A computational framework for canonical holistic morphometric analysis of trabecular bone

  • Ruff, C., Holt, B. & Trinkaus, E. Who’s afraid of the big bad Wolff?: “Wolff’s law’’ and bone functional adaptation. Am. J. Phys. Anthropol. 129, 484–498. https://doi.org/10.1002/ajpa.20371 (2006).

    Article 
    PubMed 

    Google Scholar 

  • Seeman, E. Bone modeling and remodeling. Crit. Rev. Eukaryot. Gene Expr. 19, 219–233. https://doi.org/10.1615/critreveukargeneexpr.v19.i3.40 (2009).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Carlson, K. J. & Judex, S. Increased non-linear locomotion alters diaphyseal bone shape. J. Exp. Biol. 210, 3117–3125. https://doi.org/10.1242/jeb.006544 (2007).

    Article 
    PubMed 

    Google Scholar 

  • Byron, C. D., Herrel, A., Pauwels, E., Muynck, A. D. & Patel, B. A. Mouse hallucal metatarsal cross-sectional geometry in a simulated fine branch niche. J. Morphol. 276, 759–765. https://doi.org/10.1002/jmor.20376 (2015).

    Article 
    PubMed 

    Google Scholar 

  • Turcotte, C. M., Rabey, K. N., Green, D. J. & McFarlin, S. C. Muscle attachment sites and behavioral reconstruction: An experimental test of muscle-bone structural response to habitual activity. Am. J. Biol. Anthropol. 177, 63–82. https://doi.org/10.1002/ajpa.24410 (2022).

    Article 

    Google Scholar 

  • Karakostis, F. A., Jeffery, N. & Harvati, K. Experimental proof that multivariate patterns among muscle attachments (entheses) can reflect repetitive muscle use. Sci. Rep. 9, 16577. https://doi.org/10.1038/s41598-019-53021-8 (2019).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pontzer, H. et al. Trabecular bone in the bird knee responds with high sensitivity to changes in load orientation. J. Exp. Biol. 209, 57–65. https://doi.org/10.1242/jeb.01971 (2006).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Barak, M. M., Lieberman, D. E. & Hublin, J.-J. A wolff in sheep’s clothing: Trabecular bone adaptation in response to changes in joint loading orientation. Bone 49, 1141–1151. https://doi.org/10.1016/j.bone.2011.08.020 (2011).

    Article 
    PubMed 

    Google Scholar 

  • Currey, J. D. The structure and mechanics of bone. J. Mater. Sci. 47, 41–54. https://doi.org/10.1007/s10853-011-5914-9 (2011).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • Wallace, I. J., Demes, B. & Judex, S. Ontogenetic and genetic influences on bone’s responsiveness to mechanical signals. In Building Bones: Bone Formation and Development in Anthropology (eds Percival, C. J. & Richtsmeier, J. T.) 233–253 (Cambridge University Press, 2017).

    Chapter 

    Google Scholar 

  • Tsegai, Z. J., Skinner, M. M., Pahr, D. H., Hublin, J.-J. & Kivell, T. L. Systemic patterns of trabecular bone across the human and chimpanzee skeleton. J. Anat. 232, 641–656. https://doi.org/10.1111/joa.12776 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tsegai, Z. J. et al. Trabecular bone structure correlates with hand posture and use in hominoids. PLoS ONE 8, e78781. https://doi.org/10.1371/journal.pone.0078781 (2013).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Skinner, M. M. et al. Human-like hand use in Australopithecus africanus. Science 347, 395–399. https://doi.org/10.1126/science.1261735 (2015).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Stephens, N. B. et al. Trabecular architecture in the thumb of pan and homo: Implications for investigating hand use, loading, and hand preference in the fossil record. Am. J. Phys. Anthropol. 161, 603–619. https://doi.org/10.1002/ajpa.23061 (2016).

    Article 
    PubMed 

    Google Scholar 

  • Dunmore, C. J., Bardo, A., Skinner, M. M. & Kivell, T. L. Trabecular variation in the first metacarpal and manipulation in hominids. Am. J. Phys. Anthropol. 171, 219–241. https://doi.org/10.1002/ajpa.23974 (2019).

    Article 
    PubMed 

    Google Scholar 

  • Dunmore, C. J., Kivell, T. L., Bardo, A. & Skinner, M. M. Metacarpal trabecular bone varies with distinct hand-positions used in hominid locomotion. J. Anat. 235, 45. https://doi.org/10.1111/joa.12966 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tsegai, Z., Skinner, M., Pahr, D., Hublin, J.-J. & Kivell, T. Ontogeny and variability of trabecular bone in the chimpanzee humerus, femur and tibia. Am. J. Phys. Anthropol. 167, 713–736. https://doi.org/10.1002/ajpa.23696 (2018).

    Article 
    PubMed 

    Google Scholar 

  • Georgiou, L., Kivell, T. L., Pahr, D. H., Buck, L. T. & Skinner, M. M. Trabecular architecture of the great ape and human femoral head. J. Anat. 234, 679–693. https://doi.org/10.1111/joa.12957 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Georgiou, L. et al. Evidence for habitual climbing in a pleistocene hominin in South Africa. Proc. Natl. Acad. Sci. 117, 8416–8423. https://doi.org/10.1073/pnas.1914481117 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Georgiou, L., Kivell, T., Pahr, D. & Skinner, M. Trabecular bone patterning in the hominoid distal femur. PeerJ 6, e5156. https://doi.org/10.7717/peerj.5156 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Colombo, A. et al. Trabecular analysis of the distal radial metaphysis during the acquisition of crawling and bipedal walking in childhood: A preliminary study. Bull. et Mem. de la Soc. d’Anthropol. de Paris 31, 43–51. https://doi.org/10.3166/bmsap-2018-0041 (2019).

    Article 

    Google Scholar 

  • Komza, K. & Skinner, M. First metatarsal trabecular bone structure in extant hominoids and swartkrans hominins. J. Hum. Evol. 131, 1–21. https://doi.org/10.1016/j.jhevol.2019.03.003 (2019).

    Article 
    PubMed 

    Google Scholar 

  • Sukhdeo, S., Parsons, J., Niu, X. M. & Ryan, T. M. Trabecular bone structure in the distal femur of humans, apes, and baboons. Anat. Rec. 303, 129–149. https://doi.org/10.1002/ar.24050 (2018).

    Article 

    Google Scholar 

  • DeMars, L. J. D. et al. Using point clouds to investigate the relationship between trabecular bone phenotype and behavior: An example utilizing the human calcaneus. Am. J. Hum. Biol. 33, e23468. https://doi.org/10.1002/ajhb.23468 (2020).

    Article 
    PubMed 

    Google Scholar 

  • Judex, S. & Carlson, K. J. Is bone’s response to mechanical signals dominated by gravitational loading? Med. Sci. Sports Exerc. 41, 2037–2043. https://doi.org/10.1249/mss.0b013e3181a8c6e5 (2009).

    Article 
    PubMed 

    Google Scholar 

  • Robling, A. G. Is bone’s response to mechanical signals dominated by muscle forces? Med. Sci. Sports Exerc. 41, 2044–2049. https://doi.org/10.1249/mss.0b013e3181a8c702 (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kivell, T. L. A review of trabecular bone functional adaptation: What have we learned from trabecular analyses in extant hominoids and what can we apply to fossils? J. Anat. 228, 569–594. https://doi.org/10.1111/joa.12446 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bouxsein, M. L. et al. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Miner. Res. 25, 1468–1486. https://doi.org/10.1002/jbmr.141 (2010).

    Article 
    PubMed 

    Google Scholar 

  • Maquer, G., Musy, S. N., Wandel, J., Gross, T. & Zysset, P. K. Bone volume fraction and fabric anisotropy are better determinants of trabecular bone stiffness than other morphological variables. J. Bone Miner. Res. 30, 1000–1008. https://doi.org/10.1002/jbmr.2437 (2015).

    Article 
    PubMed 

    Google Scholar 

  • Kivell, T. L., Skinner, M. M., Lazenby, R. & Hublin, J.-J. Methodological considerations for analyzing trabecular architecture: An example from the primate hand. J. Anat. 218, 209–225. https://doi.org/10.1111/j.1469-7580.2010.01314.x (2011).

    Article 
    PubMed 

    Google Scholar 

  • Griffin, N. L. et al. Comparative forefoot trabecular bone architecture in extant hominids. J. Hum. Evol. 59, 202–213. https://doi.org/10.1016/j.jhevol.2010.06.006 (2010).

    Article 
    PubMed 

    Google Scholar 

  • Chirchir, H., Zeininger, A., Nakatsukasa, M., Ketcham, R. A. & Richmond, B. G. Does trabecular bone structure within the metacarpal heads of primates vary with hand posture? C.R. Palevol. 16, 533–544. https://doi.org/10.1016/j.crpv.2016.10.002 (2017).

    Article 

    Google Scholar 

  • Mueller, T. L. et al. Non-invasive bone competence analysis by high-resolution pqct: An in vitro reproducibility study on structural and mechanical properties at the human radius. Bone 44, 364–371. https://doi.org/10.1016/j.bone.2008.10.045 (2009).

    Article 
    PubMed 

    Google Scholar 

  • Sode, M., Burghardt, A. J., Kazakia, G. J., Link, T. M. & Majumdar, S. Regional variations of gender-specific and age-related differences in trabecular bone structure of the distal radius and tibia. Bone 46, 1652–1660. https://doi.org/10.1016/j.bone.2010.02.021 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Rubinacci, A. et al. Comparative high-resolution pqct analysis of femoral neck indicates different bone mass distribution in osteoporosis and osteoarthritis. Osteoporos. Int. 23, 1967–1975. https://doi.org/10.1007/s00198-011-1795-7 (2011).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Stephens, N. B., Kivell, T. L., Pahr, D. H., Hublin, J.-J. & Skinner, M. M. Trabecular bone patterning across the human hand. J. Hum. Evol. 123, 1–23. https://doi.org/10.1016/j.jhevol.2018.05.004 (2018).

    Article 
    PubMed 

    Google Scholar 

  • Du, J. et al. Characterising variability and regional correlations of microstructure and mechanical competence of human tibial trabecular bone: An in-vivo hr-pqct study. Bone 121, 139–148. https://doi.org/10.1016/j.bone.2019.01.013 (2019).

    Article 
    PubMed 

    Google Scholar 

  • Gross, T., Kivell, T. L., Skinner, M. M., Nguyen, N. & Pahr, D. H. A ct-image-based framework for the holistic analysis of cortical and trabecular bone morphology. Palaeontol. Electron. 17, 1–13 (2014).

    Google Scholar 

  • Sylvester, A. D. & Terhune, C. E. Trabecular mapping: Leveraging geometric morphometrics for analyses of trabecular structure. Am. J. Phys. Anthropol. 163, 553–569. https://doi.org/10.1002/ajpa.23231 (2017).

    Article 
    PubMed 

    Google Scholar 

  • Gunz, P. & Mitteroecker, P. Semilandmarks: A method for quantifying curves and surfaces. Hystrix Ital. J. Mammal. 24, 103. https://doi.org/10.4404/hystrix-24.1-6292 (2013).

    Article 

    Google Scholar 

  • Myronenko, A. & Song, X. Point set registration: Coherent point drift. IEEE Trans. Pattern Anal. Mach. Intell. 32, 2262–2275. https://doi.org/10.1109/tpami.2010.46 (2010).

    Article 
    PubMed 

    Google Scholar 

  • Rueckert, D., Frangi, A. F. & Schnabel, J. A. Automatic construction of 3d statistical deformation models using non-rigid registration. In Medical Image Computing and Computer-Assisted Intervention—MICCAI, Vol. 77–84. https://doi.org/10.1007/3-540-45468-3_10 (Springer, 2001).

  • Bijar, A., Rohan, P.-Y., Perrier, P. & Payan, Y. Atlas-based automatic generation of subject-specific finite element tongue meshes. Ann. Biomed. Eng. 44, 16–34. https://doi.org/10.1007/s10439-015-1497-y (2016).

    Article 
    PubMed 

    Google Scholar 

  • Pahr, D. H. & Zysset, P. K. From high-resolution ct data to finite element models: Development of an integrated modular framework. Comput. Methods Biomech. Biomed. Eng. 12, 45–57. https://doi.org/10.1080/10255840802144105 (2009).

    Article 

    Google Scholar 

  • Pahr, D. H. & Zysset, P. K. Influence of boundary conditions on computed apparent elastic properties of cancellous bone. Biomech. Model. Mechanobiol. 7, 463–476. https://doi.org/10.1007/s10237-007-0109-7 (2007).

    Article 
    PubMed 

    Google Scholar 

  • Pahr, D. H. & Zysset, P. K. A comparison of enhanced continuum fe with micro fe models of human vertebral bodies. J. Biomech. 42, 455–462. https://doi.org/10.1016/j.jbiomech.2008.11.028 (2009).

    Article 
    PubMed 

    Google Scholar 

  • Steiner, L., Synek, A. & Pahr, D. H. Femoral strength can be predicted from 2D projections using a 3D statistical deformation and texture model with finite element analysis. Med. Eng. Phys. 93, 72–82. https://doi.org/10.1016/j.medengphy.2021.05.012 (2021).

    Article 
    PubMed 

    Google Scholar 

  • Markley, F. L., Cheng, Y., Crassidis, J. L. & Oshman, Y. Averaging quaternions. J. Guid. Control. Dyn. 30, 1193–1197. https://doi.org/10.2514/1.28949 (2007).

    ADS 
    Article 

    Google Scholar 

  • Taghizadeh, E. et al. Biomechanical role of bone anisotropy estimated on clinical CT scans by image registration. Ann. Biomed. Eng. 44, 2505–2517. https://doi.org/10.1007/s10439-016-1551-4 (2016).

    Article 
    PubMed 

    Google Scholar 

  • Zhu, C., Byrd, R. H., Lu, P. & Nocedal, J. L-bfgs-b: Fortran subroutines for large-scale bound-constrained optimization. ACM Trans. Math. Softw. 23, 550–560. https://doi.org/10.1145/279232.279236 (1997).

    MathSciNet 
    Article 
    MATH 

    Google Scholar 

  • Shewchuk, J. R. What is a good linear element? Interpolation, conditioning, and quality measures. In Eleventh International Meshing Roundtable (Ithaca, New York), 115–126 (2002).

  • Taha, A. A. & Hanbury, A. Metrics for evaluating 3D medical image segmentation: Analysis, selection, and tool. BMC Med. Imaging 15, 29. https://doi.org/10.1186/s12880-015-0068-x (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • MSC Software. Patran 2012 Reference Manual Part 3: Finite Element Modeling (2012).

  • Wang, B., Mei, G. & Xu, N. Method for generating high-quality tetrahedral meshes of geological models by utilizing CGAL. MethodsX 7, 101061. https://doi.org/10.1016/j.mex.2020.101061 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nichols, T. & Hayasaka, S. Controlling the familywise error rate in functional neuroimaging: A comparative review. Stat. Methods Med. Res. 12, 419–446. https://doi.org/10.1191/0962280203sm341ra (2003).

    MathSciNet 
    Article 
    PubMed 
    MATH 

    Google Scholar 

  • Lowekamp, B. C., Chen, D. T., Ibáñez, L. & Blezek, D. The design of SimpleITK. Front. Neuroinform. 7, 45. https://doi.org/10.3389/fninf.2013.00045 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • The CGAL Project. CGAL User and Reference Manual 4th edn. (CGAL Editorial Board, 2017).

    Google Scholar 

  • Virtanen, P. et al. SciPy 1.0: Fundamental algorithms for scientific computing in python. Nat. Methods 17, 261–272. https://doi.org/10.1038/s41592-019-0686-2 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Taghizadeh, E., Chandran, V., Reyes, M., Zysset, P. & Büchler, P. Statistical analysis of the inter-individual variations of the bone shape, volume fraction and fabric and their correlations in the proximal femur. Bone 103, 252–261. https://doi.org/10.1016/j.bone.2017.07.012 (2017).

    Article 
    PubMed 

    Google Scholar 

  • Marangalou, J. H., Ito, K., Taddei, F. & van Rietbergen, B. Inter-individual variability of bone density and morphology distribution in the proximal femur and t12 vertebra. Bone 60, 213–220. https://doi.org/10.1016/j.bone.2013.12.019 (2014).

    Article 

    Google Scholar 

  • Joshi, A. A., Leahy, R. M., Badawi, R. D. & Chaudhari, A. J. Registration-based morphometry for shape analysis of the bones of the human wrist. IEEE Trans. Med. Imaging 35, 416–426. https://doi.org/10.1109/TMI.2015.2476817 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Burkhart, T. A., Andrews, D. M. & Dunning, C. E. Finite element modeling mesh quality, energy balance and validation methods: A review with recommendations associated with the modeling of bone tissue. J. Biomech. 46, 1477–1488. https://doi.org/10.1016/j.jbiomech.2013.03.022 (2013).

    Article 
    PubMed 

    Google Scholar 

  • Grassi, L. et al. Evaluation of the generality and accuracy of a new mesh morphing procedure for the human femur. Med. Eng. Phys. 33, 112–120. https://doi.org/10.1016/j.medengphy.2010.09.014 (2011).

    Article 
    PubMed 

    Google Scholar 

  • Rueckert, D. & Aljabar, P. Non-rigid registration using free-form deformations. In Handbook of Biomedical Imaging (eds Paragios, N. et al.) 277–294 (Springer, 2015).

    Google Scholar 

  • Yu, W., Tannast, M. & Zheng, G. Non-rigid free-form 2d–3d registration using a b-spline-based statistical deformation model. Pattern Recogn. 63, 689–699. https://doi.org/10.1016/j.patcog.2016.09.036 (2017).

    ADS 
    Article 

    Google Scholar 

  • Rohlfing, T., Brandt, R., Maurer, C. & Menzel, R. Bee brains, B-splines and computational democracy: Generating an average shape atlas. In Proc. IEEE Workshop on Mathematical Methods in Biomedical Image Analysis (MMBIA 2001), 187–194. https://doi.org/10.1109/MMBIA.2001.991733 (2001).

  • Spoor, F., Jeffery, N. & Zonneveld, F. Development, Growth and Evolution: Implications for the Study of the Hominid Skeleton, Chap. Imaging Skeletal Growth and Evolution. Linnean Society Symposium Series, 1 edn, 123–162 (Academic Press, 2000).

  • Bishop, P. J., Clemente, C. J., Hocknull, S. A., Barrett, R. S. & Lloyd, D. G. The effects of cracks on the quantification of the cancellous bone fabric tensor in fossil and archaeological specimens: A simulation study. J. Anat. 230, 461–470. https://doi.org/10.1111/joa.12569 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Worsley, K., Andermann, M., Koulis, T., MacDonald, D. & Evans, A. Detecting changes in nonisotropic images. Hum. Brain Mapp. 8, 98–101 (1999).

    CAS 
    Article 

    Google Scholar 

  • Adler, R. J., Bartz, K., Kou, S. C. & Monod, A. Estimating Thresholding Levels for Random Fields via Euler Characteristics, Vol. 1704, 08562 (2017).