Skip to main content

Modeling the effect of brain growth on cranial bones using finite-element analysis and geometric morphometrics

Surgical and Radiologic Anatomy volume 42, pages 741–748 (2020)Cite this article

Abstract

Purpose

Brain expansion during ontogeny has been identified as a key factor for explaining the growth pattern of neurocranial bones. However, the dynamics of this relation are only partially understood and a detailed characterization of integrated morphological changes of the brain and the neurocranium along ontogeny is still lacking. The aim of this study was to model the effect of brain growth on cranial bones by means of finite-element analysis (FEA) and geometric morphometric techniques.

Methods

First, we described the postnatal changes in brain size and shape by digitizing coordinates of 3D semilandmarks on cranial endocasts, as a proxy of brain, segmented from CT-scans of an ontogenetic sample. Then, two scenarios of brain growth were simulated: one in which brain volume increases with the same magnitude in all directions, and other that includes the information on the relative expansion of brain regions obtained from morphometric analysis.

Results

Results indicate that in the first model, in which a uniform pressure is applied, the largest displacements were localized in the sutures, especially in the anterior and posterior fontanels, as well as the metopic suture. When information of brain relative growth was introduced into the model, displacements were also concentrated in the lambda region although the values along both sides of the neurocranium (parietal and temporal bones) were larger than under the first scenario.

Conclusion

In sum, we propose a realistic approach to the use of FEA based on morphometric data that offered different results to more simplified models.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Aldridge K, Kane AA, Marsh JL et al (2005) Brain morphology in nonsyndromic unicoronal craniosynostosis. Anat Rec A Discov Mol Cell Evol Biol 285:690–698. https://doi.org/10.1002/ar.a.20201

    Article  PubMed  Google Scholar 

  2. Bastir M, Rosas A, Stringer C et al (2010) Effects of brain and facial size on basicranial form in human and primate evolution. J Hum Evol 58:424–431. https://doi.org/10.1016/j.jhevol.2010.03.001

    Article  PubMed  Google Scholar 

  3. Bienvenu T, Guy F, Coudyzer W et al (2011) Assessing endocranial variations in great apes and humans using 3D data from virtual endocasts. Am J Phys Anthropol 145:231–246. https://doi.org/10.1002/ajpa.21488

    Article  PubMed  Google Scholar 

  4. Borghi A, Rodriguez-Florez N, Rodgers W et al (2018) Spring assisted cranioplasty: a patient specific computational model. Med Eng Phys 53:58–65. https://doi.org/10.1016/j.medengphy.2018.01.001

    Article  PubMed  Google Scholar 

  5. Bruner E (2018) The brain, the braincase, and the morphospace. In: Bruner E (ed) Digital endocasts. Springer Japan, Tokyo, pp 93–114

    Chapter  Google Scholar 

  6. Buikstra JA, Ubelaker DH (1994) Standards for data collection of human remains. Arkansas Archeological Survey, Fayetteville

    Google Scholar 

  7. Courchesne E, Chisum HJ, Townsend J et al (2000) Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. Radiology 216:672–682. https://doi.org/10.1148/radiology.216.3.r00au37672

    CAS  Article  PubMed  Google Scholar 

  8. Fedorov A, Beichel R, Kalpathy-Cramer J et al (2012) 3D Slicer as an image computing platform for the quantitative imaging network. Magn Reson Imaging 30:1323–1341. https://doi.org/10.1016/j.mri.2012.05.001

    Article  PubMed  PubMed Central  Google Scholar 

  9. Gunz P, Neubauer S, Golovanova L et al (2012) A uniquely modern human pattern of endocranial development. Insights from a new cranial reconstruction of the Neandertal newborn from Mezmaiskaya. J Hum Evol 62:300–313. https://doi.org/10.1016/j.jhevol.2011.11.013

    Article  PubMed  Google Scholar 

  10. Jin J, Shahbazi S, Lloyd J et al (2014) Hybrid simulation of brain–skull growth. Simulation 90:3–10. https://doi.org/10.1177/0037549713516691

    Article  Google Scholar 

  11. Li Z, Hu J, Reed MP et al (2011) Development, validation, and application of a parametric pediatric head finite element model for impact simulations. Ann Biomed Eng 39:2984–2997. https://doi.org/10.1007/s10439-011-0409-z

    Article  PubMed  Google Scholar 

  12. Libby J, Marghoub A, Johnson D et al (2017) Modelling human skull growth: a validated computational model. J R Soc Interface 14:20170202. https://doi.org/10.1098/rsif.2017.0202

    Article  PubMed  PubMed Central  Google Scholar 

  13. Lieberman DE (2011) The evolution of human head. Harvard University Press, Massachusetts

    Book  Google Scholar 

  14. Likus W, Bajor G, Gruszczyńska K et al (2014) Cephalic index in the first three years of life: study of children with normal brain development based on computed tomography. Sci World J 2014:1–6. https://doi.org/10.1155/2014/502836

    Article  Google Scholar 

  15. Malde O, Libby J, Moazen M (2019) An overview of modelling craniosynostosis using the finite element method. Mol Syndromol 10:74–82. https://doi.org/10.1159/000490833

    Article  PubMed  Google Scholar 

  16. Marcé-Nogué J, Fortuni Terricabras J, Gil Espert L, Sánchez Romero M (2015) Improving mesh generation in finite element analysis for functional morphology approaches. Spanish J Palaeontol 30:117–132

    Article  Google Scholar 

  17. Margulies SS, Thibault KL (2000) Infant skull and suture properties: Measurements and implications for mechanisms of pediatric brain injury. J Biomech Eng 122:364–371. https://doi.org/10.1115/1.1287160

    CAS  Article  PubMed  Google Scholar 

  18. Moffett EA, Aldridge K (2014) Size of the anterior fontanelle: three-Dimensional measurement of a key trait in human evolution. Anat Rec 297:234–239. https://doi.org/10.1002/ar.22830

    Article  Google Scholar 

  19. Moss ML, Young RW (1960) A functional approach to craniology. Am J Phys Anthropol 18:281–292. https://doi.org/10.1002/ajpa.1330180406

    CAS  Article  PubMed  Google Scholar 

  20. Nagasao T, Miyamoto J, Uchikawa Y et al (2010) A biomechanical study on the effect of premature fusion of the frontosphenoidal suture on orbit asymmetry in unilateral coronal synostosis. Cleft Palate Craniofac J 47:82–91. https://doi.org/10.1597/08-164.1

    Article  PubMed  Google Scholar 

  21. Neubauer S, Gunz P, Hublin J-J (2009) The pattern of endocranial ontogenetic shape changes in humans. J Anat 215:240–255. https://doi.org/10.1111/j.1469-7580.2009.01106.x

    Article  PubMed  PubMed Central  Google Scholar 

  22. Opperman LA (2000) Cranial sutures as intramembranous bone growth sites. Dev Dyn 219:472–485. https://doi.org/10.1002/1097-0177(2000)9999:9999%3c:AID-DVDY1073%3e3.0.CO;2-F

    CAS  Article  PubMed  Google Scholar 

  23. Percival CJ, Devine J, Darwin BC et al (2019) The effect of automated landmark identification on morphometric analyses. J Anat 234:917–935. https://doi.org/10.1111/joa.12973

    Article  PubMed  PubMed Central  Google Scholar 

  24. Richtsmeier JT, Flaherty K (2014) Hand in glove: brain and skull in development and dysmorphogenesis. Acta Neuropathol 125:469–489. https://doi.org/10.1007/s00401-013-1104-y.Hand

    Article  Google Scholar 

  25. Schlager S (2017) Morpho and Rvcg—shape analysis in R. In: Zheng G (ed) Statistical shape and deformation analysis. Academic Press, San Diego, pp 217–256

    Chapter  Google Scholar 

  26. Shapiro D, Richtsmeier JT (1997) Brief communication: a sample of pediatric skulls available for study. Am J Phys Anthropol 103:415–416. https://doi.org/10.1002/(SICI)1096-8644(199707)103:3%3c415:AID-AJPA11%3e3.0.CO;2-3

    CAS  Article  PubMed  Google Scholar 

  27. Virchow R (1851) Uber den Cretinismus, namentlich in franken und ueber pathologische schadelformen. Ver Physikalisch Med Ges Wurzburg 2:230

    Google Scholar 

  28. Weickenmeier J, Fischer C, Carter D et al (2017) Dimensional, geometrical, and physical constraints in skull growth. Phys Rev Lett 118:248101. https://doi.org/10.1103/PhysRevLett.118.248101

    Article  PubMed  Google Scholar 

  29. Wolański W, Larysz D, Gzik M, Kawlewska E (2013) Modeling and biomechanical analysis of craniosynostosis correction with the use of finite element method. Int J Numer Method Biomed Eng 29:916–925. https://doi.org/10.1002/cnm.2506

    Article  PubMed  Google Scholar 

  30. Zhang G, Tan H, Qian X et al (2016) A Systematic approach to predicting spring force for sagittal craniosynostosis surgery. J Craniofac Surg 27:636–643. https://doi.org/10.1097/SCS.0000000000002590

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. Joan Richtsmeier for image sharing. This work was funded by the Universidad Nacional de La Plata PI 792 and 787), the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 0729) and the Agencia Nacional para la Promoción de la Ciencia y Tecnología (ANPCyT, PICT 2134 and PICT 1810). J.M.-N. was supported by the DFG, German Research Foundation, KA 1525/9-2 and acknowledges the CERCA programme (Generalitat de Catalunya).

Author information

Affiliations

  1. Consejo Nacional de Investigaciones Científicas y Tecnológicas, La Plata, Argentina

    Jimena Barbeito-Andrés, Valeria Bernal & Paula N. Gonzalez

  2. ENyS, Estudios en Neurociencias y Sistemas Complejos, CONICET-HEC-UNAJ, Buenos Aires, Argentina

    Jimena Barbeito-Andrés & Paula N. Gonzalez

  3. Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, Argentina

    Noelia Bonfili & Valeria Bernal

  4. Centrum für Naturkunde, University of Hamburg, Martin-Luter-King-Platz 3, 20146, Hamburg, Germany

    Jordi Marcé Nogué

  5. Institut Català de Paleontologia M. Crusafont, Universitat Autónoma de Barcelona, Cerdanyola del Vallès, 08193, Barcelona, Spain

    Jordi Marcé Nogué

Authors
  1. Jimena Barbeito-Andrés
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Noelia Bonfili
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jordi Marcé Nogué
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Valeria Bernal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paula N. Gonzalez
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JB-A project development, data analysis (geometric morphometrics), manuscript writing. NB data collection (endocasts’ reconstructions and digitization of landmarks and semilandmarks). JMN data analysis (finite-element analysis). VB project development, manuscript writing. PNG project development and supervision, data analysis (geometric morphometrics), manuscript writing.

Corresponding author

Correspondence to Paula N. Gonzalez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 21 kb)

Supplementary file2 (PLY 18027 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Barbeito-Andrés, J., Bonfili, N., Nogué, J.M. et al. Modeling the effect of brain growth on cranial bones using finite-element analysis and geometric morphometrics. Surg Radiol Anat 42, 741–748 (2020). https://doi.org/10.1007/s00276-020-02466-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00276-020-02466-y

Keywords

  • Computed tomography
  • Endocast
  • Shape variation
  • Neurocranium