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Journal of theoretical biology1984; 107(2); 321-327; doi: 10.1016/s0022-5193(84)80031-4

Dynamic strain similarity in vertebrates; an alternative to allometric limb bone scaling.

Abstract: Galileo (1638) observed that "nature cannot grow a tree nor construct an animal beyond a certain size, while retaining the proportions which suffice in the case of a smaller structure". However, subsequent measurement has shown that limb bone dimensions are scaled geometrically with body size (Alexander et al., 1979a), and that the material properties of their constituent bone tissue are similar in animals over a wide range of body weight (Sedlin & Hirsch, 1966; Yamada, 1970; Burstein et al., 1972; Biewener, 1982). If, as suggested in previous scaling arguments (McMahon, 1973; Biewener, 1982), vigorous locomotion involved the same proportional forces over a wide range of animal size, this would create a paradox since large animals would be in far greater danger of skeletal failure than small ones. However, in vivo strain gauge implantations have shown that, during high speed running, axial force as a proportion of body weight (G) in the limb bones of animals decreases as a function of body size from 6.9 G in a 7 kg turkey to 2.8 G in a small (130 kg) horse. Estimates of axial force in larger animals suggest that this is further reduced to 0.8 G in a 2500 kg elephant. Nevertheless, it appears that, regardless of animal size or locomotory style, the peak stresses in the bones of these animals are remarkably similar. Therefore, throughout the range of animals considered (350 times differences in mass), we suggest that similar safety factors to failure are maintained, not by allometrically scaling bone dimensions, but rather by allometrically scaling the magnitude of the peak forces applied to them during vigorous locomotion.(ABSTRACT TRUNCATED AT 250 WORDS)
Publication Date: 1984-03-21 PubMed ID: 6717041DOI: 10.1016/s0022-5193(84)80031-4Google Scholar: Lookup
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  • Comparative Study
  • Journal Article

Summary

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This research article studies limb bone scaling in vertebrates, suggesting that similar safety factors are maintained across a wide range of body sizes, not by adjusting bone dimensions, but by changing the peak force applied to them during vigorous movement.

Overview

  • The article begins with a reference to Galileo’s observation that nature has a limit on the size it can grow a tree or an animal while maintaining the same proportions as in smaller structures. Yet, researchers have found that the size of limb bones statically scales to body size in vertebrates and the properties of their bone tissue remain mostly the same across a diverse range of body weights.

The Problem with Proportional Forces

  • Previous studies proposed that vigorous movement involves the same proportional forces across animals of different sizes. If this were the case, it would lead to a paradox; larger animals would be more susceptible to skeletal failure than smaller ones due to the increased force on their bones.

In Vivo Strain Gauge Measurements

  • The researchers measured axial force (as a proportion of body weight) in the limb bones of animals during high-speed running, which ranges from 6.9 G in turkeys (weighing 7 kg) to 0.8 G in elephants (weighing 2500 kg).
  • This measurement indicates that the axial force in limbs decreases with body size, contrary to the idea of using the same proportional forces across different animal sizes.

Similar Peak Stresses in Different Body Sizes

  • Results show that despite the size of an animal or the style of its movement, the peak stresses in the limb bones are remarkably similar.
  • This similarity suggests that the bones of all animals, whether small or large, experience comparable amounts of maximum stress.

New Hypothesis: Dynamic Strain Similarity

  • The paper postulates that the similarity in safety factors among animals is maintained by the static scaling of the peak forces applied to the bones during vigorous movement, rather than by changing the dimensions of the bones.
  • The authors call this hypothesis ‘dynamic strain similarity’, which offers an alternative to the allometric limb bone scaling suggested by previous research.

Cite This Article

APA
Rubin CT, Lanyon LE. (1984). Dynamic strain similarity in vertebrates; an alternative to allometric limb bone scaling. J Theor Biol, 107(2), 321-327. https://doi.org/10.1016/s0022-5193(84)80031-4

Publication

ISSN: 0022-5193
NlmUniqueID: 0376342
Country: England
Language: English
Volume: 107
Issue: 2
Pages: 321-327

Researcher Affiliations

Rubin, C T
    Lanyon, L E

      MeSH Terms

      • Animals
      • Body Weight
      • Bone and Bones / anatomy & histology
      • Bone and Bones / physiology
      • Buffaloes
      • Dogs
      • Elephants
      • Extremities / anatomy & histology
      • Extremities / physiology
      • Horses
      • Locomotion
      • Stress, Mechanical
      • Tibia / anatomy & histology
      • Tibia / physiology
      • Turkeys

      Citations

      This article has been cited 74 times.
      1. Rubin J, Styner M. The skeleton in a physical world.. Exp Biol Med (Maywood) 2022 Dec;247(24):2213-2222.
        doi: 10.1177/15353702221113861pubmed: 35983849google scholar: lookup
      2. Lewis KJ, Cabahug-Zuckerman P, Boorman-Padgett JF, Basta-Pljakic J, Louie J, Stephen S, Spray DC, Thi MM, Seref-Ferlengez Z, Majeska RJ, Weinbaum S, Schaffler MB. Estrogen depletion on In vivo osteocyte calcium signaling responses to mechanical loading.. Bone 2021 Nov;152:116072.
        doi: 10.1016/j.bone.2021.116072pubmed: 34171514google scholar: lookup
      3. Hutchinson JR. The evolutionary biomechanics of locomotor function in giant land animals.. J Exp Biol 2021 Jun 1;224(11).
        doi: 10.1242/jeb.217463pubmed: 34100541google scholar: lookup
      4. Thompson M, Woods K, Newberg J, Oxford JT, Uzer G. Low-intensity vibration restores nuclear YAP levels and acute YAP nuclear shuttling in mesenchymal stem cells subjected to simulated microgravity.. NPJ Microgravity 2020 Dec 1;6(1):35.
        doi: 10.1038/s41526-020-00125-5pubmed: 33298964google scholar: lookup
      5. Hu TL, Cheng F, Xu Z, Chen ZZ, Yu L, Ban Q, Li CL, Pan T, Zhang BW. Molecular and morphological evidence for a new species of the genus Typhlomys (Rodentia: Platacanthomyidae).. Zool Res 2021 Jan 18;42(1):100-107.
      6. Liedert A, Nemitz C, Haffner-Luntzer M, Schick F, Jakob F, Ignatius A. Effects of Estrogen Receptor and Wnt Signaling Activation on Mechanically Induced Bone Formation in a Mouse Model of Postmenopausal Bone Loss.. Int J Mol Sci 2020 Nov 5;21(21).
        doi: 10.3390/ijms21218301pubmed: 33167497google scholar: lookup
      7. Aguirre TG, Ingrole A, Fuller L, Seek TW, Fiorillo AR, Sertich JJW, Donahue SW. Differing trabecular bone architecture in dinosaurs and mammals contribute to stiffness and limits on bone strain.. PLoS One 2020;15(8):e0237042.
        doi: 10.1371/journal.pone.0237042pubmed: 32813735google scholar: lookup
      8. Sato T, Verma S, Andrade CDC, Omeara M, Campbell N, Wang JS, Cetinbas M, Lang A, Ausk BJ, Brooks DJ, Sadreyev RI, Kronenberg HM, Lagares D, Uda Y, Pajevic PD, Bouxsein ML, Gross TS, Wein MN. A FAK/HDAC5 signaling axis controls osteocyte mechanotransduction.. Nat Commun 2020 Jul 1;11(1):3282.
        doi: 10.1038/s41467-020-17099-3pubmed: 32612176google scholar: lookup
      9. Turcotte CM, Green DJ, Kupczik K, McFarlin S, Schulz-Kornas E. Elevated activity levels do not influence extrinsic fiber attachment morphology on the surface of muscle-attachment sites.. J Anat 2020 May;236(5):827-839.
        doi: 10.1111/joa.13137pubmed: 31845322google scholar: lookup
      10. Schlecht SH, Martin CT, Ochocki DN, Nolan BT, Wojtys EM, Ashton-Miller JA. Morphology of Mouse Anterior Cruciate Ligament-Complex Changes Following Exercise During Pubertal Growth.. J Orthop Res 2019 Sep;37(9):1910-1919.
        doi: 10.1002/jor.24328pubmed: 31042312google scholar: lookup
      11. Prasad J, Goyal A. An Invertible Mathematical Model of Cortical Bone's Adaptation to Mechanical Loading.. Sci Rep 2019 Apr 10;9(1):5890.
        doi: 10.1038/s41598-019-42378-5pubmed: 30971812google scholar: lookup
      12. Bain SD, Huber P, Ausk BJ, Kwon RY, Gardiner EM, Srinivasan S, Gross TS. Neuromuscular dysfunction, independent of gait dysfunction, modulates trabecular bone homeostasis in mice.. J Musculoskelet Neuronal Interact 2019 Mar 1;19(1):79-93.
        pubmed: 30839306
      13. 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
      14. Weiss-Bilka HE, Brill JA, Ravosa MJ. Non-sutural basicranium-derived cells undergo a unique mineralization pathway via a cartilage intermediate in vitro.. PeerJ 2018;6:e5757.
        doi: 10.7717/peerj.5757pubmed: 30386695google scholar: lookup
      15. Schlecht SH, Ramcharan MA, Yang Y, Smith LM, Bigelow EM, Nolan BT, Moss DE, Devlin MJ, Jepsen KJ. Differential Adaptive Response of Growing Bones From Two Female Inbred Mouse Strains to Voluntary Cage-Wheel Running.. JBMR Plus 2018 May;2(3):143-153.
        doi: 10.1002/jbm4.10032pubmed: 30283899google scholar: lookup
      16. Yingling VR, Ferrari-Church B, Strickland A. Tibia functionality and Division II female and male collegiate athletes from multiple sports.. PeerJ 2018;6:e5550.
        doi: 10.7717/peerj.5550pubmed: 30221092google scholar: lookup
      17. Hemmatian H, Jalali R, Semeins CM, Hogervorst JMA, van Lenthe GH, Klein-Nulend J, Bakker AD. Mechanical Loading Differentially Affects Osteocytes in Fibulae from Lactating Mice Compared to Osteocytes in Virgin Mice: Possible Role for Lacuna Size.. Calcif Tissue Int 2018 Dec;103(6):675-685.
        doi: 10.1007/s00223-018-0463-8pubmed: 30109376google scholar: lookup
      18. Bleedorn JA, Hornberger TA, Goodman CA, Hao Z, Sample SJ, Amene E, Markel MD, Behan M, Muir P. Temporal mechanically-induced signaling events in bone and dorsal root ganglion neurons after in vivo bone loading.. PLoS One 2018;13(2):e0192760.
        doi: 10.1371/journal.pone.0192760pubmed: 29486004google scholar: lookup
      19. Lewis KJ, Frikha-Benayed D, Louie J, Stephen S, Spray DC, Thi MM, Seref-Ferlengez Z, Majeska RJ, Weinbaum S, Schaffler MB. Osteocyte calcium signals encode strain magnitude and loading frequency in vivo.. Proc Natl Acad Sci U S A 2017 Oct 31;114(44):11775-11780.
        doi: 10.1073/pnas.1707863114pubmed: 29078317google scholar: lookup
      20. McHorse BK, Biewener AA, Pierce SE. Mechanics of evolutionary digit reduction in fossil horses (Equidae).. Proc Biol Sci 2017 Aug 30;284(1861).
        doi: 10.1098/rspb.2017.1174pubmed: 28835559google scholar: lookup
      21. Thompson KD, Weiss-Bilka HE, McGough EB, Ravosa MJ. Bone up: craniomandibular development and hard-tissue biomineralization in neonate mice.. Zoology (Jena) 2017 Oct;124:51-60.
        doi: 10.1016/j.zool.2017.01.002pubmed: 28807504google scholar: lookup
      22. Iwaniec UT, Turner RT. Influence of body weight on bone mass, architecture and turnover.. J Endocrinol 2016 Sep;230(3):R115-30.
        doi: 10.1530/JOE-16-0089pubmed: 27352896google scholar: lookup
      23. Hillam RA, Goodship AE, Skerry TM. Peak strain magnitudes and rates in the tibia exceed greatly those in the skull: An in vivo study in a human subject.. J Biomech 2015 Sep 18;48(12):3292-8.
      24. Wallace IJ, Pagnotti GM, Rubin-Sigler J, Naeher M, Copes LE, Judex S, Rubin CT, Demes B. Focal enhancement of the skeleton to exercise correlates with responsivity of bone marrow mesenchymal stem cells rather than peak external forces.. J Exp Biol 2015 Oct;218(Pt 19):3002-9.
        doi: 10.1242/jeb.118729pubmed: 26232415google scholar: lookup
      25. Melville KM, Kelly NH, Surita G, Buchalter DB, Schimenti JC, Main RP, Ross FP, van der Meulen MC. Effects of Deletion of ERα in Osteoblast-Lineage Cells on Bone Mass and Adaptation to Mechanical Loading Differ in Female and Male Mice.. J Bone Miner Res 2015 Aug;30(8):1468-80.
        doi: 10.1002/jbmr.2488pubmed: 25707500google scholar: lookup
      26. Novotny SA, Warren GL, Hamrick MW. Aging and the muscle-bone relationship.. Physiology (Bethesda) 2015 Jan;30(1):8-16.
        doi: 10.1152/physiol.00033.2014pubmed: 25559151google scholar: lookup
      27. Vazquez M, Evans BA, Riccardi D, Evans SL, Ralphs JR, Dillingham CM, Mason DJ. A new method to investigate how mechanical loading of osteocytes controls osteoblasts.. Front Endocrinol (Lausanne) 2014;5:208.
        doi: 10.3389/fendo.2014.00208pubmed: 25538684google scholar: lookup
      28. Rabey KN, Green DJ, Taylor AB, Begun DR, Richmond BG, McFarlin SC. Locomotor activity influences muscle architecture and bone growth but not muscle attachment site morphology.. J Hum Evol 2015 Jan;78:91-102.
        doi: 10.1016/j.jhevol.2014.10.010pubmed: 25467113google scholar: lookup
      29. Nagaraja MP, Jo H. The Role of Mechanical Stimulation in Recovery of Bone Loss-High versus Low Magnitude and Frequency of Force.. Life (Basel) 2014 Apr 2;4(2):117-30.
        doi: 10.3390/life4020117pubmed: 25370188google scholar: lookup
      30. Melville KM, Robling AG, van der Meulen MC. In vivo axial loading of the mouse tibia.. Methods Mol Biol 2015;1226:99-115.
        doi: 10.1007/978-1-4939-1619-1_9pubmed: 25331046google scholar: lookup
      31. Lynch ME, Fischbach C. Biomechanical forces in the skeleton and their relevance to bone metastasis: biology and engineering considerations.. Adv Drug Deliv Rev 2014 Dec 15;79-80:119-34.
        doi: 10.1016/j.addr.2014.08.009pubmed: 25174311google scholar: lookup
      32. Yang PF, Sanno M, Ganse B, Koy T, Brüggemann GP, Müller LP, Rittweger J. Torsion and antero-posterior bending in the in vivo human tibia loading regimes during walking and running.. PLoS One 2014;9(4):e94525.
        doi: 10.1371/journal.pone.0094525pubmed: 24732724google scholar: lookup
      33. Lin L, Oon HY, Lin W, Qin YX. Principal trabecular structural orientation predicted by quantitative ultrasound is strongly correlated with μFEA determined anisotropic apparent stiffness.. Biomech Model Mechanobiol 2014 Oct;13(5):961-71.
        doi: 10.1007/s10237-013-0547-3pubmed: 24419558google scholar: lookup
      34. Brassey CA, Holdaway RN, Packham AG, Anné J, Manning PL, Sellers WI. More than one way of being a moa: differences in leg bone robustness map divergent evolutionary trajectories in Dinornithidae and Emeidae (Dinornithiformes).. PLoS One 2013;8(12):e82668.
        doi: 10.1371/journal.pone.0082668pubmed: 24367537google scholar: lookup
      35. Kilbourne BM, Hoffman LC. Scale effects between body size and limb design in quadrupedal mammals.. PLoS One 2013;8(11):e78392.
        doi: 10.1371/journal.pone.0078392pubmed: 24260117google scholar: lookup
      36. Patel BA, Horner AM, Thompson NE, Barrett L, Henzi SP. Ontogenetic scaling of fore- and hind limb posture in wild chacma baboons (Papio hamadryas ursinus).. PLoS One 2013;8(7):e71020.
        doi: 10.1371/journal.pone.0071020pubmed: 23923046google scholar: lookup
      37. Knapik DM, Perera P, Nam J, Blazek AD, Rath B, Leblebicioglu B, Das H, Wu LC, Hewett TE, Agarwal SK Jr, Robling AG, Flanigan DC, Lee BS, Agarwal S. Mechanosignaling in bone health, trauma and inflammation.. Antioxid Redox Signal 2014 Feb 20;20(6):970-85.
        doi: 10.1089/ars.2013.5467pubmed: 23815527google scholar: lookup
      38. Chan ME, Uzer G, Rubin CT. The potential benefits and inherent risks of vibration as a non-drug therapy for the prevention and treatment of osteoporosis.. Curr Osteoporos Rep 2013 Mar;11(1):36-44.
        doi: 10.1007/s11914-012-0132-1pubmed: 23371467google scholar: lookup
      39. Rubin CT, Seeherman H, Qin YX, Gross TS. The mechanical consequences of load bearing in the equine third metacarpal across speed and gait: the nonuniform distributions of normal strain, shear strain, and strain energy density.. FASEB J 2013 May;27(5):1887-94.
        doi: 10.1096/fj.12-216804pubmed: 23355269google scholar: lookup
      40. Brassey CA, Margetts L, Kitchener AC, Withers PJ, Manning PL, Sellers WI. Finite element modelling versus classic beam theory: comparing methods for stress estimation in a morphologically diverse sample of vertebrate long bones.. J R Soc Interface 2013 Feb;10(79):20120823.
        doi: 10.1098/rsif.2012.0823pubmed: 23173199google scholar: lookup
      41. Manske SL, Lorincz CR, Zernicke RF. Bone health: part 2, physical activity.. Sports Health 2009 Jul;1(4):341-6.
        doi: 10.1177/1941738109338823pubmed: 23015892google scholar: lookup
      42. Campione NE, Evans DC. A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods.. BMC Biol 2012 Jul 10;10:60.
        doi: 10.1186/1741-7007-10-60pubmed: 22781121google scholar: lookup
      43. Pagnotti GM, Adler BJ, Green DE, Chan ME, Frechette DM, Shroyer KR, Beamer WG, Rubin J, Rubin CT. Low magnitude mechanical signals mitigate osteopenia without compromising longevity in an aged murine model of spontaneous granulosa cell ovarian cancer.. Bone 2012 Sep;51(3):570-7.
        doi: 10.1016/j.bone.2012.05.004pubmed: 22584009google scholar: lookup
      44. Thompson WR, Rubin CT, Rubin J. Mechanical regulation of signaling pathways in bone.. Gene 2012 Jul 25;503(2):179-93.
        doi: 10.1016/j.gene.2012.04.076pubmed: 22575727google scholar: lookup
      45. Das-Gupta V, Williamson RA, Pitsillides AA. Expression of endothelial nitric oxide synthase protein is not necessary for mechanical strain-induced nitric oxide production by cultured osteoblasts.. Osteoporos Int 2012 Nov;23(11):2635-47.
        doi: 10.1007/s00198-012-1957-2pubmed: 22402674google scholar: lookup
      46. Recker RR, Armas L. The effect of antiresorptives on bone quality.. Clin Orthop Relat Res 2011 Aug;469(8):2207-14.
        doi: 10.1007/s11999-011-1909-8pubmed: 21562893google scholar: lookup
      47. Jepsen KJ. Functional interactions among morphologic and tissue quality traits define bone quality.. Clin Orthop Relat Res 2011 Aug;469(8):2150-9.
        doi: 10.1007/s11999-010-1706-9pubmed: 21125361google scholar: lookup
      48. Lynch ME, Main RP, Xu Q, Walsh DJ, Schaffler MB, Wright TM, van der Meulen MC. Cancellous bone adaptation to tibial compression is not sex dependent in growing mice.. J Appl Physiol (1985) 2010 Sep;109(3):685-91.
      49. Judex S, Rubin CT. Is bone formation induced by high-frequency mechanical signals modulated by muscle activity?. J Musculoskelet Neuronal Interact 2010 Mar;10(1):3-11.
        pubmed: 20190375
      50. Capozza RF, Feldman S, Mortarino P, Reina PS, Schiessl H, Rittweger J, Ferretti JL, Cointry GR. Structural analysis of the human tibia by tomographic (pQCT) serial scans.. J Anat 2010 Apr;216(4):470-81.
      51. Jepsen KJ. Systems analysis of bone.. Wiley Interdiscip Rev Syst Biol Med 2009 Jul-Aug;1(1):73-88.
        doi: 10.1002/wsbm.15pubmed: 20046860google scholar: lookup
      52. Ozcivici E, Luu YK, Adler B, Qin YX, Rubin J, Judex S, Rubin CT. Mechanical signals as anabolic agents in bone.. Nat Rev Rheumatol 2010 Jan;6(1):50-9.
        doi: 10.1038/nrrheum.2009.239pubmed: 20046206google scholar: lookup
      53. Price C, Li W, Novotny JE, Wang L. An in-situ fluorescence-based optical extensometry system for imaging mechanically loaded bone.. J Orthop Res 2010 Jun;28(6):805-11.
        doi: 10.1002/jor.21049pubmed: 20041487google scholar: lookup
      54. Luu YK, Ozcivici E, Capilla E, Adler B, Chan E, Shroyer K, Rubin J, Judex S, Pessin JE, Rubin CT. Development of diet-induced fatty liver disease in the aging mouse is suppressed by brief daily exposure to low-magnitude mechanical signals.. Int J Obes (Lond) 2010 Feb;34(2):401-5.
        doi: 10.1038/ijo.2009.240pubmed: 19935747google scholar: lookup
      55. Zaman G, Saxon LK, Sunters A, Hilton H, Underhill P, Williams D, Price JS, Lanyon LE. Loading-related regulation of gene expression in bone in the contexts of estrogen deficiency, lack of estrogen receptor alpha and disuse.. Bone 2010 Mar;46(3):628-42.
        doi: 10.1016/j.bone.2009.10.021pubmed: 19857613google scholar: lookup
      56. Gordeladze JO, Djouad F, Brondello JM, Noël D, Duroux-Richard I, Apparailly F, Jorgensen C. Concerted stimuli regulating osteo-chondral differentiation from stem cells: phenotype acquisition regulated by microRNAs.. Acta Pharmacol Sin 2009 Oct;30(10):1369-84.
        doi: 10.1038/aps.2009.143pubmed: 19801995google scholar: lookup
      57. Christiansen BA, Kotiya AA, Silva MJ. Constrained tibial vibration does not produce an anabolic bone response in adult mice.. Bone 2009 Oct;45(4):750-9.
        doi: 10.1016/j.bone.2009.06.025pubmed: 19576309google scholar: lookup
      58. Patel MJ, Chang KH, Sykes MC, Talish R, Rubin C, Jo H. Low magnitude and high frequency mechanical loading prevents decreased bone formation responses of 2T3 preosteoblasts.. J Cell Biochem 2009 Feb 1;106(2):306-16.
        doi: 10.1002/jcb.22007pubmed: 19125415google scholar: lookup
      59. Luu YK, Capilla E, Rosen CJ, Gilsanz V, Pessin JE, Judex S, Rubin CT. Mechanical stimulation of mesenchymal stem cell proliferation and differentiation promotes osteogenesis while preventing dietary-induced obesity.. J Bone Miner Res 2009 Jan;24(1):50-61.
        doi: 10.1359/jbmr.080817pubmed: 18715135google scholar: lookup
      60. Ren L, Hutchinson JR. The three-dimensional locomotor dynamics of African (Loxodonta africana) and Asian (Elephas maximus) elephants reveal a smooth gait transition at moderate speed.. J R Soc Interface 2008 Feb 6;5(19):195-211.
        doi: 10.1098/rsif.2007.1095pubmed: 17594960google scholar: lookup
      61. Meta M, Lu Y, Keyak JH, Lang T. Young-elderly differences in bone density, geometry and strength indices depend on proximal femur sub-region: a cross sectional study in Caucasian-American women.. Bone 2006 Jul;39(1):152-8.
        doi: 10.1016/j.bone.2005.11.020pubmed: 16459156google scholar: lookup
      62. Rubin J, Rubin C, Jacobs CR. Molecular pathways mediating mechanical signaling in bone.. Gene 2006 Feb 15;367:1-16.
        doi: 10.1016/j.gene.2005.10.028pubmed: 16361069google scholar: lookup
      63. Charras GT, Horton MA. Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation.. Biophys J 2002 Jun;82(6):2970-81.
        doi: 10.1016/S0006-3495(02)75638-5pubmed: 12023220google scholar: lookup
      64. Beck BR. Tibial stress injuries. An aetiological review for the purposes of guiding management.. Sports Med 1998 Oct;26(4):265-79.
      65. Weiss SL, Lee EA, Diamond J. Evolutionary matches of enzyme and transporter capacities to dietary substrate loads in the intestinal brush border.. Proc Natl Acad Sci U S A 1998 Mar 3;95(5):2117-21.
        doi: 10.1073/pnas.95.5.2117pubmed: 9482848google scholar: lookup
      66. Jagger CJ, Chow JW, Chambers TJ. Estrogen suppresses activation but enhances formation phase of osteogenic response to mechanical stimulation in rat bone.. J Clin Invest 1996 Nov 15;98(10):2351-7.
        doi: 10.1172/JCI119047pubmed: 8941653google scholar: lookup
      67. Chow JW, Jagger CJ, Chambers TJ. Reduction in dynamic indices of cancellous bone formation in rat tail vertebrae after caudal neurectomy.. Calcif Tissue Int 1996 Aug;59(2):117-20.
        doi: 10.1007/s002239900097pubmed: 8687980google scholar: lookup
      68. Turner CH, Boivin G, Meunier PJ. A mathematical model for fluoride uptake by the skeleton.. Calcif Tissue Int 1993 Feb;52(2):130-8.
        doi: 10.1007/BF00308322pubmed: 8443689google scholar: lookup
      69. Biewener AA. Safety factors in bone strength.. Calcif Tissue Int 1993;53 Suppl 1:S68-74.
        doi: 10.1007/BF01673406pubmed: 8275382google scholar: lookup
      70. Torrance AG, Mosley JR, Suswillo RF, Lanyon LE. Noninvasive loading of the rat ulna in vivo induces a strain-related modeling response uncomplicated by trauma or periostal pressure.. Calcif Tissue Int 1994 Mar;54(3):241-7.
        doi: 10.1007/BF00301686pubmed: 8055374google scholar: lookup
      71. Rubin CT. Skeletal strain and the functional significance of bone architecture.. Calcif Tissue Int 1984;36 Suppl 1:S11-8.
        doi: 10.1007/BF02406128pubmed: 6430509google scholar: lookup
      72. Turner CH. Toward a cure for osteoporosis: reversal of excessive bone fragility.. Osteoporos Int 1991 Oct;2(1):12-9.
        doi: 10.1007/BF01627073pubmed: 1790415google scholar: lookup
      73. Diamond J, Hammond K. The matches, achieved by natural selection, between biological capacities and their natural loads.. Experientia 1992 Jun 15;48(6):551-7.
        doi: 10.1007/BF01920238pubmed: 1612134google scholar: lookup
      74. Goodship AE. Mechanical stimulus to bone.. Ann Rheum Dis 1992 Jan;51(1):4-6.
        doi: 10.1136/ard.51.1.4pubmed: 1540035google scholar: lookup