The duration of exercise as a regulator of bone mass

Bone Vol. 28, No. 1 January 2001:128 –132

The Duration of Exercise as a Regulator of Bone Mass M. K. KARLSSON,1 H. MAGNUSSON,1 C. KARLSSON,1 and E. SEEMAN2 1

Department of Orthopaedics, Malmo University Hospital, Malmo, Sweden Austin and Repatriation Medical Centre, University of Melbourne, Melbourne, Australia

2

elderly. Of these alternatives, the skeleton appears to be most responsive to physical activity during growth and adolescence.2,3,5,7,12,17–19,22,23,30,32,33,35 Available evidence suggests that the intensity rather than the duration of exercise is the main determinant of BMD.4,7 Also, BMD correlates with the numbers of cycles of repetitive strain rather than the duration of exercise.27,28 Thus, if the aim of exercise is to increase peak BMD, high-impact loading rather than longer duration of exercise appears to be preferred. The duration of a specific exercise needed to achieve a given peak BMD is poorly defined.4,7,18,35 Useful public health information would include defining the duration of activity above which no further biologically important benefits of BMD are achieved. We asked: (1) Do male soccer players have higher BMD than sedentary controls? (2) If so, do the soccer players with a longer duration of activity have higher BMD?

Exercise is associated with increased peak bone mineral density (BMD). To determine the relationship between the duration of exercise and BMD, we measured BMD of the axial and appendicular skeleton by dual-energy X-ray absorptiometry (DXA), and speed of sound (SOS), broadband attenuation (BUA), and stiffness index by quantitative ultrasound (QUS) of the calcaneus, in 67 active male national soccer players (mean age 23 years, range 17–35), which included 23 premier-league players exercising 12 h/week (range 8 –18), 23 third-league players exercising 8 h/week (range 3–18), and 21 sixth-league players exercising 6 h/week (range 2–10). Results were compared with 24 sedentary ageand gender-matched controls and presented as mean ⴞ SEM. BMD was higher in all weight-bearing regions for the whole group relative to controls (BMD: total body 6.8 ⴞ 0.7%, leg 9.6 ⴞ 0.8%, lumbar spine 13.2 ⴞ 1.2%, femoral neck 12.7 ⴞ 1.2% [all p < 0.001]; calcaneus SOS 4.2 ⴞ 0.3%, BUA 8.7 ⴞ 1.5%, and stiffness index 24.2 ⴞ 2.0% [all p < 0.01]). No differences were found in head or arm BMD. There were no differences in BMD or QUS measurements when comparing soccer players exercising for different activity durations. Duration of activity correlated with BMD weight-loaded regions and with QUS, provided it was less <6 h/week (p < 0.01 respectively), but not when exercising more frequently. Femoral neck BMD increased by 3.3% across every hour increase in activity in those with 0 – 6 h of exercise/week and by 0.7% in those exercising more than this (p < 0.01). We conclude that, in national-league soccer, the BMD needed to attain a bone strength commensurate with that of duration of activity is achieved by 6 h of exercise per week. Beyond this, additional exercise confers no higher BMD. The skeleton adapts to the prevalent level of exercise intensity required and no further. (Bone 28:128 –132; 2001) © 2001 by Elsevier Science Inc. All rights reserved.

Materials and Methods We studied 67 active male soccer players with a mean age of 22.7 years (range 17–35). These players competed at different league levels for 2–18 h/week. All had been playing soccer since puberty, and on a competitive level for at least 5 years. The training mainly consisted of weight-loaded activities such as running with constant changes of direction, jumping, and ball activities including playing soccer. Activities using external weights were done mainly during preseason training. During the season, one or two competitive matches were played every week. The controls were healthy and ambulant with no diseases known to affect bone and consisted of either volunteers or individuals selected randomly from city files. They participated in impactloaded recreational sports for 2.7 h/week (range 0 –10). A questionnaire was used to document present exercise (hours per week), occupation, alcohol and tobacco use, diseases, and medications. Three soccer players were not administered the questionnaires. Twenty-three cases (mean age 22.8 years, range 17–34) were professional athletes playing in the premier national league, 23 with a (mean age 21.8 years, range 18 –28) were playing in the third national league, and 21 (mean age of 23.8 years, range 17–35) were playing in the sixth national league. Twenty-four male volunteers (mean age 24.4 years, range 19 –29), were included as controls. The premier-league soccer players exercised at a mean of 11.9 h/week (range 8 –18), the third-league players exercised at a mean of 7.7 h/week (range 3–18), and the sixth-league players exercised at a mean of 6.0 h/week (range 2–10). Dual-energy X-ray absorptiometry (DXA; Lunar DPX-L, Lunar Corp., Madison, WI) was used to measure total body and regional BMD (g/cm2) and total body fat and lean mass. DXA

Key Words: Athletes; Bone mineral density (BMD); Dualenergy X-ray absorptiometry (DXA); Exercise; Quantitative Ultrasound (QUS). Introduction Exercise may contribute to the prevention of osteoporosis by increasing peak bone mineral density (BMD), reducing age-related bone loss, or restoring bone already lost in the Address for correspondence and reprints: Dr. Magnus Karlsson, Department of Orthopaedics, University Hospital MAS, S-205 02 Malmo, Sweden. © 2001 by Elsevier Science Inc. All rights reserved.

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8756-3282/01/$20.00 PII S8756-3282(00)00405-1

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Table 1. Age (years), height (cm), weight (kg), present activity (h/week), bone density (g/cm2), body composition (kg), and ultrasound calcaneus in active soccer players exercising at different levels and controls (mean ⫾ SEM)

Number Age Height (cm) Weight (kg) Present activity (h/wk) Bone mineral density (g/cm2) Head Arms Total body Legs Trunk Pelvic Lumbar spine (L2–4) Femoral neck Ward’s region Trochanter region Body composition (kg) Total lean mass Total fat content Quantitative ultrasound Speed of sound (m/sec) Broadband ultrasound attenuation (MHz/dB) Stiffness index

All soccer players

Premier league players

Third-league players

Sixth-league players

Controls

67 22.7 ⫾ 0.5 180.5 ⫾ 0.6 77.4 ⫾ 0.9 8.6 ⫾ 0.4c

23 22.8 ⫾ 0.8 181.0 ⫾ 1.1 77.8 ⫾ 1.5 11.9 ⫾ 0.5c,e,g

23 21.8 ⫾ 0.7c 179.7 ⫾ 1.1 75.6 ⫾ 1.4 7.7 ⫾ 0.6c,h

21 23.8 ⫾ 1.1 180.9 ⫾ 1.0 79.0 ⫾ 1.8 6.0 ⫾ 0.5c

24 24.4 ⫾ 0.6 181.3 ⫾ 1.6 77.4 ⫾ 1.8 2.7 ⫾ 0.6

2.10 ⫾ 0.02 1.01 ⫾ 0.01 1.33 ⫾ 0.01c 1.54 ⫾ 0.01c 1.13 ⫾ 0.01c 1.44 ⫾ 0.01c 1.44 ⫾ 0.02c 1.33 ⫾ 0.01c 1.32 ⫾ 0.02c 1.22 ⫾ 0.02c

2.06 ⫾ 0.04 1.02 ⫾ 0.01 1.35 ⫾ 0.01c 1.58 ⫾ 0.02c 1.16 ⫾ 0.01c 1.47 ⫾ 0.02c 1.46 ⫾ 0.02c 1.35 ⫾ 0.02c 1.33 ⫾ 0.04b 1.25 ⫾ 0.02c

2.10 ⫾ 0.05 0.99 ⫾ 0.02 1.31 ⫾ 0.02b 1.52 ⫾ 0.02c 1.13 ⫾ 0.02c 1.41 ⫾ 0.02c 1.43 ⫾ 0.03c 1.34 ⫾ 0.03c 1.33 ⫾ 0.04b 1.20 ⫾ 0.03c

2.06 ⫾ 0.03 1.03 ⫾ 0.01 1.34 ⫾ 0.01c 1.54 ⫾ 0.02c 1.11 ⫾ 0.01c 1.44 ⫾ 0.02c 1.43 ⫾ 0.03c 1.30 ⫾ 0.02b 1.31 ⫾ 0.03b 1.21 ⫾ 0.03c

2.16 ⫾ 0.04 1.00 ⫾ 0.02 1.25 ⫾ 0.01 1.41 ⫾ 0.02 1.02 ⫾ 0.01 1.26 ⫾ 0.02 1.27 ⫾ 0.03 1.18 ⫾ 0.03 1.15 ⫾ 0.04 1.04 ⫾ 0.03

62.0 ⫾ 0.5 12.0 ⫾ 0.6

64.2 ⫾ 1.0d,f 11.3 ⫾ 0.7

60.6 ⫾ 0.8 10.8 ⫾ 0.9

61.7 ⫾ 0.7 14.0 ⫾ 1.5

62.4 ⫾ 1.6 12.8 ⫾ 1.4

1641.2 ⫾ 4.7c 134.1 ⫾ 1.8b

1642.2 ⫾ 5.8c 135.8 ⫾ 2.6b

1649.8 ⫾ 9.01c 134.5 ⫾ 3.8a

1628.8 ⫾ 9.8c 131.4 ⫾ 2.8a

1577.7 ⫾ 9.1 123.3 ⫾ 2.7

128.7 ⫾ 2.0c

130.0 ⫾ 3.0c

131.4 ⫾ 3.6c

123.4 ⫾ 4.0b

103.6 ⫾ 3.8

p ⬍ 0.05; p ⬍ 0.01; p ⬍ 0.001: when comparing soccer players and controls. p ⬍ 0.01; ep ⬍ 0.01: when comparing first-league players and third-league players. f p ⬍ 0.05; gp ⬍ 0.001: when comparing first-league players and sixth-league players. h p ⬍ 0.05: when comparing third-league players and sixth-league players. a

b

c

d

also measured the amount of mineral in the bone (i.e., the absolute bone mass).9 The precision of the DXA measurements in vivo were: total body 0.4%; lumbar spine 0.5%; femoral neck 1.6%; lean mass 0.6%; and fat mass 4.1%. The hip scan was excluded in four soccer players and in three controls and the total body scan was done in four soccer players and one control due to technical errors such as small measuring areas and blurry pictures. Quantitative ultrasound (QUS) (Lunar Achilles, Lunar Corp., Madison, WI) was used to measure speed of sound (SOS) (m/sec), ultrasound broadband attenuation (BUA; dB/MHz), and the Lunar stiffness index (SI) [(0.67 ⫻ BUA) ⫹ (0.28 ⫻ SOS) ⫺ 420] of the calcaneus in 51 soccer players and 15 controls. The SI is a measurement provided from the manufacturer that takes both SOS and BUA into account. QUS may also measures qualitative factors of the skeleton such as skeletal architecture, trabecular connectivity, and bone matrix properties.9,10,14 The levels of precision for the QUS measurements in vivo were: SOS 0.3%, BUA 2.2%, and SI 2.6%. Differences between the groups were determined by multiple analysis of variance (MANOVA). If statistical significance was found, Student’s t-test between means was used to compare groups. Differences between groups after adjusting for differences in age, present activity level, and body composition were done by multiple analysis of covariance (MANCOVA). Slopes in those exercising less or more than 6 h/week were compared by analysis of covariance (ANOVA). Multiple regression was used to correlate present activity, age, total lean mass, and total fat mass with BMD and QUS measurements. The chi-square test was used for evaluating differences in lifestyle factors. Results are presented as mean ⫾ SEM, or mean and range, unless stated otherwise.

Results As shown in Table 1, the soccer players had higher BMD in weight-bearing regions compared to controls (total body 6.8 ⫾ 0.7%, legs 9.6 ⫾ 0.8%, pelvis 14.3 ⫾ 0.9%, lumbar spine 13.2 ⫾ 1.3%, and femoral neck 12.7 ⫾ 1.2%, all p ⬍ 0.001). No differences were found in head BMD or BMD of the arms. Higher BMD was found after adjusting for differences in QUS (legs 8.8 ⫾ 0.8%, p ⫽ 0.05; pelvis 14.5 ⫾ 0.9%, p ⬍ 0.001; lumbar spine 13.2 ⫾ 1.3%, p ⫽ 0.08; and femoral neck 18.7 ⫾ 1.2%, p ⬍ 0.01). QUS measurements at the calcaneus were higher in the soccer players before (SOS 4.2 ⫾ 0.3%, BUA 8.7 ⫾ 1.5%, and stiffness index 24.2 ⫾ 2.0%, all p ⬍ 0.01) and after adjusting for differences in BMD (SOS 3.6 ⫾ 0.3% and stiffness index 21.6 ⫾ 2.0%, both p ⬍ 0.01). The differences in BMD and QUS relative to controls were maintained after adjusting for differences in age and body composition (data not shown). BMD and QUS were no higher in the group exercising for ⬃12 h/week compared with the other groups exercising for a mean of 8 and 6 h/week, respectively, before or after adjusting for differences in age, current activity level, and body composition. In a multiple regression analysis correlating age, current duration of activity, total body fat, and total body lean mass with BMD in weight-loaded regions, the only consistent independent correlation was found for current duration of activity (vs. femoral neck BMD, r ⫽ 0.40, p ⬍ 0.001). Using the same model, current duration of activity was also independently correlated with SI (r ⫽ 0.42, p ⬍ 0.01) and total body fat (r ⫽ ⫺0.28, p ⬍ 0.05). There was a correlation between duration of exercise and BMD in weight-loaded regions and QUS measurements within the range of exercise of up to 6 h/week (the mean duration of

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Bone Vol. 28, No. 1 January 2001:128 –132

Figure 1. Femoral neck BMD, stiffness index, and head BMD correlated with current activity level in soccer players exercising for more or less than 6 h/week. Current activity level correlated significantly with femoral neck BMD and with stiffness index in individuals exercising ⬍6 h/week (p ⬍ 0.01, respectively), but not in athletes exercising more. When comparing individuals exercising more or less than 6 h/week, the two slopes differed significantly (femoral neck, p ⬍ 0.05; stiffness index, p ⬍ 0.01).

exercise in the sixth-league players). No correlation was observed in those exercising ⬎6 h/week (Figure 1). Femoral neck BMD increased by 3.3% across every hour increase in activity level in those exercising ⬍6 h/week, about fivefold higher than the 0.7% increase across every hour increase in activity in the those exercising more (p ⬍ 0.05). The corresponding increase in SI was 5.9% across every hour increase in activity in those exercising ⬍6 h/week, and there was a 0.2% increase in those exercising more (p ⬍ 0.01) (Figure 1). The first-league soccer players had a longer duration of activity than the third- and sixth-league players; the third-league players had a longer duration of activity than the sixth-league players (Table 1). The first-league players had higher total body lean mass than the third and sixth-league players, whereas there were no differences when comparing the third- and the sixth-league players (Table 1). The difference remained after adjusting for differences in duration of activity.

Discussion We confirm that higher BMDs were seen in weight-bearing regions in active soccer players and that the effects were regionspecific.1,6,24,37 The head and the arms, two minor loaded regions during soccer exercise, showed no increase in BMD compared to controls. Weight-bearing activity increased bone mass more than non-weight-bearing activity in weight-loaded skeletal regions, but not in unloaded regions.13,33 Also, longitudinal studies support exercise-related beneficial skeletal effects.3,5,30,32 We extend these observations by reporting that the duration of activity correlated with BMD at levels of ⬍6 h/week only. No differences were found in BMD or QUS measurements in the three groups of soccer players, all exercising ⱖ6 h/week. No correlation was found between duration of exercise and BMD in individuals exercising ⬎6 h/week, suggesting that 6 h/week of soccer is sufficient to produce the required increase in bone strength. At this level of duration of soccer exercise, any further increase in duration of activity did not appear to increase BMD

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further. No correlation was found in BMD at non-weight-bearing sites and the duration of activity, confirming the view that exercise has region-specific effects.21 These data also confirm data from MacDougall et al. who reported an increase in tibial BMD in runners up to 20 miles/week but no further BMD gain above this point.29 No correlation between duration of activity and BMD was done in this study. In addition, Granheden et al. found in weight-lifters a limit at which a further increase in duration of activity did not confer higher BMD.11 It is likely that the intensity (how hard or intense the soccer players trained during a specified training session), as well as the duration of the training, was higher in the first-league players. Even after adjusting for differences in duration of activity, the first-league players had higher lean body mass, indicating a higher intensity, resulting in higher muscle mass. Nevertheless, neither BMD nor SOS were higher in the first-league players than in the sixth-league players. Although we have no measure of the intensity of the exercise, the findings suggest that perhaps both intensity and duration of activity reach a level at which further increases do not confer higher BMD. Our studies in humans coincide with animal models, suggesting a short period of multidirectional loads to achieve the maximal increase in BMD.26 –28 The finding of a higher BMD in soccer players after adjusting for differences in QUS measurements as well as higher a SOS and SI after adjusting for differences in BMD support the notion that DXA and QUS may measure different properties of bone.31–33 We previously reported lower SOS, BUA, and SI, despite the same BMD, when comparing groups with different skeletal architecture.20 If QUS evaluates microarchitectural features, then trabecular width or connectivity, geometry, bone size, ultrastructure, quality of bone matrix or nonskeletal factors such as soft-tissue composition and thickness are unclear. No definitive morphological differences have been found to be associated with QUS.8,15,20,25,36 The findings of independently higher DXA and QUS measurements are of clinical importance, as both methods are independent predictors of bone strength and future fractures.8,10,31 In conclusion, exercise at ⬎6 h/week does not appear to confer any added BMD benefit to men playing competitive national-league soccer. Higher levels of QUS may reflect different structural changes in soccer players but few data are available defining the structural basis of any advantage over the BMD measurement. We conclude that the skeleton will adapt to the current activity needed to maintain strength, and increasing the duration of exercise above the established level confers no additional benefit.

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Acknowledgments: Financial support was obtained from the Swedish Medical Research Council (ALF) and Lund University Founds, Malmo University Hospital Foundations (HSF).

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Date Received: September 6, 1999 Date Revised: August 24, 2000 Date Accepted: August 24, 2000