The aim of this retrospective study was to determine the long-term effect of exercise on bone mineral density (BMD), bone mineral content (BMC) and body composition (BC) in post-menopausal women who were elite athletes during their youth compared with sedentary controls.
/Methods:It is a retrospective study and carried out in an outpatient clinic. A total of 48 post-menopausal women (54–73 years of age) were enrolled. Ex-elite athletes with long-term (>20 years) histories of significant training and performance were divided into two groups: weight-bearing sports (runners, n=12) and non-weight-bearing sports (swimmers, n=12). The athletes were age matched with sedentary controls (n=24). BMD, BMC and BC were measured using dual-energy X-ray absorptiometry. Healthcare and sport activity histories were evaluated using a questionnaire.
No significant differences were found with regard to body weight, height, body mass index and hours of activity between the two groups of athletes. There were no significant differences in activity levels between athletes and controls at the time of this study. BMD and BMC were not significantly different between athletes; they were significantly higher in athletes than in controls (P<0.001). Although the ex-athletes did not significantly differ in BC, left and right lean arm mass and arm BMD were significantly higher in swimmers than in runners (P<0.0001).
The high level of physical activity observed in female athletes is associated with improved muscle mass, BMD and BMC, and physical activity during youth seems to have a beneficial effect on bone mass and helps to prevent bone loss due to aging.
Osteoporosis is a major public health problem around the world, largely because of the morbidity and mortality associated with osteoporotic fractures (Becker et al., 2006). Osteoporosis is the most prevalent metabolic bone disease, characterized by diminished bone strength, predisposing the affected individual to an increased risk of fracture. Its incidence is particularly high in post-menopausal women, but it can also affect men and individuals receiving corticosteroid therapy (Drinkwater, 1994; Leung et al., 2002; Becker et al., 2006).
The pathogenesis of osteoporosis is complex and multifactorial (Gnudi et al., 2007). A decrease in physical activity may lead to an increased loss of bone mineral density (BMD) and an increase in the incidence of fragility fractures (Duncan et al., 2002; Karlsson, 2007).
It is commonly accepted that weight-bearing activities provide an osteogenic stimulus to the bones (Bassey et al., 1998). For example, athletes involved in sports that increase the mechanical stress placed on the bones (that is, weight-bearing activities) have an increased BMD compared with the general population (Taafee et al., 1995; Andreoli et al., 2001). However, swimmers, who train in a non-weight-bearing environment, have been shown to obtain less skeletal benefits than do athletes who participate in weight-bearing activities (Block et al., 1989; Taafee et al., 1995).
Researchers have studied the relationship between aerobic activities and BMD, and although the results have been equivocal, there has been more research showing that regular aerobic weight-bearing exercise has a positive impact on BMD; physically active men and women have higher BMD than those who are sedentary (Mazess and Barden, 1991; Taafee et al., 1995). Furthermore, although researchers have examined the impact of strenuous physical training on BMD in young women athletes (Etherington et al., 1996; Bassey et al., 1998; Creighton et al., 2001), there is less information regarding BMD in highly trained older women athletes.
Therefore, the aim of this retrospective study was to determine the effect of being involved in sports on BMD, bone mineral content (BMC) and body composition (BC) in women who were athletes during their youth compared with sedentary controls, and to evaluate whether the positive effects of past sports participation persisted during menopause and aging.
The study was first approved by the Ethics Committee of the University of Rome ‘Tor Vergata’. Each participant gave verbal and written informed consent before participation, and the study was carried out according to the Declaration of Helsinki protocol. None of the participants was taking medications that affected bone and muscle metabolism.
A total of 48 Caucasian women, 54–73 years of age, were enrolled in the study. The sample included two groups of athletes: swimmers (n=12) and runners (n=12). A third group of women included 24 age-matched non-athletic participants who served as the control group. Menstrual history for each participant was obtained through interview.
Information regarding the age of onset of menarche, the average number of menstrual cycles per year before menopause and the use of oral contraceptives was obtained through interview. On the basis of this interview, all participants were classified as eumenorrheic (10–13 cycles per year) during their younger years.
All measurements were recorded when participants were fasted for 12 h and had not exercised for 24 h. Participants were also to refrain from alcohol consumption for 48 h before testing.
Physical activity assessment
Current and past physical activity levels in age-matched sedentary controls were assessed using a validated physical activity questionnaire (Salvini et al., 2002). All athletes were asked to detail their physical activity patterns, including pre-season, in-season and post-season workouts. The training history, including years of active sport-specific training, training sessions per week, total training hours per year and the age of onset of the sport-specific training, was documented using a validated questionnaire (Salvini et al., 2002). Furthermore a questionnaire, including questions on medication use, known diseases, dietary intake, vitamin and mineral supplementation and the use of alcohol and cigarettes was used (Fidanza et al., 1995). Finally, a specific questionnaire regarding menstrual cycle and menopausal status of each woman was used (Salvini et al., 2002; Nappi et al., 2008).
Two categories of sports with different mechanical loading were selected for this study: weight bearing versus non-weight bearing. We classified our athletes as either swimmers or runners.
During their youth, all of the athletes competed at national and international levels and exercised regularly for at least 3 h per day, 4 days per week. Occasionally, control participants participated in activities once or twice a month, but not on a regular basis, nor in a competitive sport environment. Their overall physical activity never exceeded 1 h per week.
All athletes continued to participate in the same sport activity as when they were young; however, the intensity of training was lower and they were active about 4–5 h per week. The control group reported being active at a gymnasium for about 3 h per week.
Anthropometric measurements were taken according to conventional criteria and measurement procedures. Body weight and height were measured to the nearest 0.1 kg and 0.5 cm, respectively. Body mass index (kg/m2) was calculated using the formula: body weight (kg)/height (m)2.
Bone mineral density, bone mineral content and body composition
Total body and regional measurements of BMD, BMC, fat mass and lean body mass were recorded using dual-energy X-ray absorptiometry (software version 3.6, Lunar Corp., model DPX, Madison, WI, USA). The scanner was calibrated daily against the standard calibration block supplied by the manufacturer to control for possible baseline drift. Dual-energy X-ray absorptiometry measures total BMD and BMC with a coefficient of variation of 0.7%. For total fat mass and lean body mass, coefficient of variations=1.6% and 0.8%, respectively.
Statistical comparisons for the different variables among the four groups were made by applying a one-way analysis of variance (ANOVA). Bonferroni's post-hoc tests were conducted on all significant mean differences. Correlation and regression analyses between BMD and BC were carried out. The test of comparisons and correlation were considered significant, if P⩽0.055. All statistical analyses were carried out with the Statistical Package for Social Sciences (SPSS Inc., version 10, Chicago, IL, USA).
The characteristics of the three groups are reported in Table 1. There were no significant differences in age, body weight, height and body mass index among the groups. The age of menarche was not significantly different between the groups.
Most women were more than 7 years into menopause and not on estrogen replacement therapy. Menopausal status was not significantly different between the athletes and controls, as well as between swimmers and runners. Years of post menopause were 9.0±7.0 for the control group, 8.3±7.3 for the runners and 8.1±6.9 for the swimmers.
Physical activity levels
Table 2 shows physical activity levels for a period of 15 years. When the athletes were competing, they had a significantly greater activity level compared with the control group (P<0.01). The swimmers had significantly higher activity levels during their time of competition compared with the runners (P<0.05). At the time of this study, however, there were no significant differences in activity levels between the athletes and the control group.
Total body BMD in the control group was significantly lower (P<0.05) compared with the athletes; however, no differences were found between the swimmers and the runners (Table 3). Table 3 shows regional BMD and BMC of the three groups. BMD of the arms was not significantly different among the three groups. BMD of the spine was significantly lower in the controls compared with the runners (P<0.01). BMD of the legs was significantly higher in athletes compared with the controls (P<0.001). BMD of the legs was higher in runners compared with swimmers (P<0.01). Athletes had a significantly higher segmental BMC than the control group (P<0.001).
Lean mass was significantly lower in the control group compared with the athletes (P<0.001), but was not significantly different between runners and swimmers (Table 4). Fat mass, in kg and percentage, was significantly higher (P<0.001) in the control group compared with runners and swimmers, but was not significantly different between the runners and swimmers. Swimmers had statistically leaner arms compared with runners (P<0.001) (Table 4). The lean mass of legs between runners and swimmers was not significantly different statistically (Table 4).
When the athletes and controls were combined into one group, lean body mass was associated with BMD at all regions. Fat mass was not correlated with BMD. The correlation between BMD and lean mass was 0.488 (equation: BMD=1.16E−5lean+0.520), whereas an inverse correlation was found between BMD and fat mass (r=−0.378; equation: BMD=−8.2e−6fat+1.163) (Figure 1).
The aim of this retrospective study was to determine the effect of being involved in sports on BMD, BMC and BC in women who were athletes during their youth compared with sedentary controls, and to evaluate whether the positive effects of past sports participation persisted during menopause and aging. Another objective was to evaluate whether there were any differences in BMD, BMC and BC between athletes who have continued physical activity and those who have discontinued physical activity. Weight-bearing exercise is associated with lumbar BMD, and sports that stress the bones are associated with higher BMD than non-weight-bearing sports such as swimming (Fehling et al., 1995). When the athletes in this study were divided into weight-bearing versus non weight-bearing exercisers, runners had higher leg BMD than swimmers.
Previous researchers investigating the effects of exercise on BMD have reported increases in BMD in pre-menopausal women participating in low-intensity regular exercise (Alekel et al., 1995; Uusi-Rasi et al., 1998; Robling et al., 2002), and following the introduction of an exercise regimen (Drinkwater, 1994; Etherington et al., 1996). Although estrogen replacement therapy has been reported to increase BMD in both sedentary pre- and post-menopausal women (Heikkinen et al., 1997), the effect of exercise on post-menopausal women is less clear, with researchers reporting increases (Tinetti et al., 1994; Uusi-Rasi et al., 1998), decreases or marginal effects (Bassey et al., 1998) on BMD following exercise. Our results showed that athletes with a lifetime history of strenuous physical activity had markedly higher BMD, BMC and appendicular muscle mass than sedentary controls of similar age and menopausal status.
It is well known that BMD increases at sites of maximum stress (Wolman et al., 1991; Carter, 1992; Andreoli et al., 2001). The physiological mechanisms involved in the response of bone cells to mechanical stress are still unclear. A possible explanation may be that osteocytes functioning as mechanoreceptors respond and release chemical factors capable of promoting osteoblastic proliferation at the local bone site. Stress applied to a skeletal segment affects the geometry of the bone, the microarchitecture and the composition of the matrix (Carter, 1992).
Physical activity leads to greater BMD in children and adolescents and, to a minor extent, in adults (Carter, 1992). Weight-bearing activities, such as walking or running, have a greater effect than non-weight-bearing activities, such as cycling and swimming, whereas a reduction in mechanical loading, that is, bed rest or space flight, leads to bone loss (Heer et al., 1999).
Therefore, weight-bearing activity has been widely recommended as a possible prophylaxis for age-related bone loss. The skeleton provides more than just a framework for the body. Bone is a calcified conjunctive tissue sensitive to various mechanical stimuli, mainly to those resulting from gravity and muscular contractions.
We have shown that muscle mass in legs was higher in runners compared with swimmers and that swimmers had leaner arms compared with runners.
The increased muscle mass in the athletes probably reflects the significant physical training they undergo. The physical training, in turn, positively affected BMD and BMC. In this regard, one might expect that the amount of muscle mass might have a role in skeletal maintenance, which has been reported by others who have conducted prospective studies in this area (Andreoli et al., 2001).
Furthermore, exercise during growth is important because of the associated changes in bone geometry that translate into greater increases in bone strength than provided by an increase in BMC alone (Ahlborg et al., 2003).
Exercise during growth may be followed by long-term beneficial skeletal effects, which could possibly reduce the incidence of fractures. Exercise during adulthood seems to partly preserve these benefits and reduce age-related bone loss. (Karlsson, 2007; Karlsson et al., 2008a, 2008b, 2008c). The beneficial effect could be due to an exercise-induced periosteal expansion. Alternatively, bone mineral may be deposited on the endosteal surface, producing a thicker cortical shell without a wider bone. (Duncan et al., 2002; Greene et al., 2005; Ward et al., 2005).
The complexity of the skeletal response to loading is also illustrated by the heterogeneity of the geometrical adaptations along the length of a bone (Nappi et al., 2008).
Randomized controlled trials study related to the effects of exercise on BMD in older women and men are required. Impact and resistance exercise should aid in the prevention of osteoporosis. Weight-bearing exercise in general, and resistance exercise in particular, along with exercise targeted to improve balance, mobility and posture, should be recommended to reduce the likelihood of falling and its associated morbidity and mortality (Guadalupe-Grau et al., 2009).
In fact, observational studies have reported that the risk of falling decreases with increased physical activity (Tinetti et al., 1994), and that low physical activity, presently or previously, is associated with an increased risk of sustaining a hip fracture (Gregg et al., 1998). Other studies conclude that daily physical activity is associated with a reduced risk of hip fracture (Kritz-Silverstein and Barrett-Connor, 1994; Karlsson et al., 2008c). Existing data indicate that exercise, in both men and women and independently of age, improves muscle strength even when performed for a short period. Muscle strength improves far more and much faster than the increase in muscle mass.
The high levels of physical activity observed in women athletes may help prevent a decline in muscle mass and also are sufficient to prevent bone loss due to aging.
The limitation of this study is that it is a retrospective study and not a longitudinal one. However, in this regard, we should recognize the fact that it is not easy to conduct a study such as the present one in a prospective way; in fact, in the literature there are no other studies that have taken into account the physical activity levels, BMD, BMC and segmental BC of different groups at the same time. This study has shown that physical activity during youth has beneficial effects on all the studied parameters in later age.
Future longitudinal studies should provide more details on the effect of physical activity during youth and confirm the long-term effects during menopause and aging.
In conclusion, physical activity during youth appears to have a beneficial effect on bone mass in later age; physical activity with greater mechanical loading appears to result in a greater bone mass than non-weight-bearing activities; and there appears to be a site-specific skeletal response to the type of loading at each BMD site.
Ahlborg HG, Johnell O, Turner CH, Rannevik G, Karlsson MK (2003). Bone loss and bone size after menopause. N Engl J Med 349, 327–334.
Alekel L, Clasey J, Fehling P, Weigel R, Boileau R, Erdman J et al. (1995). Contributions of exercise, body composition and age to bone mineral density in premenopausal women. Med Sci Sports Exerc 27, 1477–1485.
Andreoli A, Monteleone M, Van Loan M, Promezio OL, Tarantino U, De Lorenzo A (2001). Effects of different sports on bone density and muscle mass in highly trained athletes. Med Sci Sports Exerc 3, 507–511.
Bassey EJ, Rothwell MC, Littlewood JJ, Pye DW (1998). Pre and post-menopausal women have different bone mineral density responses to the same high impact exercise. J Bone Miner Res 13, 1805–1813.
Becker C, Crow S, Toman J, Lipton C, McMahon DJ, Macaulay W et al. (2006). Characteristics of elderly patients admitted to an urban tertiary care hospital with osteoporotic fractures: correlations with risk factors, fracture type, gender and ethnicity. Osteoporos Int 17, 410–416.
Block JE, Friedlander AL, Brooks GA, Steiger P, Stubbs HA, Genant HK (1989). Determinants of bone density among athletes engaged in weight-bearing and non-weight-bearing activity. J Appl Physiol 67, 1100–1105.
Carter DR (1992). Skeletal development and bone functional adaptation. J Bone Miner Res 7, s389–s395.
Creighton DL, Morgan AL, Boardley D, Brolinson PG (2001). Weight-bearing exercise and markers of bone turnover in female athletes. J Appl Physiol 90, 565–570.
Drinkwater BL (1994). Does physical activity play a role in preventing osteoporosis? Res Q Exerc Sport 65, 197–206.
Duncan CS, Blimkie CJ, Kemp A, Higgs W, Cowell CT, Woodhead H (2002). Mid-femur geometry and biomechanical properties in 15- to 18-yr-old female athletes. Med Sci Sports Exerc 34, 673–681.
Etherington J, Harris PA, Nandra D, Hart DJ, Wolman RL, Doyle DV et al. (1996). The effect of weight-bearing exercise on bone mineral density: a study of female ex-elite athletes and the general population. J Bone Miner Res 11, 1333–1338.
Fehling PC, Alekel L, Clasey J, Rector A, Stillman RJ (1995). A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone 17, 205–210.
Fidanza F, Gentile MG, Porrini MA (1995). Self-administered semiquantitative food frequency questionnaire with optical reading and its concurrent validation. Eur J Epidemiol 11, 163–170.
Gnudi S, Sitta E, Fiumi N (2007). Relationship between body composition and bone mineral density in women with and without osteoporosis: relative contribution of lean and fat mass. J Bone Miner Metab 25, 326–332.
Greene DA, Naughton GA, Briody JN, Kemp A, Woodhead H, Corrigan L (2005). Bone strength index in adolescent girls: does physical activity make a difference? Br J Sports Med 39, 622–627.
Gregg EW, Cauley JA, Seeley DG, Ensrud KE, Bauer DC (1998). Physical activity and osteoporotic fracture risk in older women. Study of Osteoporotic Fractures Research Group. Ann Intern Med 129, 81–88.
Guadalupe-Grau A, Fuentes T, Guerra B, Calbet JA (2009). Exercise and bone mass in adults. Sports Med 29, 439–468.
Heer M, Kamps N, Biener C, Korr C, Boerger A, Zittermann A et al. (1999). Calcium metabolism in microgravity. Eur J Med Res 9, 357–360.
Heikkinen J, Kyllonen E, Kurttila-Matero E, Wilen Rosenquist G, Lankinen K, Rita H et al. (1997). HRT and exercise: effects on bone density, muscle strength and lipid metabolism in healthy postmenopausal women. Maturitas 26, 139–149.
Karlsson MK (2007). Does exercise during growth prevent fractures in later life? Rev Med Sport Sci 51, 121–136.
Karlsson MK, Nordqvist A, Karlsson C (2008a). Physical activity increases bone mass during growth. Food Nutr Res 52; e-pub ahead of print 1 October 2008; doi:10.3402/fnr.v52i0.1871.
Karlsson MK, Nordqvist A, Karlsson C (2008b). Sustainability of exercise-induced increases in bone density and skeletal structure. Food Nutr Res 52; e-pub ahead of print 1 October 2008; doi:0.3402/fnr.v52i0.1872.
Karlsson MK, Nordqvist A, Karlsson C (2008c). Physical activity, muscle function, falls and fractures. Food Nutr Res 52; e-pub ahead of print 30 December 2008; doi:10.3402/fnr.v52i0.1920.
Kritz-Silverstein D, Barrett-Connor E (1994). Grip strength and bone mineral density in older women. J Bone Miner Res 9, 45–51.
Leung MM, Corliss AB, Volpe SL (2002). Effect of cortisone injections on college athletes’ bone mineral density and biochemical markers of bone turnover. J Med Sciences 2, 124–129.
Mazess RB, Barden HS (1991). Bone density in premenopausal women: effects of age, dietary intake, physical activity, smoking, and birth-control pills. Am J Clin Nutr 53, 132–142.
Nappi RE, Albani F, Vaccaro P, Gardella B, Salonia A, Chiovato L et al. (2008). Use of the Italian translation of the Female Sexual Function Index (FSFI) in routine gynecological practice. Gynecol Endocrinol 24, 214–219.
Robling AG, Hinant FM, Burr DB, Turner CH (2002). Shorter more frequent mechanical loading sessions enhance bone mass. Med Sci Sports Exerc 34, 196–202.
Salvini S, Saieva C, Sieri S, Vineis P, Panico S, Tumino R et al. (2002). Physical Activity in the EPIC Cohort in Italy IARC Scientific Publications, Vol 6 IARC: Lyon, France. pp 267–269.
Taafee DR, Snow-Harter C, Connolly DA, Robinson TL, Brown MD, Marcus R (1995). Differential effects of swimming versus weight-bearing activity on bone mineral status of eumenorrheic athletes. J Bone Miner Res 10, 586–593.
Tinetti ME, Baker DI, McAvay G, Claus EB, Garrett P, Gottschalk M et al. (1994). A multifactorial intervention to reduce the risk of falling among elderly people living in the community. N Engl J Med 331, 821–827.
Ward KA, Roberts SA, Adams JE, Mughal MZ (2005). Bone geometry and density in the skeleton of pre-pubertal gymnasts and school children. Bone 36, 1012–1018.
Wolman RL, Faulman L, Clark P, Hesp R, Harries MG (1991). Different training patterns and bone mineral density of the femoral shaft in elite, female athletes. Ann Rheum Dis 50, 487–498.
The authors declare no conflict of interest.
Guarantor: Angela Andreoli. Contributors: AA, UT and SL designed the study. AA and MC were responsible for data collection. RS performed the statistical calculations and data analyses. AA, UT and SLV conducted analyses and wrote the original manuscript. All authors contributed to interpretation of data and critically revised the manuscript.
About this article
Cite this article
Andreoli, A., Celi, M., Volpe, S. et al. Long-term effect of exercise on bone mineral density and body composition in post-menopausal ex-elite athletes: a retrospective study. Eur J Clin Nutr 66, 69–74 (2012) doi:10.1038/ejcn.2011.104
- bone mineral density
- body composition
- female athletes
Low serum concentrations of Irisin are associated with increased risk of hip fracture in Chinese older women
Joint Bone Spine (2018)
BioMed Research International (2018)
Journal of Bone Metabolism (2016)
Revista Brasileira de Reumatologia (English Edition) (2016)