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Exercise and bone mineral density in mature female athletes


Medicine & Science in Sports & Exercise: March 1997 - Volume 29 - Issue 3 - p 291-296
Clinical Sciences: Clinical Investigations

An understanding of the relationship between weight-bearing activity and bone mineral density (BMD) is important in devising strategies to maximize and maintain skeletal strength in the female population, particularly those entering menopause. Three contrasting groups (N = 20) of mature female athletes (42-50 yr) with long-term (>20 yr) histories of significant training and performance in their chosen sport were studied cross-sectionally. The groups were: (i) high impact sport (netball/basketball; HIGH), (ii) medium impact sport (running/field hockey; MED) and (iii) a nonimpact sport(swimming; NON) and (iv) a nonsport control group (CON; N = 20). Whole body and regional BMD and body composition (fat and lean mass) were measured by dual-energy x-ray absorptiometry. Isometric strength of dominant arm flexors and leg extensors was measured by a strain tensiometer. With an alpha level of significance of 0.05, HIGH showed significantly greater whole body and regional leg BMD than NON or CON. MED registered higher values than CON for whole body and regional leg BMD. Only HIGH had significantly greater leg strength than CON. Regional arm BMD was significantly greater in all exercising groups compared with CON, but no significant difference in arm strength was found between any groups. The athletic groups all had significantly lower body fat and higher height-corrected lean mass than CON. Height-corrected lean mass, height and leg extensor strength, but not calcium intake, arm flexor strength or body fat, were significant predictors of whole body and regional arm and leg BMD. Using the significant predictors as covariates, the impact groups (HIGH/MED) had significantly higher whole body BMD than CON. HIGH also had significantly higher whole body BMD than NON and both impact groups were greater than NON in regional leg BMD. Results suggest that females who participate regularly in the premenopausal years in high impact physical activity tend to have higher BMD than nonathletic controls.

Department of Human Movement, Edith Cowan University, Joondalup, WESTERN AUSTRALIA; Department of Endocrinology and Diabetes, Sir Charles Gairdner Hospital, Nedlands, WESTERN AUSTRALIA; and Department of Medical Technology and Physics, Sir Charles Gairdner Hospital, Nedlands, WESTERN AUSTRALIA

Submitted for publication December 1995.

Accepted for publication August 1996.

Address for correspondence: Mrs. Jan Dook, Department of Biochemistry, University of Western Australia, Nedlands, 6907 Western Australia.

Present address for Dr. Colin James: Department of Physiology and Science, University of Greenwich, Avery Hill Campus, Woolwich, London, U.K.

Present address for Dr. Kathy Henderson: Garvan Institute of Medical Research, St Vincents Hospital, Darlinghurst, NSW Australia.

The inevitable age-related loss of bone tissue and muscle strength can be very debilitating in the elderly, leading to a loss of independent living and a deterioration in the quality of life. With no completely effective treatment to restore lost bone or deformity resulting from fracture, prevention is an important management strategy. The accumulation of bone tissue has been found to be strongly influenced by hormonal and nutritional status (4), genetic inheritance(16,17,19) and physical activity or mechanical usage (8). Exercise, a factor that can be relatively easily manipulated, has been associated with higher bone mineral density (BMD) in a variety of populations ranging from adolescents(18) to elderly females(25,28).

Muscle strength is also a factor to be considered. There is an age related loss of muscle function, but aging athletes are stronger than their sedentary counterparts (33). Lack of muscle strength has been implicated as a factor in the incidence of falls leading to bone fracture(15) and can influence the ability to perform simple tasks such as rising out of a chair or visiting the toilet(13).

The most effective exercise protocols to maximize and maintain BMD have not been firmly established. There is some indication that exercise that is weight bearing is more beneficial for bone health than non-weight-bearing activities(18). It has also been suggested that exercise producing versatile impact-type loading on the skeleton may be more osteogenic(11). In a cross-sectional analysis, Nilsson and Westlin(22) found the highest bone density in weight lifters followed (in descending order) by throwers, runners, soccer players, and swimmers. They noted increasing bone density of the leg with increasing loads on the lower limbs within the group of athletes. However, Orwoll et al.(24) found that female swimmers aged 40-65 yr did not have higher vertebral BMD than age-matched sedentary women although male swimmers had significantly higher BMD than sedentary males.

The purpose of this study was to determine if more than 20 years of consistent athletic training and competition in mature women involved in nonimpact, medium impact, or high impact disciplines had a positive effect on BMD compared with sedentary controls.

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Different sports place different mechanical loads on the body. Three categories of sports with different levels of ground reaction forces were selected for the present study. Netball, a game similar to basketball has been found to generate ground reaction forces of 3.9-4.6 times body weight(30). Both netball and basketball are running games that include vertical jump-landing sequences as an integral part of the game and are therefore likely to produce a variable pattern of high strain rates within the skeleton. They were designated HIGH. Running has produced ground reaction forces of about 2-3 times body weight (3). Field hockey, a team game involving running but little in the way of substantial jumpland sequences, and running were combined to represent medium impact activity(MED). The third activity selected was swimming representing nonimpact activity (NON).

Subjects. Female athletes participating in the Australian Masters Games were screened as possible subjects. Athletes participating in the identified activities were approached individually by telephone and invited to participate. Volunteers provided additional information regarding their menstrual history, training status, smoking, and alcohol use. To determine their competition standard and lifelong commitment, volunteers were requested to list activities in which they currently or had previously participated, time commitments to those activities, and their highest sporting achievement. To ensure there were no prolonged breaks (greater than 3 yr), volunteers were also asked to recall historical physical activity in hours/week which was condensed to 3 age groupings: 13-20 yr, 21-30 yr, and 31-50 yr.

To meet the criteria for inclusion in the study, the subjects: (a) were older than 40 yr (mean, 45.8 yr), (b) had the last menstrual period within last 12 months, (c) were nonsmoking, (d) had long and consistent training history (a minimum of 20 yr) in their chosen sport, (e) participated in only one of the identified activities: netball and/or basketball, running and/or field hockey, or swimming, (f) were competition standard: a minimum of“A” grade, district or state representative, and (g) had begun participation in the sport prior to 13 yr of age. In this study 76% of subjects reported normal menstruation, 18% reported altered menses, and 6% had finished menstruation within the preceding 12 months. Athletes who had participated regularly in any other sport were excluded. No subjects were taking medication or had a medical condition known to alter bone or calcium metabolism. With the exception of one netball/basketball player who consumed 56 standard drinks per week, all subjects consumed a moderate amount of alcohol (14 units per week) or less.

From these data three groups of 20 athletes were selected. In addition, a control group (CON, N = 20) of nonsmoking, age, and menstrual-status matched females, who throughout life had not participated in any form of regular sporting activity were recruited from the institution where the study was conducted. The protocol for the study was approved by the Ethics Committee of Edith Cowan University and volunteers gave their written informed consent.

Bone mineral density and body composition evaluation. Bone mineral density (BMD, in g·cm-2), total body fat (kg), and total lean mass (kg) were assessed using dual energy x-ray absorptiometry (DXA; Hologic QDR 2000, Hologic, Inc., Waltham, MA). Measurement consisted of a whole body scan using an array beam. Subjects removed all metal objects and were positioned in the supine position with hands placed prone on either side of the body and with legs held 10 cm apart according to the specifications of the manufacturer. Measurement of whole body BMD using DXA has a reproducibility of 0.96% in our laboratory. Reproducibility for regional leg and arm BMD is 2%. Measurement of body fat (kg) has a reproducibility of 1.12% and lean mass (kg) of 0.44% (N = 5, duplicate studies on the same day with repositioning). The total radiation dose of one DXA scan is 10-30μSv (9). All bone scans were analyzed by the same operator with subregions positioned according to manufacturer's instructions. The arm subregions were defined by a vertical division positioned through the glenoid fossa, and the leg subregions were defined by angled dividers bisecting the femoral neck. Therefore, shoulder and pelvic subregions were not included in the limb subregional analyses.

Muscle strength assessment. Isometric muscle strength (N) of the dominant arm flexors and leg extensors was measured at 90° flexion(checked by a goniometer) using an electronic cable tensiometer attached to a strength chair (5,20). Subjects were stabilized by inextensible straps across the chest and hips to prevent undue body movement. The limb was placed in a cuff, and limb position measured to be at 90° flexion. The cuff was placed around the volunteer's supinated wrist at the level of the styloid processes for measurement of the arm flexors and at the level of the lateral and medial malleoli (ankle) for measurement of the leg extensors. Participants performed three isometric contractions with approximately 10 s rest between attempts. The force produced was measured using an electronic force transducer (14) with output fed into an analog to digital converter (Boston Technology PC30G, Cambridge, MA) and displayed on a PC. The measurement of leg extensor strength has a reproducibility of 1.4% and arm flexor strength 2.3% in our laboratory(N = 7, duplicate studies on consecutive days).

Calcium intake assessment. Daily calcium intake(mg·d-1) was estimated by an adapted food frequency questionnaire (2). The results from the food frequency questionnaire were analyzed on a spreadsheet using PC Diet software (Version 4.0. Peter Austin, Edith Cowan University).

Anthropometric measurements. Height was measured by a stadiometer to the nearest 0.5 cm. Weight was measured by a “chair” beam balance to the nearest 0.5 kg.

Data management and analysis. Statistical analyses were performed using the software packages Statview SE+Graphics (1988 Abacus Concepts, Inc., Berkeley, CA), Super ANOVA (1989-1991 Abacus Concepts, Inc.) and SPSS® 4(1990 Norusis & SPSS, Inc., Chicago, IL). Data for variables were compared between groups using one-way ANOVA with post-hoc Tukey Compromise tests to determine any significant differences between groups. Bivariate correlations were assessed by Pearson's correlations and used to identify potential covariates. The influence of the potential covariates was evaluated using ANCOVA. Possible confounding problems related to differences in stature were controlled for by correcting lean mass for its association with height using regression residuals in the manner described by Willet and Stampfer(32). An alpha level of 0.05 was accepted for significance.

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Anthropometric and dietary descriptors for the four groups are shown inTable 1. There were no significant differences between groups in age, height, weight, calcium intake, or alcohol intake. All athletic groups reported significantly more historical activity (h·wk-1) at all ages than the sedentary controls. Although there were no significant differences between groups in total body weight or height, examination of the data (Table 1) suggested that the MED group tended to be smaller in stature than the HIGH group with the other two groups intermediate. As height was a determinant of lean mass (r = 0.74, P < 0.01), lean mass was corrected for its association with body height prior to further analyses. The resultant variable is referred to as corrected lean mass(Table 2).

Body composition. All exercising groups had significantly higher corrected lean mass than the control group (P < 0.05,Table 2). The control group had significantly higher fat mass than each of the exercising groups (P < 0.05). There were no differences between exercising groups in fat mass or corrected lean mass.

Muscle strength. The HIGH group had significantly greater leg extensor strength than the CON group (P < 0.05,Table 2). There were no other significant between group differences in leg extensor strength. There were no significant differences between groups in arm flexor strength.

Bone mineral density. There were significant between-group differences in BMD at all sites (whole body P < 0.0001; regional leg P < 0.0001; regional arm P < 0.001,Table 2). Post-hoc Tukey Compromise tests(P < 0.05) showed the differences in whole body BMD were significant between HIGH and NON and HIGH and CON. The whole body BMD of the MED group was also significantly higher than CON. Both HIGH and MED impact groups had significantly higher leg BMD than NON and CON groups. All of the exercising groups had higher arm BMD than the control group (P < 0.05). Bone mineral density of the two impact groups did not differ significantly at any of the sites tested.

To identify potential covariates that may have been accentuating or masking the between group differences in BMD related to the impact-loading characteristics of their sporting participation, all groups were considered simultaneously and correlations between whole body BMD, regional leg BMD, and regional arm BMD as the dependent variables, and the independent variables calcium intake, height, corrected lean mass, fat mass, leg extensor strength, and arm flexor strength were computed. Height, corrected lean mass, and leg extensor strength correlated significantly with BMD at all sites(Table 3). Calcium intake, fat mass, and arm flexor strength did not correlate with BMD at any site.

To focus on between-group differences in BMD related only to the impact-loading nature of the subjects' exercise participation, the previously determined significant predictors of BMD (height, corrected lean mass, and leg extensor strength) were incorporated into the ANOVA model as covariates. As there were no significant interactions between the covariates and exercise group, the models were estimated using a common slope. The resultant models showed a significant difference between groups in whole body BMD corrected for height, corrected lean mass, and leg extensor strength (P < 0.005). Post-hoc Tukey Compromise tests (P < 0.05) showed that both impact groups (HIGH and MED) had significantly higher corrected whole body BMD than the control group. Differences between HIGH and NON were also significant. There were significant between-group differences in regional leg BMD (P < 0.005). Post-hoc tests showed that HIGH and MED groups had significantly higher corrected regional leg BMD than CON. Differences between HIGH and MED groups and NON were also significant. There were no significant between group differences in corrected regional arm BMD (P < 0.3). Least squares means of BMD at each site corrected for height, corrected lean mass, and leg extensor strength derived from the ANCOVA models are presented in Table 4.

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This study has examined cross-sectionally the effects of prolonged, life-long, participation in sports that involve different levels of impact loading. A major finding of the study is that long-term involvement in an impact-loading activity, such as netball/basketball or running/field hockey is associated with greater whole body and regional leg BMD than long-term abstinence from sporting participation. Long-term participation in swimming, a non-impact-loading activity, was associated with intermediate levels of BMD that did not differ significantly from those of the nonsporting subjects. Owing to the cross-sectional nature of this study, it is impossible to be certain whether this relationship is causal. Women with the potential for high level athletic performance may have a genetic blueprint favoring muscle and bone development and may have achieved higher BMD regardless of their training history. However, the evidence suggests that even though heredity exerts a major influence lifestyle factors such as exercise are important in maximizing bone and muscle development (16,17).

Lanyon (19) reviewed animal studies and concluded that repetitive, lower peak loads do not exert as great an osteogenic response as high strain loads. Therefore, it was postulated in this study that subjects with a long history of participation in sports associated with differing levels of impact loading would have detectable differences in BMD.

Although running (and field hockey, MED) can be considered as a series of repetitive jump-land phases with landing from an airborne phase subjecting the body to ground reaction forces of 1.6-3.0 times body weight(6,23) these sports involve little in the way of pronounced jump-landing sequences. In contrast, netball and basketball (HIGH), also both running games, incorporate vertical jump-landing sequences as an integral part of the game. Ground reaction forces of 4.1-6.0 times body weight while landing from a basketball rebound have been reported(31), and netball players have generated ground reaction forces of 3.9-4.6 times body weight (30). Swimming is an active but non-weight-bearing sport. The impact activities (HIGH, MED) are essentially “leg” dominated, while swimming (NON) uses forces generated from both arms and legs to generate forward motion.

The results from the BMD measurements are consistent with Lanyon's(19) theory. The impact-loading activities were associated with higher BMD values at the whole body and regional leg sites. Regional arm BMD, not subjected to impact loading in any of the sports, did not differ among groups after covariates were added to the ANOVA models. The ground reaction forces generated from activities such as netball and basketball would exert high strain loads on the body while swimming exerts little impact loading. Running (and field hockey) could be considered to be repetitive, and although there are no significant differences between HIGH and MED, there is a trend that the greater the impact the higher the BMD score. The inability to detect significant differences in BMD among groups participating in activities considered to be of different levels of impact loading (HIGH and MED) may be a result of insufficient subject numbers (Type II error) or insufficient difference in the magnitude of impact loading between the sports selected. Furthermore, other factors such as the rate of strain, strain distribution, and playing surface not considered in the selection of activities for this study may also be associated with the skeletal adaptive response (11). These factors may be blurring impact-loading related differences in BMD between HIGH and MED.

The lack of a significant difference between the NON and CON may underlie the importance of impact. Fehling et al. (7) found premenopausal athletes participating in the impact activities of gymnastics and volleyball had higher whole body BMD than swimmers and sedentary controls. It is significant that (as with our results) there was no statistical difference in BMD between the swimmers and controls. It appears that non-weight-bearing activities do not offer a sufficiently high level or diversity of strain to the skeleton to influence bone remodeling.

All of the exercising groups had greater lean mass (corrected for body height) than CON. This is an expected outcome since exercise is often associated with hypertrophy of muscle tissue (13). The finding of a significant correlation between whole body BMD and lean body mass is in contrast to Reid et al. (26) who reported no association between lean body mass and BMD but is in keeping with the findings of Henderson et al. (12). Possibly the athleticism of this sample makes their body composition quite different from the subjects studied by Reid et al. (26) who were normal, healthy nonathletic women. Interestingly, participation in impact-loading sport (HIGH, MED) remained a significant determinant of whole body and regional leg BMD even after the addition of corrected lean mass as a covariate to the ANOVA model. This suggests that although exercise participation is associated with favorable changes to body composition there remains an additional benefit to be gained from regular participation in impact-loading activity.

A strong correlation between muscle strength and whole body BMD and regional leg BMD was found when all subjects were considered together. The effect of muscular contractions has been assumed to be site specific(29), and these data support such claims. All of the sports represented in this study involve a high degree of leg activity. However, only HIGH was significantly stronger in leg extensor strength than CON. The weight-bearing sports involve repetitive antigravity activity of the leg extensor muscles. In addition, netball and basketball involve many landings and quick changes of direction. The forces experienced during these activities may positively influence leg strength and are in keeping with the trend for increasing strength with increasing impact. The muscular contractions generated by the activity together with the stress from impact may contribute to BMD. However, the ANCOVA models showed that participation in impact-loading activity had a beneficial effect on whole body and regional leg BMD independent of variations in leg strength.

Significant differences between groups in regional arm BMD were not maintained when the covariates height, corrected lean mass, and quadriceps strength were factored into the model. This suggests that the differences identified in the ANOVA model were related to the covariates rather than the impact-loading nature of the exercise participation. This finding is not surprising since the activities represented in this study (including swimming) generate little impact loading on the arms. Fehling et al.(7) found the only site that gymnasts had greater BMD than volleyball players was in the arms. Unlike volleyball and the sports represented in this study, gymnastics substantially loads the arms. If impact is site specific this could account for the lack of differences in arm BMD among the study groups.

The mean dietary calcium intake of these women was approximately equal to the recommended intake of 800 mg for premenopausal Australian women(21) and did not differ significantly among the four study groups. Dietary calcium intake was not significantly correlated with BMD at any site. A number of other studies have also failed to show any relationship between current calcium intake and BMD(1,27). Another factor possibly obscuring the relationship between current dietary calcium intake and BMD is the poor stability of calcium intake reported by Heaney et al.(10). An integrated measurement of lifetime calcium intake may be necessary to identify potential associations between calcium intake and BMD.

In conclusion, this study has found that a lifetime of impact-loading exercise is associated with greater whole body BMD and regional leg BMD in contrast to involvement in a nonimpact activity or a sedentary lifestyle. The impact associated differences in BMD of the whole body and leg were independent of other activity associated variables such as lean mass and muscle strength. Current dietary calcium intake had no relationship with BMD. In addition to increased BMD, all athletic participants had lower body fat and greater lean mass than the sedentary controls. All of these associations indicate the beneficial effects of regular exercise and should provide a useful basis for the development of recommendations for longterm exercise programs for skeletal maintenance. While it would be desirable to undertake a randomized, prospective study evaluating the effects of long-term participation in different impact-loading sports, realistically such a study would be impossible to conduct. Therefore, the cross-sectional evaluation of unique groups of volunteers such as the women participating in this study must be relied upon to provide insight into the effects of lifelong exercise habits.

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