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The biomechanics of chewing and suckling in the infant: A potential mechanism for physiologic metopic suture closure

Author

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  • Pranav N Haravu
  • Miguel Gonzalez
  • Shelby L Nathan
  • Callum F Ross
  • Olga Panagiotopoulou
  • Russell R Reid

Abstract

Craniosynostosis is a condition with neurologic and aesthetic sequelae requiring invasive surgery. Understanding its pathobiology requires familiarity with the processes underlying physiologic suture closure. Animal studies have shown that cyclical strain from chewing and suckling influences the closure of cranial vault sutures, especially the metopic, an important locus of craniosynostosis. However, there are no human data correlating strain patterns during chewing and suckling with the physiologically early closure pattern of the metopic suture. Furthermore, differences in craniofacial morphology make it challenging to directly extrapolate animal findings to humans. Eight finite-element analysis (FEA) models were built from craniofacial computer tomography (CT) scans at varying stages of metopic suture closure, including two with isolated non-syndromic metopic craniosynostosis. Muscle forces acting on the cranium during chewing and suckling were simulated using subject-specific jaw muscle cross-sectional areas. Chewing and suckling induced tension at the metopic and sagittal sutures, and compressed the coronal, lambdoid, and squamous sutures. Relative to other cranial vault sutures, the metopic suture experienced larger magnitudes of axial strain across the suture and a lower magnitude of shear strain. Strain across the metopic suture decreased during suture closure, but other sutures were unaffected. Strain patterns along the metopic suture mirrored the anterior to posterior sequence of closure: strain magnitudes were highest at the glabella and decreased posteriorly, with minima at the nasion and the anterior fontanelle. In models of physiologic suture closure, increased degree of metopic suture closure correlated with higher maximum principal strains across the frontal bone and mid-face, a strain regime not observed in models of severe metopic craniosynostosis. In summary, our work provides human evidence that bone strain patterns from chewing and suckling correlate with the physiologically early closure pattern of the metopic suture, and that deviations from physiologic strain regimes may contribute to clinically observed craniofacial dysmorphism.Author summary: Developing infant skulls have multiple “sutures”, which are gaps between the different bones of skull. The sutures fuse together and close at different times, and the proper sequence and timing of closure is important to allow the skull and brain to grow. If the sutures fuse together too early, children can develop a condition called craniosynostosis, which requires intensive surgical intervention to fix. However, understanding the pathologic state necessitates understanding what drives the timing of suture closure in the healthy state. There is limited human data investigating the role of mechanical forces in that process. Our work shows that chewing and suckling in infants causes unique strain patterns conducive to closure across the metopic suture (the suture that closes first in normal development), the first suture to close in normal development. Specifically, the metopic suture experienced larger amounts of compressive and tensile strain with less shearing strain i.e., sideways movement. Along the metopic suture, this strain pattern was most prominent in regions that close first, and least prominent in regions that close last. In short, our work suggests that the forces generated from chewing and suckling may be partially responsible for the timing of metopic suture closure.

Suggested Citation

  • Pranav N Haravu & Miguel Gonzalez & Shelby L Nathan & Callum F Ross & Olga Panagiotopoulou & Russell R Reid, 2023. "The biomechanics of chewing and suckling in the infant: A potential mechanism for physiologic metopic suture closure," PLOS Computational Biology, Public Library of Science, vol. 19(6), pages 1-26, June.
  • Handle: RePEc:plo:pcbi00:1011227
    DOI: 10.1371/journal.pcbi.1011227
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