CoChat
Sign Up
Cited by 64Bone health and osteoporosis researchLower Extremity Biomechanics and PathologiesSports Performance and Training

Effects of Low Energy Availability on Bone Health in Endurance Athletes and High-Impact Exercise as A Potential Countermeasure: A Narrative Review

Open access
Hutson, Mark J., O’Donnell, Emma, Brooke-Wavell, Katherine, Sale, Craig, Blagrove, Richard C.·2021·Sports Medicine
DOI 10.1007/s40279-020-01396-4PMC PMC7900047
Open this paper in CoChat — free accountOpen PDF

Abstract

Endurance athletes expend large amounts of energy in prolonged high-intensity exercise and, due to the weight-sensitive nature of most endurance sports, often practice periods of dietary restriction. The Female Athlete Triad and Relative Energy Deficiency in Sport models consider endurance athletes at high-risk for suffering from low energy availability and associated health complications, including an increased chance of bone stress injury. Several studies have examined the effects of low energy availability on various parameters of bone structure and markers of bone (re)modelling; however, there are differences in findings and research methods and critical summaries are lacking. It is difficult for athletes to reduce energy expenditure or increase energy intake (to restore energy availability) in an environment where performance is a priority. Development of an alternative tool to help protect bone health would be beneficial. High-impact exercise can be highly osteogenic and energy efficient; however, at present, it is rarely utilized to promote bone health in endurance athletes. Therefore, with a view to reducing the prevalence of bone stress injury, the objectives of this review are to evaluate the effects of low energy availability on bone health in endurance athletes and explore whether a high-impact exercise intervention may help to prevent those effects from occurring.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1007/s40279-020-01396-4

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 85

  1. [3]Loucks AB Kiens B Wright HH Energy availability in athletes J Sports Sci. 2011 29 Suppl 1 S7 S15 10.1080/02640414.2011.588958 21793767 · DOI · Paper page
  2. [4]De Souza MJ Nattiv A Joy E Misra M Williams NI Mallinson RJ 2014 Female Athlete Triad coalition consensus statement on treatment and return to play of the Female Athlete Triad: 1st international conference held in San Francisco, California, May 2012 and 2nd international conference held in Indianapolis, Indiana M. Br J Sports Med. 2014 48 289 10.1136/bjsports-2013-093218 24463911 · DOI · Paper page
  3. [5]Heikura IA Uusitalo ALT Stellingwerff T Bergland D Mero AA Burke LM Low energy availability is difficult to assess but outcomes have large impact on bone injury rates in elite distance athletes Int J Sport Nutr Exerc Metab. 2018 28 403 411 10.1123/ijsnem.2017-0313 29252050 · DOI · Paper page
  4. [6]Loucks AB Thuma JR Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women J Clin Endocrinol Metab 2003 88 297 311 10.1210/jc.2002-020369 12519869 · DOI · Paper page
  5. [7]Koehler K Hoerner NR Gibbs JC Zinner C Braun H De Souza MJ Low energy availability in exercising men is associated with reduced leptin and insulin but not with changes in other metabolic hormones J Sports Sci. 2016 34 1921 1929 10.1080/02640414.2016.1142109 26852783 · DOI · Paper page
  6. [8]Elliott-Sale KJ, Tenforde AS, Parziale AL, Holtzman B, Ackerman KE. Endocrine effects of relative energy deficiency in sport. Int J Sport Nutr Exerc Metab [Internet]. 2018;28:335–49. Available from: https://journals.humankinetics.com/view/journals/ijsnem/28/4/article-p335.xml. 30008240
  7. [9]Chen XX Yang T Roles of leptin in bone metabolism and bone diseases J Bone Miner Metab. 2015 33 474 485 10.1007/s00774-014-0569-7 25777984 · DOI
  8. [10]Papageorgiou M Elliott-Sale KJ Parsons A Tang JCY Greeves JP Fraser WD Effects of reduced energy availability on bone metabolism in women and men Bone 2017 105 191 199 10.1016/j.bone.2017.08.019 28847532 · DOI · Paper page
  9. [11]Tenforde AS, Nattiv A, Barrack M, Kraus E, Kim B, Kussman A, et al. Distribution of bone stress injuries in elite male and female collegiate runners. Med Sci Sport Exerc [Internet]. 2015;47:905. Available from: http://journals.lww.com/00005768-201505001-02795.
  10. [12]Bennell KL Malcolm SA Thomas SA Wark JD Brukner PD The incidence and distribution of stress fractures in competitive track and field athletes: a twelve-month prospective study Am J Sports Med 1996 24 211 217 10.1177/036354659602400217 8775123 · DOI
  11. [13]Kelsey JL, Bachrach LK, Procter-Gray E, Nieves J, Greendale GA, Sowers M, et al. Risk factors for stress fracture among young female cross-country runners. Med Sci Sport Exerc [Internet]. 2007;39:1457–63. Available from: https://insights.ovid.com/crossref?an=00005768-200709000-00003. 17805074
  12. [14]Duckham RL Brooke-Wavell K Summers GD Cameron N Peirce N Stress fracture injury in female endurance athletes in the United Kingdom: a 12-month prospective study Scand J Med Sci Sports. 2015 25 854 859 10.1111/sms.12453 25892560 · DOI
  13. [15]Barrack MT Gibbs JC De Souza MJ Williams NI Nichols JF Rauh MJ Higher incidence of bone stress injuries with increasing Female Athlete Triad-related risk factors Am J Sports Med. 2014 42 949 958 10.1177/0363546513520295 24567250 · DOI · Paper page
  14. [16]Kraus E Tenforde AS Nattiv A Sainani KL Kussman A Deakins-Roche M Bone stress injuries in male distance runners: higher modified Female Athlete Triad cumulative risk assessment scores predict increased rates of injury Br J Sports Med. 2019 53 237 242 10.1136/bjsports-2018-099861 30580252 · DOI
  15. [17]Williams NI Helmreich DL Parfitt DB Caston-Balderrama A Cameron JL Evidence for a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training J Clin Endocrinol Metab. 2001 86 5184 5193 10.1210/jcem.86.11.8024 11701675 · DOI
  16. [19]Melin A Tornberg ÅB Skouby S Møller SS Sundgot-Borgen J Faber J Energy availability and the Female Athlete Triad in elite endurance athletes Scand J Med Sci Sports. 2015 25 610 622 10.1111/sms.12261 24888644 · DOI
  17. [20]Dusek T Influence of high intensity training on menstrual cycle disorders in athletes Croat Med J. 2001 42 79 82 11172662
  18. [21]Mitchell DM Tuck P Ackerman KE Cano Sokoloff N Woolley R Slattery M Altered trabecular bone morphology in adolescent and young adult athletes with menstrual dysfunction Bone 2015 81 24 30 10.1016/j.bone.2015.06.021 26123592 PMC4745258 · DOI
  19. [22]Ackerman KE, Cano Sokoloff N, De Nardo Maffazioli G, Clarke HM, Lee H, Misra M. Fractures in relation to menstrual status and bone parameters in young athletes. Med Sci Sport Exerc [Internet]. 2015;47:1577–86. Available from: https://insights.ovid.com/crossref?an=00005768-201508000-00004. PMC4430468 25397605
  20. [23]Hart NH Nimphius S Rantalainen T Ireland A Siafarikas A Newton RU Mechanical basis of bone strength: influence of bone material, bone structure and muscle action J Musculoskelet Neuronal Interact. 2017 17 114 139 28860414 PMC5601257
  21. [24]Kato T Terashima T Yamashita T Hatanaka Y Honda A Umemura Y Effect of low-repetition jump training on bone mineral density in young women J Appl Physiol. 2006 100 839 843 10.1152/japplphysiol.00666.2005 16269526 · DOI
  22. [25]Bennell KL Malcolm SA Thomas SA Reid SJ Brukner PD Ebeling PR Risk factors for stress fractures in track and field athletes Am J Sports Med. 1996 24 810 818 10.1177/036354659602400617 8947404 · DOI
  23. [26]Nattiv A Stress fractures and bone health in track and field athletes J Sci Med Sport. 2000 3 268 279 10.1016/S1440-2440(00)80036-5 11101266 · DOI
  24. [27]Nattiv A Kennedy G Barrack MT Abdelkerim A Goolsby MA Arends JC Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play Am J Sports Med. 2013 41 1930 1941 10.1177/0363546513490645 23825184 PMC4367232 · DOI
  25. [28]Tenforde AS Kraus E Fredericson M Bone stress injuries in runners Phys Med Rehabil Clin N Am. 2016 27 139 149 10.1016/j.pmr.2015.08.008 26616181 · DOI
  26. [29]Singhal V Reyes KC Pfister B Ackerman K Slattery M Cooper K Bone accrual in oligo-amenorrheic athletes, eumenorrheic athletes and non-athletes Bone 2019 120 305 313 10.1016/j.bone.2018.05.010 29758361 PMC6636860 · DOI
  27. [30]Ackerman KE Putman M Guereca G Taylor AP Pierce L Herzog DB Cortical microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non-athletes Bone 2012 51 680 687 10.1016/j.bone.2012.07.019 22878154 PMC3482939 · DOI
  28. [31]Pollock N, Grogan C, Perry M, Pedlar C, Cooke K, Morrissey D, et al. Bone-mineral density and other features of the Female Athlete Triad in elite endurance runners: a longitudinal and cross-sectional observational study. Int J Sport Nutr Exerc Metab [Internet]. 2010;20:418–26. Available from: https://journals.humankinetics.com/view/journals/ijsnem/20/5/article-p418.xml. 20975110
  29. [32]Baxter-Jones AD Faulkner RA Forwood MR Mirwald RL Bailey DA Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass J Bone Miner Res. 2011 26 1729 1739 10.1002/jbmr.412 21520276 · DOI · Paper page
  30. [33]Burke LM Lundy B Fahrenholtz IL Melin AK Pitfalls of conducting and interpreting estimates of energy availability in free-living athletes Int J Sport Nutr Exerc Metab. 2018 28 350 363 10.1123/ijsnem.2018-0142 30029584 · DOI · Paper page
  31. [34]Duckham RL Peirce N Bailey CA Summers G Cameron N Brooke-Wavell K Bone geometry according to menstrual function in female endurance athletes Calcif Tissue Int. 2013 92 444 450 10.1007/s00223-013-9700-3 23361333 · DOI
  32. [35]Ackerman KE, Nazem T, Chapko D, Russell M, Mendes N, Taylor AP, et al. Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J Clin Endocrinol Metab [Internet]. 2011;96:3123–33. Available from: https://academic.oup.com/jcem/article/96/10/3123/2834899. PMC3200253 21816790
  33. [36]Piasecki J Ireland A Piasecki M Cameron J McPhee JS Degens H The strength of weight-bearing bones is similar in amenorrheic and eumenorrheic elite long-distance runners Scand J Med Sci Sports. 2018 28 1559 1568 10.1111/sms.13062 29380429 · DOI · Paper page
  34. [37]Lieberman JL De Souza MJ Wagstaff DA Williams NI Menstrual disruption with exercise is not linked to an energy availability threshold Med Sci Sport Exerc. 2018 50 551 561 10.1249/MSS.0000000000001451 PMC5820163 29023359 · DOI · Paper page
  35. [38]De Souza MJ Koltun KJ Williams NI The role of energy availability in reproductive function in the Female Athlete Triad and extension of its effects to men: an initial working model of a similar syndrome in male athletes Sport Med. 2019 48 Suppl 2 S125 137 10.1007/s40279-019-01217-3 PMC6901401 31696452 · DOI
  36. [39]Hackney AC Hypogonadism in exercising males: dysfunction or adaptive-regulatory adjustment? Front Endocrinol (Lausanne). 2020 11 11 10.3389/fendo.2020.00011/full 32082255 PMC7005256 · DOI
  37. [41]Tenforde AS Barrack MT Nattiv A Fredericson M Parallels with the Female Athlete Triad in male athletes Sports Med. 2016 46 171 182 10.1007/s40279-015-0411-y 26497148 · DOI
  38. [42]Tenforde AS Fredericson M Sayres LC Cutti P Sainani KL Identifying sex-specific risk factors for low bone mineral density in adolescent runners Am J Sports Med. 2015 43 1494 1504 10.1177/0363546515572142 25748470 · DOI
  39. [43]Mallinson RJ Southmayd EA De Souza MJ Geometric and “true” densitometric characteristics of bones in athletes with stress fracture and menstrual disturbances: a systematic review Sport Med. 2019 49 1059 1078 10.1007/s40279-019-01109-6 31041601 · DOI
  40. [44]Duckham RL Bialo SR Machan J Kriz P Gordon CM A case-control pilot study of stress fracture in adolescent girls: the discriminative ability of two imaging technologies to classify at-risk athletes Osteoporos Int. 2019 30 1573 1580 10.1007/s00198-019-05001-x 31143993 · DOI
  41. [45]Schnackenburg KE, Macdonald HM, Ferber R, Wiley JP, Boyd SK. Bone quality and muscle strength in female athletes with lower limb stress fractures. Med Sci Sport Exerc [Internet]. 2011;43:2110–9. Available from: http://journals.lww.com/00005768-201111000-00012. 21552163
  42. [46]Southmayd EA Mallinson RJ Williams NI Mallinson DJ De Souza MJ Unique effects of energy versus estrogen deficiency on multiple components of bone strength in exercising women Osteoporos Int. 2017 28 1365 1376 10.1007/s00198-016-3887-x 28032184 · DOI
  43. [47]Popp KL Frye AC Stovitz SD Hughes JM Bone geometry and lower extremity bone stress injuries in male runners J Sci Med Sport. 2020 23 145 150 10.1016/j.jsams.2019.09.009 31594711 · DOI
  44. [48]Ackerman KE, Pierce L, Guereca G, Slattery M, Lee H, Goldstein M, et al. Hip structural analysis in adolescent and young adult oligoamenorrheic and eumenorrheic athletes and nonathletes. J Clin Endocrinol Metab [Internet]. 2013;98:1742–9. Available from: https://academic.oup.com/jcem/article/98/4/1742/2537074. PMC3615200 23476076
  45. [49]Beck T Ruff C Shaffer R Betsinger K Trone D Brodine S Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors Bone 2000 27 437 444 10.1016/S8756-3282(00)00342-2 10962357 · DOI
  46. [50]Ruffing JA Nieves JW Zion M Tendy S Garrett P Lindsay R The influence of lifestyle, menstrual function and oral contraceptive use on bone mass and size in female military cadets Nutr Metab (Lond). 2007 4 17 10.1186/1743-7075-4-17 17683610 PMC1997123 · DOI
  47. [51]Pistoia W van Rietbergen B Lochmüller E-M Lill C Eckstein F Rüegsegger P Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images Bone 2002 30 842 848 10.1016/S8756-3282(02)00736-6 12052451 · DOI
  48. [52]Sale C Elliott-Sale KJ Nutrition and athlete bone health Sport Med. 2019 10.1007/s40279-019-01161-2 PMC6901417 31696454 · DOI
  49. [53]De Souza MJ West SL Jamal SA Hawker GA Gundberg CM Williams NI The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women Bone 2008 43 140 148 10.1016/j.bone.2008.03.013 18486582 · DOI
  50. [54]McGrath C Sankaran JS Misaghian-Xanthos N Sen B Xie Z Styner MA Exercise degrades bone in caloric restriction, despite suppression of marrow adipose tissue (MAT) J Bone Miner Res. 2020 35 106 115 10.1002/jbmr.3872 31509274 PMC6980282 · DOI
  51. [55]Frost HM Bone “mass” and the “mechanostat”: a proposal Anat Rec. 1987 219 1 9 10.1002/ar.1092190104 3688455 · DOI · Paper page
  52. [56]Burr DB Robling AG Turner CH Effects of biomechanical stress on bones in animals Bone 2002 30 781 786 10.1016/S8756-3282(02)00707-X 11996920 · DOI
  53. [57]Rubin CT Lanyon LE Regulation of bone formation by applied dynamic loads J Bone Joint Surg Am. 1984 66 397 402 10.2106/00004623-198466030-00012 6699056 · DOI
  54. [58]Vlachopoulos D Barker AR Ubago-Guisado E Williams CA Gracia-Marco L A 9-month jumping intervention to improve bone geometry in adolescent male athletes Med Sci Sport Exerc. 2018 50 2544 2554 10.1249/MSS.0000000000001719 30067592 · DOI
  55. [59]Vlachopoulos D Barker AR Ubago-Guisado E Williams CA Gracia-Marco L The effect of a high-impact jumping intervention on bone mass, bone stiffness and fitness parameters in adolescent athletes Arch Osteoporos. 2018 13 128 10.1007/s11657-018-0543-4 30446875 PMC6244891 · DOI
  56. [60]Hinton PS Nigh P Thyfault J Effectiveness of resistance training or jumping-exercise to increase bone mineral density in men with low bone mass: a 12-month randomized, clinical trial Bone 2015 79 203 212 10.1016/j.bone.2015.06.008 26092649 PMC4503233 · DOI
  57. [61]Fredericson M Chew K Ngo J Cleek T Kiratli J Cobb K Regional bone mineral density in male athletes: a comparison of soccer players, runners and controls Br J Sports Med. 2007 41 664 668 10.1136/bjsm.2006.030783 17473003 PMC2465163 · DOI
  58. [62]Niu K Ahola R Guo H Korpelainen R Uchimaru J Vainionpää A Effect of office-based brief high-impact exercise on bone mineral density in healthy premenopausal women: the Sendai Bone Health Concept Study J Bone Miner Metab. 2010 28 568 577 10.1007/s00774-010-0163-6 20349354 · DOI
  59. [63]Bailey CA Brooke-Wavell K Optimum frequency of exercise for bone health: randomised controlled trial of a high-impact unilateral intervention Bone 2010 46 1043 1049 10.1016/j.bone.2009.12.001 20004758 · DOI
  60. [64]Heinonen A Mäntynen J Kannus P Uusi-Rasi K Nikander R Kontulainen S Effects of high-impact training and detraining on femoral neck structure in premenopausal women: a hip structural analysis of an 18-month randomized controlled exercise intervention with 3.5-year follow-up Physiother Canada. 2012 64 98 105 10.3138/ptc.2010-37 PMC3280715 23277691 · DOI
  61. [65]Petit MA Mckay HA Mackelvie KJ Heinonen A Khan KM Beck TJ A randomized school-based jumping intervention confers site and maturity-specific benefits on bone structural properties in girls: a hip structural analysis study J Bone Miner Res. 2002 17 363 372 10.1359/jbmr.2002.17.3.363 11874228 · DOI
  62. [66]Tucker LA Strong JE LeCheminant JD Bailey BW Effect of two jumping programs on hip bone mineral density in premenopausal women: a randomized controlled trial Am J Health Promot. 2015 29 158 164 10.4278/ajhp.130430-QUAN-200 24460005 · DOI
  63. [67]Suominen TH Korhonen MT Alén M Heinonen A Mero A Törmäkangas T Effects of a 20-week high-intensity strength and sprint training program on tibial bone structure and strength in middle-aged and older male sprint athletes: a randomized controlled trial Osteoporos Int. 2017 28 2663 2673 10.1007/s00198-017-4107-z 28623425 · DOI
  64. [68]Lambert C Beck BR Harding AT Watson SL Weeks BK Regional changes in indices of bone strength of upper and lower limbs in response to high-intensity impact loading or high-intensity resistance training Bone 2020 132 115192 10.1016/j.bone.2019.115192 31846824 · DOI
  65. [69]Piasecki J McPhee JS Hannam K Deere KC Elhakeem A Piasecki M Hip and spine bone mineral density are greater in master sprinters, but not endurance runners compared with non-athletic controls Arch Osteoporos. 2018 13 72 10.1007/s11657-018-0486-9 29971503 PMC6028830 · DOI
  66. [70]Sundh D Nilsson M Zoulakis M Pasco C Yilmaz M Kazakia GJ High-impact mechanical loading increases bone material strength in postmenopausal women-a 3-month intervention study J Bone Miner Res. 2018 33 1242 1251 10.1002/jbmr.3431 29578618 PMC6055617 · DOI
  67. [71]Hartley C Folland JP Kerslake R Brooke-Wavell K High-impact exercise increased femoral neck bone density with no adverse effects on imaging markers of knee osteoarthritis in postmenopausal women J Bone Miner Res. 2020 35 53 63 10.1002/jbmr.3867 31498922 · DOI
  68. [72]De Souza MJ Williams NI Beyond hypoestrogenism in amenorrheic athletes: energy deficiency as a contributing factor for bone loss Curr Sports Med Rep. 2005 4 38 44 10.1097/01.CSMR.0000306070.67390.cb 15659278 · DOI
  69. [73]Villareal DT Bone mineral density response to caloric restriction–induced weight loss or exercise-induced weight loss Arch Intern Med. 2006 166 2502 10.1001/archinte.166.22.2502 17159017 · DOI · Paper page
  70. [74]Seeman E Bone quality: the material and structural basis of bone strength J Bone Miner Metab. 2008 26 1 8 10.1007/s00774-007-0793-5 18095057 · DOI
  71. [75]Judex S Zernicke RF High-impact exercise and growing bone: relation between high strain rates and enhanced bone formation J Appl Physiol. 2000 88 2183 2191 10.1152/jappl.2000.88.6.2183 10846034 · DOI
  72. [76]Schipilow JD Macdonald HM Liphardt AM Kan M Boyd SK Bone micro-architecture, estimated bone strength, and the muscle-bone interaction in elite athletes: an HR-pQCT study Bone 2013 56 281 289 10.1016/j.bone.2013.06.014 23800515 · DOI
  73. [77]Vasikaran S Eastell R Bruyère O Foldes AJ Garnero P Griesmacher A Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards Osteoporos Int. 2011 22 391 420 10.1007/s00198-010-1501-1 21184054 · DOI · Paper page
  74. [78]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 83 434 440 10.1007/s004210000293 11138586 · DOI
  75. [79]Papageorgiou M Martin D Colgan H Cooper S Greeves JP Tang JCY Bone metabolic responses to low energy availability achieved by diet or exercise in active eumenorrheic women Bone 2018 114 181 188 10.1016/j.bone.2018.06.016 29933113 · DOI
  76. [80]Ihle R Loucks AB Dose–response relationships between energy availability and bone turnover in young exercising women J Bone Miner Res. 2004 19 1231 1240 10.1359/JBMR.040410 15231009 · DOI · Paper page
  77. [81]Hammond KM Sale C Fraser W Tang J Shepherd SO Strauss JA Post-exercise carbohydrate and energy availability induce independent effects on skeletal muscle cell signalling and bone turnover: implications for training adaptation J Physiol. 2019 597 4779 4796 10.1113/JP278209 31364768 · DOI · Paper page
  78. [82]Bennell KL Malcolm SA Wark JD Brukner PD Models for the pathogenesis of stress fractures in athletes Br J Sports Med. 1996 30 200 204 10.1136/bjsm.30.3.200 8889110 PMC1332329 · DOI
  79. [83]Schilcher J Bernhardsson M Aspenberg P Chronic anterior tibial stress fractures in athletes: no crack but intense remodeling Scand J Med Sci Sports. 2019 29 1521 1528 10.1111/sms.13466 31102562 · DOI
  80. [84]Bennell KL Malcolm SA Brukner PD Green RM Hopper JL Wark JD A 12-month prospective study of the relationship between stress fractures and bone turnover in athletes Calcif Tissue Int. 1998 63 80 85 10.1007/s002239900493 9632851 · DOI
  81. [85]Yanovich R Evans RK Friedman E Moran DS Bone turnover markers do not predict stress fracture in elite combat recruits Clin Orthop Relat Res. 2013 471 1365 1372 10.1007/s11999-012-2727-3 23239391 PMC3586020 · DOI
  82. [86]Hlaing TT Compston JE Biochemical markers of bone turnover—uses and limitations Ann Clin Biochem. 2014 51 189 202 10.1177/0004563213515190 24399365 · DOI
  83. [87]Dolan E Varley I Ackerman KE Pereira RMR Elliott-Sale KJ Sale C The bone metabolic response to exercise and nutrition Exerc Sport Sci Rev. 2020 48 49 58 10.1249/JES.0000000000000215 31913188 · DOI
  84. [88]Kishimoto K Lynch RP Reiger J Yingling VR Short-term jump activity on bone metabolism in female college-aged nonathletes J Sports Sci Med. 2012 11 31 38 24149120 PMC3737855
  85. [89]Martin SPK Bachrach LK Golden NH Controlled pilot study of high-impact low-frequency exercise on bone loss and vital-sign stabilization in adolescents with eating disorders J Adolesc Health 2017 60 33 37 10.1016/j.jadohealth.2016.08.028 27836532 · DOI

Cited by

Sorted by citations

Authors
Hutson, M. J., O’Donnell, E., Brooke-Wavell, K., Sale, C., & Blagrove, R. C.
Affiliations
  • Loughborough University (GB)
  • Nottingham Trent University (GB)
Corresponding author
Hutson, Mark J.
ORCID
Venue
Sports Medicine
Publisher
Springer Science and Business Media LLC
Published
2020-12-21
Volume
51
Issue
3
Pages
391-403
ISSN
  • 0112-1642 (ISSN-L)
  • 1179-2035
DOI
10.1007/s40279-020-01396-4
PMC
PMC7900047
OpenAlex
W3114455018
Cited by
64
References
4
Citations by year
2026: 9 · 2025: 12 · 2024: 18 · 2023: 13 · 2022: 8 · 2021: 4
FWCI
1.23
Type
journal article
Language
en
Open access
Licence
Locations
  • Sports Medicine (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Nottingham Trent University's Institutional Repository (Nottingham Trent Repository) (acceptedVersion)
  • Ulster University Research Portal (Ulster University) (submittedVersion, cc-by)
  • Figshare (submittedVersion, cc-by)
Funders
Loughborough University
Topics
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
  • Physical Sciences › Engineering › Biomedical Engineering › Lower Extremity Biomechanics and Pathologies
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
Keywords
low energy availability, bone health, endurance athletes, high-impact exercise, bone stress injuries, female athlete triad, relative energy deficiency in sport, bone remodeling, bone turnover markers, caloric restriction, countermeasures
MeSH terms
Energy Intake, Energy Metabolism, Female, Humans, Nutritional Status, Bone Density, Female Athlete Triad Syndrome, Athletes

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review