ORIGINAL RESEARCH
Comparisons of Bone Mineral Density Between Recreational and Trained Male Road Cyclists Christopher D. Mojock, PhD,* Michael J. Ormsbee, PhD,†‡ Jeong-Su Kim, PhD,†‡¶ Bahram H. Arjmandi, PhD, RD,†¶ Gideon A. Louw, MS,† Robert J. Contreras, PhD,§ and Lynn B. Panton, PhD†‡
Objective: To compare measures of training, performance, body composition, and areal bone mineral density (aBMD) between agematched recreational and competitively trained male road cyclists.
Design: Cross-sectional. Setting: Laboratory. Participants: Male cyclists (N = 28) aged 21–54 years riding more
Clinical Relevance: This study suggests road cycling may compromise aBMD and potentially increase the likelihood of low-trauma fractures; health care professionals should consider this exposure when exercise prescriptions are designed for patients at-risk for osteopenia/ osteoporosis, for example, women and older adults. Key Words: cycling, aBMD, body composition, DXA (Clin J Sport Med 2016;26:152–156)
than 3 hours per week.
Assessment of Risk Factors: Men who train at high ($8 h/wk) and moderate volumes (3–8 h/wk). Main Outcome Measures: Areal bone mineral density assessments by dual energy x-ray absorptiometry of the whole body, lumbar spine (L1-L4), right and left hips, maximal oxygen uptake (V̇ O2max), and training history. Results: Trained cyclists had higher power to weight (5.3 6 0.4 vs 4.7 6 0.3 W/kg, P = 0.001), V̇ O2max (57.2 6 4.5 vs 53.0 6 6.1 mL$kg21$min21, P = 0.049) and training volume (10.6 6 2.1 vs 6.3 6 0.9 h/wk, P , 0.001) than recreational cyclists. Trained cyclists had lower right (0.898 6 0.090 vs 0.979 6 0.107 g/cm2, P = 0.047) and left hip aBMD (0.891 6 0.079 vs 0.973 6 0.104 g/cm2, P = 0.032). Z-scores identified lumbar (L1-L4) aBMD as osteopenic (22.5 , Z-score , 21.0) in trained cyclists (21.39 6 1.09). Lumbar scans identified 12 trained and 4 recreational cyclists as osteopenic and 3 trained cyclists as osteoporotic. Conclusions: Areal bone mineral density is lower in trained male road cyclists compared with recreational, specifically at the hips. Lumbar aBMD is low in both trained and recreational cyclists. Research is needed to determine the chronic effects of cycling on aBMD and interventions that improve aBMD in this population.
Submitted for publication March 26, 2014; accepted November 1, 2014. From the *Department of Kinesiology and Health Science, Georgia Regents University, Augusta, Georgia; †Department of Nutrition, Food and Exercise Sciences, Florida State University, Tallahassee, Florida; ‡Institute of Sports Sciences and Medicine, Florida State University, Tallahassee, Florida; §Department of Psychology, Florida State University, Tallahassee, Florida; and ¶Center for Advancing Exercise and Nutrition Research on Aging, Florida State University, Tallahassee, Florida. The authors report no conflicts of interest. Corresponding Author: Christopher D. Mojock, PhD, Department of Kinesiology and Health Science, Georgia Regents University, 2500 Walton Way, Augusta, GA 30904 ([email protected]). Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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INTRODUCTION The cardiovascular benefits of cycling are achievable without the potentially injurious ground impact side effects of other activities, such as running and racket sports. However, this orthopedic advantage has been proposed as a potential mechanism for increased bone turnover that favors bone loss in weight-supported athletes, accelerated resorption, and reduced accrual.1–8 The osteogenic stimulus from exercise is the result of joint-reaction (muscle contraction) and ground reaction (impact) forces transmitted through the skeleton.9,10 Cross-sectional analyses and prospective investigations of male and female cyclists have shown site-specific reductions in areal bone mineral density (aBMD) at the hip and lumbar spine, which suggests the lack of ground reaction forces during prolonged exercise in a weight-supported position may be the driving factor for bone loss.11–22 Exercise, as prevention and treatment of osteoporosis, affects bone through increased strain placed on the bone during physical activity. Sports with the highest strain intensities, for example, gymnastics and weight lifting, have often been associated with significantly higher aBMD at the loaded sites.2– 5,7 In contrast, when the ground reaction forces are reduced, the osteogenic stimulus seems to be attenuated. For example, when a group of trained cyclists were compared with age-matched and weight-matched recreationally active noncyclist controls, anterior–posterior lumbar spine (L1-L4) aBMD was 7.1% lower in the cyclists.20 Similarly, when aBMD was compared in a group of age, weight, and training volume–matched runners (high ground reaction forces) to that of cyclists (low ground reaction forces), whole-body and lumbar spine scans were found to be 5% and 11% lower in the cyclists, respectively.18 Lower weekly training volume would limit exposure to non–weight-bearing activity in recreational cyclists, when compared with competitively trained cyclists, and limit the negative effect on aBMD. However, the effect of moderate levels of endurance cycle training in recreationally active Clin J Sport Med Volume 26, Number 2, March 2016
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Clin J Sport Med Volume 26, Number 2, March 2016
cyclists has not been investigated. Highly trained athletes are a relatively small group; recreationally active men will likely represent a larger portion of the estimated 15% to 30% of men who will suffer from an osteoporotic-related fracture in their lifetime.23 Therefore, the purpose of this cross-sectional analysis was to compare various measures of training, performance, and body composition, most importantly, aBMD, between agematched recreationally active and competitively trained male road cyclists. We hypothesized that the trained road cyclists would exhibit lower aBMD at the lumbar spine and hip, compared with recreationally trained road cyclists, and these values would be inversely related to measures of training volume.
METHODS Participants Normal weight healthy men engaged in more than 3 hours per week of road cycle training were recruited for the study through local cycling-specific social media groups (Facebook), flyers, and e-mails distributed throughout the Tallahassee, FL area, and surrounding counties. Men engaged in any exercise, other than cycling, for more than 2 days per week for more than 40 minutes per session (within the past 6 months) were excluded from the study. Additionally, those men who had uncontrolled hypertension (blood pressure .160/100 mm Hg), currently taking blood pressure medications, diagnosed with cardiovascular disease, stroke, diabetes, thyroid, or kidney dysfunction, those who smoked, were prescribed cholesterol medication or used any medications known to affect bone metabolism and/or had any musculoskeletal complications (ie, osteoarthritis or injury) that would impede exercise testing and training were not eligible to participate in the study. All participants provided written informed consent to participate, and the study was approved by the Human Subjects Committee of Florida State University. After a telephone screening, participants reported to the laboratory to complete health and training history questionnaires as well as exercise testing to determine their status as a recreational or trained road cyclist. Participants were asked to complete a 3-day dietary record, report to the laboratory after a 3-hour fast, and refrain from exercise for 24 hours. Before a body composition assessment, measurements of height (in centimeters), weight (in kilograms), resting heart rate (in beats per minute), blood pressure (in millimeter of mercury), and handgrip strength (in kilograms) were performed. Resting blood pressure and heart rate were taken in duplicate after participants had been seated for at least 5 minutes. Height and weight were measured through the use of a wall-mounted stadiometer and a digital scale, respectively (Seca Corporation; Hanover, Maryland), and body mass index (in kilograms per square meter) was calculated. Handgrip strength was assessed using a handheld dynamometer (Jamar; Sammons Preston Rolyon, Bolingbrook, Illinois) following validated procedures.24 Briefly, the participants stood with the handgrip dynamometer parallel to the side of the body with the forearm at approximately waist level. The grip bar was adjusted to fit comfortably in the participant’s Copyright Ó 2015 Wolters Kluwer Health, Inc. All rights reserved.
BMD in Recreational Versus Trained Cyclists
hand with the intermediate phalanges over the grip handle. Participants were requested to perform a maximal squeeze while exhaling. Each hand was tested, alternating right and left, for 3 trials. The highest force (in kilograms) production for each hand was totaled for the final handgrip strength score.
Body Composition Assessments Lean body mass (LBM), fat mass, and aBMD (in grams per square centimeter) were assessed through dual energy x-ray absorptiometry on a Hologic Discovery-W series scanner (Bedford, Massachusetts). A total of 4 scans were performed on each participant: (1) anteroposterior (AP) view of the total body with the participant lying supine; (2) AP view of the lumbar (L1-L4) spine with the participant lying supine with hips and knees supported at a 908 angle; and (3) AP view of the right and left femoral neck with the participant lying supine with thigh internally rotated. The quality analysis for the densitometer was conducted on a daily basis using a standard aluminum spine block (phantom) provided by the manufacturer. Measurements of the phantom were within the manufacturer’s precision standard with a coefficient of variation ,0.5%. Testing was completed according to the manufacturer’s instructions and specifications by a certified x-ray technician. The same technician evaluated all scans.
Exercise Performance Participants performed an incremental exercise test on an electronically braked cycle ergometer (RacerMate; Velotron Dynafit Pro, Seattle, Washington). The ergometer was fitted with their personal saddle, pedals, and based on their road cycle’s geometry. Participants were fitted with a heart rate monitor chest strap (Polar Electro Inc., Lake Success, New York) and performed a 5-minute self-selected warmup before the graded exercise test. Expired gasses were measured continuously using a TrueOne 2400 metabolic cart (ParvoMedics, Sandy, Utah). Participants began the exercise test at 50 W; resistance increased by 50 W every 2 minutes up to 150 W. Thereafter, resistance increased by 25 W every minute until volitional fatigue. The criterion for achievement of maximal oxygen uptake (V̇ O2max) was fulfilled by reaching at least 3 of the following: (1) a plateau in oxygen consumption for an increase in exercise intensity (,2.0 mL$kg21$min21 increase), (2) respiratory exchange ratio $ 1.15, (3) heart rate $ 85% of an age-predicted maximum (as determined by 220 participant’s age), (4) voluntary cessation of the test by the participant, and (5) a rating of perceived exertion $18 on the Borg Scale.25
Statistical Analyses
Descriptive statistics (mean 6 SD) were performed on demographic, training, and anthropometric variables. A 1-way analysis of variance was used to evaluate the differences on dependent measures between the recreational and trained road cyclists. Because of the small unequivocal groups, analysis of covariance was used to examine the effects of weight and LBM on the measures of aBMD between trained and recreational road cyclists. The x2 analysis was used to compare the incidence of low (osteopenia and osteoporosis) and normal aBMD between groups. Pearson product–moment correlations were www.cjsportmed.com |
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used to examine relationships between descriptive variables, both anthropometric and performance measurements, and measures of aBMD. Significance was accepted at P , 0.05.
RESULTS Participant Data and Performance Measures Thirty-nine healthy nonsmoking men, currently riding a cycle at least 3 hours per week on the road, volunteered to participate in the study. Six of the men were excluded from participating because they performed running exercise more than 2 days per week. Four were excluded for participating (within the last 6 months) in a resistance training program and 1 was excluded for participating in collegiate long-distance swimming. Therefore, 28 men (21-54 years) were included in the study. After initial screening and V̇ O2max testing, the participants were separated into 2 groups: those who had previous race experience, trained $8 h/wk, and had V̇ O2max $ 50 mL$kg21$min21, qualified as trained (n = 19), and the others were classified as recreational cyclists (n = 9). All cyclists were classified as road cyclists; review of their training logs identified 1 or no mountain bike rides per week. Table 1 presents descriptive characteristics of the trained and recreational road cyclists. It should be noted that one of the trained cyclists fell below 50 mL$kg21$min21 for his V̇ O2max but was included in the analysis based on his racing history (20 years) and weekly training hours (9 hours). Also, 1 recreational cyclist had a V̇ O2max value higher than the mean for the trained group but was not included in the trained group because he did not meet the minimum number of weekly training hours, had only recently started riding (2-3 years), and had no racing experience. This individual competed at the collegiate level as a kicker in football; it had been more than 10 years since he participated in his sport. The only significant differences (P , 0.05) between the groups were found in the training-related variables; trained cyclists had higher handgrip strength (108.8 6 15.3 vs 95.0 6 12.6 kg),
V̇ O2max (57.2 6 4.5 vs 53.0 6 6.1 mL$kg21$min21), power to weight ratio (5.3 6 0.4 vs 4.7 6 0.3 W/kg), and weekly training volume (10.6 6 2.1 vs 6.3 6 0.9 h/wk) than recreational cyclists.
Bone Mineral Density Comparisons Areal bone mineral density measurements are presented in Table 2. Trained road cyclists had lower aBMD at the right hip (0.898 6 0.090 vs 0.979 6 0.107 g/cm2, P = 0.047) and left hip (0.891 6 0.079 vs 0.973 6 0.104 g/cm2, P = 0.032) when compared with the recreational cyclists. Differences in lumbar aBMD between the 2 groups approached significance, with lower values measured in trained cyclists (0.924 6 0.122 vs 1.000 6 0.504 g/cm2, P = 0.085). Although there were no mean differences between the trained and recreational cyclists in weight (76.5 6 9.2 vs 75.6 6 8.2 kg, P = 0.821, respectively) or LBM (57.9 6 6.2 vs 55.5 6 6.5 kg, P = 0.346, respectively), they were considered as covariates due to their associations with aBMD and the small, unequal groups. However, there was no significant covariate by group interaction for weight or LBM on any measures of aBMD. The evaluation of Z-scores identified lumbar aBMD as osteopenic in trained cyclists and normal in recreational cyclists (21.39 6 1.09 vs 20.91 6 0.78, P = 0.251, respectively); the difference between groups was not significant. When lumbar scans were evaluated individually, 11 trained cyclists (58%) and 4 recreational cyclists (44%) were identified as osteopenic (22.5 , Z-score , 21.0); 3 trained cyclists (16%) were identified as osteoporotic (Z-score # 22.5). None of the recreational cyclists were classified as osteoporotic. Z-scores are considered more appropriate for populations under the age of 50; however, T-scores identified the same individuals as osteopenic and osteoporotic.26 Although 14 trained cyclists (74%) had lumbar aBMD classified as low (osteopenic or osteoporotic) compared with only 4 recreational cyclists (44%), the x2 analysis between groups was not significant (P = 0.132). The x2 analyses
TABLE 1. Descriptive Characteristics of the Male Road Cyclists (N = 28) Trained Cyclists Variables Age, yr Height, m Weight, kg BMI, kg/m2 Body fat,‡ % LBM,‡ kg Handgrip strength, kg V̇ O2max, mL$kg21$min21 MaxTest power: weight, W/kg Training history, yr Training volume, h/wk
n = 19 38.7 1.79 76.5 23.8 19.5 57.9 108.8 57.2 5.3 14.7 10.6
(8.9) (0.07) (9.2) (1.6) (3.7) (6.2) (15.3)* (4.5)* (0.4)† (9.1) (2.1)†
Recreational Cyclists Range 21-54 1.68-1.95 65.0-99.4 20.8-26.7 14.2-27.9 48.3-74.9 87.0-138.0 48.2-65.4 4.6-6.1 4.0-30.0 8.0-16.0
n=9 38.8 1.77 75.6 24.3 22.0 55.5 95.0 53.0 4.7 9.6 6.3
(8.7) (0.09) (8.2) (2.0) (3.2) (6.5) (12.6) (6.1) (0.3) (7.3) (0.9)
Range 22-53 1.61-1.89 64.2-88.7 21.8-27.0 17.9-28.0 45.1-66.4 83.5-123.0 38.8-59.8 4.1-5.1 3.0-25.0 5.0-7.5
Values are mean (SD). *Trained cyclists significantly greater than recreational cyclists, P , 0.05. †Trained cyclists significantly greater than recreational cyclists, P , 0.001. ‡Assessed by DXA. BMI = body mass index; LBM = lean body mass; V̇ O2max = maximal oxygen uptake.
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BMD in Recreational Versus Trained Cyclists
TABLE 2. Bone Mineral Density (g/cm2) of the Male Road Cyclists (N = 28) Variables (g/cm2) Whole body Lumbar spine (L1-L4) Right hip Left hip
Trained Cyclists (n = 19) 1.114 0.924 0.898 0.891
(0.085) (0.122) (0.090)* (0.079)*
Z-Score 20.73 21.39 20.71 20.75
(0.81) (1.09) (0.56) (0.49)
Recreational Cyclists (n = 9) 1.139 1.000 0.979 0.973
(0.084) (0.054) (0.107) (0.104)
Z-Score 20.32 20.91 20.32 20.36
(0.52) (0.78) (0.73) (0.67)
Values are mean (SD). *Trained cyclists significantly less than recreational cyclists, P , 0.05.
between groups at the whole body, right, and left hips were also not significant. Significant Pearson product–moment correlations were found when whole-body aBMD was compared with weight (r = 0.488, P = 0.008), height (r = 0.459, P = 0.014), LBM (r = 0.474, P = 0.014), and power achieved during the V̇ O2max test (r = 0.393, P = 0.039); no other significant correlations were found.
DISCUSSION Previous research found highly trained cyclists to be an at-risk population for low aBMD.11,13,14,16–22 However in our society, the majority of cyclists are recreational and not highly trained cyclists. We therefore, decided to compare age-matched recreational cyclists (3–8 h/wk) with trained cyclists ($8 h/wk) in an effort to further clarify the relationship between training volume and aBMD in male road cyclists. A cross-sectional analysis was performed between 2 groups of healthy adult male cyclists who train, almost exclusively, on the road to improve their fitness. The fundamental difference between these 2 groups of men was that 1 group was “competitive racers,” whereas the other group was “recreational cyclists.” This distinction was supported by significant differences in training hours per week, V̇ O2max values, and power to weight ratio; higher values were measured in the competitively trained group. Our data support part 1 of our hypothesis and found aBMD of the right and left hip regions significantly lower in competitively trained road cyclists when compared with recreational cyclists. However, our data do not support an inverse relationship between training volume and aBMD at the whole body, lumbar spine, or hip regions. In addition to differences in these cycling-specific training variables, the trained group also had higher handgrip strength than the recreational cyclists. It should be noted that both trained (87.0-138.0 kg) and recreational (83.5-103.3 kg) cyclists had very large ranges of handgrip performance. Anecdotally, the trained group seemed to have a more “athletic and competitive” background. Therefore, this score may have been due to inherently better motor control and coordination, which afforded the trained group better performance on a test of upper-body strength, an area in which neither group specifically targeted to train. Comparison of aBMD between the trained and recreational groups found the trained cyclists to have lower right and left hip aBMD. Although the values measured at the lumbar spine were not significantly different between groups, the Z-score for the trained cyclists was classified as osteopenic, while the recreational cyclists were normal. Similar to Copyright Ó 2015 Wolters Kluwer Health, Inc. All rights reserved.
the study by Smathers et al,20 in which they found a 7.1% lower L1-L4 lumbar aBMD in competitive road cyclists when compared with age-matched and body mass–matched controls, our lumbar scans show an 8.2% difference in aBMD, which approached significance (P = 0.085); it is possible that the small sample size or significant training effect in the recreational group affected the analysis. When the lumbar scans were evaluated individually, 14 (74%) of the trained cyclists were identified as osteopenic (n = 11; 58%) or osteoporotic (n = 3; 16%); 4 in the recreational group (44%) were identified as osteopenic, and none of the recreational cyclists were classified as osteoporotic. Taken in total, this is a noteworthy observation, 64% of all participants had low aBMD at the lumbar spine. Limitations to this study included small unequal groups; recruitment for the recreational group proved difficult; many individuals who were recruited were involved in too many hours of load-bearing exercise to be eligible for participation. Second, by design, cross-sectional analyses do not allow the determination of cause and effect. A third limitation concerned the training status of the recreational group. When the aerobic fitness and/or training volume of our recreational group were compared to other investigations of aBMD, they were considerably higher than recreationally active groups in other studies.16,17,20 It is possible, that the recreational group from our study participated in too much endurance cycling training and blurred the line between recreational and trained. The 6-hour weekly training volume in the recreational group may have been enough to contribute to the non–weight-bearing effects from cycling proposed by previous research.11,16,18 Finally, dual energy x-ray absorptiometry–derived measurements of aBMD are based on 2-dimensional analyses of tissue density and therefore do not represent potential adaptations to the volumetric properties of the bone. In addition to the relationship between density, stiffness, and strength, cortical bone thickness, bone diameter, and other shape changes affect bone’s ability to resist fractures.5,8 Measurement of these variables would present a clearer picture of the effects of cycling on bone health.
CONCLUSIONS The results of our study suggest that while cycling is beneficial to cardiovascular, pulmonary, and metabolic health outcomes, bone does not respond in the same favorable manner. Those men who participated in high-volume endurance cycling training ($8 h/wk) had lower aBMD than those with moderate training volumes (3-8 h/wk). However, both www.cjsportmed.com |
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groups had lower than normal aBMD, the greatest concern was a high prevalence of osteopenic aBMD at the lumbar spine. Previous work with cyclists has focused on those individuals involved in racing and who participate in excessively large volumes of training.11,14,16–18,20,27 Our work identifies the need to investigate the effects of cycling in more recreational populations, particularly considering the charge in our society to maintain activity level as we age and the increasing popularity of the sport of cycling. Future work in this area should be performed with larger and more distinctly separate groups of competitively trained and recreationally active cyclists to determine what effects moderate levels of endurance cycling training will have on bone health. More longitudinal investigations are necessary to identify the long-term effects of cycling as well as enhance the clarity on the mechanisms responsible for the resultant bone loss caused by increased bone turnover. Research is also needed to identify interventions that may attenuate or reverse the declines in aBMD present in cyclists. REFERENCES 1. 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;20:477–484. 2. Hind K, Gannon L, Whatley E, et al. Bone cross-sectional geometry in male runners, gymnasts, swimmers and non-athletic controls: a hipstructural analysis study. Eur J Appl Physiol. 2012;112:535–541. 3. Morel J, Combe B, Francisco J, et al. Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporos Int. 2001;12:152–157. 4. Nichols JF, Ruah MJ, Barrack MT, et al. Bone mineral density in female high school athletes: interactions of menstrual function and type of mechanical loading. Bone. 2007;41:371–377. 5. Nikander R, Sievanen H, Uusi-Rasi K, et al. Loading modalities and bone structures at nonweight-bearing upper extremity and weightbearing lower extremity: a pQCT study of adult female athletes. Bone. 2006;39:886–894. 6. Olmedillas H, Gonzalez-Aguero A, Moreno LA, et al. Cycling and bone health: a systematic review. BMC Med. 2012;10:168–178. 7. Taffe DR, Robinson TL, Snow CM, et al. High-impact exercise promotes bone gain in well-trained female athletes. J Bone Miner Res. 1997;12: 255–260. 8. Wilks DC, Winwood K, Gilliver SF, et al. Bone mass and geometry of the tibia and the radius of master sprinters, middle and long distance runners, race-walkers and sedentary control participants: a pQCT study. Bone. 2009;45:91–97.
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9. Barry DW, Kohrt WM. Exercise and the preservation of bone health. J Cardiopulm Rehabil Prev. 2008;28:153–162. 10. Burr DB, Robling AG, Turner CH. Effects of biomechanical stress on bones in animals. Bone. 2002;30:781–786. 11. Barry DW, Kohrt WM. BMD decreases over the course of a year in competitive male cyclists. J Bone Miner Res. 2008;23:484–491. 12. Barry DW, Hansen KC, Van Pelt RE, et al. Acute calcium ingestion attenuates exercise-induced disruption of calcium homeostasis. Med Sci Sports Exerc. 2011;43:617–623. 13. Beshgetoor D, Nichols JF, Rego I. Effect of training mode and calcium intake on bone mineral density in female master cyclist, runners, and non-athletes. Int J Sport Nutr Exerc Metab. 2000;10: 290–301. 14. Campion F, Nevill AM, Karlsson MK, et al. Bone status in professional cyclists. Int J Sports Med. 2010;31:511–515. 15. Guillemant J, Accarie C, Peres G, et al. Acute effects of an oral calcium load on markers of bone metabolism during endurance cycling exercise in male athletes. Calcif Tissue Int. 2004;74:407–414. 16. Nichols JF, Palmer JE, Levy SS. Low bone mineral density in highly trained male master cyclists. Osteoporos Int. 2003;14:644–649. 17. Nichols JF, Rauh MJ. Longitudinal changes in bone mineral density in male master cyclists and nonathletes. J Strength Cond Res. 2011;25: 727–734. 18. 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;57:226–232. 19. Sherk VD, Barry DW, Villalon KL, et al. Bone loss over 1 year of training and competition in female cyclists. Clin J Sport Med. 2014;24: 331–336. 20. Smathers AM, Bembem MG, Bembem DA. Bone density comparisons in male competitive road cyclists and untrained controls. Med Sci Sports Exerc. 2009;41:290–296. 21. Stewart AD, Hannan J. Total and regional bone density in male runners, cyclists, and controls. Med Sci Sports Exerc. 2000;32:1373–1377. 22. Warner SE, Shaw JM, Dalsky GP. Bone mineral density of competitive male mountain and road cyclists. Bone. 2002;30:281–286. 23. Nikander R, Sievanen H, Heinonen A, et al. Targeted exercise against osteoporosis: a systematic review and meta-analysis for optimising bone strength throughout life. BMC Med. 2010;8:1–16. 24. Trampisch US, Franke J, Jedamzik N, et al. Optimal Jamar dynamometer handle position to assess maximal isometric handgrip strength in epidemiological studies. J Hand Surg Am. 2012;37: 2368–2373. 25. Chen MJ, Fan X, Moe ST. Criterion-related validity of the Borg ratings of perceived exertion scale in healthy individuals: a meta-analysis. J Sports Sci. 2002;20:873–899. 26. Nagle KB, Brooks MA. A systematic review of bone health in cyclists. Sports Health. 2011;3:235–243. 27. Guillaume G, Chappard D, Audran M. Evaluation of the bone status in high-level cyclists. J Clin Densitom. 2012;15:103–107.
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Comparisons of Bone Mineral Density Between Recreational and Trained Male Road Cyclists Christopher D. Mojock, PhD,* Michael J. Ormsbee, PhD,†‡ Jeong-Su Kim, PhD,†‡¶ Bahram H. Arjmandi, PhD, RD,†¶ Gideon A. Louw, MS,† Robert J. Contreras, PhD,§ and Lynn B. Panton, PhD†‡
Objective: To compare measures of training, performance, body composition, and areal bone mineral density (aBMD) between agematched recreational and competitively trained male road cyclists.
Design: Cross-sectional. Setting: Laboratory. Participants: Male cyclists (N = 28) aged 21–54 years riding more
Clinical Relevance: This study suggests road cycling may compromise aBMD and potentially increase the likelihood of low-trauma fractures; health care professionals should consider this exposure when exercise prescriptions are designed for patients at-risk for osteopenia/ osteoporosis, for example, women and older adults. Key Words: cycling, aBMD, body composition, DXA (Clin J Sport Med 2016;26:152–156)
than 3 hours per week.
Assessment of Risk Factors: Men who train at high ($8 h/wk) and moderate volumes (3–8 h/wk). Main Outcome Measures: Areal bone mineral density assessments by dual energy x-ray absorptiometry of the whole body, lumbar spine (L1-L4), right and left hips, maximal oxygen uptake (V̇ O2max), and training history. Results: Trained cyclists had higher power to weight (5.3 6 0.4 vs 4.7 6 0.3 W/kg, P = 0.001), V̇ O2max (57.2 6 4.5 vs 53.0 6 6.1 mL$kg21$min21, P = 0.049) and training volume (10.6 6 2.1 vs 6.3 6 0.9 h/wk, P , 0.001) than recreational cyclists. Trained cyclists had lower right (0.898 6 0.090 vs 0.979 6 0.107 g/cm2, P = 0.047) and left hip aBMD (0.891 6 0.079 vs 0.973 6 0.104 g/cm2, P = 0.032). Z-scores identified lumbar (L1-L4) aBMD as osteopenic (22.5 , Z-score , 21.0) in trained cyclists (21.39 6 1.09). Lumbar scans identified 12 trained and 4 recreational cyclists as osteopenic and 3 trained cyclists as osteoporotic. Conclusions: Areal bone mineral density is lower in trained male road cyclists compared with recreational, specifically at the hips. Lumbar aBMD is low in both trained and recreational cyclists. Research is needed to determine the chronic effects of cycling on aBMD and interventions that improve aBMD in this population.
Submitted for publication March 26, 2014; accepted November 1, 2014. From the *Department of Kinesiology and Health Science, Georgia Regents University, Augusta, Georgia; †Department of Nutrition, Food and Exercise Sciences, Florida State University, Tallahassee, Florida; ‡Institute of Sports Sciences and Medicine, Florida State University, Tallahassee, Florida; §Department of Psychology, Florida State University, Tallahassee, Florida; and ¶Center for Advancing Exercise and Nutrition Research on Aging, Florida State University, Tallahassee, Florida. The authors report no conflicts of interest. Corresponding Author: Christopher D. Mojock, PhD, Department of Kinesiology and Health Science, Georgia Regents University, 2500 Walton Way, Augusta, GA 30904 ([email protected]). Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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INTRODUCTION The cardiovascular benefits of cycling are achievable without the potentially injurious ground impact side effects of other activities, such as running and racket sports. However, this orthopedic advantage has been proposed as a potential mechanism for increased bone turnover that favors bone loss in weight-supported athletes, accelerated resorption, and reduced accrual.1–8 The osteogenic stimulus from exercise is the result of joint-reaction (muscle contraction) and ground reaction (impact) forces transmitted through the skeleton.9,10 Cross-sectional analyses and prospective investigations of male and female cyclists have shown site-specific reductions in areal bone mineral density (aBMD) at the hip and lumbar spine, which suggests the lack of ground reaction forces during prolonged exercise in a weight-supported position may be the driving factor for bone loss.11–22 Exercise, as prevention and treatment of osteoporosis, affects bone through increased strain placed on the bone during physical activity. Sports with the highest strain intensities, for example, gymnastics and weight lifting, have often been associated with significantly higher aBMD at the loaded sites.2– 5,7 In contrast, when the ground reaction forces are reduced, the osteogenic stimulus seems to be attenuated. For example, when a group of trained cyclists were compared with age-matched and weight-matched recreationally active noncyclist controls, anterior–posterior lumbar spine (L1-L4) aBMD was 7.1% lower in the cyclists.20 Similarly, when aBMD was compared in a group of age, weight, and training volume–matched runners (high ground reaction forces) to that of cyclists (low ground reaction forces), whole-body and lumbar spine scans were found to be 5% and 11% lower in the cyclists, respectively.18 Lower weekly training volume would limit exposure to non–weight-bearing activity in recreational cyclists, when compared with competitively trained cyclists, and limit the negative effect on aBMD. However, the effect of moderate levels of endurance cycle training in recreationally active Clin J Sport Med Volume 26, Number 2, March 2016
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cyclists has not been investigated. Highly trained athletes are a relatively small group; recreationally active men will likely represent a larger portion of the estimated 15% to 30% of men who will suffer from an osteoporotic-related fracture in their lifetime.23 Therefore, the purpose of this cross-sectional analysis was to compare various measures of training, performance, and body composition, most importantly, aBMD, between agematched recreationally active and competitively trained male road cyclists. We hypothesized that the trained road cyclists would exhibit lower aBMD at the lumbar spine and hip, compared with recreationally trained road cyclists, and these values would be inversely related to measures of training volume.
METHODS Participants Normal weight healthy men engaged in more than 3 hours per week of road cycle training were recruited for the study through local cycling-specific social media groups (Facebook), flyers, and e-mails distributed throughout the Tallahassee, FL area, and surrounding counties. Men engaged in any exercise, other than cycling, for more than 2 days per week for more than 40 minutes per session (within the past 6 months) were excluded from the study. Additionally, those men who had uncontrolled hypertension (blood pressure .160/100 mm Hg), currently taking blood pressure medications, diagnosed with cardiovascular disease, stroke, diabetes, thyroid, or kidney dysfunction, those who smoked, were prescribed cholesterol medication or used any medications known to affect bone metabolism and/or had any musculoskeletal complications (ie, osteoarthritis or injury) that would impede exercise testing and training were not eligible to participate in the study. All participants provided written informed consent to participate, and the study was approved by the Human Subjects Committee of Florida State University. After a telephone screening, participants reported to the laboratory to complete health and training history questionnaires as well as exercise testing to determine their status as a recreational or trained road cyclist. Participants were asked to complete a 3-day dietary record, report to the laboratory after a 3-hour fast, and refrain from exercise for 24 hours. Before a body composition assessment, measurements of height (in centimeters), weight (in kilograms), resting heart rate (in beats per minute), blood pressure (in millimeter of mercury), and handgrip strength (in kilograms) were performed. Resting blood pressure and heart rate were taken in duplicate after participants had been seated for at least 5 minutes. Height and weight were measured through the use of a wall-mounted stadiometer and a digital scale, respectively (Seca Corporation; Hanover, Maryland), and body mass index (in kilograms per square meter) was calculated. Handgrip strength was assessed using a handheld dynamometer (Jamar; Sammons Preston Rolyon, Bolingbrook, Illinois) following validated procedures.24 Briefly, the participants stood with the handgrip dynamometer parallel to the side of the body with the forearm at approximately waist level. The grip bar was adjusted to fit comfortably in the participant’s Copyright Ó 2015 Wolters Kluwer Health, Inc. All rights reserved.
BMD in Recreational Versus Trained Cyclists
hand with the intermediate phalanges over the grip handle. Participants were requested to perform a maximal squeeze while exhaling. Each hand was tested, alternating right and left, for 3 trials. The highest force (in kilograms) production for each hand was totaled for the final handgrip strength score.
Body Composition Assessments Lean body mass (LBM), fat mass, and aBMD (in grams per square centimeter) were assessed through dual energy x-ray absorptiometry on a Hologic Discovery-W series scanner (Bedford, Massachusetts). A total of 4 scans were performed on each participant: (1) anteroposterior (AP) view of the total body with the participant lying supine; (2) AP view of the lumbar (L1-L4) spine with the participant lying supine with hips and knees supported at a 908 angle; and (3) AP view of the right and left femoral neck with the participant lying supine with thigh internally rotated. The quality analysis for the densitometer was conducted on a daily basis using a standard aluminum spine block (phantom) provided by the manufacturer. Measurements of the phantom were within the manufacturer’s precision standard with a coefficient of variation ,0.5%. Testing was completed according to the manufacturer’s instructions and specifications by a certified x-ray technician. The same technician evaluated all scans.
Exercise Performance Participants performed an incremental exercise test on an electronically braked cycle ergometer (RacerMate; Velotron Dynafit Pro, Seattle, Washington). The ergometer was fitted with their personal saddle, pedals, and based on their road cycle’s geometry. Participants were fitted with a heart rate monitor chest strap (Polar Electro Inc., Lake Success, New York) and performed a 5-minute self-selected warmup before the graded exercise test. Expired gasses were measured continuously using a TrueOne 2400 metabolic cart (ParvoMedics, Sandy, Utah). Participants began the exercise test at 50 W; resistance increased by 50 W every 2 minutes up to 150 W. Thereafter, resistance increased by 25 W every minute until volitional fatigue. The criterion for achievement of maximal oxygen uptake (V̇ O2max) was fulfilled by reaching at least 3 of the following: (1) a plateau in oxygen consumption for an increase in exercise intensity (,2.0 mL$kg21$min21 increase), (2) respiratory exchange ratio $ 1.15, (3) heart rate $ 85% of an age-predicted maximum (as determined by 220 participant’s age), (4) voluntary cessation of the test by the participant, and (5) a rating of perceived exertion $18 on the Borg Scale.25
Statistical Analyses
Descriptive statistics (mean 6 SD) were performed on demographic, training, and anthropometric variables. A 1-way analysis of variance was used to evaluate the differences on dependent measures between the recreational and trained road cyclists. Because of the small unequivocal groups, analysis of covariance was used to examine the effects of weight and LBM on the measures of aBMD between trained and recreational road cyclists. The x2 analysis was used to compare the incidence of low (osteopenia and osteoporosis) and normal aBMD between groups. Pearson product–moment correlations were www.cjsportmed.com |
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used to examine relationships between descriptive variables, both anthropometric and performance measurements, and measures of aBMD. Significance was accepted at P , 0.05.
RESULTS Participant Data and Performance Measures Thirty-nine healthy nonsmoking men, currently riding a cycle at least 3 hours per week on the road, volunteered to participate in the study. Six of the men were excluded from participating because they performed running exercise more than 2 days per week. Four were excluded for participating (within the last 6 months) in a resistance training program and 1 was excluded for participating in collegiate long-distance swimming. Therefore, 28 men (21-54 years) were included in the study. After initial screening and V̇ O2max testing, the participants were separated into 2 groups: those who had previous race experience, trained $8 h/wk, and had V̇ O2max $ 50 mL$kg21$min21, qualified as trained (n = 19), and the others were classified as recreational cyclists (n = 9). All cyclists were classified as road cyclists; review of their training logs identified 1 or no mountain bike rides per week. Table 1 presents descriptive characteristics of the trained and recreational road cyclists. It should be noted that one of the trained cyclists fell below 50 mL$kg21$min21 for his V̇ O2max but was included in the analysis based on his racing history (20 years) and weekly training hours (9 hours). Also, 1 recreational cyclist had a V̇ O2max value higher than the mean for the trained group but was not included in the trained group because he did not meet the minimum number of weekly training hours, had only recently started riding (2-3 years), and had no racing experience. This individual competed at the collegiate level as a kicker in football; it had been more than 10 years since he participated in his sport. The only significant differences (P , 0.05) between the groups were found in the training-related variables; trained cyclists had higher handgrip strength (108.8 6 15.3 vs 95.0 6 12.6 kg),
V̇ O2max (57.2 6 4.5 vs 53.0 6 6.1 mL$kg21$min21), power to weight ratio (5.3 6 0.4 vs 4.7 6 0.3 W/kg), and weekly training volume (10.6 6 2.1 vs 6.3 6 0.9 h/wk) than recreational cyclists.
Bone Mineral Density Comparisons Areal bone mineral density measurements are presented in Table 2. Trained road cyclists had lower aBMD at the right hip (0.898 6 0.090 vs 0.979 6 0.107 g/cm2, P = 0.047) and left hip (0.891 6 0.079 vs 0.973 6 0.104 g/cm2, P = 0.032) when compared with the recreational cyclists. Differences in lumbar aBMD between the 2 groups approached significance, with lower values measured in trained cyclists (0.924 6 0.122 vs 1.000 6 0.504 g/cm2, P = 0.085). Although there were no mean differences between the trained and recreational cyclists in weight (76.5 6 9.2 vs 75.6 6 8.2 kg, P = 0.821, respectively) or LBM (57.9 6 6.2 vs 55.5 6 6.5 kg, P = 0.346, respectively), they were considered as covariates due to their associations with aBMD and the small, unequal groups. However, there was no significant covariate by group interaction for weight or LBM on any measures of aBMD. The evaluation of Z-scores identified lumbar aBMD as osteopenic in trained cyclists and normal in recreational cyclists (21.39 6 1.09 vs 20.91 6 0.78, P = 0.251, respectively); the difference between groups was not significant. When lumbar scans were evaluated individually, 11 trained cyclists (58%) and 4 recreational cyclists (44%) were identified as osteopenic (22.5 , Z-score , 21.0); 3 trained cyclists (16%) were identified as osteoporotic (Z-score # 22.5). None of the recreational cyclists were classified as osteoporotic. Z-scores are considered more appropriate for populations under the age of 50; however, T-scores identified the same individuals as osteopenic and osteoporotic.26 Although 14 trained cyclists (74%) had lumbar aBMD classified as low (osteopenic or osteoporotic) compared with only 4 recreational cyclists (44%), the x2 analysis between groups was not significant (P = 0.132). The x2 analyses
TABLE 1. Descriptive Characteristics of the Male Road Cyclists (N = 28) Trained Cyclists Variables Age, yr Height, m Weight, kg BMI, kg/m2 Body fat,‡ % LBM,‡ kg Handgrip strength, kg V̇ O2max, mL$kg21$min21 MaxTest power: weight, W/kg Training history, yr Training volume, h/wk
n = 19 38.7 1.79 76.5 23.8 19.5 57.9 108.8 57.2 5.3 14.7 10.6
(8.9) (0.07) (9.2) (1.6) (3.7) (6.2) (15.3)* (4.5)* (0.4)† (9.1) (2.1)†
Recreational Cyclists Range 21-54 1.68-1.95 65.0-99.4 20.8-26.7 14.2-27.9 48.3-74.9 87.0-138.0 48.2-65.4 4.6-6.1 4.0-30.0 8.0-16.0
n=9 38.8 1.77 75.6 24.3 22.0 55.5 95.0 53.0 4.7 9.6 6.3
(8.7) (0.09) (8.2) (2.0) (3.2) (6.5) (12.6) (6.1) (0.3) (7.3) (0.9)
Range 22-53 1.61-1.89 64.2-88.7 21.8-27.0 17.9-28.0 45.1-66.4 83.5-123.0 38.8-59.8 4.1-5.1 3.0-25.0 5.0-7.5
Values are mean (SD). *Trained cyclists significantly greater than recreational cyclists, P , 0.05. †Trained cyclists significantly greater than recreational cyclists, P , 0.001. ‡Assessed by DXA. BMI = body mass index; LBM = lean body mass; V̇ O2max = maximal oxygen uptake.
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BMD in Recreational Versus Trained Cyclists
TABLE 2. Bone Mineral Density (g/cm2) of the Male Road Cyclists (N = 28) Variables (g/cm2) Whole body Lumbar spine (L1-L4) Right hip Left hip
Trained Cyclists (n = 19) 1.114 0.924 0.898 0.891
(0.085) (0.122) (0.090)* (0.079)*
Z-Score 20.73 21.39 20.71 20.75
(0.81) (1.09) (0.56) (0.49)
Recreational Cyclists (n = 9) 1.139 1.000 0.979 0.973
(0.084) (0.054) (0.107) (0.104)
Z-Score 20.32 20.91 20.32 20.36
(0.52) (0.78) (0.73) (0.67)
Values are mean (SD). *Trained cyclists significantly less than recreational cyclists, P , 0.05.
between groups at the whole body, right, and left hips were also not significant. Significant Pearson product–moment correlations were found when whole-body aBMD was compared with weight (r = 0.488, P = 0.008), height (r = 0.459, P = 0.014), LBM (r = 0.474, P = 0.014), and power achieved during the V̇ O2max test (r = 0.393, P = 0.039); no other significant correlations were found.
DISCUSSION Previous research found highly trained cyclists to be an at-risk population for low aBMD.11,13,14,16–22 However in our society, the majority of cyclists are recreational and not highly trained cyclists. We therefore, decided to compare age-matched recreational cyclists (3–8 h/wk) with trained cyclists ($8 h/wk) in an effort to further clarify the relationship between training volume and aBMD in male road cyclists. A cross-sectional analysis was performed between 2 groups of healthy adult male cyclists who train, almost exclusively, on the road to improve their fitness. The fundamental difference between these 2 groups of men was that 1 group was “competitive racers,” whereas the other group was “recreational cyclists.” This distinction was supported by significant differences in training hours per week, V̇ O2max values, and power to weight ratio; higher values were measured in the competitively trained group. Our data support part 1 of our hypothesis and found aBMD of the right and left hip regions significantly lower in competitively trained road cyclists when compared with recreational cyclists. However, our data do not support an inverse relationship between training volume and aBMD at the whole body, lumbar spine, or hip regions. In addition to differences in these cycling-specific training variables, the trained group also had higher handgrip strength than the recreational cyclists. It should be noted that both trained (87.0-138.0 kg) and recreational (83.5-103.3 kg) cyclists had very large ranges of handgrip performance. Anecdotally, the trained group seemed to have a more “athletic and competitive” background. Therefore, this score may have been due to inherently better motor control and coordination, which afforded the trained group better performance on a test of upper-body strength, an area in which neither group specifically targeted to train. Comparison of aBMD between the trained and recreational groups found the trained cyclists to have lower right and left hip aBMD. Although the values measured at the lumbar spine were not significantly different between groups, the Z-score for the trained cyclists was classified as osteopenic, while the recreational cyclists were normal. Similar to Copyright Ó 2015 Wolters Kluwer Health, Inc. All rights reserved.
the study by Smathers et al,20 in which they found a 7.1% lower L1-L4 lumbar aBMD in competitive road cyclists when compared with age-matched and body mass–matched controls, our lumbar scans show an 8.2% difference in aBMD, which approached significance (P = 0.085); it is possible that the small sample size or significant training effect in the recreational group affected the analysis. When the lumbar scans were evaluated individually, 14 (74%) of the trained cyclists were identified as osteopenic (n = 11; 58%) or osteoporotic (n = 3; 16%); 4 in the recreational group (44%) were identified as osteopenic, and none of the recreational cyclists were classified as osteoporotic. Taken in total, this is a noteworthy observation, 64% of all participants had low aBMD at the lumbar spine. Limitations to this study included small unequal groups; recruitment for the recreational group proved difficult; many individuals who were recruited were involved in too many hours of load-bearing exercise to be eligible for participation. Second, by design, cross-sectional analyses do not allow the determination of cause and effect. A third limitation concerned the training status of the recreational group. When the aerobic fitness and/or training volume of our recreational group were compared to other investigations of aBMD, they were considerably higher than recreationally active groups in other studies.16,17,20 It is possible, that the recreational group from our study participated in too much endurance cycling training and blurred the line between recreational and trained. The 6-hour weekly training volume in the recreational group may have been enough to contribute to the non–weight-bearing effects from cycling proposed by previous research.11,16,18 Finally, dual energy x-ray absorptiometry–derived measurements of aBMD are based on 2-dimensional analyses of tissue density and therefore do not represent potential adaptations to the volumetric properties of the bone. In addition to the relationship between density, stiffness, and strength, cortical bone thickness, bone diameter, and other shape changes affect bone’s ability to resist fractures.5,8 Measurement of these variables would present a clearer picture of the effects of cycling on bone health.
CONCLUSIONS The results of our study suggest that while cycling is beneficial to cardiovascular, pulmonary, and metabolic health outcomes, bone does not respond in the same favorable manner. Those men who participated in high-volume endurance cycling training ($8 h/wk) had lower aBMD than those with moderate training volumes (3-8 h/wk). However, both www.cjsportmed.com |
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groups had lower than normal aBMD, the greatest concern was a high prevalence of osteopenic aBMD at the lumbar spine. Previous work with cyclists has focused on those individuals involved in racing and who participate in excessively large volumes of training.11,14,16–18,20,27 Our work identifies the need to investigate the effects of cycling in more recreational populations, particularly considering the charge in our society to maintain activity level as we age and the increasing popularity of the sport of cycling. Future work in this area should be performed with larger and more distinctly separate groups of competitively trained and recreationally active cyclists to determine what effects moderate levels of endurance cycling training will have on bone health. More longitudinal investigations are necessary to identify the long-term effects of cycling as well as enhance the clarity on the mechanisms responsible for the resultant bone loss caused by increased bone turnover. Research is also needed to identify interventions that may attenuate or reverse the declines in aBMD present in cyclists. REFERENCES 1. 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;20:477–484. 2. Hind K, Gannon L, Whatley E, et al. Bone cross-sectional geometry in male runners, gymnasts, swimmers and non-athletic controls: a hipstructural analysis study. Eur J Appl Physiol. 2012;112:535–541. 3. Morel J, Combe B, Francisco J, et al. Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporos Int. 2001;12:152–157. 4. Nichols JF, Ruah MJ, Barrack MT, et al. Bone mineral density in female high school athletes: interactions of menstrual function and type of mechanical loading. Bone. 2007;41:371–377. 5. Nikander R, Sievanen H, Uusi-Rasi K, et al. Loading modalities and bone structures at nonweight-bearing upper extremity and weightbearing lower extremity: a pQCT study of adult female athletes. Bone. 2006;39:886–894. 6. Olmedillas H, Gonzalez-Aguero A, Moreno LA, et al. Cycling and bone health: a systematic review. BMC Med. 2012;10:168–178. 7. Taffe DR, Robinson TL, Snow CM, et al. High-impact exercise promotes bone gain in well-trained female athletes. J Bone Miner Res. 1997;12: 255–260. 8. Wilks DC, Winwood K, Gilliver SF, et al. Bone mass and geometry of the tibia and the radius of master sprinters, middle and long distance runners, race-walkers and sedentary control participants: a pQCT study. Bone. 2009;45:91–97.
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9. Barry DW, Kohrt WM. Exercise and the preservation of bone health. J Cardiopulm Rehabil Prev. 2008;28:153–162. 10. Burr DB, Robling AG, Turner CH. Effects of biomechanical stress on bones in animals. Bone. 2002;30:781–786. 11. Barry DW, Kohrt WM. BMD decreases over the course of a year in competitive male cyclists. J Bone Miner Res. 2008;23:484–491. 12. Barry DW, Hansen KC, Van Pelt RE, et al. Acute calcium ingestion attenuates exercise-induced disruption of calcium homeostasis. Med Sci Sports Exerc. 2011;43:617–623. 13. Beshgetoor D, Nichols JF, Rego I. Effect of training mode and calcium intake on bone mineral density in female master cyclist, runners, and non-athletes. Int J Sport Nutr Exerc Metab. 2000;10: 290–301. 14. Campion F, Nevill AM, Karlsson MK, et al. Bone status in professional cyclists. Int J Sports Med. 2010;31:511–515. 15. Guillemant J, Accarie C, Peres G, et al. Acute effects of an oral calcium load on markers of bone metabolism during endurance cycling exercise in male athletes. Calcif Tissue Int. 2004;74:407–414. 16. Nichols JF, Palmer JE, Levy SS. Low bone mineral density in highly trained male master cyclists. Osteoporos Int. 2003;14:644–649. 17. Nichols JF, Rauh MJ. Longitudinal changes in bone mineral density in male master cyclists and nonathletes. J Strength Cond Res. 2011;25: 727–734. 18. 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;57:226–232. 19. Sherk VD, Barry DW, Villalon KL, et al. Bone loss over 1 year of training and competition in female cyclists. Clin J Sport Med. 2014;24: 331–336. 20. Smathers AM, Bembem MG, Bembem DA. Bone density comparisons in male competitive road cyclists and untrained controls. Med Sci Sports Exerc. 2009;41:290–296. 21. Stewart AD, Hannan J. Total and regional bone density in male runners, cyclists, and controls. Med Sci Sports Exerc. 2000;32:1373–1377. 22. Warner SE, Shaw JM, Dalsky GP. Bone mineral density of competitive male mountain and road cyclists. Bone. 2002;30:281–286. 23. Nikander R, Sievanen H, Heinonen A, et al. Targeted exercise against osteoporosis: a systematic review and meta-analysis for optimising bone strength throughout life. BMC Med. 2010;8:1–16. 24. Trampisch US, Franke J, Jedamzik N, et al. Optimal Jamar dynamometer handle position to assess maximal isometric handgrip strength in epidemiological studies. J Hand Surg Am. 2012;37: 2368–2373. 25. Chen MJ, Fan X, Moe ST. Criterion-related validity of the Borg ratings of perceived exertion scale in healthy individuals: a meta-analysis. J Sports Sci. 2002;20:873–899. 26. Nagle KB, Brooks MA. A systematic review of bone health in cyclists. Sports Health. 2011;3:235–243. 27. Guillaume G, Chappard D, Audran M. Evaluation of the bone status in high-level cyclists. J Clin Densitom. 2012;15:103–107.
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