia of 2.6% and 2.1%, respectively, after 14 weeks of football with premenopausal sedentary women (Helge et al., 2010). Thus, from the present BMD results after 4 months of football training, it seems that elderly men exhibit a lower osteogenic response to exercise than younger individuals. However, given that the relative increases in BMD in the PF regions overall were doubled from 4 to 12 months, and that the profound BMD increases in right and left femoral neck of 3.8% and 5.4%, respectively, were not seen until 12 months of football suggest that the osteogenic BMD response in elderly men is not lower, but rather slower, compared with younger age groups. The osteogenic response after 4 and 12 months in the football group was supported by a pronounced rise in plasma BTMs. Thus, plasma OC was elevated by 45% already after 4 months of football and maintained higher after 12 months (46%), while P1NP was 41% and 40% higher after 4 and 12 months, respectively, compared with baseline. Remarkably, the bone resorption marker CTX-1 was not elevated before 12 months (43%) and only with a main effect of time. Other studies have examined the bone turnover response to training and
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Helge et al. Table 3. Femoral bone mineral density at baseline normalized in relation to body mass (g/cm2/kg) for a football training (F), resistance training (R), and control (C) group
Bone region
F (n = 9)
R (n = 8)
C (n = 6)
Femoral neck (FN), right Femoral neck (FN), left Femoral shaft (FS), right Femoral shaft (FS), left Total proximal femur (TPF), right Total proximal femur (TPF), left
0.0114 ± 0.0004 0.0115 ± 0.0004 0.0144 ± 0.0006 0.0144 ± 0.0005 0.0123 ± 0.0004 0.0124 ± 0.0004
0.0121 ± 0.0011 0.0121 ± 0.0009 0.0150 ± 0.0015 0.0149 ± 0.0014 0.0130 ± 0.0013 0.0129 ± 0.0012
0.0116 ± 0.0011 0.0117 ± 0.0008 0.0144 ± 0.0012 0.0147 ± 0.0010 0.0125 ± 0.0011 0.0129 ± 0.0008
Values are given as means ± standard error.
0 months 4 months 12 months
(a)
BMD right femoral neck (g/cm2)
1.10 1.05 1.00
#§
0.95 0.90 0.85 0.80 0.00 F
R
C
(b)
0 months 4 months 12 months
BMD left femoral neck (g/cm2)
1.10 1.05 1.00
#§
0.95 0.90 0.85 0.80 0.00 F
R
C
Fig. 2. Bone mineral density (BMD) in the right femoral neck (a) and the left femoral neck; (b) for elderly men in the football training group (F), the resistance training group (R) and the control group (C) at baseline, after 4 months and after 12 months of intervention. #, > 0 months; P < 0.001. §, > 4 months; P < 0.05.
acute changes in the physical activity level in younger age groups, reporting an opposite response in bone resorption and bone formation markers with changes in physical activity (Karlsson et al., 2003; Scott et al., 2011; Weiler et al., 2012). Thus, it has been reported (Karlsson et al., 2003) that in male premier league football players, that plasma OC and CTX-1 at the end of the
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season were 22% and 34% higher, respectively, compared with a control group. However, after 2 weeks of rest between the football seasons the CTX-1 concentration was elevated by 8%, and the P1CP concentration was reduced by 21% compared with the end of the season, while OC and P1CP did no longer differ from the controls, whereas CTX-1 still was higher than in the controls. Ten days into the new football season, these changes were no longer present; P1CP was elevated by 23%, and CTX-1 was decreased by 4% compared with the end of the resting period. The time course of these changes in BTM (the elevation of the bone formation markers first, followed by a delayed elevation of bone resorption markers) induced by exercise is similar to the anabolic effect of PTH treatment (Glover et al., 2009), which indicate that exercise and PTH acts through a similar anabolic mechanism. However, from the present study, it cannot be determined whether both stimuli act through the same regulatory pathway. To further examine the mechanism behind the osteogenic stimulus of exercise, future studies may include analysis of plasma sclerostin, which is an antagonist of the Wnt signaling pathway that increases osteoblast activity, and which might be down-regulated due to mechanical loading (Ardawi et al., 2012). In contrast to recreational football, resistance training in the present study did not seem to have any osteogenic effect, neither after 4 nor 12 months, and the plasma BTM did not change in this group. This is not in agreement with a review on exercise and bone mass (Guadalupe-Grau et al., 2009), reporting that in elderly men, BMD improvements of 1–3% in the appendicular weight-bearing bones and in the lumbar spine can be expected after 6 months of high intensity (> 70% 1 RM) resistance training. A reason to the finding of no osteogenic effect of resistance training in the present study may have been too low intensity, only progressively increased to 8 RM after 13 weeks of training. This progression was chosen to minimize the risk of muscle and back injuries as the participants were sedentary and elderly men. Nevertheless, it appears that football has the potential to induce an earlier and more pronounced osteogenic response than resistance training likely because of the combination of muscle and gravitational forces in football (Kohrt et al., 2009).
BMD and bone turnover markers in elderly men In conclusion, 4 months of recreational football for elderly men had an osteogenic impact, which was further developed after 12 months. The osteogenic impact, evaluated from BMD as well as bone formation and bone resorption markers, was higher after football than after resistance training, which showed no osteogenic effect. The anabolic response induced by football may be due to increased bone turnover, especially improved bone formation. The present results are promising regarding the osteogenic effect of football as a health-enhancing physical activity for elderly males that may diminish the age-dependent bone loss and the risk of osteoporosis.
BTM profile, the anabolic response in the football group may be due to a substantial improvement in bone formation already after 4 months, while there seemed to be a delayed increase in bone resorption. Overall, the bone turnover rate was increased in the football group, but in favor of bone formation, which in the long run may diminish the age-dependent decrease in bone mass. Thus, it seems that recreational football can be recommended as physical activity that improves bone health and diminishes the risk of osteoporosis, even in elderly people. Key words: Bone metabolism, BMD, soccer, resistance training, osteogenic impact.
Perspectives After only 4 months, recreational football for elderly men had a marked osteogenic effect on BMD in the weight-bearing bones, and after 12 months, the improvement was more than doubled. Resistance training had no impact on BMD. As evaluated from the
Acknowledgements The study was supported by Nordea-fonden, FIFA – Medical Assessment and Research Centre (F-MARC), Preben and Anna Simondsen fonden, and The Danish Ministry of Culture (Kulturministeriets Udvalg for Idrætsforskning).
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Vincent KR, Braith RW. Resistance exercise and bone turnover in elderly men and women. Med Sci Sports Exerc 2002: 34: 17–23. Weiler R, Keen R, Wolman R. Changes in bone turnover markers during the close season in elite football (soccer) players. J Sci Med Sport 2012: 15: 255–258. WHO. Global recommendations on physical activity for health. Geneva: World Health Organization, 2010. Wilks DC, Winwood K, Gilliver SF, Kwiet A, Chatfield M, Michaelis I, Sun LW, Ferretti JL, Sargeant AJ, Felsenberg D, Rittweger J. Bone mass and geometry of the tibia and the radius of master sprinters, middle and long distance runners, race-walkers and sedentary control participants: a PQCT study. Bone 2009: 45: 91–97.
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Recreational football improves bone mineral density and bone turnover marker profile in elderly men E. W. Helge1, T. R. Andersen1, J. F. Schmidt1,2, N. R. Jørgensen3, T. Hornstrup1, P. Krustrup1,4, J. Bangsbo1 1
Copenhagen Centre for Team Sport and Health, Department of Nutrition, Exercise and Sports, University of Copenhagen, Copenhagen, Denmark, 2Department of Cardiology, Gentofte Hospital, Gentofte, Denmark, 3Research Center for Ageing and Osteoporosis, Departments of Diagnostics and Medicine, Copenhagen University Hospital Glostrup, Glostrup, Denmark, 4Sport and Health Sciences, College of Life and Environmental Sciences, University of Exeter, Exeter, UK Corresponding author: Eva W. Helge, PhD, Department of Nutrition, Exercise and Sports, Section of Integrated Physiology, University of Copenhagen, Nørre Allé 51, Copenhagen N DK-2200, Denmark. Tel: +45 3532 0803, Fax: +45 3532 0870, E-mail: [email protected] Accepted for publication 28 March 2014
This study examined the effect of recreational football and resistance training on bone mineral density (BMD) and bone turnover markers (BTMs) in elderly men. Twenty-six healthy sedentary men (age 68.2 ± 3.2 years) were randomized into three groups: football (F; n = 9) and resistance training (R; n = 9), completing 45–60 min training two to three times weekly, and inactive controls (C; n = 8). Before, after 4 months, and after 12 months, BMD in proximal femur (PF) and whole body (WB) were determined together with plasma osteocalcin (OC), procollagen type-1 amino-terminal propeptide (P1NP), and carboxy-terminal type-1 collagen crosslinks (CTX-1). In F, BMD in PF increased up to 1.8% (P < 0.05) from 0
to 4 months and up to 5.4% (P < 0.001) from 0 to 12 months; WB-BMD remained unchanged. After 4 and 12 months of football, OC was 45% and 46% higher (P < 0.001), and P1NP was 41% and 40% higher (P < 0.001) than at baseline, respectively. After 12 months, CTX-1 showed a main effect of 43% (P < 0.05). In R and C, BMD and BTM remained unchanged. In conclusion, 4 months of recreational football for elderly men had an osteogenic effect, which was further developed after 12 months, whereas resistance training had no effect. The anabolic response may be due to increased bone turnover, especially improved bone formation.
As the amount of physical activity afforded by daily living and work in the Western countries is becoming lesser and the populations are growing older, the prevalence of osteoporosis is increasing, which impose a large health burden on the society and a negative effect on life quality for the individual patients. It is therefore of utmost relevance to examine whether the recommendations of physical activity to increase bone mass and diminish the risk of osteoporosis and bone fractures in elderly people (WHO, 2010) can be improved. Previously, the prevention of osteoporosis has mainly focused upon women, but recently, the attention has also been directed toward the need for a better understanding of osteoporosis prevention in the male population (Madeo et al., 2007) and the role of physical activity. Animal studies have shown that the osteogenic stimulus from mechanical impact is depending on the deformation (strain) of the bones induced by the external forces applied to them. Thus, the larger the strain, the higher the strain rate, and the more differentiated the strain distribution, the larger the osteogenic stimulus (Turner, 1991; Turner & Robling, 2003; Lee & Lanyon, 2004). In accordance with this, it has been reported from
cross-sectional studies that athletes engaged in oddimpact and high-impact sports, which impose large and varied strains on the skeleton, exhibit larger bone mass and bone mineral density (BMD) than age-matched counterparts not engaged in that type of exercise (Fehling et al., 1995; Heinonen et al., 1995; Taaffe et al., 1995; Alfredson et al., 1996; Söderman et al., 2000; Calbet et al., 2001; Helge & Kanstrup, 2002; Nikander et al., 2005; Fredericson et al., 2007; Wilks et al., 2009), but it has been hypothesized that after the attainment of peak bone mass, the augmentation of bone mass due to mechanical impact from exercise would only be sparse. However, intervention studies examining the musculoskeletal health-enhancing effect of recreational football in different middle-aged populations (Krustrup et al., 2009, 2010; Helge et al., 2010; Randers et al., 2010) have reported an osteogenic effect in this age group. In addition to the osteogenic effect of high- and oddimpact exercise, the osteogenic effect of resistance training in elderly people has been studied (Vincent & Braith, 2002; Kohrt et al., 2004; von Stengel et al., 2007; Guadalupe-Grau et al., 2009; Bolam et al., 2013), and it is reported that the loading magnitude (Vincent &
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BMD and bone turnover markers in elderly men Table 1. Baseline characteristics of subjects randomized to football training (F), resistance training (R), or controls (C)
Age (years) Height (cm) Body mass (kg) BMI (kg/m2) VO2max (mL/min/kg)
F (n = 9)
R (n = 9)
C (n = 8)
68.0 ± 4.0 173.3 ± 7.8 77.7 ± 9.4 26.1 ± 3.9 27.5 ± 5.4
69.1 ± 3.1 176.7 ± 9.8 85.8 ± 12.0 27.4 ± 2.8 28.9 ± 5.5
67.4 ± 2.7 179.0 ± 6.2 89.3 ± 12.4 27.9 ± 4.6 30.8 ± 3.3
Values are given as means ± standard deviation. BMI, body mass index; VO2max, maximum oxygen uptake.
Braith, 2002) as well as the movement velocity and power output during the resistance training (von Stengel et al., 2007) are independent predictors of the anabolic bone response. Most studies have included postmenopausal women, and it has been proposed that with a similar training regimen, the bone adaptation is similar in men and women and that common recommendations of physical activity are applicable (Kohrt et al., 2004). However, as hormonal factors influence the bone metabolism, it seems relevant and highly needed to conduct studies on men separately. Thus, the aim of the present study was to examine the osteogenic effect of recreational football compared with resistance training in elderly sedentary men. The intervention lasted 12 months, and the BMD was evaluated by Dual-Energy X-ray Absorptiometry (DXA) scanning; to examine the response in bone turnover, the concentration of plasma bone turnover markers (BTMs) was measured.
intensity were progressively increased. In F, the training consisted of small-sided play on a natural grass pitch: 3 × 15-min play interspersed with 2-min rest periods (week 0–12) and 4 × 15-min play interspersed with 2-min rest periods (week 13–52). To evaluate the exercise intensity of the participants during the football training, HR was measured during most training sessions over the first 4 months of training using Polar Team 2 system chest belts (Polar Oy, Kempele, Finland). These results revealed an average intensity of 82% (range 64–90%) of maximal HR. In R, 5 min of low intensity warm-up was followed by resistance training including five exercises: leg press, seated leg extension, hamstring curl, pull-down, and lateral dumbbell raises. Each set of exercises was separated by 1.5-min rest, and at the end of each training session, 5 min of core training was performed. The individual training loads were set using the “RM” (repetition maximum) notion for resistance training, which is defined as the maximal load an individual is able to lift a given number of times. This means that the higher the number of RM, the lower the absolute load in each repetition. In this way, the training load in each exercise was progressively increased as follows: three sets of 16–20 RM (week 0–4), three sets of 12 RM (week 5–8), three sets of 10 RM (week 9–12), and four sets of 8 RM (week 13–52), and as the training progressed, the participants were encouraged to perform the exercises with maximal speed in the concentric phase. From week 25 onwards, lunges and seated row (both with four sets of 8 RM) were added to the training program. The lunges were performed as standing lunges with dumbbells, and seated row was performed in a cable pull machine. During the 1-year intervention, the attendance rate for F and R was 66% ± 4% (range 61–114 training sessions) and 73% ± 3% (range 77–116 training sessions), respectively. The average number of training sessions per week in F and R were 1.7 ± 0.3 (range 1.2–2.2) and 1.9 ± 0.2 (range 1.4–2.2), respectively. There was no difference between the groups.
Methods
Testing procedures
Participants
To evaluate the osteogenic adaptations induced by the intervention, BMD in the proximal femur (PF) and in whole body (WB) was determined together with the plasma concentration of BTM at baseline and after 4 and 12 months, the participants showed up in the early morning after an overnight fast and without any strenuous exercise during the preceding day or the same morning. BMD in WB and PF (femoral neck, femoral shaft, and total PF) was measured by DXA scanning (iDXA, Lunar Corporation, Madison, WI, USA) according to standard procedures. Before the scanning the participants were asked to use the toilet to empty the bladder. A resting blood sample was drawn from the antecubital vein for later analysis of the plasma concentrations of osteocalcin (OC), procollagen type-1 amino-terminal propeptide (P1NP) and carboxy-terminal type-1 collagen crosslinks (CTX-1), which were evaluated by a fully automated immunoassay system (iSYS, Immunodiagnostic Systems Ltd., Boldon, England) by method of Chemiluminescence. The performance of the assay, expressed as inter-run coefficients of variation, were 9% for P-OC, 10% for P-CTX-1, and 8% for P-PINP.
Thirty-two elderly men responded to recruitment advertisements in local newspapers, seeking non-smoking healthy men without chronic diseases, aged 65–75 years, who had not participated in regular physical activity during the preceding 5 years. After a medical examination, four subjects were excluded due to a history of cardiovascular disease (n = 2), type 2 diabetes mellitus (n = 1), and obstructive lung disease (n = 1) and one never showed up for baseline testing. Twenty-seven of the 32 elderly men, who responded initially, were therefore included in the study and were randomized and stratified by body mass index (BMI) and maximum oxygen uptake (VO2max) into a football group (F), a resistance training group (R), and an inactive control group (C). At the first training session, one subject in F suffered from an Achilles tendon rupture and was excluded from all analyses, and thus the final numbers in the three groups were: F = 9, R = 9, and C = 8; with a total of n = 26. There were no statistical differences in age, height, body mass, BMI, and VO2max between F, R, and C (Table 1). All participants were fully informed of experimental procedures and possible discomfort associated with the study before giving their written informed consent to participate. The study was carried out in accordance with the Declaration of Helsinki and approved by the local ethics committee of the Capital Region of Denmark, H-1-2011-013; ClinicalTrials.gov identifier: NCT01530035.
Training In both F and R supervised training was offered during the total intervention period of 12 months, and the training volume and
Statistical analysis Differences at baseline between F, R, and C, and longitudinal changes within and between groups were tested by two-way repeated measures ANOVA with Holm–Sidak post-hoc testing. Statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS), version 20.0 and SigmaStat, version 3.5. Results are presented as means ± standard error unless otherwise stated.
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Helge et al. Results Plasma BTMs No differences in plasma BTMs between the groups were observed before the intervention period (Fig. 1). (a)
1.0
#
0.8
CTX (ug/L)
0 months 4 months 12 months
BMD
0.6
0.4
0.2
0.0
F
(b)
80 70
#
R
C
#
0 months 4 months 12 months
P1NP (ug/L)
60 50 40 30 20 10 0
F
(c)
40
#
R
0 months 4 months 12 months
#
Osteocalcin (ug/L)
20
10
0
F
R
Prior to the intervention period, BMD in the PF did not differ between F, R, and C, except for the left total PF, which was lower (P < 0.05) in F compared with C (Table 2). A normalization of femoral BMD in relation to body mass (Table 3) revealed no difference in femoral BMD between the groups (0.79 ≤ P ≤ 1.00). Compared with baseline, the absolute BMD values after 4 and 12 months of intervention (Table 2) were changed in F, and the relative increase in BMD corresponded to 1.0% ± 0.5% (P < 0.05) and 2.9% ± 0.7% (P < 0.001), respectively, in the right total PF, and 1.1% ± 0.5% (P < 0.05) and 2.4% ± 0.8% (P < 0.001), respectively, in the left total PF. In the right femoral shaft, BMD after 4 and 12 months was 1.8% ± 0.4% (P < 0.005) and 3.5% ± 0.8% (P < 0.001) increased, respectively. After 12 months, BMD in the right and left femoral neck was increased (P < 0.001) by 3.8% ± 1.2% and 5.4% ± 2.6%, respectively (Fig. 2). For WB and left femoral shaft BMD, no interaction between group and time was observed. Discussion
C
30
C
Fig. 1. Concentration of the plasma bone turnover markers carboxy-terminal type-1 collagen crosslinks (CTX-1) (a), procollagen type-1 amino-terminal propeptide (P1NP) (b) and osteocalcin (c) for elderly men in the football training group (F), the resistance training group (R), and the control group (C) at baseline after 4 months and after 12 months of intervention. #, > 0 months; P < 0.001.
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After 4 and 12 months of football training, plasma OC was 45% ± 12% and 46% ± 11% higher (P < 0.001), respectively, than before the intervention, and plasma P1NP was 41% ± 16% and 40% ± 17% higher (P < 0.001), respectively. Plasma OC and P1NP were higher (P < 0.05) in F than in R and C after 4 and 12 months. For CTX-1, there was no interaction between time and group, but after 12 months, there was a main effect of time at 43% ± 13% (P < 0.05).
This intervention is the first to study the osteogenic effect of recreational football in comparison with resistance training in elderly men. The main findings were that football participation resulted in an augmentation in BMD in the weight bearing appendicular skeleton and a marked increase in bone formation markers, which was not seen after participation in resistance training. In addition, the bone resorption was similar after football and resistance training, which indicates that the osteogenic impact of football is primarily due to an effect on bone formation, which leads to a positive bone balance and an increase in BMD. As the osteogenic stimulus from exercise is mainly depending on the strain rate and magnitude induced by various muscle and ground reaction forces acting upon the bone (Rubin & Lanyon, 1984; Turner & Pavalko, 1998; Kohrt et al., 2009; Robling, 2009), it seems reasonable to hypothesize that an odd-impact physical activity like recreational football, which involves both kind of forces, would have a large osteogenic potential in elderly men. The hypothesis was confirmed by the findings of a profound augmentation in BMD in the left
1.008 ± 0.063 1.018 ± 0.043 1.254 ± 0.059 1.282 ± 0.045 1.083 ± 0.048 1.117 ± 0.041 1.268 ± 0.030 1.015 ± 0.066 1.009 ± 0.045 1.247 ± 0.057 1.283 ± 0.044 1.081 ± 0.046 1.112 ± 0.040 1.262 ± 0.030 1.007 ± 0.065 1.017 ± 0.043 1.243 ± 0.056 1.282 ± 0.043 1.080 ± 0.048 1.121 ± 0.038 1.266 ± 0.031 1.000 ± 0.042 1.006 ± 0.036 1.229 ± 0.056 1.229 ± 0.057 1.066 ± 0.048 1.069 ± 0.048 1.225 ± 0.024 *< C, P < 0.05. † > T0, P < 0.05. ‡ > T0, P < 0.005. § > T0, P < 0.001. ¶ > T4, P < 0.05. **> T4, P < 0.01. †† > T4, P < 0.001. Values are given as means ± standard error.
Femoral neck (FN), right Femoral neck (FN), left Femoral shaft (FS), right Femoral shaft (FS), left Total proximal femur (TPF), right Total proximal femur (TPF), left Whole body (WB)
0.921 ± 0.034§¶ 0.939 ± 0.034§†† 1.156 ± 0.042§** 1.143 ± 0.043 0.982 ± 0.031§†† 0.989 ± 0.031§¶ 1.211 ± 0.036
1.000 ± 0.043 1.010 ± 0.040 1.236 ± 0.059 1.231 ± 0.059 1.070 ± 0.049 1.068 ± 0.048 1.227 ± 0.024 0.893 ± 0.034 0.917 ± 0.032 1.138 ± 0.044‡ 1.133 ± 0.043 0.965 ± 0.032† 0.977 ± 0.031† 1.174 ± 0.035 0.888 ± 0.034 0.893 ± 0.034 1.117 ± 0.042 1.120 ± 0.041 0.955 ± 0.030 0.966 ± 0.030* 1.167 ± 0.035
1.011 ± 0.042 1.015 ± 0.037 1.237 ± 0.057 1.234 ± 0.057 1.070 ± 0.047 1.073 ± 0.046 1.227 ± 0.024
12 months (T12) 4 months (T4) 0 months (T0) 0 months (T0) 12 months (T12) 4 months (T4) 0 months (T0)
4 months (T4)
12 months (T12)
C (n = 6) R (n = 8) F (n = 9) Bone region
Table 2. Bone mineral density (g/cm2) in proximal femur and whole body for a football training (F), resistance training (R) and control (C) group before (T0) as well as after 4 (T4) and 12 (T12) months of intervention
BMD and bone turnover markers in elderly men (5.4%) and the right femoral neck (3.8%) as well as in the left (2.4%) and the right (2.9%) total PF after 12 months of recreational football, which is markedly higher than in other intervention studies examining the skeletal effect of physical activity in elderly men (Vincent & Braith, 2002; Guadalupe-Grau et al., 2009; Bolam et al., 2013). It should be emphasized that the absolute values for femoral BMD was lower in F than in R and C, albeit not significantly different, and that BMD in the left total femur was significantly lower than in C. However, when analyzing the individual responses in F, it was observed that the three subjects that had baseline BMDs above 1.0 had a similar training-induced increase in BMD as the other six subjects and that no correlations were found when correlating the BMD in PF at baseline to the absolute delta values in BMD after 4 and 12 months of football. Thus, it seems as if the marked increase in femoral BMD in F is not due to simple regression to the mean. This notion is supported by a similar finding of no correlation between BTM concentrations at baseline and absolute delta values in BTM in F. All together, this indicates that the increase in femoral BMD in F and the reported differences between the intervention groups were due to the training itself. Already after 4 months of football training in the present study, BMD in left and right total PF was augmented by 1.1% and 1.0%, respectively, which is marginally lower compared with other football interventions from our lab examining the osteogenic effects but in younger age groups and with different methods. Thus, we have found an increase in lower extremity bone mass of 41 g (P < 0.05) after 12 weeks of recreational football with 20- to 40-year-old sedentary men (Krustrup et al., 2009), and an increase in total volumetric BMD in left and right tibia of 2.6% and 2.1%, respectively, after 14 weeks of football with premenopausal sedentary women (Helge et al., 2010). Thus, from the present BMD results after 4 months of football training, it seems that elderly men exhibit a lower osteogenic response to exercise than younger individuals. However, given that the relative increases in BMD in the PF regions overall were doubled from 4 to 12 months, and that the profound BMD increases in right and left femoral neck of 3.8% and 5.4%, respectively, were not seen until 12 months of football suggest that the osteogenic BMD response in elderly men is not lower, but rather slower, compared with younger age groups. The osteogenic response after 4 and 12 months in the football group was supported by a pronounced rise in plasma BTMs. Thus, plasma OC was elevated by 45% already after 4 months of football and maintained higher after 12 months (46%), while P1NP was 41% and 40% higher after 4 and 12 months, respectively, compared with baseline. Remarkably, the bone resorption marker CTX-1 was not elevated before 12 months (43%) and only with a main effect of time. Other studies have examined the bone turnover response to training and
101
Helge et al. Table 3. Femoral bone mineral density at baseline normalized in relation to body mass (g/cm2/kg) for a football training (F), resistance training (R), and control (C) group
Bone region
F (n = 9)
R (n = 8)
C (n = 6)
Femoral neck (FN), right Femoral neck (FN), left Femoral shaft (FS), right Femoral shaft (FS), left Total proximal femur (TPF), right Total proximal femur (TPF), left
0.0114 ± 0.0004 0.0115 ± 0.0004 0.0144 ± 0.0006 0.0144 ± 0.0005 0.0123 ± 0.0004 0.0124 ± 0.0004
0.0121 ± 0.0011 0.0121 ± 0.0009 0.0150 ± 0.0015 0.0149 ± 0.0014 0.0130 ± 0.0013 0.0129 ± 0.0012
0.0116 ± 0.0011 0.0117 ± 0.0008 0.0144 ± 0.0012 0.0147 ± 0.0010 0.0125 ± 0.0011 0.0129 ± 0.0008
Values are given as means ± standard error.
0 months 4 months 12 months
(a)
BMD right femoral neck (g/cm2)
1.10 1.05 1.00
#§
0.95 0.90 0.85 0.80 0.00 F
R
C
(b)
0 months 4 months 12 months
BMD left femoral neck (g/cm2)
1.10 1.05 1.00
#§
0.95 0.90 0.85 0.80 0.00 F
R
C
Fig. 2. Bone mineral density (BMD) in the right femoral neck (a) and the left femoral neck; (b) for elderly men in the football training group (F), the resistance training group (R) and the control group (C) at baseline, after 4 months and after 12 months of intervention. #, > 0 months; P < 0.001. §, > 4 months; P < 0.05.
acute changes in the physical activity level in younger age groups, reporting an opposite response in bone resorption and bone formation markers with changes in physical activity (Karlsson et al., 2003; Scott et al., 2011; Weiler et al., 2012). Thus, it has been reported (Karlsson et al., 2003) that in male premier league football players, that plasma OC and CTX-1 at the end of the
102
season were 22% and 34% higher, respectively, compared with a control group. However, after 2 weeks of rest between the football seasons the CTX-1 concentration was elevated by 8%, and the P1CP concentration was reduced by 21% compared with the end of the season, while OC and P1CP did no longer differ from the controls, whereas CTX-1 still was higher than in the controls. Ten days into the new football season, these changes were no longer present; P1CP was elevated by 23%, and CTX-1 was decreased by 4% compared with the end of the resting period. The time course of these changes in BTM (the elevation of the bone formation markers first, followed by a delayed elevation of bone resorption markers) induced by exercise is similar to the anabolic effect of PTH treatment (Glover et al., 2009), which indicate that exercise and PTH acts through a similar anabolic mechanism. However, from the present study, it cannot be determined whether both stimuli act through the same regulatory pathway. To further examine the mechanism behind the osteogenic stimulus of exercise, future studies may include analysis of plasma sclerostin, which is an antagonist of the Wnt signaling pathway that increases osteoblast activity, and which might be down-regulated due to mechanical loading (Ardawi et al., 2012). In contrast to recreational football, resistance training in the present study did not seem to have any osteogenic effect, neither after 4 nor 12 months, and the plasma BTM did not change in this group. This is not in agreement with a review on exercise and bone mass (Guadalupe-Grau et al., 2009), reporting that in elderly men, BMD improvements of 1–3% in the appendicular weight-bearing bones and in the lumbar spine can be expected after 6 months of high intensity (> 70% 1 RM) resistance training. A reason to the finding of no osteogenic effect of resistance training in the present study may have been too low intensity, only progressively increased to 8 RM after 13 weeks of training. This progression was chosen to minimize the risk of muscle and back injuries as the participants were sedentary and elderly men. Nevertheless, it appears that football has the potential to induce an earlier and more pronounced osteogenic response than resistance training likely because of the combination of muscle and gravitational forces in football (Kohrt et al., 2009).
BMD and bone turnover markers in elderly men In conclusion, 4 months of recreational football for elderly men had an osteogenic impact, which was further developed after 12 months. The osteogenic impact, evaluated from BMD as well as bone formation and bone resorption markers, was higher after football than after resistance training, which showed no osteogenic effect. The anabolic response induced by football may be due to increased bone turnover, especially improved bone formation. The present results are promising regarding the osteogenic effect of football as a health-enhancing physical activity for elderly males that may diminish the age-dependent bone loss and the risk of osteoporosis.
BTM profile, the anabolic response in the football group may be due to a substantial improvement in bone formation already after 4 months, while there seemed to be a delayed increase in bone resorption. Overall, the bone turnover rate was increased in the football group, but in favor of bone formation, which in the long run may diminish the age-dependent decrease in bone mass. Thus, it seems that recreational football can be recommended as physical activity that improves bone health and diminishes the risk of osteoporosis, even in elderly people. Key words: Bone metabolism, BMD, soccer, resistance training, osteogenic impact.
Perspectives After only 4 months, recreational football for elderly men had a marked osteogenic effect on BMD in the weight-bearing bones, and after 12 months, the improvement was more than doubled. Resistance training had no impact on BMD. As evaluated from the
Acknowledgements The study was supported by Nordea-fonden, FIFA – Medical Assessment and Research Centre (F-MARC), Preben and Anna Simondsen fonden, and The Danish Ministry of Culture (Kulturministeriets Udvalg for Idrætsforskning).
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