Abstract
Purpose
To determine the effects of US Army Ranger Training, an 8-week, physically demanding program (energy expenditure of 2,500–4,500 kcal/day) with energy restriction (deficit of 1,000–4,000 kcal/day) and sleep deprivation (<4 h sleep/night) on bone metabolism.
Methods
Blood was collected from 22 men (age 24 ± 4 years) before and after training. Follow-up measurements were made in a subset of 8 subjects between 2 and 6 weeks after training. Serum was analyzed for bone formation biomarkers [bone alkaline phosphatase (BAP) and osteocalcin (OCN)], bone resorption biomarkers [C-telopeptide cross-links of type I collagen (CTX) and tartrate-resistant acid phosphatase (TRAP5b)], calcium, parathyroid hormone (PTH), and vitamin D (25(OH)D). Data were analyzed using a paired t test to compare baseline to immediate post-training measures. A repeated-measures ANOVA with time as the only factor was used to analyze data on the subset of 8 subjects who completed follow-up data collection.
Results
BAP and OCN significantly decreased by 22.8 ± 15.5 % (pre 41.9 ± 10.1; post 31.7 ± 7.8 ng/ml) and 21.0 ± 23.3 % (pre 15.0 ± 3.5; post 11.3 ± 2.1 ng/ml), respectively, with training, suggesting suppressed bone formation. OCN returned to baseline, while BAP remained suppressed 2–6 weeks post-training. TRAP5b significantly increased by 57.5 ± 51.6 % (pre 3.0 ± 0.9; post 4.6 ± 1.4 ng/ml) from pre- to post-training, suggesting increased bone resorption, and returned to baseline 2–6 weeks post-training. PTH Increased significantly by 37.3 ± 45.2 % with training. No changes in CTX, calcium, or PTH were detected.
Conclusions
These data indicate that multi-stressor military training results in increased bone resorption and suppressed bone formation, with recovery of bone metabolism 2–6 weeks after completion of training.
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Abbreviations
- 25(OH)D:
-
25-Hydroxyvitamin D
- ANOVA:
-
Analysis of variance
- BAP:
-
Bone alkaline phosphatase
- CTX:
-
C-Telopeptide cross-links of type I collagen
- CV:
-
Coefficient of variation
- OCN:
-
Osteocalcin
- P1NP:
-
Procollagen 1 N-terminal peptide
- PTH:
-
Parathyroid Hormone
- TRAP5b:
-
Tartrate-resistant acid phosphatase
References
Almeida SA, Williams KM, Shaffer RA, Brodine SK (1999) Epidemiological patterns of musculoskeletal injuries and physical training. Med Sci Sports Exerc 31(8):1176–1182
Andersen NE, Karl JP, Cable SJ, Williams KW, Rood JC, Young AJ, Lieberman HR, McClung JP (2010) Vitamin D status in female military personnel during combat training. J Int Soc Sports Nutr 7:38. doi:10.1186/1550-2783-7-38
Bedford JL, Barr SI (2010) The relationship between 24-h urinary cortisol and bone in healthy young women. Int J Behav Med 17(3):207–215. doi:10.1007/s12529-009-9064-2
Bentolila V, Boyce TM, Fyhrie DP, Drumb R, Skerry TM, Schaffler MB (1998) Intracortical remodeling in adult rat long bones after fatigue loading. Bone 23(3):275–281
Biagioni MF, Mendes AL, Nogueira CR, Paiva SA, Leite CV, Mazeto GM (2014) Weight-reducing gastroplasty with Roux-en-Y gastric bypass: impact on vitamin D status and bone remodeling markers. Metab Syndr Relat Disord 12(1):11–15. doi:10.1089/met.2013.0026
Chomistek AK, Chiuve SE, Jensen MK, Cook NR, Rimm EB (2011) Vigorous physical activity, mediating biomarkers, and risk of myocardial infarction. Med Sci Sports Exerc 43(10):1884–1890. doi:10.1249/MSS.0b013e31821b4d0a
Dennison E, Hindmarsh P, Fall C, Kellingray S, Barker D, Phillips D, Cooper C (1999) Profiles of endogenous circulating cortisol and bone mineral density in healthy elderly men. J Clin Endocrinol Metab 84(9):3058–3063
Diment BC, Fortes MB, Greeves JP, Casey A, Costa RJ, Walters R, Walsh NP (2012) Effect of daily mixed nutritional supplementation on immune indices in soldiers undertaking an 8-week arduous training programme. Eur J Appl Physiol 112(4):1411–1418. doi:10.1007/s00421-011-2096-8
Evans RK, Antczak AJ, Lester M, Yanovich R, Israeli E, Moran DS (2008) Effects of a 4-month recruit training program on markers of bone metabolism. Med Sci Sports Exerc 40(11 Suppl):S660–S670. doi:10.1249/MSS.0b013e318189422b
Everson CA, Folley AE, Toth JM (2012) Chronically inadequate sleep results in abnormal bone formation and abnormal bone marrow in rats. Exp Biol Med (Maywood) 237(9):1101–1109. doi:10.1258/ebm.2012.012043
Friedl KE, Moore RJ, Hoyt RW, Marchitelli LJ, Martinez-Lopez LE, Askew EW (2000) Endocrine markers of semistarvation in healthy lean men in a multistressor environment. J Appl Physiol 88(5):1820–1830
Gertz ER, Silverman NE, Wise KS, Hanson KB, Alekel DL, Stewart JW, Perry CD, Bhupathiraju SN, Kohut ML, Van Loan MD (2010) Contribution of serum inflammatory markers to changes in bone mineral content and density in postmenopausal women: a 1-year investigation. J Clin Densitom 13(3):277–282. doi:10.1016/j.jocd.2010.04.003
Greendale GA, Unger JB, Rowe JW, Seeman TE (1999) The relation between cortisol excretion and fractures in healthy older people: results from the MacArthur studies-Mac. J Am Geriatr Soc 47(7):799–803
Heaney RP (1994) The bone-remodeling transient: implications for the interpretation of clinical studies of bone mass change. J Bone Miner Res 9(10):1515–1523. doi:10.1002/jbmr.5650091003
Henning PC, Scofield DE, Spiering BA, Staab JS, Matheny RW Jr, Smith MA, Bhasin S, Nindl BC (2014) Recovery of endocrine and inflammatory mediators following an extended energy deficit. J Clin Endocrinol Metab 99(3):956–964. doi:10.1210/jc.2013-3046
Jackson AS, Pollock ML (1978) Generalized equations for predicting body density of men. Br J Nutr 40(3):497–504
Jones BH, Cowan DN, Tomlinson JP, Robinson JR, Polly DW, Frykman PN (1993) Epidemiology of injuries associated with physical training among young men in the army. Med Sci Sports Exerc 25(2):197–203
Kaufman K, Brodine S, Shaffer R (1995) Musculoskeletal injuries in the military: literature review, summary, and recommendations. vol Technical Report. Naval Health Research Center San Diego, California
Kaufman KR, Brodine SK, Shaffer RA, Johnson CW, Cullison TR (1999) The effect of foot structure and range of motion on musculoskeletal overuse injuries. Am J Sports Med 27(5):585–593
Kerschan-Schindl K, Thalmann M, Sodeck GH, Skenderi K, Matalas AL, Grampp S, Ebner C, Pietschmann P (2009) A 246-km continuous running race causes significant changes in bone metabolism. Bone 45(6):1079–1083. doi:10.1016/j.bone.2009.07.088
Kyrolainen H, Karinkanta J, Santtila M, Koski H, Mantysaari M, Pullinen T (2008) Hormonal responses during a prolonged military field exercise with variable exercise intensity. Eur J Appl Physiol 102(5):539–546. doi:10.1007/s00421-007-0619-0
Lanyon LE (1987) Functional strain in bone tissue as an objective, and controlling stimulus for adaptive bone remodelling. J Biomech 20(11–12):1083–1093
Lester ME, Urso ML, Evans RK, Pierce JR, Spiering BA, Maresh CM, Hatfield DL, Kraemer WJ, Nindl BC (2009) Influence of exercise mode and osteogenic index on bone biomarker responses during short-term physical training. Bone 45(4):768–776. doi:10.1016/j.bone.2009.06.001
Lieberman HR, Castellani JW, Young AJ (2009) Cognitive function and mood during acute cold stress after extended military training and recovery. Aviat Space Environ Med 80(7):629–636
Lips P, Hosking D, Lippuner K, Norquist JM, Wehren L, Maalouf G, Ragi-Eis S, Chandler J (2006) The prevalence of vitamin D inadequacy amongst women with osteoporosis: an international epidemiological investigation. J Intern Med 260(3):245–254. doi:10.1111/j.1365-2796.2006.01685.x
Lutz LJ, Karl JP, Rood JC, Cable SJ, Williams KW, Young AJ, McClung JP (2012) Vitamin D status, dietary intake, and bone turnover in female Soldiers during military training: a longitudinal study. J Int Soc Sports Nutr 9(1):38. doi:10.1186/1550-2783-9-38
Martin R (2001) The role of bone remodeling in preventing or promoting stress fracture. In: Burr D, Milgrom C (eds) Musculoskeletal fatigue and stress fracture. CRC Press, Boca Raton
Martin RB, Burr DB, Sharkey NA (1998) Skeletal tissue mechanics. Springer, New York
Mori S, Burr DB (1993) Increased intracortical remodeling following fatigue damage. Bone 14(2):103–109
Nindl BC, Friedl KE, Marchitelli LJ, Shippee RL, Thomas CD, Patton JF (1996) Regional fat placement in physically fit males and changes with weight loss. Med Sci Sports Exerc 28(7):786–793
Nindl BC, Barnes BR, Alemany JA, Frykman PN, Shippee RL, Friedl KE (2007) Physiological consequences of US Army Ranger training. Med Sci Sports Exerc 39(8):1380–1387. doi:10.1249/MSS.0b013e318067e2f700005768-200708000-00022
Rauh MJ, Macera CA, Trone DW, Shaffer RA, Brodine SK (2006) Epidemiology of stress fracture and lower-extremity overuse injury in female recruits. Med Sci Sports Exerc 38(9):1571–1577. doi:10.1249/01.mss.0000227543.51293.9d
Robling AG, Hinant FM, Burr DB, Turner CH (2002) Improved bone structure and strength after long-term mechanical loading is greatest if loading is separated into short bouts. J Bone Miner Res 17(8):1545–1554. doi:10.1359/jbmr.2002.17.8.1545
Sheehan KM, Murphy MM, Reynolds K, Creedon JF, White J, Kazel M (2003) The response of a bone resorption marker to marine recruit training. Mil Med 168(10):797–801
Shin KA, Kim AC, Kim YJ, Lee YH, Shin YO, Kim SH, Park YS, Nam HS, Kim T, Kim HS, Park Y (2012) Effect of ultra-marathon (308 km) race on bone metabolism and cartilage damage biomarkers. Ann Rehabil Med 36(1):80–87. doi:10.5535/arm.2012.36.1.80
Sugiyama T, Meakin LB, Browne WJ, Galea GL, Price JS, Lanyon LE (2012) Bones’ adaptive response to mechanical loading is essentially linear between the low strains associated with disuse and the high strains associated with the lamellar/woven bone transition. J Bone Miner Res 27(8):1784–1793. doi:10.1002/jbmr.1599
Takahashi H, Epker B, Frost HM (1964) Resorption precedes formative activity. Surg Forum 15:437–438
Warden SJ, Hurst JA, Sanders MS, Turner CH, Burr DB, Li J (2005) Bone adaptation to a mechanical loading program significantly increases skeletal fatigue resistance. J Bone Miner Res 20(5):809–816. doi:10.1359/jbmr.041222
Zanker CL, Cooke CB (2004) Energy balance, bone turnover, and skeletal health in physically active individuals. Med Sci Sports Exerc 36(8):1372–1381
Zanker CL, Swaine IL (2000) Responses of bone turnover markers to repeated endurance running in humans under conditions of energy balance or energy restriction. Eur J Appl Physiol 83(4–5):434–440
Acknowledgments
This work was supported by appointments to the Postgraduate Research Participation Program at the US Army Research Institute of Environmental Medicine administered by the Oak Ridge Institute for Science and Education through interagency agreement between the US Department of Energy and US Army Medical Research and Material Command (JMH and JRH).
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The authors declare that they have no conflict of interest.
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Communicated by Olivier Seynnes.
The views, opinions, and/or findings in this report are those of the authors, and should not be construed as an official department of the army position, policy, or decision, unless so designated by other official documentation
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Hughes, J.M., Smith, M.A., Henning, P.C. et al. Bone formation is suppressed with multi-stressor military training. Eur J Appl Physiol 114, 2251–2259 (2014). https://doi.org/10.1007/s00421-014-2950-6
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DOI: https://doi.org/10.1007/s00421-014-2950-6