The ontogeny of human fetal trabecular bone architecture occurs in a limb-specific manner.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
31 Aug 2024
Historique:
received: 05 12 2023
accepted: 12 07 2024
medline: 1 9 2024
pubmed: 1 9 2024
entrez: 31 8 2024
Statut: epublish

Résumé

Gestational growth and development of bone is an understudied process compared to soft tissues and has implications for lifelong health. This study investigated growth and development of human fetal limb bone trabecular architecture using 3D digital histomorphometry of microcomputed tomography data from the femora and humeri of 35 skeletons (17 female and 18 male) with gestational ages between 4 and 9 months. Ontogenetic data revealed: (i) fetal trabecular architecture is similar between sexes; (ii) the proximal femoral metaphysis is physically larger, with thicker trabeculae and greater bone volume fraction relative to the humerus, but other aspects of trabecular architecture are similar between the bones; (iii) between 4 and 9 months gestation there is no apparent sexual or limb dimorphism in patterns of growth, but the size of the humerus and femur diverges early in development. Additionally, both bones exhibit significant increases in mean trabecular thickness (and for the femur alone, bone volume fraction) but minimal trabecular reorganisation (i.e., no significant changes in degree of anisotropy, connectivity density, or fractal dimension). Overall, these data suggest that in contrast to data from the axial skeleton, prenatal growth of long bones in the limbs is characterised by size increase, without major reorganizational changes in trabecular architecture.

Identifiants

pubmed: 39217219
doi: 10.1038/s41598-024-67566-w
pii: 10.1038/s41598-024-67566-w
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

20261

Informations de copyright

© 2024. The Author(s).

Références

Rauch, F. & Schoenau, E. The developing bone: slave or master of its cells and molecules?. Pediatr. Res. 50, 309–314. https://doi.org/10.1203/00006450-200109000-00003 (2001).
doi: 10.1203/00006450-200109000-00003 pubmed: 11518815
Berendsen, A. D. & Olsen, B. R. Bone development. Bone 80, 14–18. https://doi.org/10.1016/j.bone.2015.04.035 (2015).
doi: 10.1016/j.bone.2015.04.035 pubmed: 26453494 pmcid: 4602167
Salhotra, A., Shah, H. N., Levi, B. & Longaker, M. T. Mechanisms of bone development and repair. Nat. Rev. Mol. Cell Biol. 21, 696–711. https://doi.org/10.1038/s41580-020-00279-w (2020).
doi: 10.1038/s41580-020-00279-w pubmed: 32901139 pmcid: 7699981
Godfrey, K. M., Inskip, H. M. & Hanson, M. A. The long-term effects of prenatal development on growth and metabolism. Semin. Reprod. Med. 29, 257–265. https://doi.org/10.1055/s-0031-1275518 (2011).
doi: 10.1055/s-0031-1275518 pubmed: 21769765 pmcid: 3685133
Kwon, E. J. & Kim, Y. J. What is fetal programming? A lifetime health is under the control of in utero health. Obstet. Gynecol. Sci. 60, 506–519. https://doi.org/10.5468/ogs.2017.60.6.506 (2017).
doi: 10.5468/ogs.2017.60.6.506 pubmed: 29184858 pmcid: 5694724
Xia, J. W. et al. Both indirect maternal and direct fetal genetic effects reflect the observational relationship between higher birth weight and lower adult bone mass. BMC Med. 20, 361. https://doi.org/10.1186/s12916-022-02531-w (2022).
doi: 10.1186/s12916-022-02531-w pubmed: 36192722 pmcid: 9531399
Done, S. L. Fetal and neonatal bone health: Update on bone growth and manifestations in health and disease. Pediatr. Radiol. 42(Suppl 1), S158-176. https://doi.org/10.1007/s00247-011-2251-8 (2012).
doi: 10.1007/s00247-011-2251-8 pubmed: 22395728
Yu, X. H., Wei, Y. Y., Zeng, P. & Lei, S. F. Birth weight is positively associated with adult osteoporosis risk: Observational and Mendelian randomization studies. J. Bone Miner. Res. 36, 1469–1480. https://doi.org/10.1002/jbmr.4316 (2021).
doi: 10.1002/jbmr.4316 pubmed: 34105796
Ryan, T. M. & Krovitz, G. E. Trabecular bone ontogeny in the human proximal femur. J. Hum. Evol. 51, 591–602. https://doi.org/10.1016/j.jhevol.2006.06.004 (2006).
doi: 10.1016/j.jhevol.2006.06.004 pubmed: 16963108
Gosman, J. H. & Ketcham, R. A. Patterns in ontogeny of human trabecular bone from SunWatch Village in the Prehistoric Ohio Valley: general features of microarchitectural change. Am. J. Phys. Anthropol. 138, 318–332. https://doi.org/10.1002/ajpa.20931 (2009).
doi: 10.1002/ajpa.20931 pubmed: 18785633
Milovanovic, P. et al. Region-dependent patterns of trabecular bone growth in the human proximal femur: A study of 3D bone microarchitecture from early postnatal to late childhood period. Am. J. Phys. Anthropol. 164, 281–291. https://doi.org/10.1002/ajpa.23268 (2017).
doi: 10.1002/ajpa.23268 pubmed: 28631293
Cunningham, C. A. & Black, S. M. Anticipating bipedalism: Trabecular organization in the newborn ilium. J. Anatom. 214, 817–829. https://doi.org/10.1111/j.1469-7580.2009.01073.x (2009).
doi: 10.1111/j.1469-7580.2009.01073.x
Reissis, D. & Abel, R. L. Development of fetal trabecular micro-architecture in the humerus and femur. J. Anatom. 220, 496–503. https://doi.org/10.1111/j.1469-7580.2012.01487.x (2012).
doi: 10.1111/j.1469-7580.2012.01487.x
Acquaah, F., Robson Brown, K. A., Ahmed, F., Jeffery, N. & Abel, R. L. Early Trabecular Development in Human Vertebrae: Overproduction, Constructive Regression, and Refinement. Front. Endocrinol. 6, 67. https://doi.org/10.3389/fendo.2015.00067 (2015).
doi: 10.3389/fendo.2015.00067
Gray, D. J. & Gardner, E. The prenatal development of the human humerus. Am. J. Anat. 124, 431–445. https://doi.org/10.1002/aja.1001240403 (1969).
doi: 10.1002/aja.1001240403 pubmed: 5774654
Burkus, J. K. & Ogden, J. A. Development of the distal femoral epiphysis: A microscopic morphological investigation of the zone of Ranvier. J. Pediatr. Orthop. 4, 661–668. https://doi.org/10.1097/01241398-198411000-00001 (1984).
doi: 10.1097/01241398-198411000-00001 pubmed: 6511891
Cunningham, C. L., Scheuer, L. & Black, S. Developmental Juvenile Osteology (Academic Press, 2016).
Glorieux, F. H., Salle, B. L., Travers, R. & Audra, P. H. Dynamic histomorphometric evaluation of human fetal bone formation. Bone 12, 377–381 (1991).
doi: 10.1016/8756-3282(91)90025-E pubmed: 1797052
Salle, B. L., Rauch, F., Travers, R., Bouvier, R. & Glorieux, F. H. Human fetal bone development: Histomorphometric evaluation of the proximal femoral metaphysis. Bone 30, 823–828. https://doi.org/10.1016/s8756-3282(02)00724-x (2002).
doi: 10.1016/s8756-3282(02)00724-x pubmed: 12052448
Muller, R., Hahn, M., Vogel, M., Delling, G. & Ruegsegger, P. Morphometric analysis of noninvasively assessed bone biopsies: Comparison of high-resolution computed tomography and histologic sections. Bone 18, 215–220 (1996).
doi: 10.1016/8756-3282(95)00489-0 pubmed: 8703575
Hart, N. H. et al. Mechanical basis of bone strength: Influence of bone material, bone structure and muscle action. J. Musculoskelet. Neuronal Interact. 17, 114–139 (2017).
pubmed: 28860414 pmcid: 5601257
van der Linden, J. C., Homminga, J., Verhaar, J. A. & Weinans, H. Mechanical consequences of bone loss in cancellous bone. J. Bone Miner. Res. 16, 457–465. https://doi.org/10.1359/jbmr.2001.16.3.457 (2001).
doi: 10.1359/jbmr.2001.16.3.457 pubmed: 11277263
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).
doi: 10.1111/joa.12446 pubmed: 26879841 pmcid: 4804137
Cooper, D. M., Turinsky, A. L., Sensen, C. W. & Hallgrimsson, B. Quantitative 3D analysis of the canal network in cortical bone by micro-computed tomography. Anat. Rec. B New Anat. 274, 169–179. https://doi.org/10.1002/ar.b.10024 (2003).
doi: 10.1002/ar.b.10024 pubmed: 12964207
Nuzzo, S. et al. Microarchitectural and physical changes during fetal growth in human vertebral bone. J. Bone Miner. Res. 18, 760–768. https://doi.org/10.1359/jbmr.2003.18.4.760 (2003).
doi: 10.1359/jbmr.2003.18.4.760 pubmed: 12674337
Saers, J. P. P., Ryan, T. M. & Stock, J. T. Baby steps towards linking calcaneal trabecular bone ontogeny and the development of bipedal human gait. J. Anatom. 236, 474–492. https://doi.org/10.1111/joa.13120 (2020).
doi: 10.1111/joa.13120
Chevalier, T. et al. Early ontogeny of humeral trabecular bone in Neandertals and recent modern humans. J. Hum. Evol. 154, 102968. https://doi.org/10.1016/j.jhevol.2021.102968 (2021).
doi: 10.1016/j.jhevol.2021.102968 pubmed: 33774376
Saers, J. P. P., Gordon, A. D., Ryan, T. M. & Stock, J. T. Trabecular bone ontogeny tracks neural development and life history among humans and non-human primates. Proc. Natl. Acad. Sci. USA 119, e2208772119. https://doi.org/10.1073/pnas.2208772119 (2022).
doi: 10.1073/pnas.2208772119 pubmed: 36459637 pmcid: 9894110
Galjaard, S. et al. Sex differences in fetal growth and immediate birth outcomes in a low-risk Caucasian population. Biol. Sex Differ. 10, 48. https://doi.org/10.1186/s13293-019-0261-7 (2019).
doi: 10.1186/s13293-019-0261-7 pubmed: 31500671 pmcid: 6734449
Broere-Brown, Z. A. et al. Sex-specific differences in fetal and infant growth patterns: A prospective population-based cohort study. Biol. Sex Differ. 7, 65. https://doi.org/10.1186/s13293-016-0119-1 (2016).
doi: 10.1186/s13293-016-0119-1 pubmed: 27980713 pmcid: 5135770
Rodríguez, J. I., Palacios, J. & Rodríguez, S. Transverse bone growth and cortical bone mass in the human prenatal period. Biol. Neonate 62, 23–31. https://doi.org/10.1159/000243849 (1992).
doi: 10.1159/000243849 pubmed: 1391272
Scherf, H. & Tilgner, R. A new high-resolution computed tomography (CT) segmentation method for trabecular bone architectural analysis. Am. J. Phys. Anthropol. 140, 39–51. https://doi.org/10.1002/ajpa.21033 (2009).
doi: 10.1002/ajpa.21033 pubmed: 19280676
Cheuk, K. Y. et al. Sexual dimorphism in cortical and trabecular bone microstructure appears during puberty in Chinese children. J. Bone Miner. Res. 33, 1948–1955. https://doi.org/10.1002/jbmr.3551 (2018).
doi: 10.1002/jbmr.3551 pubmed: 30001459
Chen, H., Zhou, X., Shoumura, S., Emura, S. & Bunai, Y. Age- and gender-dependent changes in three-dimensional microstructure of cortical and trabecular bone at the human femoral neck. Osteoporosis Int. 21, 627–636. https://doi.org/10.1007/s00198-009-0993-z (2010).
doi: 10.1007/s00198-009-0993-z
Kindler, J. M., Lewis, R. D. & Hamrick, M. W. Skeletal muscle and pediatric bone development. Curr. Opin. Endocrinol. Diabetes Obes. 22, 467–474. https://doi.org/10.1097/MED.0000000000000201 (2015).
doi: 10.1097/MED.0000000000000201 pubmed: 26414082
Ryan, B. A. & Kovacs, C. S. Calciotropic and phosphotropic hormones in fetal and neonatal bone development. Semin. Fetal Neonatal Med. 25, 101062. https://doi.org/10.1016/j.siny.2019.101062 (2020).
doi: 10.1016/j.siny.2019.101062 pubmed: 31786156
Christine-Knickmeyer, R. & Baron-Cohen, S. Fetal testosterone and sex differences. Early Hum. Dev. 82, 755–760. https://doi.org/10.1016/j.earlhumdev.2006.09.014 (2006).
doi: 10.1016/j.earlhumdev.2006.09.014 pubmed: 17084045
de Zegher, F., Devlieger, H. & Eeckels, R. Fetal growth: Boys before girls. Hormone Res. 51, 258–259. https://doi.org/10.1159/000023382 (1999).
doi: 10.1159/000023382 pubmed: 10559673
Kallak, T. K. et al. Maternal and female fetal testosterone levels are associated with maternal age and gestational weight gain. Eur. J. Endocrinol. 177, 379–388. https://doi.org/10.1530/EJE-17-0207 (2017).
doi: 10.1530/EJE-17-0207 pubmed: 28705923 pmcid: 5597951
Kovacs, C. S. Bone development and mineral homeostasis in the fetus and neonate: Roles of the calciotropic and phosphotropic hormones. Physiol. Rev. 94, 1143–1218. https://doi.org/10.1152/physrev.00014.2014 (2014).
doi: 10.1152/physrev.00014.2014 pubmed: 25287862
Smith, E. P. et al. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N. Engl. J. Med. 331, 1056–1061. https://doi.org/10.1056/NEJM199410203311604 (1994).
doi: 10.1056/NEJM199410203311604 pubmed: 8090165
Miao, D., He, B., Karaplis, A. C. & Goltzman, D. Parathyroid hormone is essential for normal fetal bone formation. J. Clin. Invest. 109, 1173–1182. https://doi.org/10.1172/jci0214817 (2002).
doi: 10.1172/jci0214817 pubmed: 11994406 pmcid: 150965
Almli, C. R., Ball, R. H. & Wheeler, M. E. Human fetal and neonatal movement patterns: Gender differences and fetal-to-neonatal continuity. Dev. Psychobiol. 38, 252–273 (2001).
doi: 10.1002/dev.1019 pubmed: 11319731
Macho, G. A., Abel, R. L. & Schutkowski, H. Age changes in bone microstructure: do they occur uniformly?. Int. J. Osteoarchaeol. 15, 421–430. https://doi.org/10.1002/oa.797 (2005).
doi: 10.1002/oa.797
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).
doi: 10.1016/j.bone.2011.08.020 pubmed: 21893221
Skerry, T. M. One mechanostat or many? Modifications of the site-specific response of bone to mechanical loading by nature and nurture. J. Musculoskel. Neuron. Interact. 6, 122–127 (2006).
Iwaniec, U. T. & Turner, R. T. Influence of body weight on bone mass, architecture and turnover. J. Endocrinol. 230, R115-130. https://doi.org/10.1530/JOE-16-0089 (2016).
doi: 10.1530/JOE-16-0089 pubmed: 27352896 pmcid: 4980254
Frost, H. M. A 2003 update of bone physiology and Wolff’s Law for clinicians. Angle Orthodont. 74, 3–15. https://doi.org/10.1043/0003-3219(2004)074%3c0003:AUOBPA%3e2.0.CO;2 (2004).
doi: 10.1043/0003-3219(2004)074<0003:AUOBPA>2.0.CO;2 pubmed: 15038485
Ryan, T. M., Raichlen, D. A. & Gosman, J. H. Structural and mechanical changes in trabecular bone during early development in the human femur and humerus. In Building Bones: Bone Formation and Development in Anthropology (eds Percival, C. J. & Richtsmeier, J. T.) 281–302 (Cambridge University Press, 2017). https://doi.org/10.1017/9781316388907.013 .
doi: 10.1017/9781316388907.013
Carter, D. H., Sloan, P. & Aaron, J. E. Trabecular generation de novo: A morphological and immunohistochemical study of primary ossification in the human femoral anlagen. Anatom. Embryol. 186, 229–239 (1992).
doi: 10.1007/BF00174144
Shea, C. A., Rolfe, R. A. & Murphy, P. The importance of foetal movement for co-ordinated cartilage and bone development in utero: Clinical consequences and potential for therapy. Bone Jnt. Res. 4, 105–116. https://doi.org/10.1302/2046-3758.47.2000387 (2015).
doi: 10.1302/2046-3758.47.2000387
Carter, D. R., van der Meulen, M. C. H. & Beaupré, G. S. Mechanical factors in bone growth and development. Bone 18, 5S-10S (1996).
doi: 10.1016/8756-3282(95)00373-8 pubmed: 8717541
Sun, Y., Yuan, Y., Wu, W., Lei, L. & Zhang, L. The effects of locomotion on bone marrow mesenchymal stem cell fate: Insight into mechanical regulation and bone formation. Cell Biosci. 11, 88. https://doi.org/10.1186/s13578-021-00601-9 (2021).
doi: 10.1186/s13578-021-00601-9 pubmed: 34001272 pmcid: 8130302
Herberg, S. et al. Combinatorial morphogenetic and mechanical cues to mimic bone development for defect repair. Sci. Adv. https://doi.org/10.1126/sciadv.aax2476 (2019).
doi: 10.1126/sciadv.aax2476 pubmed: 31489377 pmcid: 6713501
de Vries, J. I. & Fong, B. F. Normal fetal motility: An overview. Ultrasound Obstetr. Gynecol. 27, 701–711. https://doi.org/10.1002/uog.2740 (2006).
doi: 10.1002/uog.2740
Luchinger, A. B., Hadders-Algra, M., van Kan, C. M. & de Vries, J. I. Fetal onset of general movements. Pediatr. Res. 63, 191–195. https://doi.org/10.1203/PDR.0b013e31815ed03e (2008).
doi: 10.1203/PDR.0b013e31815ed03e pubmed: 18091359
Rodríguez, J. I., Garcia-Alix, A., Palacios, J. & Paniagua, R. Changes in the long bones due to fetal immobility caused by neuromuscular disease: A radiographic and histological study. J. Bone Jnt. Surg. 70, 1052–1060 (1988).
doi: 10.2106/00004623-198870070-00014
Ireland, A. et al. Breech presentation is associated with lower bone mass and area: Findings from the Southampton Women’s Survey. Osteoporos. Int. 29, 2275–2281. https://doi.org/10.1007/s00198-018-4626-2 (2018).
doi: 10.1007/s00198-018-4626-2 pubmed: 30003305 pmcid: 6173302
Verbruggen, S. W. et al. Modeling the biomechanics of fetal movements. Biomech. Model. Mechanobiol. 15, 995–1004. https://doi.org/10.1007/s10237-015-0738-1 (2016).
doi: 10.1007/s10237-015-0738-1 pubmed: 26534772
Land, C. & Schoenau, E. Fetal and postnatal bone development: Reviewing the role of mechanical stimuli and nutrition. Best Pract. Res. Clin. Endocrinol. Metab. 22, 107–118. https://doi.org/10.1016/j.beem.2007.09.005 (2008).
doi: 10.1016/j.beem.2007.09.005 pubmed: 18279783
Ilich, J. Z. & Kerstetter, J. E. Nutrition in bone health revisited: A story beyond calcium. J. Am. Coll. Nutr. 19, 715–737. https://doi.org/10.1080/07315724.2000.10718070 (2000).
doi: 10.1080/07315724.2000.10718070 pubmed: 11194525
Barak, M. M., Sherratt, E. & Lieberman, D. E. Using principal trabecular orientation to differentiate joint loading orientation in the 3rd metacarpal heads of humans and chimpanzees. J. Hum. Evol. 113, 173–182. https://doi.org/10.1016/j.jhevol.2017.08.018 (2017).
doi: 10.1016/j.jhevol.2017.08.018 pubmed: 29054167
Ketcham, R. A. & Ryan, T. M. Quantification and visualization of anisotropy in trabecular bone. J. Microsc. 213, 158–171. https://doi.org/10.1111/j.1365-2818.2004.01277.x (2004).
doi: 10.1111/j.1365-2818.2004.01277.x pubmed: 14731299
Saers, J. P., Cazorla-Bak, Y., Shaw, C. N., Stock, J. T. & Ryan, T. M. Trabecular bone structural variation throughout the human lower limb. J. Hum. Evol. 97, 97–108. https://doi.org/10.1016/j.jhevol.2016.05.012 (2016).
doi: 10.1016/j.jhevol.2016.05.012 pubmed: 27457548
Hammer, A. The structure of the femoral neck: A physical dissection with emphasis on the internal trabecular system. Ann. Anatom. 192, 168–177. https://doi.org/10.1016/j.aanat.2010.02.007 (2010).
doi: 10.1016/j.aanat.2010.02.007
Birnholz, J. C., Stephens, J. C. & Faria, M. Fetal movement patterns: A possible means of defining neurologic developmental milestones in utero. Am. J. Roentgenol. 130, 537–540 (1978).
doi: 10.2214/ajr.130.3.537
Martin, R. B., Burr, D. B., Sharkey, N. A. & Fyhrie, D. P. Skeletal Tissue Mechanics 2nd edn. (Springer, 2015).
doi: 10.1007/978-1-4939-3002-9
Reznikov, N. et al. Inter-trabecular angle: A parameter of trabecular bone architecture in the human proximal femur that reveals underlying topological motifs. Acta Biomater. 44, 65–72. https://doi.org/10.1016/j.actbio.2016.08.040 (2016).
doi: 10.1016/j.actbio.2016.08.040 pubmed: 27554017
Ben-Zvi, Y., Reznikov, N., Shahar, R. & Weiner, S. 3D Architecture of trabecular bone in the pig mandible and femur: Inter-trabecular angle distributions. Front. Mater. https://doi.org/10.3389/fmats.2017.00029 (2017).
doi: 10.3389/fmats.2017.00029
Reznikov, N. et al. Functional adaptation of the calcaneus in historical foot binding. J. Bone Miner. Res. 32, 1915–1925. https://doi.org/10.1002/jbmr.3185 (2017).
doi: 10.1002/jbmr.3185 pubmed: 28561380
Reznikov, N., Liang, H., McKee, M. D. & Piché, N. Technical note: Mapping of trabecular bone anisotropy and volume fraction in 3D using μCT images of the human calcaneus. Am. J. Biol. Anthropol. 177, 566–580. https://doi.org/10.1002/ajpa.24474 (2022).
doi: 10.1002/ajpa.24474
Doube, M. et al. BoneJ: Free and extensible bone image analysis in ImageJ. Bone 47, 1076–1079. https://doi.org/10.1016/j.bone.2010.08.023 (2010).
doi: 10.1016/j.bone.2010.08.023 pubmed: 20817052 pmcid: 3193171
Schindelin, J. et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676–682. https://doi.org/10.1038/nmeth.2019 (2012).
doi: 10.1038/nmeth.2019 pubmed: 22743772
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).
doi: 10.1002/jbmr.141 pubmed: 20533309
Doube, M., Klosowski, M. M., Wiktorowicz-Conroy, A. M., Hutchinson, J. R. & Shefelbine, S. J. Trabecular bone scales allometrically in mammals and birds. Proc. Biol. Sci. 278, 3067–3073. https://doi.org/10.1098/rspb.2011.0069 (2011).
doi: 10.1098/rspb.2011.0069 pubmed: 21389033 pmcid: 3158937
Hildebrand, T. & Ruegsegger, P. A new method for the model-independent assessment of thickness in three-dimensional images. J. Microsc. 185, 67–75. https://doi.org/10.1046/j.1365-2818.1997.1340694.x (1997).
doi: 10.1046/j.1365-2818.1997.1340694.x
Odgaard, A. Three-dimensional methods for quantification of cancellous bone architecture. Bone 20, 315–328 (1997).
doi: 10.1016/S8756-3282(97)00007-0 pubmed: 9108351
Odgaard, A. & Gundersen, H. J. Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 14, 173–182 (1993).
doi: 10.1016/8756-3282(93)90245-6 pubmed: 8334036
Fazzalari, N. L. & Parkinson, I. H. Fractal dimension and architecture of trabecular bone. J. Pathol. 178, 100–105. https://doi.org/10.1002/(SICI)1096-9896(199601)178:1%3c100::AID-PATH429%3e3.0.CO;2-K (1996).
doi: 10.1002/(SICI)1096-9896(199601)178:1<100::AID-PATH429>3.0.CO;2-K pubmed: 8778308
Parkinson, I. & Fazzalari, N. Fractal analysis of trabecular bone: A standardised methodology. Image Anal. Stereol. 19, 45–49 (2000).
doi: 10.5566/ias.v19.p45-49
Hildebrand, T. & Ruegsegger, P. Quantification of bone microarchitecture with the structure model index. Comput. Methods Biomech. Biomed. Eng. 1, 15–23. https://doi.org/10.1080/01495739708936692 (1997).
doi: 10.1080/01495739708936692
Salmon, P. L., Ohlsson, C., Shefelbine, S. J. & Doube, M. Structure model index does not measure rods and plates in trabecular bone. Front. Endocrinol. 6, 162. https://doi.org/10.3389/fendo.2015.00162 (2015).
doi: 10.3389/fendo.2015.00162

Auteurs

Crispin Charles Wiles (CC)

MSk Laboratory, Sir Michael Uren Hub, Department of Surgery and Cancer, Faculty of Medicine, Imperial College London, London, W12 7ED, UK. crispin.wiles@warwick.ac.uk.
Centre for Blast Injury Studies, Department of Bioengineering, Faculty of Engineering, Imperial College London, London, SW7 2AZ, UK. crispin.wiles@warwick.ac.uk.
Warwick Medical School, University of Warwick, Coventry, CV4 8JE, UK. crispin.wiles@warwick.ac.uk.

Sarah Holly Suh (SH)

MSk Laboratory, Sir Michael Uren Hub, Department of Surgery and Cancer, Faculty of Medicine, Imperial College London, London, W12 7ED, UK.

Katharine Robson Brown (KR)

Jean Golding Institute for Data Science, University of Bristol, Bristol, BS8 IUU, UK.
School of Engineering, University of Bristol, Bristol, BS8 1UU, UK.
Department of Mechanical Engineering, University of Bristol, Bristol, BS8 1UB, UK.

Richard Leslie Abel (RL)

MSk Laboratory, Sir Michael Uren Hub, Department of Surgery and Cancer, Faculty of Medicine, Imperial College London, London, W12 7ED, UK.

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