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Journal of anatomy2011; 219(6); 722-733; doi: 10.1111/j.1469-7580.2011.01428.x

Relationships between in vivo microdamage and the remarkable regional material and strain heterogeneity of cortical bone of adult deer, elk, sheep and horse calcanei.

Abstract: Natural loading of the calcanei of deer, elk, sheep and horses produces marked regional differences in prevalent/predominant strain modes: compression in the dorsal cortex, shear in medial-lateral cortices, and tension/shear in the plantar cortex. This consistent non-uniform strain distribution is useful for investigating mechanisms that mediate the development of the remarkable regional material variations of these bones (e.g. collagen orientation, mineralization, remodeling rates and secondary osteon morphotypes, size and population density). Regional differences in strain-mode-specific microdamage prevalence and/or morphology might evoke and sustain the remodeling that produces this material heterogeneity in accordance with local strain characteristics. Adult calcanei from 11 animals of each species (deer, elk, sheep and horses) were transversely sectioned and examined using light and confocal microscopy. With light microscopy, 20 linear microcracks were identified (deer: 10; elk: six; horse: four; sheep: none), and with confocal microscopy substantially more microdamage with typically non-linear morphology was identified (deer: 45; elk: 24; horse: 15; sheep: none). No clear regional patterns of strain-mode-specific microdamage were found in the three species with microdamage. In these species, the highest overall concentrations occurred in the plantar cortex. This might reflect increased susceptibility of microdamage in habitual tension/shear. Absence of detectable microdamage in sheep calcanei may represent the (presumably) relatively greater physical activity of deer, elk and horses. Absence of differences in microdamage prevalence/morphology between dorsal, medial and lateral cortices of these bones, and the general absence of spatial patterns of strain-mode-specific microdamage, might reflect the prior emergence of non-uniform osteon-mediated adaptations that reduce deleterious concentrations of microdamage by the adult stage of bone development.
Publication Date: 2011-09-26 PubMed ID: 21951210PubMed Central: PMC3237880DOI: 10.1111/j.1469-7580.2011.01428.xGoogle Scholar: Lookup
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Summary

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This research investigates the relationship between microscopic bone damage and the different material and strain properties of calcaneal bones in deer, elk, sheep and horses. The study suggests these properties are highly regionalized due to differing mechanical strains and potentially contributes to the local remodeling and heterogeneity of the bone.

Objective and Methodology

  • The objective of this research was to understand how regionalized microscopic bone damage (microdamage) and strain heterogeneity contribute to the development and variations of the calcaneal bone – the prominent bone at the back of the foot. The study focused on deer, elk, sheep, and horses.
  • The researchers hypothesized that the regional differences in mechanical strain modes might cause strain-specific microdamage, which in turn drives regional bone remodeling. This remodeling process maintains bone health and adapts the bone strength according to the patterns of usage.
  • To investigate, researchers collected calcanei from 11 adult animals of each species and prepared them for light and confocal microscopy. This method allows for the visualization of different types of bone damage on a microscopic level.

Findings

  • The results from light microscopy showed the occurrence of linear microcracks with highest numbers in deer followed by elk, horses, and none in sheep.
  • Confocal microscopy, which is a more powerful and precise imaging tool, revealed an even greater amount of microdamage, but with non-linear morphology. Again, deer showed the highest numbers, followed by elk, horses, and none in sheep.
  • No clear pattern of region-specific microdamage was identified in relation to strain modes for the species showing microdamage.
  • The plantar cortex had the highest concentration of microdamage, possibly indicating increased damage susceptibility under habitual tension or shear loads. The absence of microdamage in sheep is potentially due to them being less physically active compared to rest of the studied species.

Implications

  • One possible interpretation for the absence of clear correlation between strain modes and microdamage patterns could be due to existing adaptive responses emerging prior to adulthood. These adaptive responses possibly reduce the harmful concentrations of microdamage. This could include the formation of secondary osteons, which help to repair and reinforce the bone structure.
  • The findings suggest that understanding regional microdamage, as well as local strain patterns, could be beneficial in comprehending the role of microscale adaptations in maintaining overall bone health and integrity.

Cite This Article

APA
Skedros JG, Sybrowsky CL, Anderson WE, Chow F. (2011). Relationships between in vivo microdamage and the remarkable regional material and strain heterogeneity of cortical bone of adult deer, elk, sheep and horse calcanei. J Anat, 219(6), 722-733. https://doi.org/10.1111/j.1469-7580.2011.01428.x

Publication

ISSN: 1469-7580
NlmUniqueID: 0137162
Country: England
Language: English
Volume: 219
Issue: 6
Pages: 722-733

Researcher Affiliations

Skedros, John G
  • Department of Orthopaedic Surgery, University of Utah and the Utah Bone and Joint Center, Salt Lake City, UT, USA. jskedros@utahboneandjoint.com
Sybrowsky, Christian L
    Anderson, Wm Erick
      Chow, Frank

        MeSH Terms

        • Analysis of Variance
        • Animals
        • Biomechanical Phenomena
        • Bone Remodeling / physiology
        • Calcaneus / anatomy & histology
        • Calcaneus / physiology
        • Deer / anatomy & histology
        • Deer / physiology
        • Horses / anatomy & histology
        • Horses / physiology
        • Sheep / anatomy & histology
        • Sheep / physiology
        • Stress, Mechanical

        References

        This article includes 66 references
        1. Badoux DM. Some biomechanical aspects of the structure of the equine tarsus.. Anat Anz 1987;164(1):53-61.
          pubmed: 3662028
        2. Banks WJ Jr, Epling GP, Kainer RA, Davis RW. Antler growth and osteoporosis. I. Morphological and morphometric changes in the costal compacta during the antler growth cycle.. Anat Rec 1968 Dec;162(4):387-98.
          pubmed: 5701619doi: 10.1002/ar.1091620401google scholar: lookup
        3. Bentolila V, Boyce TM, Fyhrie DP, Drumb R, Skerry TM, Schaffler MB. Intracortical remodeling in adult rat long bones after fatigue loading.. Bone 1998 Sep;23(3):275-81.
          pubmed: 9737350doi: 10.1016/s8756-3282(98)00104-5google scholar: lookup
        4. Biewener AA, Bertram JEA. Mechanical loading and bone growth in vivo. In: Hall BK, editor. Bone, Volume 7, Bone Growth-B. Boca Raton, FL: CRC Press; 1993. pp. 1–36.
        5. Boyce TM, Fyhrie DP, Glotkowski MC, Radin EL, Schaffler MB. Damage type and strain mode associations in human compact bone bending fatigue.. J Orthop Res 1998 May;16(3):322-9.
          pubmed: 9671927doi: 10.1002/jor.1100160308google scholar: lookup
        6. Burr DB. Targeted and nontargeted remodeling.. Bone 2002 Jan;30(1):2-4.
          pubmed: 11792556doi: 10.1016/s8756-3282(01)00619-6google scholar: lookup
        7. Burr DB, Hooser M. Alterations to the en bloc basic fuchsin staining protocol for the demonstration of microdamage produced in vivo.. Bone 1995 Oct;17(4):431-3.
          pubmed: 8573418doi: 10.1016/s8756-3282(95)00241-3google scholar: lookup
        8. Burr DB, Stafford T. Validity of the bulk-staining technique to separate artifactual from in vivo bone microdamage.. Clin Orthop Relat Res 1990 Nov;(260):305-8.
          pubmed: 1699696
        9. Cardoso L, Herman BC, Verborgt O, Laudier D, Majeska RJ, Schaffler MB. Osteocyte apoptosis controls activation of intracortical resorption in response to bone fatigue.. J Bone Miner Res 2009 Apr;24(4):597-605.
          pmc: PMC2659511pubmed: 19049324doi: 10.1359/jbmr.081210google scholar: lookup
        10. Colopy SA, Benz-Dean J, Barrett JG, Sample SJ, Lu Y, Danova NA, Kalscheur VL, Vanderby R Jr, Markel MD, Muir P. Response of the osteocyte syncytium adjacent to and distant from linear microcracks during adaptation to cyclic fatigue loading.. Bone 2004 Oct;35(4):881-91.
          pubmed: 15454095doi: 10.1016/j.bone.2004.05.024google scholar: lookup
        11. Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2002.
        12. Da Costa Gómez TM, Barrett JG, Sample SJ, Radtke CL, Kalscheur VL, Lu Y, Markel MD, Santschi EM, Scollay MC, Muir P. Up-regulation of site-specific remodeling without accumulation of microcracking and loss of osteocytes.. Bone 2005 Jul;37(1):16-24.
          pubmed: 15908291doi: 10.1016/j.bone.2004.12.016google scholar: lookup
        13. Diab T, Vashishth D. Morphology, localization and accumulation of in vivo microdamage in human cortical bone.. Bone 2007 Mar;40(3):612-8.
          pmc: PMC2013741pubmed: 17097933doi: 10.1016/j.bone.2006.09.027google scholar: lookup
        14. Donahue SW, Galley SA. Microdamage in bone: implications for fracture, repair, remodeling, and adaptation.. Crit Rev Biomed Eng 2006;34(3):215-71.
        15. Donahue SW, Sharkey NA, Modanlou KA, Sequeira LN, Martin RB. Bone strain and microcracks at stress fracture sites in human metatarsals.. Bone 2000 Dec;27(6):827-33.
          pubmed: 11113394doi: 10.1016/s8756-3282(00)00402-6google scholar: lookup
        16. Ebacher V, Tang C, McKay H, Oxland TR, Guy P, Wang R. Strain redistribution and cracking behavior of human bone during bending.. Bone 2007 May;40(5):1265-75.
          pubmed: 17317352doi: 10.1016/j.bone.2006.12.065google scholar: lookup
        17. Fritton SP, Rubin CT. In vivo measurement of bone deformations using strain gauges. In: Cowin SC, editor. Bone Biomechanics Handbook. Boca Raton: CRC Press; 2001.
        18. Frost HM. Presence of microscopic cracks in vivo in bone. Henry Ford Hosp Med Bull 1960;8:25–35.
        19. George WT, Vashishth D. Damage mechanisms and failure modes of cortical bone under components of physiological loading.. J Orthop Res 2005 Sep;23(5):1047-53.
          pubmed: 16140189doi: 10.1016/j.orthres.2005.02.008google scholar: lookup
        20. Gibson VA, Stover SM, Gibeling JC, Hazelwood SJ, Martin RB. Osteonal effects on elastic modulus and fatigue life in equine bone.. J Biomech 2006;39(2):217-25.
        21. Goodwin KJ, Sharkey NA. Material properties of interstitial lamellae reflect local strain environments.. J Orthop Res 2002 May;20(3):600-6.
          pubmed: 12038637doi: 10.1016/s0736-0266(01)00152-8google scholar: lookup
        22. Hazenberg JG, Freeley M, Foran E, Lee TC, Taylor D. Microdamage: a cell transducing mechanism based on ruptured osteocyte processes.. J Biomech 2006;39(11):2096-103.
        23. Herman BC, Cardoso L, Majeska RJ, Jepsen KJ, Schaffler MB. Activation of bone remodeling after fatigue: differential response to linear microcracks and diffuse damage.. Bone 2010 Oct;47(4):766-72.
          pmc: PMC2939191pubmed: 20633708doi: 10.1016/j.bone.2010.07.006google scholar: lookup
        24. Hiller LP, Stover SM, Gibson VA, Gibeling JC, Prater CS, Hazelwood SJ, Yeh OC, Martin RB. Osteon pullout in the equine third metacarpal bone: effects of ex vivo fatigue.. J Orthop Res 2003 May;21(3):481-8.
          pubmed: 12706021doi: 10.1016/s0736-0266(02)00232-2google scholar: lookup
        25. Hillman JR, Davis RW, Abdelbaki YZ. Cyclic bone remodeling in deer.. Calcif Tissue Res 1973;12(4):323-30.
          pubmed: 4746698doi: 10.1007/bf02013745google scholar: lookup
        26. Hughes JM, Petit MA. Biological underpinnings of Frost's mechanostat thresholds: the important role of osteocytes.. J Musculoskelet Neuronal Interact 2010 Jun;10(2):128-35.
          pubmed: 20516629
        27. Kennedy OD, Brennan O, Mauer P, Rackard SM, O'Brien FJ, Taylor D, Lee TC. The effects of increased intracortical remodeling on microcrack behaviour in compact bone.. Bone 2008 Nov;43(5):889-93.
          pubmed: 18706535doi: 10.1016/j.bone.2008.07.235google scholar: lookup
        28. Lanyon LE. Analysis of surface bone strain in the calcaneus of sheep during normal locomotion. Strain analysis of the calcaneus.. J Biomech 1973 Jan;6(1):41-9.
          pubmed: 4693867doi: 10.1016/0021-9290(73)90036-5google scholar: lookup
        29. Lanyon LE. Experimental support for the trajectorial theory of bone structure.. J Bone Joint Surg Br 1974 Feb;56(1):160-6.
          pubmed: 4818846
        30. Lanyon LE, Magee PT, Baggott DG. The relationship of functional stress and strain to the processes of bone remodelling. An experimental study on the sheep radius.. J Biomech 1979;12(8):593-600.
          pubmed: 479211doi: 10.1016/0021-9290(79)90079-4google scholar: lookup
        31. Launey ME, Buehler MJ, Ritchie RO. On the mechanistic origins of toughness in bone. Annu Rev Mater Res 2010;40:25–53.
        32. Lee TC, Myers ER, Hayes WC. Fluorescence-aided detection of microdamage in compact bone.. J Anat 1998 Aug;193 ( Pt 2)(Pt 2):179-84.
        33. Lieberman DE, Pearson OM, Polk JD, Demes B, Crompton AW. Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs.. J Exp Biol 2003 Sep;206(Pt 18):3125-38.
          pubmed: 12909694doi: 10.1242/jeb.00514google scholar: lookup
        34. Martin RB. Is all cortical bone remodeling initiated by microdamage?. Bone 2002 Jan;30(1):8-13.
          pubmed: 11792558doi: 10.1016/s8756-3282(01)00620-2google scholar: lookup
        35. Martin RB. The importance of mechanical loading in bone biology and medicine.. J Musculoskelet Neuronal Interact 2007 Jan-Mar;7(1):48-53.
          pubmed: 17396005
        36. Martin RB, Burr DB, Sharkey NA. Skeletal Tissue Mechanics. New York, NY: Springer; 1998.
        37. McMahon JM, Boyde A, Bromage TG. Pattern of collagen fiber orientation in the ovine calcaneal shaft and its relation to locomotor-induced strain.. Anat Rec 1995 Jun;242(2):147-58.
          pubmed: 7668399doi: 10.1002/ar.1092420203google scholar: lookup
        38. Moreno CA, Main RP, Biewener AA. Variability in forelimb bone strains during non-steady locomotor activities in goats.. J Exp Biol 2008 Apr;211(Pt 7):1148-62.
          pubmed: 18344490doi: 10.1242/jeb.012419google scholar: lookup
        39. Norman TL, Wang Z. Microdamage of human cortical bone: incidence and morphology in long bones.. Bone 1997 Apr;20(4):375-9.
          pubmed: 9108359doi: 10.1016/s8756-3282(97)00004-5google scholar: lookup
        40. O'Brien FJ, Taylor D, Lee TC. Microcrack accumulation at different intervals during fatigue testing of compact bone.. J Biomech 2003 Jul;36(7):973-80.
          pubmed: 12757806doi: 10.1016/s0021-9290(03)00066-6google scholar: lookup
        41. O'Brien FJ, Taylor D, Clive Lee T. The effect of bone microstructure on the initiation and growth of microcracks.. J Orthop Res 2005 Mar;23(2):475-80.
          pubmed: 15734265doi: 10.1016/j.orthres.2004.08.005google scholar: lookup
        42. Parfitt AM. Targeted and nontargeted bone remodeling: relationship to basic multicellular unit origination and progression.. Bone 2002 Jan;30(1):5-7.
          pubmed: 11792557doi: 10.1016/s8756-3282(01)00642-1google scholar: lookup
        43. Pattin CA, Caler WE, Carter DR. Cyclic mechanical property degradation during fatigue loading of cortical bone.. J Biomech 1996 Jan;29(1):69-79.
          pubmed: 8839019doi: 10.1016/0021-9290(94)00156-1google scholar: lookup
        44. Reilly GC. Observations of microdamage around osteocyte lacunae in bone.. J Biomech 2000 Sep;33(9):1131-4.
          pubmed: 10854886doi: 10.1016/s0021-9290(00)00090-7google scholar: lookup
        45. Reilly GC, Currey JD. The development of microcracking and failure in bone depends on the loading mode to which it is adapted.. J Exp Biol 1999 Mar;202(Pt 5):543-52.
          pubmed: 9929457doi: 10.1242/jeb.202.5.543google scholar: lookup
        46. Reilly GC, Currey JD, Goodship AE. Exercise of young thoroughbred horses increases impact strength of the third metacarpal bone.. J Orthop Res 1997 Nov;15(6):862-8.
          pubmed: 9497811doi: 10.1002/jor.1100150611google scholar: lookup
        47. Robling AG, Castillo AB, Turner CH. Biomechanical and molecular regulation of bone remodeling.. Annu Rev Biomed Eng 2006;8:455-98.
        48. Skedros JG. Interpreting load history in limb-bone diaphyses: important considerations and their biomechanical foundations. In: Crowder C, Stout S, editors. Bone Histology: an Anthropological Perspective. Boca Raton, Florida: CRC Press; 2011.
        49. Skedros JG, Mason MW, Bloebaum RD. Differences in osteonal micromorphology between tensile and compressive cortices of a bending skeletal system: indications of potential strain-specific differences in bone microstructure.. Anat Rec 1994 Aug;239(4):405-13.
          pubmed: 7978364doi: 10.1002/ar.1092390407google scholar: lookup
        50. Skedros JG, Su SC, Bloebaum RD. Biomechanical implications of mineral content and microstructural variations in cortical bone of horse, elk, and sheep calcanei.. Anat Rec 1997 Nov;249(3):297-316.
        51. Skedros JG, Mason MW, Bloebaum RD. Modeling and remodeling in a developing artiodactyl calcaneus: a model for evaluating Frost's Mechanostat hypothesis and its corollaries.. Anat Rec 2001 Jun 1;263(2):167-85.
          pubmed: 11360234doi: 10.1002/ar.1094google scholar: lookup
        52. Skedros JG, Sybrowsky CL, Parry TR, Bloebaum RD. Regional differences in cortical bone organization and microdamage prevalence in Rocky Mountain mule deer.. Anat Rec A Discov Mol Cell Evol Biol 2003 Sep;274(1):837-50.
          pubmed: 12923894doi: 10.1002/ar.a.10102google scholar: lookup
        53. Skedros JG, Hunt KJ, Bloebaum RD. Relationships of loading history and structural and material characteristics of bone: development of the mule deer calcaneus.. J Morphol 2004 Mar;259(3):281-307.
          pubmed: 14994328doi: 10.1002/jmor.10167google scholar: lookup
        54. Skedros JG, Dayton MR, Sybrowsky CL, Bloebaum RD, Bachus KN. The influence of collagen fiber orientation and other histocompositional characteristics on the mechanical properties of equine cortical bone.. J Exp Biol 2006 Aug;209(Pt 15):3025-42.
          pubmed: 16857886doi: 10.1242/jeb.02304google scholar: lookup
        55. Skedros JG, Sorenson SM, Takano Y, Turner CH. Dissociation of mineral and collagen orientations may differentially adapt compact bone for regional loading environments: results from acoustic velocity measurements in deer calcanei.. Bone 2006 Jul;39(1):143-51.
          pubmed: 16459155doi: 10.1016/j.bone.2005.12.007google scholar: lookup
        56. Skedros JG, Sorenson SM, Hunt KJ, Holyoak JD. Ontogenetic structural and material variations in ovine calcanei: a model for interpreting bone adaptation.. Anat Rec (Hoboken) 2007 Mar;290(3):284-300.
          pubmed: 17525944doi: 10.1002/ar.20423google scholar: lookup
        57. Skedros JG, Mendenhall SD, Kiser CJ, Winet H. Interpreting cortical bone adaptation and load history by quantifying osteon morphotypes in circularly polarized light images.. Bone 2009 Mar;44(3):392-403.
          pubmed: 19049911doi: 10.1016/j.bone.2008.10.053google scholar: lookup
        58. Sokal RR, Rohlf FJ. Biometry. The Principles and Practice of Statistics in Biological Research. 3rd edn. New York: W.H. Freeman; 1995.
        59. Su SC. Microstructure and mineral content correlations to strain parameters in cortical bone of the artiodactyl calcaneus. Department of Bioengineering. Salt Lake City, UT: University of Utah; 1998. Masters Thesis.
        60. Su SC, Skedros JG, Bachus KN, Bloebaum RD. Loading conditions and cortical bone construction of an artiodactyl calcaneus.. J Exp Biol 1999 Nov;202(Pt 22):3239-54.
          pubmed: 10539972doi: 10.1242/jeb.202.22.3239google scholar: lookup
        61. Taylor D, Lee TC. Measuring the shape and size of microcracks in bone.. J Biomech 1998 Dec;31(12):1177-80.
          pubmed: 9882051doi: 10.1016/s0021-9290(98)00133-xgoogle scholar: lookup
        62. Vander Sloten J, Van der Perre G. Trabecular structure compared to stress trajectories in the proximal femur and the calcaneus.. J Biomed Eng 1989 May;11(3):203-8.
          pubmed: 2724941doi: 10.1016/0141-5425(89)90142-8google scholar: lookup
        63. Vashishth D. Rising crack-growth-resistance behavior in cortical bone: implications for toughness measurements.. J Biomech 2004 Jun;37(6):943-6.
        64. Vashishth D, Koontz J, Qiu SJ, Lundin-Cannon D, Yeni YN, Schaffler MB, Fyhrie DP. In vivo diffuse damage in human vertebral trabecular bone.. Bone 2000 Feb;26(2):147-52.
          pubmed: 10678409doi: 10.1016/s8756-3282(99)00253-7google scholar: lookup
        65. Wang X, Niebur GL. Microdamage propagation in trabecular bone due to changes in loading mode.. J Biomech 2006;39(5):781-90.
        66. Zioupos P, Currey JD. The extent of microcracking and the morphology of microcracks in damaged bone. J Mater Sci 1994;29:978–986.

        Citations

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        1. Nguyen JT, Barak MM. Secondary osteon structural heterogeneity between the cranial and caudal cortices of the proximal humerus in white-tailed deer. J Exp Biol 2020 Jun 11;223(Pt 11).
          doi: 10.1242/jeb.225482pubmed: 32366689google scholar: lookup
        2. Skedros JG, Su SC, Knight AN, Bloebaum RD, Bachus KN. Advancing the deer calcaneus model for bone adaptation studies: ex vivo strains obtained after transecting the tension members suggest an unrecognized important role for shear strains. J Anat 2019 Jan;234(1):66-82.
          doi: 10.1111/joa.12905pubmed: 30411344google scholar: lookup
        3. Agnew AM, Dominguez VM, Sciulli PW, Stout SD. Variability of in vivo linear microcrack accumulation in the cortex of elderly human ribs. Bone Rep 2017 Jun;6:60-63.
          doi: 10.1016/j.bonr.2017.02.004pubmed: 28377983google scholar: lookup
        4. Gocha TP, Agnew AM. Spatial variation in osteon population density at the human femoral midshaft: histomorphometric adaptations to habitual load environment. J Anat 2016 May;228(5):733-45.
          doi: 10.1111/joa.12433pubmed: 26708961google scholar: lookup
        5. Harrison KD, Cooper DM. Modalities for Visualization of Cortical Bone Remodeling: The Past, Present, and Future. Front Endocrinol (Lausanne) 2015;6:122.
          doi: 10.3389/fendo.2015.00122pubmed: 26322017google scholar: lookup
        6. Carter Y, Suchorab JL, Thomas CD, Clement JG, Cooper DM. Normal variation in cortical osteocyte lacunar parameters in healthy young males. J Anat 2014 Sep;225(3):328-36.
          doi: 10.1111/joa.12213pubmed: 25040136google scholar: lookup
        7. Skedros JG, Knight AN, Farnsworth RW, Bloebaum RD. Do regional modifications in tissue mineral content and microscopic mineralization heterogeneity adapt trabecular bone tracts for habitual bending? Analysis in the context of trabecular architecture of deer calcanei. J Anat 2012 Mar;220(3):242-55.
        8. Miszkiewicz JJ, Cooke KM, Reid HE, Louys J. Interdisciplinarity of secondary osteons: relevance of bioarchaeological and palaeontological research in biomedical cortical bone histology studies. Bone Rep 2026 Mar;28:101893.
          doi: 10.1016/j.bonr.2025.101893pubmed: 41480160google scholar: lookup
        9. Skedros JG. A 50-year perspective on the use and potential of artiodactyl calcanei in bone adaptation studies. Biol Rev Camb Philos Soc 2026 Feb;101(1):437-485.
          doi: 10.1111/brv.70089pubmed: 41147243google scholar: lookup