SMATHERS, AARON M.; BEMBEN, MICHAEL G.; BEMBEN, DEBRA A.
Osteoporosis is a debilitating disease characterized by low bone mineral density (BMD) and deterioration of the microarchitecture that weakens the bone and increases risk of fracture (19). The World Health Organization (WHO) has established criteria for the densitometric diagnosis of osteoporosis in Caucasian women based on the SD units relative to the young adult population known as t-scores. Osteoporosis is defined as a t-score of −2.5 or less, and low bone mass, termed osteopenia, is defined as a t-score in the range of −1.1 to −2.4 (19). Although osteoporosis is more prevalent in postmenopausal women, it is now recognized that men are also at risk because approximately 27% of all hip fractures occur in men, and vertebral fractures may be as common in men as in women (27). The two primary strategies for reducing osteoporosis risk are to maximize the attainment of peak bone mass and to reduce age-related bone loss (22). There are many contributing factors to skeletal health, including genetics, physical activity, nutrition, and reproductive hormones (16).
The relationship between physical activity and BMD has been the focus of many studies in the past decade, providing growing evidence that moderate- to high-intensity weight-bearing physical activity is positively related to BMD (4,5,15,22,35,37). Bone adapts to the mechanical stresses imposed upon it, such as external loads from ground reaction forces and forces exerted by muscular contraction (11,22). Cross-sectional studies have documented that athletes tend to have higher BMD than control subjects (5), particularly those participating in sports involving high impact forces or mechanical strains on the skeleton such as gymnastics, rowing, or boxing (35,36). Generally, strength- and power-trained athletes have higher BMD than endurance-trained athletes (5), and male long-distance runners have been reported to have lower BMD than controls (5,6,17,29,35,37).
Competitive road cyclists represent another group of athletes whose skeletons may undergo differential mechanical loading due to the nature of the exercise. Several studies have examined the effects of cycling on BMD (29,32,35,37,41). Lower BMD compared with age-matched controls has been reported in adult male cyclists (37), in master cyclists with a long history of exclusive training in cycling (29), and in postpubertal adolescent male cyclists (33). In contrast, Warner et al. (41) did not find BMD differences between road cyclists and controls who were not matched for age or body mass. The underlying reasons for these findings are not clear; however, hormone levels, calcium intake, energy imbalance, and mechanical loading patterns are possible contributors to the reduced bone mass in cyclists. The biomechanics of cycling (i.e., the relatively fixed body position) and its lack of impact on the skeleton result in relatively low strain magnitudes; therefore, cycling provides little osteogenic stimulus to bones (29,37). Testosterone has a significant role in the development of peak bone mass and in the maintenance of BMD throughout life (31). Decreased testosterone levels found in male endurance athletes (14,24,25,39,42) may have a negative effect on the bone health of these athletes. Alterations in bone biomarkers have been reported in distance runners (44) and in physically active persons in low energy availability states (18,43), suggesting that energy balance may affect bone turnover rates.
There are critical health risks associated with low BMD that make it imperative to examine the bone health of competitive cyclists. One immediate consequence of low BMD for these athletes is increased risk for traumatic fractures caused by falls during a race or training, which may require surgical treatment to repair the broken bone. Avascular necrosis is a serious complication of traumatic femoral neck fractures necessitating joint reconstruction (i.e., total hip replacement) or other procedures to preserve the femoral head (2). In addition, cyclists with low BMD put themselves at risk for osteoporosis at a younger age because their peak bone mass is attenuated and they may experience bone loss due to the low mechanical loading nature of their sport. The purpose of this cross-sectional study was to compare total body, lumbar spine, and dual proximal femur BMD in male competitive road cyclists of club to professional caliber and in age- and body mass-matched controls. The hip and the spine skeletal sites are recommended sites to measure because they are prone to osteoporotic fracture (23). A secondary purpose of this study was to determine whether BMD in cyclists was related to training characteristics, testosterone levels, or calcium intake. We hypothesized that the total body and spine BMD would be lower in cyclists and that BMD would be positively related to testosterone levels and negatively related to training volume in these athletes.
Sixty-two men participated in this study: 32 cyclists (CYC) and 30 recreationally active controls (CON) matched for age (±2 yr) and body mass (±2.27 kg). The required subject number per group for a one-tailed test was 26, based on an effect size of 0.70% and an 80% power for the L2-L4 BMD site. Cyclists had to have been racing and training for a minimum of 1 yr continuously, with no more than 6 months off for illness or injury. Control subjects were required to be moderately physically active to maximize potential group differences because BMD can be affected by either very low levels or very high levels of endurance or resistance exercise. We chose a cutoff frequency of 3 d·wk−1 based on the ACSM guidelines (1) for maintaining cardiorespiratory and muscular components of fitness. Individuals with the following conditions were excluded from the study: those taking thiazide diuretics, testosterone, calcitonin, chemotherapeutics, corticosteroids, or anticonvulsants within the past 2 yr; those with a history of osteoporosis, osteopenia, hypogonadism, thyroid disease, epilepsy, diabetes, kidney stones, or smoking; controls who participated in endurance or resistance exercise four times or more per week; and those who were sedentary.
Each subject read and signed a written informed consent approved by the Institutional Review Board at the University of Oklahoma, Norman, OK. Subjects completed a validated calcium intake questionnaire (28) to estimate daily calcium intake, including supplements, at the beginning of the study. Physical activity outside of training was assessed using the Baecke Physical Activity Questionnaire (3). Cyclists also completed a Cycling Training Questionnaire to assess volume of training in current average weekly hours, current racing category, age, number of years racing, and number of months of weight lifting included in their training program in the previous year.
Dual energy x-ray absorptiometry (DXA) (GE Lunar-Prodigy, Software Version 6.70.021) was used to measure the BMD (g·cm−2) of the total body, anterior-posterior (AP) lumbar spine, lateral spine (LS), and dual proximal femur (femoral neck, trochanter, and total hip). The LS site assesses vertebral body BMD without the non-weight-bearing posterior elements of the spine (8). Scan modes were determined by the subject's AP thickness as measured at the umbilicus by a straight-edged ruler placed on the scan table while the subject was laying flat (standard 13-25 cm, slow >25 cm); all subjects qualified for standard scan speeds in this study. All scanning procedures were standardized for all subjects following the guidelines of the DXA manufacturer. Quality assurance procedures were performed daily. The acquisition and the analysis of all bone scans were performed by the same DXA technician. In the Bone Density Research Laboratory, coefficients of variation (CV) for precision and accuracy for the spine phantom are 0.6% and 0.8%, respectively. In vivo precision CV for this technician are 0.9% for total body, 0.8% for AP spine (L1-L4), 0.2% for left total hip, and 0.4% for right total hip BMD sites. Total body and regional body composition was measured using the total body DXA scan to obtain percent body fat, fat mass, bone-free lean tissue mass, and bone mass values. The prevalence of osteoporosis and osteopenia was estimated based on the WHO classifications (normal, t-score ≥ -1.0; osteopenia, t-score -1.1 to -2.4; and osteoporosis, t-score ≤ -2.5) using the young adult male reference database (23).
Blood samples were obtained in the morning after an overnight fast via venipuncture by a phlebotomist at the university Student Health Center. Serum was frozen at −84°C and thawed only once for the hormone assays. Total testosterone (TT) and free testosterone (FT) were measured in duplicate using an I25I radioimmunoassay kits (Diagnostic Systems Laboratories, Inc., Webster, Texas) with a detection limit of 0.28 nmol·L−1 for TT and 0.62 pmol·L−1 for FT. A RIASTAR Gamma Counter (Packard Instruments. Meriden, CT) was used to count the radioactivity in the assay tubes and to determine the hormone concentration readings. The intraassay CV for both hormone assays were <10%. Reference ranges for normal androgen levels vary according to the assay technique used (40); therefore, it is appropriate to use the adult male reference ranges established by the manufacturer specifically for these assays kits (9.7-30.5 nmol·L−1 for TT; 30.2-189.8 pmol·L−1 for FT). Vermeulen (40) recommended using the lower normal limits of 11 nmol·L−1 for TT and 22.5 pmol·L−1 for FT as cutoffs for androgen deficiency in men.
All data are reported as mean ± SE. Statistical Package for the Social Sciences for Windows version 11.0.04 (SPSS, Inc., Chicago, IL) was used to execute all statistical analyses including descriptive statistics and one-way ANOVA to determine group differences in the dependent variables. Pearson correlation coefficients were used to determine relationships between BMD, body composition, calcium intake, training characteristics, and testosterone variables separately for cyclists and controls. ANCOVA was used to adjust BMD for group differences in body composition variables. Chi-square analysis was used to determine the association between the CYC and the CON groups and osteoporosis classifications. The level of significance was set at P ≤ 0.050.
Table 1 presents the physical characteristics of the two groups of men. As expected, age (P = 0.280) and body mass (P = 0.956) were not significantly different between the two groups. The age ranges were 20-45 yr for cyclists and 20-43 yr for controls. The ethnicities of the subjects included 1 Hispanic, 1 American Indian, 4 Asians, and 56 Caucasians. Cyclists were classified by their respective United States Cycling Federation racing categories; 8 category Pro/1, 2 category 2, 15 category 3, and 7 category 4 participated. Nineteen of the cyclists reported weight lifting 2-6 months (3.6 ± 0.2 months) in the previous year, whereas the remaining 13 cyclists reported 0 months of weight lifting in the previous year. Both calcium intake (P = 0.004) and Baecke Total Physical Activity Score (P = 0.001) of the cyclists were significantly higher than controls.
There were no significant differences between groups for either resting TT (CYC = 24.6 ± 1.4 nmol·L−1; CON = 27.1 ± 1.4 nmol·L−1, P = 0.230) or FT (CYC = 42.7 ± 3.47 pmol·L−1; CON = 46.2 ± 2.8 pmol·L−1, P = 0.343). All subjects' levels were within the assay reference ranges for TT; however, six subjects (two controls; four cyclists) were below 30.2 pmol·L−1 for FT. One cyclist had both TT (11.9 nmol·L−1) and FT (22.0 pmol·L−1) near or slightly below the recommended cutoffs for androgen deficiency (40).
Table 2 presents the total body and the regional lean tissue composition of the subjects. The cyclists had significantly lower total body fat percentage (P = 0.001) and significantly higher total bone-free lean tissue mass (P = 0.012). Leg (P = 0.002) and trunk lean tissue mass (P = 0.001) also were significantly higher in the CYC compared with CON. No significant differences were found for total bone mass (P = 0.076) and arm lean tissue mass (P = 0.836) between the groups.
Bone mineral density.
No significant group differences were found for total body BMD (CYC = 1.213 ± 0.013 g·cm−2; CON = 1.232 ± 0.015 g·cm−2, P = 0.349), t-scores (CYC = −0.084 ± 0.160; CON = 0.147 ± 0.190, P = 0.354), or z-scores (CYC = 0.177 ± 0.147; CON = 0.380 ± 0.l77, P = 0.381). The positive z-scores indicated that both groups exhibited slightly higher total body BMD values than the average for individuals of the same age, gender, weight, and ethnicity.
Table 3 presents the group comparisons for the AP spine and the LS BMD. Both AP lumbar BMD sites, L1-L4 (P = 0.017) and L2-L4 (P = 0.028), were significantly lower for CYC compared with CON. Also, the LS BMD (B2-B3) was significantly lower (P = 0.001) for the cyclists. The t-scores and the z-scores for all of the spine sites were significantly lower (P < 0.050) for the cyclists. The left hip BMD variables are shown in Table 4. There were no significant (P > 0.050) group differences for the BMD, the t-scores, or the z-scores for any of the left hip regions of interest. Similarly, there were no significant (P > 0.050) group differences in the right hip BMD variables (data not shown). Adjusting the BMD variables for regional lean tissue mass using ANCOVA did not alter the significant group differences for any site.
In a secondary analysis, we divided the cyclists into weight-lifting (WL CYC, n = 19) and non-weight-lifting (NONWL CYC, n = 13) subgroups based on whether they reported performing weight lifting in the previous year (WL CYC = 2-6 months; NONWL CYC = 0 months). In addition, the control subjects who were matched to the weight-lifting cyclists were designated as WL CYC CON (n = 19), and those controls matched to the nonweight-lifting cyclists were classified as NONWL CYC CON (n = 13). One-way ANOVA determined that all three spine BMD sites were significantly lower for WL CYC compared with WL CYC CON (L1-L4, P = 0.007; L2-L4, P = 0.010; LS, P = 0.004), whereas only the LS spine BMD was lower (P = 0.050) in NONWL CYC compared with their control group (Fig. 1). In comparison to the NONWL CYC subgroup, the WL CYC subgroup was significantly shorter (172.4 ± 1.2 vs 178.5 ± 1.8 cm, P = 0.006) and lighter (70.1 ± 1.5 vs 76.2 ± 1.9 kg, P = 0.018). The only significant BMD variable between the cyclist subgroups was total body BMD, which was significantly lower (P = 0.035) for WL CYC (1.191 ± 0.015 g·cm−2) than for NONWL CYC (1.245 ± 0.021 g·cm−2).
FIGURE 1-Spine bone ...Image Tools
The WHO classifications for osteopenia and osteoporosis diagnoses are a t-score value >1.0 to <2.5 SD below the young adult mean and ≥2.5 SD below the young adult mean, respectively (19,23). Figure 2 presents the prevalence (%) of osteopenia and osteoporosis for the L1-L4 spine and the hip sites for each group. Based on chi-square analysis, there were no significant associations (P > 0.050) between groups and these osteoporosis classifications at any site.
FIGURE 2-Prevalence ...Image Tools
For cyclists, no significant correlations (P > 0.050) were found between the BMD variables and the number of years of training, the training volume, the calcium intake levels, or the Baecke Total Physical Activity Score. The only significant relationship observed for TT was for the right femoral neck BMD (r = 0.380, P = 0.032) in cyclists. Body mass (CYC r = 0.381, P = 0.032; CON r = 0.421, P = 0.021) and fat mass (CYC r = 0.434, P = 0.013; CON r = 0.532, P = 0.002) were significantly related to LS spine BMD in both groups, whereas total bone-free lean body mass was positively correlated to AP spine L1-L4 BMD (r = 0.386, P = 0.029) and L2-L4 (r = 0.385 P = 0.030) in cyclists only. The control group also had a positive relationship between AP spine BMD variables and arm lean tissue mass (L1-L4 r = 0.409, P = 0.025; L2-L4 r = 0.431, P = 0.017).
The results of our study support previous reports (29,32,37) of lower spine BMD in cyclists, which was not accounted for by group differences in serum testosterone levels or calcium intake. We did not find lower total body BMD in cyclists, likely a result of the research design that matched cyclists and controls for age and body mass. Further evidence of compromised bone health was that 25% of the cyclists had lumbar spine (L2-L4) t-scores in the osteopenia range (−1.1 to −2.4) and 9% in the osteoporosis range (−2.5 or less). The group difference in BMD was site specific because it was not observed at the hip sites, possibly related to the bone composition of the hip, which is composed of a higher proportion of cortical bone than the spine (7). Another potential explanation is that the cyclists experienced greater mechanical loading at the hip than at the spine, possibly from the stress induced by high-intensity contractions by the leg and hip musculature during this type of exercise. Additionally, because the leg lean tissue in cyclists was greater than controls, there is more muscle mass to exert force on the leg and hip areas.
Several studies have examined bone health in cyclists (29,32,37,41); however, the only other study that age- and body mass-matched control subjects was conducted by Nichols et al. (29) in master cyclists who had been training exclusively for cycling for at least 10 yr. The master cyclists had significantly lower spine and total hip BMD than the control group and significantly lower BMD at all measured sites compared with a group of young cyclists. Our finding of low spine BMD in cyclists is also in agreement with Stewart and Hannan (37) who compared runners (n = 12), cyclists (n = 14), those who competed in both running and cycling events ("both"; n = 13), and healthy, nonexercising controls (n = 23). Cyclists had significantly (P < 0.050) reduced spine BMD (L1-L4) when compared with runners and age-matched controls. Because the control subjects were heavier than the athletes, regression analysis was used to account for weight, which explained 14% of the variation in spine BMD for athletes. Recently, Rector et al. (32) also reported that male cyclists had lower spine and total body BMD than male runners, which was not explained by group differences in body size, hormone status, physical activity levels, or nutritional intakes.
Low BMD in endurance athletes has been reported by many other studies (5,6,12,29,37,38), but no causal mechanism has been established. Frost (11) hypothesized that bone remodeling relies on a "mechanostat" that responds based upon strain magnitudes placed on bones by impact or muscular forces. The flat positioning of the upper body over the bike during cycling, with the arms providing the majority of the support, may not induce sufficient loading on the spine to cause adjustments to be made to the "mechanostat." The average weekly training time of 13 h·wk−1 represents a substantial proportion of total waking hours that exposes the skeleton to minimal strain (37).
Adequate calcium intake is important for the achievement of peak bone mass and influences the bone loss associated with aging (30). The mean calcium intake (1557 ± 132 mg·d−1) for the cyclists exceeded the Institute of Medicine recommendation (10) for optimal intake (1000 mg·d−1) for men age 19-50 yr and was greater than the average intake of the control group. It has been previously reported that athletes exercising in hot and humid environments may experience reduced bone mineral content due to calcium loss through sweating, suggesting that a calcium intake of approximately 2000 mg·d−1 is needed to prevent bone loss in athletes training two or more hours at a given time (21). This finding has implications for the cyclists in our study who were training in the hot summer climate of Oklahoma (average June-September temperature >26°C). In the present study, a food frequency questionnaire was used to estimate daily calcium intake, but calcium losses associated with intense exercise of the cyclists were not measured. Additional research is needed to determine whether the calcium requirements of athletes are higher than the current Institute of Medicine recommendations to account for losses of calcium in sweat.
Another postulated mechanism for low BMD observed in male endurance athletes is a decrease in circulating testosterone levels (13,14,24,25,39,42). We did not find significant group differences for free or TT serum levels, and testosterone levels, generally, were not related to the cyclists' BMD. It is interesting to note that the one cyclist whose FT concentration was below the cutoff for androgen deficiency had spine t-scores in the normal range, but he was osteopenic at the hip. Warner et al. (41) found that testosterone levels in road and mountain cyclists were within normal ranges; however, bioavailable testosterone was positively related to total body and hip BMD sites in the entire subject sample of cyclists and controls. Estrogen may be a better predictor of BMD in men than testosterone because studies in elderly men suggest that there may be a threshold level of estradiol needed to maintain BMD at multiple sites, particularly at the spine (20). Estrogen levels were not measured in our study; however, Maimoun et al. (26) did not find reduced estrogen levels in endurance-trained males. Further research is needed to evaluate the influence of estradiol levels on the BMD of male endurance athletes.
There are several limitations to our study in that we did not exclude cyclists who performed weight lifting as part of their yearly training regimen and we did not obtain dietary information other than calcium intake from the subjects. Our secondary analysis showed that the weight-lifting cyclists still had lower AP and LS BMD than their specific age- and body mass-matched controls, whereas only the LS BMD was lower in the non-weight-lifting subjects compared with their controls. These results should be interpreted cautiously because detailed information was not obtained about the types, intensity, or frequency of resistance exercises performed, and the sample sizes are smaller.
Recent evidence suggests that nutrition and energy balance are important for skeletal health by providing the substrate for bone tissue synthesis and by affecting the bone-regulating hormones (43). Therefore, the BMD differences between cyclists and controls may be related to energy balance because energy deficits have been reported to alter bone turnover in young women (18) and in male runners (44). Although this relationship has not been reported in cyclists, several studies have found disordered eating behaviors in male cyclists (9,34), suggesting that these athletes may be at risk for nutritional deficits. Interestingly, Rector et al. (32) did not find significant differences in physical activity energy expenditure or in energy intakes between runners and cyclists, yet the cyclists had significantly lower spine and total body BMD than runners.
The results of this cross-sectional study along with findings of previous research in cyclists present an alarming observation for bone health in what would seem to be very fit and healthy athletes. Cyclists are susceptible to falls and impact injuries because they wear little protective equipment (only helmet, glasses, and gloves), can reach speeds of 45 mph on level ground, 65 mph on mountain descents, and compete in numbers exceeding 100 participants at a time. One cyclist from this study later suffered a hip fracture at the neck of the femur resulting from a cycling-related fall. The cyclist's total body BMD z-score was −0.6, AP spine (L2-L4) z-score was −1.0, and femoral neck z-score was −1.2 compared with age-, body weight-, and ethnicity-matched reference population (GE Lunar Database). Hip fractures in cyclists are not well documented in the literature but occasionally do occur. In this particular subject, the relationship between the hip fracture and the BMD is speculative and may be more related to the effects of the speed and the impact of the fall on the hip joint.
In conclusion, the male competitive road cyclists in our study had lower spine BMD than controls matched for age and body mass. The underlying mechanisms for these findings are not well understood; therefore, further research is needed to determine causes for low bone mass in this population of athletes.
The authors had no professional relationships with companies or manufacturers who will benefit from the results of the present study. The results of the present study do not constitute endorsement by ACSM.
The authors thank Jeremy Baker for his assistance with the hormone assays. This study was funded in part by the College of Arts and Sciences at the University of Oklahoma.
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