Resistance Training Is Associated With Higher Bone Mineral Density Among Young Adult Male Distance Runners Independent of Physiological Factors : The Journal of Strength & Conditioning Research

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Original Research

Resistance Training Is Associated With Higher Bone Mineral Density Among Young Adult Male Distance Runners Independent of Physiological Factors

Duplanty, Anthony A.1,2,3; Levitt, Danielle E.2,3; Hill, David W.2; McFarlin, Brian K.2,3; DiMarco, Nancy M.4; Vingren, Jakob L.2,3

Author Information
Journal of Strength and Conditioning Research: June 2018 - Volume 32 - Issue 6 - p 1594-1600
doi: 10.1519/JSC.0000000000002504
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Abstract

Introduction

Increases in bone mineral density (BMD) are stimulated by mechanical loading, including weight-bearing physical activities (6). Running is a weight-bearing exercise and as such should provide potent stimulus for bone growth and maintenance. Surprisingly, numerous studies report low BMD in male and female distance runners (2,5,12,13). The underlying causes of low BMD in female runners are well established and associated with a syndrome termed relative energy deficiency in sport (RED-S), previously known as the female athlete triad (23).

The syndrome of RED-S, caused by energy deficiency, can lead to serious consequences for the endocrine, reproductive, and skeletal systems (23). Relative energy deficiency in sport is usually found in female athletes participating in sports where athletes might have, or are perceived to have, a competitive advantage by being very lean. However, the presence of RED-S can result in decreased physical performance and increased morbidity and mortality (25). The change to the term RED-S reflects the fact that male athletes can encounter factors similar to those involved in the female athlete triad: low energy availability (32), hypothalamic-pituitary-gonadal axis hormone deficiency (19), and low BMD, especially in the lumbar vertebrae (2,12,13). In contrast to female distance runners, the mechanisms resulting in low BMD in male distance runners are not well understood. However, given the importance of sex hormones in regulating bone health (29), and previous reports of low serum testosterone in male distance runners (9,21,30,31), testosterone dysregulation could play an important role in low BMD in male distance runners.

Beyond testosterone, a host of other physiological factors also contribute to the dynamic balance between bone mineralization and resorption. Aerobic and resistance exercise are associated with changes in circulating concentrations of these bone metabolism biomarkers acutely after exercise (3,7,18) and at rest after a training period (7,17). Compared with nonrunners, some (but not all) biomarkers of bone metabolism seem to be lower in runners (4). Therefore, bone metabolism biomarkers could help explain the low BMD previously found in male distance runners.

Mechanical loading is an essential factor in bone mass accretion. Cyclists, who have only limited loading and impact of the spine during exercise, are up to 7 times more likely than runners to have osteopenia of the lumbar spine (26). In contrast, power athletes (sprinters, jumpers, weightlifters, etc.) have greater BMD compared with distance runners who do not participate in those types of high impact or high load exercises (1,10,11). Furthermore, among masters runners (40–64 years), those who participate in training regimens that elicit higher magnitudes of ground impact and mechanical loading (e.g., speed-power training) have higher BMD than those who only train in distance running (24). Therefore, the nature of the impact and loading that occurs during running is important in understanding the apparent BMD paradox in male distance runners.

Resistance exercise provides a potent stimulus for bone growth and maintenance and, therefore, is often prescribed to those with osteopenia/osteoporosis (16). The magnitude of mechanical loading is important for bone formation, and resistance exercise elicits a magnitude of strain that exceeds the threshold required for increased bone modelling (6). Considering the positive effects of resistance exercise training on bone growth and the potential negative effects of distance running on testosterone concentration and BMD in men, an investigation of the relationship between BMD and participation in regular resistance exercise among adult male distance runners is warranted.

Currently, there is a paucity of data on the effects of resistance exercise training on BMD in male distance runners. Identifying factors associated with low BMD in male distance runners is important in the prevention of developing osteopenia/osteoporosis. Unless injured, osteopenia/osteoporosis is generally painless and without obvious symptoms. Addition of resistance exercise to a distance running training regimen could potentially attenuate detrimental effects on BMD in male endurance runners. Here, we hypothesize that runners who regularly participate in resistance training have higher BMD than untrained control participants and runners who do not engage in resistance training. Therefore, the purpose of this study was to investigate the relationship between resistance training, testosterone and bone metabolism biomarker concentrations, and BMD in young adult male distance runners.

Methods

Experimental Approach to the Problem

This study evaluated associations between resistance exercise participation, bone mineral density, and related biomarkers in male distance runners. Twenty-five apparently healthy men were categorized based on exercise participation. Each participant completed questionnaires, BMD measurement, and provided blood for circulating biomarker analysis.

Subjects

Twenty-five healthy Caucasian men (mean ± SD: 26 ± 3 years, range 23–32; 1.77 ± 0.04 m; 75.4 ± 8.5 kg) participated in this study, which was approved by the University of North Texas Institutional Review Board. All procedures were conducted in accordance with the Declaration of Helsinki. After providing written informed consent, participants completed medical history and exercise training questionnaires. Then, each participant was assigned to 1 of the following 3 groups based on exercise engagement over the previous 3 years: untrained control participants (CON; n = 8; <1 hour of exercise per week), nonresistance-trained recreational runners (NRT; n = 8; ran ≥32 km per week and did not engage in resistance training), and resistance-trained runners (RT; n = 9; ran ≥32 km·wk−1 and engaged in at least one recreational [nonpower sport] resistance training session per week). The NRT and RT had not regularly participated in any cross-training (biking, swimming, etc.) over the previous 3 years. Age, height, and total body mass did not differ between groups (Table 1). The RT and NRT groups had significantly (p ≤ 0.05) greater lean body mass and lower body fat % than the CON group. The NRT group ran significantly further distances per week than the RT (mean ± SD: 69.1 ± 24.3 and 44.8 ± 13.8 km·wk−1, respectively). Participants were free of diagnosed medical conditions and did not use substances that could affect BMD or hormonal status (e.g., corticosteroids, anabolic-androgenic steroids, growth hormone). Only participants of Caucasian descent were recruited because bone structure, size, and density are known to vary by ethnicity and because of insufficient reference data for other ethnicities (8).

T1
Table 1.:
Descriptive data for untrained control participants, runners who engage in no resistance training, and runners who engage in resistance training.*†

Procedures

Dual-Energy X-ray Absorptiometry

Total body BMD, regional BMD, and soft tissue composition (fat and lean mass) were measured using dual-energy X-ray absorptiometry (DXA; Lunar Prodigy; GE Healthcare, Fairfield, CT, USA). A trained DXA technician performed all scans. Regional BMD measurements were obtained for total proximal femur, femoral neck, trochanteric region, and lumbar spine (L1–L4).

Blood Collection and Analysis

Venous blood samples were obtained via venipuncture in the early morning (07:00–09:00 hours) after a 12-hour fast and 48-hour abstention from exercise. Whole blood was allowed to clot and then centrifuged (1,500g, 4° C, 15 minutes). The resultant serum was stored at −80° C until analysis. Total testosterone (TT), free testosterone (FT), and 25-OH vitamin D were measured in duplicate using commercially available enzyme-linked immunosorbent assays (TT and FT: Alpco, Salem, NH, USA; 25-OH vitamin D: Monobind, Lake Forest, CA, USA). Intra-assay variances (CV) were 3.5% for TT, 10.3% for FT, and 5.7% for vitamin D. Biomarkers that promote bone formation/prevent bone degradation (vitamin D, osteoprotegerin [OPG], osteocalcin [OC], insulin, and leptin) and those that promote bone degradation/suppress formation (parathyroid hormone [PTH], receptor activator of nuclear factor κ-B ligand [RANKL], interleukin [IL] 1β, IL-6, tumor necrosis factor [TNF] α, fibroblast growth factor [FGF] 23, sclerostin [SOST], adrenocorticotropic hormone [ACTH], dickkopf-related protein [DKK] 1, and osteopontin [OPN]) were measured in duplicate using commercially available magnetic bead–based assays (EMD Millipore, Billerica, MA, USA). Intra-assay CV ranged from 3.0 to 6.8% for each analyte.

Statistical Analyses

Data that met assumptions of parametric statistics were analyzed using a 1-way analysis of variance (ANOVA). Where appropriate, pairwise differences were determined using Fisher's least significant difference post hoc test (IBM SPSS Statistics v20.0; IBM Corp, Armonk, NY). Data that violated the assumption of homogeneity of variances (vitamin D and DKK1) were analyzed using a Welch ANOVA, and pairwise differences were determined using the Games-Howell post hoc test. For TT and FT only, the correlation with running volume (RT and NRT only) was investigated because a negative correlation has been previously reported (21). Additionally, BMD data from the 2 running groups were analyzed with a 1-way analysis of covariance (ANCOVA) with “kilometer per week” as the covariate. Level of significance was set at p ≤ 0.05.

Results

Bone Mineral Density

Total body, femoral neck region, femoral greater trochanteric region, total proximal femur, and L1–L4 spine BMD were significantly (p ≤ 0.05) greater for RT than for NRT and CON. The NRT and CON did not differ in BMD at any measured site (Figure 1). An ANCOVA concluded that weekly running volumes did not contribute to differences in BMD between runners in NRT and RT groups.

F1
Figure 1.:
Bone mineral density (BMD) for untrained control participants (CON), runners who engage in no resistance training (NRT), and runners who engage in resistance training (RT). Bone mineral density sites: total body (TB), femoral neck region (FN), femoral greater trochanteric region (FGT), total femur (TF), and L1–L4 spine (SP). Values are mean ± SE. *Significantly different (p ≤ 0.05) from other groups.

Testosterone

No significant differences between groups were observed for TT or FT concentrations (Figure 2) nor was there a significant correlation between weekly running volume and TT or FT in the RT and NRT groups. Concentrations of TT and TF for all 3 groups were considered to be within the normal physiological range for young adult men (27).

F2
Figure 2.:
Total testosterone concentrations (A) and free testosterone concentrations (B) for untrained control participants (CON), runners who engage in no resistance training (NRT), and runners who engage in resistance training (RT). Values are mean ± SE.

Bone Metabolism Biomarkers

Vitamin D was significantly (p ≤ 0.05) greater for RT and NRT than for CON, which could be because of a potentially greater sun exposure in the runners. However, circulating concentrations of vitamin D for all 3 groups can be classified as “insufficient” (14,22). No significant differences between groups were observed for OPG, OC, insulin, leptin, PTH, RANKL, IL-1β, IL-6, TNF-α, FGF23, SOST, ACTH, DKK1, or OPN (Table 2).

T2
Table 2.:
Concentrations of bone health biomarkers including: 25-OH vitamin D, osteoprotegerin, osteocalcin, insulin, leptin, parathyroid hormone, receptor activator of nuclear factor κ-B ligand, interleukin 1β, interleukin 6, tumor necrosis factor α, fibroblast growth factor 23, sclerostin, adrenocorticotropic hormone, dickkopf-related protein 1, and osteopontin for untrained controls, nonresistance-trained runners, and resistance-trained runners.*†

Discussion

This study compared BMD and bone-relevant biomarkers of 2 groups of male distance runners (RT and NRT) and a group of age- and weight-matched, untrained, male control participants. This seems to be the first study to examine the relationship between distance running training, resistance exercise training, BMD, hormonal status, and bone metabolism biomarkers in young men. The major and novel finding of this study was that BMD was greater in RT than in NRT and CON, whereas the BMD of the NRT did not differ from the CON. This finding suggested that the stressor of resistance exercise training, but not the stressor of distance running training, was sufficient to elicit a positive effect on BMD in this age group. Another important finding was that TT and FT concentrations were within the normal physiological range for young adult men (27) and did not differ between the CON, RT, and NRT. Furthermore, among all bone metabolism biomarkers measured, differences were observed only for vitamin D, where RT and NRT presented with greater circulating vitamin D concentrations compared with CON. No other bone metabolism biomarkers differed between CON, RT, and NRT. These findings suggest that neither testosterone nor other bone metabolism biomarkers explains the greater BMD observed for RT compared with NRT and CON. Instead, the greater BMD of the RT can be attributed to participation in resistance training.

Performance of resistance exercise or power/plyometric training, such as sprinting events in track, is associated with a higher magnitude of bone strain, which is more effective for generating bone mass than distance running (1,16,24). A novel finding of the present study was that runners who regularly engaged in resistance training had higher BMD than runners who did not engage in resistance training. These results are comparable with those of a 12-month longitudinal study by Bennell et al. (1) that compared BMD of young adult male track and field power athletes and distance runners and found that the power athletes had higher lumbar spine BMD than the distance runners. Similarly, among masters track and field athletes (aged 40–64 years) who reported having participated in their sport before the age of 30 years, BMD across a range of measurement sites was greater in speed-power athletes than in endurance athletes or in age-matched and body mass–matched untrained control participants (24). In that study, BMD did not differ between the endurance athlete and control groups (24). Furthermore, as in the current study, TT and FT concentrations were not different between groups, suggesting that the higher BMD of the speed-power athletes could be attributed to the nature of speed-power training, which elicits a higher magnitude of impact and loads (24). Thus, evidence exists that despite the age-associated decline in BMD (15), runners who participate in high impact/loading exercise can achieve a greater BMD than runners who do not participate in such activities. The high magnitude of bone strain that is provided by resistance exercise is an effective stimulus for generating higher BMD (16), and the results from the present study corroborate this in young male runners.

A complex relationship exists between BMD and weekly running distance. Some studies report negative associations between running volume and BMD. MacDougall et al. (20) investigated BMD in male runners categorized into different weekly running distance groups. The authors reported that BMD was higher in participants who ran 22–32 km·wk−1 than in untrained control participants, but BMD was the same in participants who ran 96–120 km·wk−1 as in untrained control participants. Also in that study, running more than 32 km·wk−1 (40–48 and 64–88 km·wk−1 groups) was not associated with greater BMD compared with the 22–32 km·wk−1 group (20). Furthermore, the 96–120 km·wk−1 group had lower leg BMD similar to the control group (20). In another investigation of the relationship between running volume and BMD, a group running 64–80 km·wk−1 was found to have higher femoral BMD than an untrained control group and a 95+ km·wk−1 running group (21), and the 95+ km·wk−1 running group did not differ in BMD from the control group at any bone site. Together, these studies suggest that low-to-moderate running volume could lead to increases in BMD, whereas very high-volume running could negate the benefits of running on BMD. In the current study, the average weekly running volume for NRT (69.1 km·wk−1) was not associated with greater BMD as compared with CON. This is in contrast to the reports from MacDougall et al. (20) and MacKelvie et al. (21), who found greater BMD with moderate running volumes (22–88 and 64–80 km·wk−1, respectively). However, the age of participants might account for the differences in results between the current and previous studies. Mackelvie et al. (21) investigated male runners aged 40–55 years and MacDougall et al. (20) investigated male runners aged 20–45 years compared with male runners aged 23–32 years in the current study. Therefore, it is possible that for middle-aged adults, moderate-volume running results in greater BMD compared with no running (untrained control participants). Because untrained control participants in that age range typically have already experienced a decline in BMD (15), moderate-volume running might have prevented or attenuated such an age-associated decline in BMD for the runners.

Testosterone, the major gonadal androgen in males, is a potent anabolic hormone that plays an important role in regulating bone remodeling (29). Low resting concentrations of testosterone in male distance runners have previously been reported (9,21,30,31). A study that investigated male marathon runners reported that highly trained male athletes, like their female counterparts, have a deficiency of gonadotropin-releasing hormone (GnRH) (19). Deficiency of GnRH can lead to low levels of luteinizing hormone (LH), which could explain the lower circulating testosterone concentrations previously found in distance runners. Importantly, endurance running can lead to decreased concentrations of TT and FT, even if LH concentrations remain unchanged or are elevated (9,31). In the present study, NRT did not have lower circulating concentrations of TT or FT than RT or CON. However, it can be postulated that when male distance runners participate in a running volume that is higher than that of the runners in the present study, decreases in resting testosterone concentrations could occur. MacKelvie et al. (21) found a negative correlation between weekly running volume (ranging from 64 to 94 km·wk−1) and TT and FT concentrations. However, the testosterone concentrations reported by MacKelvie et al. (21) were still within the normal physiological range, although the highest volume runners presented with the lowest concentrations and had lower concentrations than the untrained control group in the present study. Therefore, there seems to be a minimum running volume threshold beyond which an inverse relationship between running volume and testosterone exists.

In addition to testosterone, other circulating biomarkers affect the balance between bone growth and degradation. After 1 month of resistance training, Oriental men aged 23–21 years had significantly greater OC concentrations than sedentary untrained control participants and this elevation was maintained throughout the remainder of the 4-month resistance training period but this was not associated with increased BMD (7), suggesting that an early elevation in OC could precede the increased BMD observed after long-term resistance training. Similarly, college-aged women who completed 8 weeks of resistance training, but not those who completed 8 weeks of aerobic only or combined aerobic and resistance training, had greater OC concentrations than sedentary untrained control participants (17). Furthermore, lower concentrations of bone metabolism biomarkers, such as PTH, carboxy-terminal propeptide of type I procollagen (bone formation marker), carboxyterminal crosslinked telopeptide of type I collagen (bone resorption marker), have been found in runners compared with nonrunners with no difference in OC (4). Together with the lack of difference in OC observed between RT, NRT, and CON in the present study, these results suggest that resistance exercise training elevates bone formation-promoting OC but not when combined with aerobic exercise. In the current study, vitamin D was greater in the 2 running groups compared with CON, potentially because of more sun exposure for the runners, but the average circulating vitamin D concentration for all 3 groups can be categorized as “insufficient” (14,22). Furthermore, no differences were observed in any of the remaining biomarkers of bone metabolism. Thus, it does not seem that changes in biomarkers of bone metabolism with running or combined running and resistance exercise training explain the greater BMD found for the RT group.

In conclusion, the major finding of this study was that young adult male distance runners who participated in resistance training at least once per week had greater BMD (whole body, lumber spine, and femoral) than their nonresistance-trained and untrained peers. Distance running alone, according to our findings, does not seem to affect BMD in young adult Caucasian men. However, it is important to note that BMD generally declines with aging (15) and that low-to-moderate running volume might prevent or attenuate this decline; whereas, high running volume does not seem to have such protective effect on BMD (21). Furthermore, testosterone declines with age (28), and this could further contribute to dysregulation of bone remodeling because of distance running.

Practical Applications

The effect of resistance training on BMD has been well documented and is largely regarded as an effective method of building bone mass and, in the present study, is associated with higher BMD in runners who lift weights versus runners who do not. Thus, incorporating resistance training at least once per week into a distance running program is associated with greater BMD and thus could be an effective method to protect or improve BMD in adult male distance runners.

Acknowledgments

This study was funded in part by awards from the American College of Sports Medicine—Texas Chapter (A.A.D.) and from the College of Education at the University of North Texas (A.A.D.). Funding agencies had no involvement in study design, data collection, data analysis, interpretation of results, writing of the manuscript, or the decision to submit the manuscript for publication.

A. A. Duplanty led study design, study implementation, data acquisition, data analysis, data interpretation, and manuscript preparation. D. E. Levitt assisted in data analysis, data interpretation, and manuscript preparation. D. W. Hill, B. K. McFarlin, and N. M. DiMarco assisted in study design, data interpretation, and manuscript preparation. J. L. Vingren directed study design, oversaw all procedures and analyses, and assisted in manuscript preparation. The authors have no conflicts of interest to disclose.

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Keywords:

DXA; resistance exercise; resistance training; testosterone; running

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