Intracortical remodelling increases in highly loaded bone after exercise cessation.
bone
exercise
resorption
rest
Journal
Journal of anatomy
ISSN: 1469-7580
Titre abrégé: J Anat
Pays: England
ID NLM: 0137162
Informations de publication
Date de publication:
12 Nov 2023
12 Nov 2023
Historique:
revised:
18
10
2023
received:
16
06
2023
accepted:
18
10
2023
medline:
13
11
2023
pubmed:
13
11
2023
entrez:
12
11
2023
Statut:
aheadofprint
Résumé
Resorption within cortices of long bones removes excess mass and damaged tissue and increases during periods of reduced mechanical loading. Returning to high-intensity exercise may place bones at risk of failure due to increased porosity caused by bone resorption. We used point-projection X-ray microscopy images of bone slices from highly loaded (metacarpal, tibia) and minimally loaded (rib) bones from 12 racehorses, 6 that died during a period of high-intensity exercise and 6 that had a period of intense exercise followed by at least 35 days of rest prior to death, and measured intracortical canal cross-sectional area (Ca.Ar) and number (N.Ca) to infer remodelling activity across sites and exercise groups. Large canals that are the consequence of bone resorption (Ca.Ar >0.04 mm
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Arthritis Research UK
Pays : United Kingdom
Informations de copyright
© 2023 The Authors. Journal of Anatomy published by John Wiley & Sons Ltd on behalf of Anatomical Society.
Références
Allen, M.R., Iwata, K., Phipps, R. & Burr, D.B. (2006) Alterations in canine vertebral bone turnover, microdamage accumulation, and biomechanical properties following 1-year treatment with clinical treatment doses of risedronate or alendronate. Bone, 39, 872-879. Available from: https://doi.org/10.1016/j.bone.2006.04.028
Andreasen, C.M., Bakalova, L.P., Brüel, A., Hauge, E.M., Kiil, B.J., Delaisse, J.-M. et al. (2020) The generation of enlarged eroded pores upon existing intracortical canals is a major contributor to endocortical trabecularization. Bone, 130, 115127. Available from: https://doi.org/10.1016/j.bone.2019.115127
Andreasen, C.M., Delaisse, J.-M., van der Eerden, B.C., van Leeuwen, J.P., Ding, M. & Andersen, T.L. (2018) Understanding age-induced cortical porosity in women: the accumulation and coalescence of eroded cavities upon existing intracortical canals is the Main contributor. Journal of Bone and Mineral Research, 33, 606-620. Available from: https://doi.org/10.1002/jbmr.3354
Armstrong, D.W., Rue, J.-P.H., Wilckens, J.H. & Frassica, F.J. (2004) Stress fracture injury in young military men and women. Bone, 35, 806-816. Available from: https://doi.org/10.1016/j.bone.2004.05.014
Bakalova, L.P., Andreasen, C.M., Thomsen, J.S., Brüel, A., Hauge, E.-M., Kiil, B.J. et al. (2018) Intracortical bone mechanics are related to pore morphology and remodeling in human bone. Journal of Bone and Mineral Research, 33, 2177-2185. Available from: https://doi.org/10.1002/jbmr.3561
Behrens, J.C., Walker, P.S. & Shoji, H. (1974) Variations in strength and structure of cancellous bone at the knee. Journal of Biomechanics, 7, 201-207. Available from: https://doi.org/10.1016/0021-9290(74)90010-4
Bell, K.L., Loveridge, N., Power, J., Garrahan, N., Meggitt, B.F. & Reeve, J. (1999) Regional differences in cortical porosity in the fractured femoral neck. Bone, 24, 57-64. Available from: https://doi.org/10.1016/S8756-3282(98)00143-4
Boyde, A. (2003) The real response of bone to exercise. Journal of Anatomy, 203, 173-189. Available from: https://doi.org/10.1046/j.1469-7580.2003.00213.x
Boyde, A. & Firth, E.C. (2005) Musculoskeletal responses of 2-year-old thoroughbred horses to early training. 8. Quantitative back-scattered electron scanning electron microscopy and confocal fluorescence microscopy of the epiphysis of the third metacarpal bone. New Zealand Veterinary Journal, 53, 123-132. Available from: https://doi.org/10.1080/00480169.2005.36489
Burr, D.B., Schaffler, M.B., Yang, K.H., Lukoschek, M., Sivaneri, N., Blaha, J.D. et al. (1989a) Skeletal change in response to altered strain environments: is woven bone a response to elevated strain? Bone, 10, 223-233. Available from: https://doi.org/10.1016/8756-3282(89)90057-4
Burr, D.B., Schaffler, M.B., Yang, K.H., Wu, D.D., Lukoschek, M., Kandzari, D. et al. (1989b) The effects of altered strain environments on bone tissue kinetics. Bone, 10, 215-221. Available from: https://doi.org/10.1016/8756-3282(89)90056-2
Busse, B., Hahn, M., Schinke, T., Püschel, K., Duda, G.N. & Amling, M. (2010) Reorganization of the femoral cortex due to age-, sex-, and endoprosthetic-related effects emphasized by osteonal dimensions and remodeling. Journal of Biomedical Materials Research Part A, 92A, 1440-1451. Available from: https://doi.org/10.1002/jbm.a.32432
Cappariello, A., Maurizi, A., Veeriah, V. & Teti, A. (2014) The great beauty of the osteoclast. Archives of Biochemistry and Biophysics, 558, 70-78. Available from: https://doi.org/10.1016/j.abb.2014.06.017
Carrier, T.K., Estberg, L., Stover, S.M., Gardner, I.A., Johnson, B.J., Read, D.H. et al. (1998) Association between long periods without high-speed workouts and risk of complete humeral or pelvic fracture in thoroughbred racehorses: 54 cases (1991-1994). Journal of the American Veterinary Medical Association, 212, 1582-1587.
Chalupa, R.L., Aberle, C. & Johnson, A.E. (2016) Observed rates of lower extremity stress fractures after implementation of the Army physical readiness training program at JBSA fort Sam Houston. U.S. Army Medical Department Journal, 6-9.
Collins, C.J., Kozyrev, M., Frank, M., Andriotis, O.G., Byrne, R.A., Kiener, H.P. et al. (2020) The impact of age, mineralization, and collagen orientation on the mechanics of individual osteons from human femurs. Materialia, 9, 100573. Available from: https://doi.org/10.1016/j.mtla.2019.100573
Cooper, D.M.L., Kawalilak, C.E., Harrison, K., Johnston, B.D. & Johnston, J.D. (2016) Cortical bone porosity: what is it, why is it important, and how can we detect it? Current Osteoporosis Reports, 14, 187-198. Available from: https://doi.org/10.1007/s11914-016-0319-y
Davies, H.M.S. (2005) The timing and distribution of strains around the surface of the midshaft of the third metacarpal bone during treadmill exercise in one thoroughbred racehorse. Australian Veterinary Journal, 83, 157-162. Available from: https://doi.org/10.1111/j.1751-0813.2005.tb11628.x
Davies, H.M.S. (2006) Estimating peak strains associated with fast exercise in thoroughbred racehorses. Equine Veterinary Journal, 38, 383-386. Available from: https://doi.org/10.1111/j.2042-3306.2006.tb05573.x
Dempster, D.W., Compston, J.E., Drezner, M.K., Glorieux, F.H., Kanis, J.A., Malluche, H. et al. (2013) Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR histomorphometry nomenclature committee. Journal of Bone and Mineral Research, 28, 2-17. Available from: https://doi.org/10.1002/jbmr.1805
Dittmer, K.E. & Firth, E.C. (2017) Mechanisms of bone response to injury. Journal of Veterinary Diagnostic Investigation, 29, 385-395. Available from: https://doi.org/10.1177/1040638716679861
Doube, M. (2022) Closing cones create conical lamellae in secondary osteonal bone. Royal Society Open Science, 9, 220712. Available from: https://doi.org/10.1098/rsos.220712
Felder, A.A., Phillips, C., Cornish, H., Cooke, M., Hutchinson, J.R. & Doube, M. (2017) Secondary osteons scale allometrically in mammalian humerus and femur. Royal Society Open Science, 4, 170431. Available from: https://doi.org/10.1098/rsos.170431
Firth, E.C., Rogers, C.W., Doube, M. & Jopson, N.B. (2005) Musculoskeletal responses of 2-year-old thoroughbred horses to early training. 6. Bone parameters in the third metacarpal and third metatarsal bones. New Zealand Veterinary Journal, 53, 101-112. Available from: https://doi.org/10.1080/00480169.2005.36487
Frank, J.D., Ryan, M., Kalscheur, V.L., Ruaux-Mason, C.P., Hozak, R.R. & Muir, P. (2002) Aging and accumulation of microdamage in canine bone. Bone, 30, 201-206. Available from: https://doi.org/10.1016/S8756-3282(01)00623-8
Frost, H.M. (1969) Tetracycline-based histological analysis of bone remodeling. Calcified Tissue Research, 3, 211-237. Available from: https://doi.org/10.1007/bf02058664
Frost, H.M. (2003) Bone's mechanostat: a 2003 update. Anatomical Record, 275A, 1081-1101. Available from: https://doi.org/10.1002/ar.a.10119
Gibson, V.A., Stover, S.M., Gibeling, J.C., Hazelwood, S.J. & Martin, R.B. (2006) Osteonal effects on elastic modulus and fatigue life in equine bone. Journal of Biomechanics, 39, 217-225. Available from: https://doi.org/10.1016/j.jbiomech.2004.12.002
Goldman, H.M., Bromage, T.G., Thomas, C.D.L. & Clement, J.G. (2003) Preferred collagen fiber orientation in the human mid-shaft femur. The Anatomical Record, 272A, 434-445. Available from: https://doi.org/10.1002/ar.a.10055
Goldman, H.M., Hampson, N.A., Guth, J.J., Lin, D. & Jepsen, K.J. (2014) Intracortical remodeling parameters are associated with measures of bone robustness. The Anatomical Record, 297, 1817-1828. Available from: https://doi.org/10.1002/ar.22962
Herbst, E.C., Doube, M., Smithson, T.R., Clack, J.A. & Hutchinson, J.R. (2019) Bony lesions in early tetrapods and the evolution of mineralized tissue repair. Paleobiology, 45, 676-697. Available from: https://doi.org/10.1017/pab.2019.31
Hernandez, C.J. & Keaveny, T.M. (2006) A biomechanical perspective on bone quality. Bone, 39, 1173-1181. Available from: https://doi.org/10.1016/j.bone.2006.06.001
Holmes, J.M., Mirams, M., Mackie, E.J. & Whitton, R.C. (2014) Thoroughbred horses in race training have lower levels of subchondral bone remodelling in highly loaded regions of the distal metacarpus compared to horses resting from training. The Veterinary Journal, 202, 443-447. Available from: https://doi.org/10.1016/j.tvjl.2014.09.010
Hughes, J.M., Castellani, C.M., Popp, K.L., Guerriere, K.I., Matheny, R.W., Nindl, B.C. et al. (2020) The central role of osteocytes in the four adaptive pathways of Bone's Mechanostat. Exercise and Sport Sciences Reviews, 48, 140-148. Available from: https://doi.org/10.1249/JES.0000000000000225
Hughes, J.M., Smith, M.A., Henning, P.C., Scofield, D.E., Spiering, B.A., Staab, J.S. et al. (2014) Bone formation is suppressed with multi-stressor military training. European Journal of Applied Physiology, 114, 2251-2259. Available from: https://doi.org/10.1007/s00421-014-2950-6
Ireland, A., Maden-Wilkinson, T., Ganse, B., Degens, H. & Rittweger, J. (2014) Effects of age and starting age upon side asymmetry in the arms of veteran tennis players: a cross-sectional study. Osteoporosis International, 25, 1389-1400. Available from: https://doi.org/10.1007/s00198-014-2617-5
Jacobs, J.M., Cameron, K.L. & Bojescul, J.A. (2014) Lower extremity stress fractures in the military. Clinics in Sports Medicine, 33, 591-613. Available from: https://doi.org/10.1016/j.csm.2014.06.002
Jaworski, Z.F. & Lok, E. (1972) The rate of osteoclastic bone erosion in Haversian remodeling sites of adult dog's rib. Calcified Tissue Research, 10, 103-112. Available from: https://doi.org/10.1007/BF02012540
Jaworski, Z.F., Meunier, P. & Frost, H.M. (1972) Observations on two types of resorption cavities in human lamellar cortical bone. Clinical Orthopaedics and Related Research, 83, 279-285. Available from: https://doi.org/10.1097/00003086-197203000-00048
Komori, T. (2013) Functions of the osteocyte network in the regulation of bone mass. Cell and Tissue Research, 352, 191-198. Available from: https://doi.org/10.1007/s00441-012-1546-x
Lassen, N.E., Andersen, T.L., Pløen, G.G., Søe, K., Hauge, E.M., Harving, S. et al. (2017) Coupling of bone resorption and formation in real time: new knowledge gained from human Haversian BMUs. Journal of Bone and Mineral Research, 32, 1395-1405. Available from: https://doi.org/10.1002/jbmr.3091
Li, J., Mashiba, T. & Burr, D.B. (2001) Bisphosphonate treatment suppresses not only stochastic remodeling but also the targeted repair of microdamage. Calcified Tissue International, 69, 281-286. Available from: https://doi.org/10.1007/s002230010036
Martin, R.B. (2007) Targeted bone remodeling involves BMU steering as well as activation. Bone, 40, 1574-1580. Available from: https://doi.org/10.1016/j.bone.2007.02.023
Martin, R.B., Stover, S.M., Gibson, V.A., Gibeling, J.C. & Griffin, L.V. (1996) In vitro fatigue behavior of the equine third metacarpus: remodeling and microcrack damage analysis. Journal of Orthopaedic Research: Official Publication of the Orthopaedic Research Society, 14, 794-801. Available from: https://doi.org/10.1002/jor.1100140517
Mashiba, T., Hirano, T., Turner, C.H., Forwood, M.R., Johnston, C.C. & Burr, D.B. (2000) Suppressed bone turnover by bisphosphonates increases microdamage accumulation and reduces some biomechanical properties in dog rib. Journal of Bone and Mineral Research, 15, 613-620. Available from: https://doi.org/10.1359/jbmr.2000.15.4.613
McCalden, R.W., McGeough, J.A., Barker, M.B. & Court-Brown, C.M. (1993) Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure. The Journal of Bone and Joint Surgery. American, 75, 1193-1205. Available from: https://doi.org/10.2106/00004623-199308000-00009
McCalden, R.W., McGeough, J.A. & Court-Brown, C.M. (1997) Age-related changes in the compressive strength of cancellous bone. The relative importance of changes in density and trabecular architecture. The Journal of Bone and Joint Surgery American, 79, 421-427. Available from: https://doi.org/10.2106/00004623-199703000-00016
McCarthy, R.N. & Jeffcott, L.B. (1988) Monitoring the effects of treadmill exercise on bone by non-invasive means during a progressive fitness programme. Equine Veterinary Journal, 20, 88-92. Available from: https://doi.org/10.1111/j.2042-3306.1988.tb04653.x
McFarlin, S.C., Terranova, C.J., Zihlman, A.L., Enlow, D.H. & Bromage, T.G. (2008) Regional variability in secondary remodeling within long bone cortices of catarrhine primates: the influence of bone growth history. Journal of Anatomy, 213, 308-324. Available from: https://doi.org/10.1111/j.1469-7580.2008.00947.x
Merritt, J.S. & Davies, H.M.S. (2010) Metacarpal geometry changes during thoroughbred race training are compatible with sagittal-plane cantilever bending: cantilever bending of the equine metacarpus. Equine Veterinary Journal, 42, 407-411. Available from: https://doi.org/10.1111/j.2042-3306.2010.00209.x
Milgrom, C. & Finestone, A.S. (2017) The effect of stress fracture interventions in a single elite infantry training unit (1983-2015). Bone, 103, 125-130. Available from: https://doi.org/10.1016/j.bone.2017.06.026
Mori, S. & Burr, D.B. (1993) Increased intracortical remodeling following fatigue damage. Bone, 14, 103-109. Available from: https://doi.org/10.1016/8756-3282(93)90235-3
Nalla, R.K., Stölken, J.S., Kinney, J.H. & Ritchie, R.O. (2005) Fracture in human cortical bone: local fracture criteria and toughening mechanisms. Journal of Biomechanics, 38, 1517-1525. Available from: https://doi.org/10.1016/j.jbiomech.2004.07.010
Norman, T.L., Yeni, Y.N., Brown, C.U. & Wang, Z. (1998) Influence of microdamage on fracture toughness of the human femur and tibia. Bone, 23, 303-306. Available from: https://doi.org/10.1016/s8756-3282(98)00103-3
Nunamaker, D.M., Butterweck, D.M. & Provost, M.T. (1989) Some geometric properties of the third metacarpal bone: a comparison between the thoroughbred and standardbred racehorse. Journal of Biomechanics, 22, 129-134. Available from: https://doi.org/10.1016/0021-9290(89)90035-3
Nunamaker, D.M., Butterweck, D.M. & Provost, M.T. (1990) Fatigue fractures in thoroughbred racehorses: relationships with age, peak bone strain, and training. Journal of Orthopaedic Research, 8, 604-’611.
O'Sullivan, C.B. & Lumsden, J.M. (2003) Stress fractures of the tibia and humerus in thoroughbred racehorses: 99 cases (1992-2000). Journal of the American Veterinary Medical Association, 222, 491-498 12597423.
Parfitt, A.M. (2002) Targeted and nontargeted bone remodeling: relationship to basic multicellular unit origination and progression. Bone, 30, 5-7. Available from: https://doi.org/10.1016/S8756-3282(01)00642-1
Piotrowski, G., Sullivan, M. & Colahan, P.T. (1983) Geometric properties of equine metacarpi. Journal of Biomechanics, 16, 129-139. Available from: https://doi.org/10.1016/0021-9290(83)90036-2
Plotkin, L.I. (2014) Apoptotic osteocytes and the control of targeted bone resorption. Current Osteoporosis Reports, 12, 121-126. Available from: https://doi.org/10.1007/s11914-014-0194-3
Riggs, C.M., Lanyon, L.E. & Boyde, A. (1993a) Functional associations between collagen fibre orientation and locomotor strain direction in cortical bone of the equine radius. Anatomy and Embryology, 187, 231-238. Available from: https://doi.org/10.1007/BF00195760
Riggs, C.M. & Pilsworth, R. (2014) Repetitive strain injuries of the skeleton in high performance equine athletes. In: Hinchcliff, K.W., Kaneps, A.J. & Geor, R.J. (Eds.) Equine sports medicine and surgery, 2nd edition. Edinburgh: W.B. Saunders, pp. 457-471. Available from: https://doi.org/10.1016/B978-0-7020-4771-8.00022-3
Riggs, C.M., Vaughan, L.C., Evans, G.P., Lanyon, L.E. & Boyde, A. (1993b) Mechanical implications of collagen fibre orientation in cortical bone of the equine radius. Anatomy and Embryology, 187, 239-248. Available from: https://doi.org/10.1007/BF00195761
Riggs, C.M., Whitehouse, G.H. & Boyde, A. (1999) Pathology of the distal condyles of the third metacarpal and third metatarsal bones of the horse. Equine Veterinary Journal, 31, 140-148. Available from: https://doi.org/10.1111/j.2042-3306.1999.tb03807.x
Rueden, C.T., Schindelin, J., Hiner, M.C., DeZonia, B.E., Walter, A.E., Arena, E.T. et al. (2017) ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics, 18, 529. Available from: https://doi.org/10.1186/s12859-017-1934-z
Samol, M.A., Uzal, F.A., Hill, A.E., Arthur, R.M. & Stover, S.M. (2021) Characteristics of complete tibial fractures in California racehorses. Equine Veterinary Journal, 53, 911-922. Available from: https://doi.org/10.1111/evj.13375
Schaffler, M.B. & Burr, D.B. (1988) Stiffness of compact bone: effects of porosity and density. Journal of Biomechanics, 21, 13-16. Available from: https://doi.org/10.1016/0021-9290(88)90186-8
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T. et al. (2012) Fiji: an open-source platform for biological-image analysis. Nature Methods, 9, 676-682. Available from: https://doi.org/10.1038/nmeth.2019
Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675. Available from: https://doi.org/10.1038/nmeth.2089
SciPy 1.0 Contributors, Virtanen, P., Gommers, R., Oliphant, T.E., Haberland, M., Reddy, T. et al. (2020) SciPy 1.0: fundamental algorithms for scientific computing in Python. Nature Methods, 17, 261-272. Available from: https://doi.org/10.1038/s41592-019-0686-2
Seref-Ferlengez, Z., Basta-Pljakic, J., Kennedy, O.D., Philemon, C.J. & Schaffler, M.B. (2014) Structural and mechanical repair of diffuse damage in cortical bone in vivo. Journal of Bone and Mineral Research, 29, 2537-2544. Available from: https://doi.org/10.1002/jbmr.2309
Seref-Ferlengez, Z., Kennedy, O.D. & Schaffler, M.B. (2015) Bone microdamage, remodeling and bone fragility: how much damage is too much damage? BoneKEy Reports, 4, 644. Available from: https://doi.org/10.1038/bonekey.2015.11
Shahar, R., Lukas, C., Papo, S., Dunlop, J.W.C. & Weinkamer, R. (2011) Characterization of the spatial arrangement of secondary osteons in the diaphysis of equine and canine long bones. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, 294, 1093-1102. Available from: https://doi.org/10.1002/ar.21405
Shan, R., Johnston, A.S., Rosanowski, S.M., O'Shea, J. & Riggs, C.M. (2022) Stress fracture of the palmar, distal cortex of the third metacarpal bone: a diagnostic challenge with a good prognosis. Equine Veterinary Journal, 54, 74-81. Available from: https://doi.org/10.1111/evj.13426
Shaw, C.N. & Ryan, T.M. (2012) Does skeletal anatomy reflect adaptation to locomotor patterns? Cortical and trabecular architecture in human and nonhuman anthropoids. American Journal of Physical Anthropology, 147, 187-200. Available from: https://doi.org/10.1002/ajpa.21635
Shaw, C.N. & Stock, J.T. (2009) Intensity, repetitiveness, and directionality of habitual adolescent mobility patterns influence the tibial diaphysis morphology of athletes. American Journal of Physical Anthropology, 140, 149-159. Available from: https://doi.org/10.1002/ajpa.21064
Stover, S.M., Pool, R.R., Martin, R.B. & Morgan, J.P. (1992) Histological features of the dorsal cortex of the third metacarpal bone mid-diaphysis during postnatal growth in thoroughbred horses. Journal of Anatomy, 181(Pt 3), 455-469.
The Hong Kong Jockey Club. (2021) Racing Information Database. The Hong Kong Jockey Club. https://racing.hkjc.com/racing/information/english/Horse/SelectHorse.aspx
Turnbull, T.L., Baumann, A.P. & Roeder, R.K. (2014) Fatigue microcracks that initiate fracture are located near elevated intracortical porosity but not elevated mineralization. Journal of Biomechanics, 47, 3135-3142. Available from: https://doi.org/10.1016/j.jbiomech.2014.06.022
Ural, A. & Vashishth, D. (2007) Effects of intracortical porosity on fracture toughness in aging human bone: a microCT-based cohesive finite element study. Journal of Biomechanical Engineering, 129, 625-631. Available from: https://doi.org/10.1115/1.2768377
Vallance, S.A., Entwistle, R.C., Hitchens, P.L., Gardner, I.A. & Stover, S.M. (2013) Case-control study of high-speed exercise history of thoroughbred and quarter horse racehorses that died related to a complete scapular fracture: exercise history of racehorses with a catastrophic scapular fracture. Equine Veterinary Journal, 45, 284-292. Available from: https://doi.org/10.1111/j.2042-3306.2012.00644.x
Wachter, N.J., Krischak, G.D., Mentzel, M., Sarkar, M.R., Ebinger, T., Kinzl, L. et al. (2002) Correlation of bone mineral density with strength and microstructural parameters of cortical bone in vitro. Bone, 31, 90-95. Available from: https://doi.org/10.1016/S8756-3282(02)00779-2
Whitton, R.C., Mirams, M., Mackie, E.J., Anderson, G.A. & Seeman, E. (2013) Exercise-induced inhibition of remodelling is focally offset with fatigue fracture in racehorses. Osteoporosis International, 24, 2043-2048. Available from: https://doi.org/10.1007/s00198-013-2291-z
Whitton, R.C., Trope, G.D., Ghasem-Zadeh, A., Anderson, G.A., Parkin, T.D.H., Mackie, E.J. et al. (2010) Third metacarpal condylar fatigue fractures in equine athletes occur within previously modelled subchondral bone. Bone, 47, 826-831. Available from: https://doi.org/10.1016/j.bone.2010.07.019
Wik, E.H., Lolli, L., Chamari, K., Materne, O., Salvo, V.D., Gregson, W. et al. (2020) Injury patterns differ with age in male youth football: a four-season prospective study of 1111 time-loss injuries in an elite national academy. British Journal of Sports Medicine, 55, 794-800. Available from: https://doi.org/10.1136/bjsports-2020-103430
Yeni, Y.N., Brown, C.U., Wang, Z. & Norman, T.L. (1997) The influence of bone morphology on fracture toughness of the human femur and tibia. Bone, 21, 453-459. Available from: https://doi.org/10.1016/S8756-3282(97)00173-7
Zack, G.W., Rogers, W.E. & Latt, S.A. (1977) Automatic measurement of sister chromatid exchange frequency. Journal of Histochemistry & Cytochemistry, 25, 741-753. Available from: https://doi.org/10.1177/25.7.70454