Journal of Strength and Conditioning Research Publish Ahead of Print

DOI: 10.1519/JSC.0000000000002504

TITLE

Resistance training is associated with higher bone mineral density among young adult male
distance runners independent of physiological factors

AUTHORS

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Anthony A. Duplantyabc, Danielle E. Levittbc, David W. Hillb, Brian K. McFarlinbc , Nancy M.
DiMarcod, Jakob L. Vingrenbc
a
Department of Kinesiology, Texas Woman’s University, Denton, TX, USA

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b
Applied Physiology Laboratory, Department of Kinesiology, Health Promotion, and
Recreation, University of North Texas, Denton, TX, USA
c
Department of Biological Sciences, University of North Texas, Denton TX, USA
d
Institute for Women’s Health, Texas Woman’s University, Denton, TX, USA

CORRESPONDING AUTHOR
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Jakob L. Vingren, PhD, CSCS,*D
Jakob.vingren@unt.edu
1155 Union Circle #310769 Denton, TX 76203-5017 USA
Office Phone: 940-565-3899
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CONTRIBUTIONS

AAD led study design, study implementation, data acquisition, data analysis, data interpretation,
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and manuscript preparation. DEL assisted in data analysis, data interpretation, and manuscript
preparation. DWH, BKM, and NMD assisted in study design, data interpretation, and manuscript
preparation. JLV directed study design, oversaw all procedures and analyses, and assisted in
manuscript preparation.
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Copyright ª 2018 National Strength and Conditioning Association

KEYWORDS

Bone mineral density, resistance exercise, resistance training, testosterone, running

WORD COUNT

Abstract- 242; Paper- 2,985

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NUMBER OF FIGURES AND TABLES

Figures- 2; Tables- 2

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CONFLICT OF INTEREST DECLARATION

The authors declare that they have no conflicts of interest.

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Copyright ª 2018 National Strength and Conditioning Association

ABSTRACT

Low bone mineral density (BMD) in male distance runners is common and could be modulated

by a host of biomarkers involved in the dynamic balance of bone tissue. In contrast, resistance

training can increase BMD; however, the efficacy of resistance training in protecting BMD in

distance runners has not been elucidated. Objective: To investigate the relationship between

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resistance training, testosterone and bone metabolism biomarker concentrations, and BMD in

young adult male distance runners. Methods: Twenty-five apparently healthy men (23-32 y;

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mean ± SD: 25.9 ± 2.9 y; 1.77 ± 0.04 m, 75.4 ± 8.5 kg) were categorized into one of three

groups: untrained controls (CON; n=8); non-resistance-trained runners (NRT; n=8); or

resistance-trained runners (RT; n=9). Blood was collected and analyzed for concentrations of

free and total testosterone and 14 bone metabolism biomarkers. BMD was assessed using dual
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energy X-ray absorptiometry. Results: At all measured sites, BMD was greater (p<0.05) for RT

compared to NRT and CON. Vitamin D concentration was greater (p<0.05) in RT and NRT

compared to CON. Concentrations of testosterone and remaining bone biomarkers did not differ
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between groups (p>0.05). Conclusion: Resistance-trained runners had greater BMD than non-

resistance-trained runners and untrained peers. This difference did not appear to be modulated by
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biomarkers that contribute to bone formation or resorption, indicating that differences in BMD

are associated with habitual load-bearing exercise using external resistance. Runners should
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perform resistance exercise at least once per week since this is associated with greater BMD.

KEYWORDS

Bone mineral density, resistance exercise, testosterone, running

Copyright ª 2018 National Strength and Conditioning Association

INTRODUCTION
Increases in bone mineral density (BMD) are stimulated by mechanical loading,

including weight-bearing physical activities[1]. 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]. The underlying causes of low BMD

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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[6].

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The syndrome of RED-S, caused by energy deficiency, can lead to serious consequences

for the endocrine, reproductive, and skeletal systems[6]. RED-S is usually found in females

participating in sports where athletes might have, or are perceived to have, a competitive
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advantage by being very lean. However, the presence of RED-S can result in decreased physical

performance and increased morbidity and mortality[7]. The change to the term RED-S reflects

the fact that male athletes can encounter factors similar to those involved in the Female Athlete
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Triad: low energy availability[8], hypothalamic-pituitary-gonadal axis hormone deficiency[9],

and low BMD, especially in the lumbar vertebrae[2,4,5]. In contrast to female distance runners,
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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[10], and previous
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reports of low serum testosterone in male distance runners[11–14], 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

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acutely after exercise[15–17] and at rest after a training period[16,18]. Compared to non-runners,

some (but not all) biomarkers of bone metabolism appear to be lower in runners[19]. Therefore,

bone metabolism biomarkers could help explain the low BMD previously found in male distance

runners.

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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 seven times more likely than

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runners to have osteopenia of the lumbar spine[20]. In contrast, power athletes (sprinters,

jumpers, weight lifters, etc.) have greater BMD compared with distance runners who do not

participate in those types of high impact and/or high load exercises[21–23]. Furthermore, among

masters runners (40-64 yr), those who participate in training regimens that elicit higher
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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
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male distance runners.

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Resistance exercise provides a potent stimulus for bone growth and maintenance and,

therefore, is often prescribed to those with osteopenia/osteoporosis[25]. The magnitude of

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mechanical loading is important for bone formation and resistance exercise elicits a magnitude of

strain that exceeds the threshold required for increased bone modelling[1].

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 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.

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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

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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
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participate in resistance training have higher BMD than untrained controls 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

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concentrations, and BMD in young adult male distance runners.

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METHODS

Participants
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Twenty-five healthy Caucasian men (mean ± SD: 26 ± 3 y; 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.

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 Then, each participant was assigned to one of the following three groups based on

exercise engagement over the previous three years: untrained controls (CON; n=8; < 1 hour of

exercise per week), non-resistance-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 per week and engaged in at least one recreational (non-power sport) resistance training

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session per week). NRT and RT had not regularly participated in any cross-training (biking,

swimming, etc.) over the previous three years. Age, height, and total body mass did not differ

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between groups (see 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 km/wk and 44.8 ± 13.8 km/wk,

respectively). Participants were free of diagnosed medical conditions and did not use substances
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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
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other ethnicities[26].
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[Table 1 here]
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Procedures

Dual energy X-ray absorptiometry

Total body BMD, regional BMD, and soft tissue composition (fat and lean mass), were

measured using DXA (Lunar Prodigy, GE Healthcare, Fairfield, CT). A trained DXA technician

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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 (0700-

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0900h) after a 12-hr fast and 48-hr abstention from exercise. Whole blood was allowed to clot

and then centrifuged (1,500×g, 4°C, 15 min). The resultant serum was stored at -80°C until

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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; 25-OH Vitamin D: Monobind, Lake Forest, CA). Intra-assay variances (CV)

were 3.5% for TT, 10.3% for FT, and 5.7% for Vitamin D. Biomarkers that promote bone
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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,
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IL-6, tumor necrosis factor (TNF)-α, fibroblast growth factor (FGF)23, sclerostin (SOST),

adrenocorticotropic hormone (ACTH), dickkopf-related protein (DDK)1, and osteopontin

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(OPN)] were measured in duplicate using commercially available magnetic bead-based assays

(EMD Millipore, Billerica, MA). Intra-assay CV ranged from 3.0%-6.8% for each analyte.
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Statistical analyses

Data that met assumptions of parametric statistics were analyzed using a one-way

ANOVA. Where appropriate, pairwise differences were determined using Fisher’s LSD post hoc

test (IBM SPSS Statistics v20, Chicago, IL). Data that violated the assumption of homogeneity

of variances (Vitamin D and DKK1) were analyzed using a Welch ANOVA and pairwise

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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 since a negative

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correlation has been previously reported[12]. Additionally, BMD data from the two running

groups were analyzed with a one-way ANCOVA with “km/wk” as the covariate. Level of

significance was set at p<0.05.

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RESULTS

Bone Mineral Density

Total body, femoral neck region, femoral greater trochanteric region, total proximal
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femur, and L1-L4 spine BMD were significantly (p<0.05) greater for RT than for NRT and

CON. NRT and CON did not differ in BMD at any measured site (see Figure 1). An ANCOVA
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concluded that weekly running volumes did not contribute to differences in BMD between

runners in NRT and RT groups.

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[Figure 1 here]

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Testosterone

No significant differences between groups were observed for TT or FT concentrations

(see 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].

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[Figure 2 here]

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Bone metabolism biomarkers

Vitamin D was significantly (p<0.05) greater for RT and NRT than for CON, which

could be due to a potentially greater sun exposure in the runners. However, circulating
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concentrations of Vitamin D for all 3 groups can be classified as “insufficient”[28,29]. 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 (see Table 2).
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[Table 2 here]
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DISCUSSION

This study compared BMD and bone-relevant biomarkers of two groups of male distance

runners (resistance-trained and non-resistance-trained) and a group of age- and weight-matched,

untrained, male controls. This appears to be the first study to examine the relationship between

distance running training, resistance exercise training, BMD, hormonal status, and bone

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metabolism biomarkers in young men. The major and novel finding of this study was that BMD

was greater in resistance-trained runners than in non-resistance-trained runners and untrained

controls, whereas the BMD of the non-resistance-trained runners did not differ from the

untrained controls. 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

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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.

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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 to CON. No other bone metabolism biomarkers differed between CON, RT, and NRT.

These findings suggest that neither testosterone nor other bone metabolism biomarkers explains
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the greater BMD observed for RT compared to NRT and CON. Instead, the greater BMD of the

resistance-trained runners can be attributed to participation in resistance training.

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Exercise Training mode and BMD

Performance of resistance exercise or power/plyometric training, such as sprinting events

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in track, is associated with a higher magnitude of bone strain, which is more effective for

generating bone mass than distance running[21,24,25]. A novel finding of the present study was
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that runners who regularly engaged in resistance training had higher BMD than runners who did

not engage in resistance training. These results are comparable to those of a 12-month

longitudinal study by Bennell et al.[21] 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.

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 Similarly, among masters track and field athletes (aged 40-64 years) who reported having

participated in their sport before the age of 30, BMD across a range of measurement sites was

greater in speed-power athletes than in endurance athletes or in age-and body mass-matched

controls[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

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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].

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Thus, evidence exists that despite the age-associated decline in BMD[30], 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[25], and the results from the present
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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.[31]
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investigated BMD in male runners categorized into different weekly running distance groups.

The authors reported that BMD was higher in participants who ran 22 to 32 km/wk than in
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untrained controls, but BMD was the same in participants who ran 96 to 120 km/wk as in

controls. Also in that study, running more than 32 km/wk (40-48 and 64-88 km/wk groups) was
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not associated with greater BMD compared to the 22 to 32 km/wk group[31]. Furthermore, the

96-120 km/week group had lower leg BMD similar to the control group[31]. In another

investigation of the relationship between running volume and BMD, a group running 64-80

km/wk was found to have higher femoral BMD than an untrained control group and a 95+

km/wk running group[12], and the 95+ km/week running group did not differ in BMD from the

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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) was not associated with greater BMD as compared to untrained controls. This is in

contrast to the reports from MacDougall et al.[31] and MacKelvie et al.[12], who found greater

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BMD with moderate running volumes (22-88 km/wk and 64-80 km/wk, respectively). However,

the age of participants might account for the differences in results between the current and

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previous studies. Mackelvie et al.[12] investigated male runners aged 40-55 years and

MacDougall et al.[31] investigated male runners aged 20-45 years compared to 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 to no running (untrained controls).

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Since untrained controls in that age range typically have already experienced a decline in

BMD[30], moderate-volume running might have prevented or attenuated such an age-associated

decline in BMD for the runners.

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Testosterone, bone metabolism biomarkers, and BMD

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Testosterone, the major gonadal androgen in males, is a potent anabolic hormone that

plays an important role in regulating bone remodeling[10]. Low resting concentrations of

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testosterone in male distance runners have previously been reported[11–14]. 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)[9]. 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,

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endurance running can lead to decreased concentrations of TT and FT, even if LH concentrations

remain unchanged or are elevated[11,13]. 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

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al.[12] found a negative correlation between weekly running volume (ranging from 64 to 94 km

per week) and TT and FT concentrations. However, the testosterone concentrations reported by

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MacKelvie et al.[12] 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 appears to be a minimum running

volume threshold beyond which an inverse relationship between running volume and
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testosterone exists.

In addition to testosterone, other circulating biomarkers affect the balance between bone
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growth and degradation. After one month of resistance training, Oriental men aged 23-21 y had

significantly greater OC concentrations than sedentary controls and this elevation was
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maintained throughout the remainder of the 4-month resistance training period but this was not

associated with increased BMD[16], suggesting that an early elevation in OC could precede the
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increased BMD observed after longer-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

controls[18]. Furthermore, lower concentrations of bone metabolism biomarkers such as PTH,

carboxyterminal propeptide of type I procollagen (bone formation marker), carboxyterminal

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crosslinked telopeptide of type I collagen (bone resorption marker), and have been found in

runners compared to non-runners with no difference in OC[19]. 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 two running

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groups compared CON, potentially due to more sun exposure for the runners, but the average

circulating Vitamin D concentration for all three groups can be categorized as

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“insufficient”[28,29]. Furthermore, no differences were observed in any of the remaining

biomarkers of bone metabolism. Thus, it does not appear 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.

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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,
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lumber spine, and femoral) than their non-resistance-trained and untrained peers. Distance

running alone, according to our findings, does not appear to affect BMD in young adult
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Caucasian men. However, it is important to note that BMD generally declines with aging[30] and

that low-to-moderate running volume might prevent or attenuate this decline; whereas, high
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running volume does not appear to have such protective effect on BMD[12]. Furthermore,

testosterone declines with age[32] and this could further contribute to dysregulation of bone

remodeling due to distance running.

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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

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greater BMD and thus could be an effective method to protect or improve BMD in adult male

distance runners.

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ACKNOWLEDGEMENTS

Competing interests: The authors declare no conflicts of interest.

Funding: This study was funded in part by awards from the American College of Sports
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Medicine- Texas Chapter (AAD) and from the College of Education at the University of North

Texas (AAD). 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
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manuscript for publication.

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REFERENCES
1 Frost HM. Bone “mass” and the “mechanostat”: A proposal. Anat Rec 1987;219:1–9.
doi:10.1002/ar.1092190104
A

2 Bilanin JE, Blanchard MS, Russek-Cohen E. Lower vertebral bone density in male long
distance runners. Med Sci Sports Exerc 1989;21:66–70.

3 Burrows M, Nevill AM, Bird S, et al. Physiological factors associated with low bone mineral
density in female endurance runners. Br J Sports Med 2003;37:67–71.

4 Hetland ML, Haarbo J, Christiansen C. Low bone mass and high bone turnover in male long
distance runners. J Clin Endocrinol Metab 1993;77:770–5. doi:10.1210/jcem.77.3.8370698

5 Hind K, Truscott JG, Evans JA. Low lumbar spine bone mineral density in both male and
female endurance runners. Bone 2006;39:880–5. doi:10.1016/j.bone.2006.03.012

Copyright ª 2018 National Strength and Conditioning Association

6 Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consensus statement: beyond the
Female Athlete Triad—Relative Energy Deficiency in Sport (RED-S). Br J Sports Med
2014;48:491–7. doi:10.1136/bjsports-2014-093502

7 Otis C, Drinkwater B, Johnson M, et al. ACSM position stand: the female athlete triad. Med
Sci Sports Exerc 1997;29:i–ix.

8 Zanker CL, Swaine IL. Responses of bone turnover markers to repeated endurance running
in humans under conditions of energy balance or energy restriction. Eur J Appl Physiol
2000;83:434–40. doi:10.1007/s004210000293

D
9 MacConnie SE, Barkan A, Lampman RM, et al. Decreased hypothalamic gonadotropin-
releasing hormone secretion in male marathon runners. N Engl J Med 1986;315:411–7.
doi:10.1056/NEJM198608143150702

TE
10 Vanderschueren D, Vandenput L, Boonen S, et al. Androgens and bone. Endocr Rev
2004;25:389–425. doi:10.1210/er.2003-0003

11 Hackney AC, Sinning WE, Bruot BC. Reproductive hormonal profiles of endurance-trained
and untrained males. Med Sci Sports Exerc 1988;20:60–5.
EP
12 MacKelvie KJ, Taunton JE, McKay HA, et al. Bone mineral density and serum testosterone
in chronically trained, high mileage 40-55 year old male runners. Br J Sports Med
2000;34:273–8.

13 Wheeler GD, Singh M, Pierce WD, et al. Endurance training decreases serum testosterone
levels in men without change in luteinizing hormone pulsatile release. J Clin Endocrinol
Metab 1991;72:422–5. doi:10.1210/jcem-72-2-422
C

14 Wheeler GD, Wall SR, Belcastro AN, et al. Reduced serum testosterone and prolactin levels
in male distance runners. JAMA 1984;252:514–6.

15 Li D-J, Fu H, Zhao T, et al. Exercise-stimulated FGF23 promotes exercise performance via

C

controlling the excess reactive oxygen species production and enhancing mitochondrial
function in skeletal muscle. Metabolism 2016;65:747–56. doi:10.1016/j.metabol.2016.02.009

16 Fujimura R, Ashizawa N, Watanabe M, et al. Effect of resistance exercise training on bone

A

formation and resorption in young male subjects assessed by biomarkers of bone

metabolism. J Bone Miner Res Off J Am Soc Bone Miner Res 1997;12:656–62.
doi:10.1359/jbmr.1997.12.4.656

17 Brahm H, Piehl-Aulin K, Ljunghall S. Biochemical markers of bone metabolism during

distance running in healthy, regularly exercising men and women. Scand J Med Sci Sports
1996;6:26–30.

18 Lester ME, Urso ML, Evans RK, et al. Influence of exercise mode and osteogenic index on
bone biomarker responses during short-term physical training. Bone 2009;45:768–76.
doi:10.1016/j.bone.2009.06.001

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19 Brahm H, Ström H, Piehl-Aulin K, et al. Bone metabolism in endurance trained athletes: a
comparison to population-based controls based on DXA, SXA, quantitative ultrasound, and
biochemical markers. Calcif Tissue Int 1997;61:448–54.

20 Rector RS, Rogers R, Ruebel M, et al. Participation in road cycling vs running is associated
with lower bone mineral density in men. Metabolism 2008;57:226–32.
doi:10.1016/j.metabol.2007.09.005

21 Bennell KL, Malcolm SA, Khan KM, et al. Bone mass and bone turnover in power athletes,
endurance athletes, and controls: a 12-month longitudinal study. Bone 1997;20:477–84.

D
22 Heinrich CH, Going SB, Pamenter RW, et al. Bone mineral content of cyclically
menstruating female resistance and endurance trained athletes. Med Sci Sports Exerc
1990;22:558–63.

TE
23 Hamdy RC, Anderson JS, Whalen KE, et al. Regional differences in bone density of young
men involved in different exercises. Med Sci Sports Exerc 1994;26:884–8.

24 Nowak A, Straburzyńska-Lupa A, Kusy K, et al. Bone mineral density and bone turnover in
male masters athletes aged 40–64. Aging Male 2010;13:133–41.
doi:10.3109/13685531003657776
EP
25 Layne JE, Nelson ME. The effects of progressive resistance training on bone density: a
review. Med Sci Sports Exerc 1999;31:25–30.

26 Gilsanz V, Skaggs DL, Kovanlikaya A, et al. Differential effect of race on the axial and
appendicular skeletons of children. J Clin Endocrinol Metab 1998;83:1420–7.
doi:10.1210/jcem.83.5.4765
C

27 Swerdloff R, Wang C. The testis and male sexual function. In: Cecil Medicine. Philadelphia,
PA: : Saunders Elsevier 2011. Chapter 242.

28 Holick MF. Vitamin D status: measurement, interpretation, and clinical application. Ann
C

Epidemiol 2009;19:73–8. doi:10.1016/j.annepidem.2007.12.001

29 Morris HA. Vitamin D: A hormone for all seasons - How much is enough? Understanding
the new pressures. Clin Biochem Rev 2005;26:21–32.
A

30 Kelepouris N, Harper KD, Gannon F, et al. Severe osteoporosis in men. Ann Intern Med
1995;123:452–60.

31 MacDougall JD, Webber CE, Martin J, et al. Relationship among running mileage, bone
density, and serum testosterone in male runners. J Appl Physiol Bethesda Md 1985
1992;73:1165–70.

32 Tenover JL. Testosterone and the aging male. J Androl 1997;18:103–6.

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FIGURE LEGENDS

Figure 1. BMD for untrained control participants (CON), runners who engage in no resistance

training (NRT), and runners who engage in resistance training (RT). BMD sites: total body (TB),

femoral neck region (FN), femoral greater trochanteric region (FGT), total femur (TF), L1-L4

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spine (SP). Values are means ± SE. *Significantly different (p<0.05) from other groups.

Figure 2. (A) Total testosterone concentrations and (B) Free testosterone concentrations for

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untrained control participants (CON), runners who engage in no resistance training (NRT), and

runners who engage in resistance training (RT). Values are means ± SE.
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Table 1. Descriptive data for untrained control participants (CON), runners who engage in no
resistance training (NRT), and runners who engage in resistance training (RT). Values are means
± SD. *Significantly different (p<0.05) from CON.

CON NRT RT
Age (y) 27 ± 2.7 26.1 ± 3.5 24.8 ± 2.3

Height (cm) 176.8 ± 3.9 179.1 ± 3.7 176.2 ± 5.0

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Mass (kg) 74.8 ± 8.3 73.2 ± 7.0 77.8 ± 10.1
CON NRT RT
Lean mass (kg) 53.8 ± 3.2 59.5 ± 4.4* 62.7 ± 5.8*

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Body fat % 23.5 ± 8.5 13.9 ± 6.7* 14.4 ± 7.9*
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Copyright ª 2018 National Strength and Conditioning Association

Vitamin D (ng·mL-1) 13.7 ± 1.2 22.9 ± 2.4 * 26.0 ± 3.0 *
OPG (pg·mL-1) 205.6 ± 13.0 217.0 ± 9.5 201.2 ± 9.2
OC (ng·mL-1) 8.5 ± 1.1 11.5 ± 2.0 10.2 ± 0.8
Insulin (pg·mL-1) 754.4 ± 65.1 934.2 ± 171.4 820.0 ± 105.8
Leptin (pg·mL-1) a 1213.2 ± 332.4 551.4 ± 98.6 809.0 ± 262.6
PTH (pg·mL-1) 88.1 ± 6.8 124.8 ± 31.6 120.2 ± 33.6

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RANKL (pg·mL-1) 108.1 ± 4.0 148.0 ± 27.1 158.2 ± 37.7
IL-1β (pg·mL-1) 1.9 ± 0.1 1.8 ± 0.1 1.8 ± 0.1
IL-6 (pg·mL-1) 7.9 ± 0.5 7.7 ± 0.4 7.9 ± 0.6

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TNF-α (pg·mL-1) 2.1 ± 0.1 1.9 ± 0.1 2.1 ± 0.1
FGF23 (pg·mL-1) 168.0 ± 17.6 174.0 ± 15.5 182.2 ± 29.3
SOST (pg·mL-1) 1718.6 ± 139.1 1744.1 ± 69.6 1898.4 ± 143.1
ACTH (pg·mL-1) 15.3 ± 0.9 16.6 ± 1.2 15.6 ± 0.8
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DKK1 (pg·mL-1) 1558.7 ± 221.3 1504.3 ± 363.1 1103.2 ± 83.8
OPN (pg·mL-1)a 4164.8 ± 1946.4 4791.0 ± 1225.3 5155.4 ± 928.2

Table 2. Concentrations of bone health biomarkers including: 25-OH Vitamin D,

osteoprotegerin (OPG), osteocalcin (OC), insulin, leptin, parathyroid hormone (PTH), receptor
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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) for untrained controls (CON),
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non-resistance-trained runners (NRT), and resistance-trained runners (RT). Values are means ±
SE. *Significantly (p<0.05) different from CON. aData from two outliers were disregarded.
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Copyright ª 2018 National Strength and Conditioning Association

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Copyright ª 2018 National Strength and Conditioning Association