Skip to main content
Log in

Development of Mechanical and Failure Properties in Sheep Cerebral Arteries

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Traumatic brain injury (TBI) is a devastating problem for people of all ages, but the nature of the response to such injury is often different in children than in adults. Cerebral vessel damage and dysfunction are common following TBI, but age-dependent, large-deformation vessel response has not been characterized. Our objective was to investigate the mechanical properties of cerebral arteries as a function of development. Sheep middle cerebral arteries from four age groups (fetal, newborn, juvenile, and adult) were subjected to biaxial loading around physiological conditions and then to failure in the axial direction. Results show little difference among age groups under physiological loading conditions, but response varied significantly with age in response to large axial deformation. Vessels from all age groups reached the same ultimate stretch level, but the amount of stress carried at a given level of stretch increased significantly with age through the developmental period (fetal to juvenile). Our results are the first to identify changes in cerebral vessel response to large deformations with age and may lead to new insights regarding differences in response to TBI with age.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  1. Alford, P. W., B. E. Dabiri, J. A. Goss, M. A. Hemphill, M. D. Brigham, and K. K. Parker. Blast-induced phenotypic switching in cerebral vasospasm. Proc. Natl. Acad. Sci. USA 108:12705–12710, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Armstead, W. M. Cerebral hemodynamics after traumatic brain injury of immature brain. Exp. Toxicol. Pathol. 51:137–142, 1999.

    Article  CAS  PubMed  Google Scholar 

  3. Bell, E. D., R. S. Kunjir, and K. L. Monson. Biaxial and failure properties of passive rat middle cerebral arteries. J. Biomech. 46:91–96, 2013.

    Article  PubMed  Google Scholar 

  4. Bell, E. D., J. W. Sullivan, and K. L. Monson. Subfailure overstretch induces persistent changes in the passive mechanical response of cerebral arteries. Front. Bioeng. Biotechnol. 3:2, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Bevan, R. D., E. Vijayakumaran, A. Gentry, T. Wellman, and J. A. Bevan. Intrinsic tone of cerebral artery segments of human infants between 23 weeks of gestation and term. Pediatr. Res. 43:20–27, 1998.

    Article  CAS  PubMed  Google Scholar 

  6. Boock, R. Vascular Response to Mechanical Deformations. Philadephia: University of Pennsylvania, 1991.

    Google Scholar 

  7. Bruce, D. A. Head injuries in the pediatric population. Curr. Probl. Pediatr. 20:61–107, 1990.

    CAS  PubMed  Google Scholar 

  8. Buehler, M. J. Nanomechanics of collagen fibrils under varying cross-link densities: atomistic and continuum studies. J. Mech. Behav. Biomed. Mater. 1:59–67, 2008.

    Article  PubMed  Google Scholar 

  9. Busby, D., and A. Burton. The effect of age on the elasticity of the major brain arteries. Can. J. Physiol. Pharmacol. 43:185–202, 1965.

    Article  CAS  PubMed  Google Scholar 

  10. Cox, R. H. Effects of age on the mechanical properties of rat carotid artery. Am. J. Physiol. 233:H256–H263, 1977.

    CAS  PubMed  Google Scholar 

  11. Cox, R. H. Comparison of carotid artery mechanics in the rat, rabbit, and dog. Am. J. Physiol. 234:H280–H288, 1978.

    CAS  PubMed  Google Scholar 

  12. Dawes, G., B. M. Johnston, and D. Walker. Relationship of arterial pressure and heart rate in fetal, new-born and adult sheep. J. Physiol. 309:405, 1980.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Depalle, B., Z. Qin, S. J. Shefelbine, and M. J. Buehler. Influence of cross-link structure, density and mechanical properties in the mesoscale deformation mechanisms of collagen fibrils. J. Mech. Behav. Biomed. Mater. 52:1–13, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  14. DeWitt, D., and D. S. Prough. Traumatic cerebral vascular injury: the effects of concussive brain injury on the cerebral vasculature. J. Neurotrauma 20:795–825, 2003.

    Article  PubMed  Google Scholar 

  15. Dobrin, P., and A. Rovick. Influence of vascular smooth muscle on contractile mechanics and elasticity of arteries. Am. J. Physiol. 217:1644–1651, 1969.

    CAS  PubMed  Google Scholar 

  16. Docherty, C. C., J. Kalmar-Nagy, M. Engelen, and P. W. Nathanielsz. Development of fetal vascular responses to endothelin-1 and acetylcholine in the sheep. Am. J. Physiol. 280:R554–R562, 2001.

    CAS  Google Scholar 

  17. Faul, M., L. Xu, M. M. Wald, and V. G. Coronado. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations and Deaths 2002–2006. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control, 2010.

    Google Scholar 

  18. Goyal, R., D. A. Henderson, N. Chu, and L. D. Longo. Ovine middle cerebral artery characterization and quantification of ultrastructure and other features: changes with development. Am. J. Physiol. 302:R433–R445, 2012.

    CAS  Google Scholar 

  19. Ho, J., and S. Kleiven. Dynamic response of the brain with vasculature: a three-dimensional computational study. J Biomech 40:3006–3012, 2007.

    Article  PubMed  Google Scholar 

  20. Humphrey, J. D. Cardiovascular Solid Mechanics: Cells, Tissues, and Organs. New York: Springer, 2002.

    Book  Google Scholar 

  21. Kelleher, C. M., S. E. McLean, and R. P. Mecham. Vascular extracellular matrix and aortic development. In: Current Topics in Developmental Biology, edited by P. S. Gerald. New York: Academic Press, 2004, pp. 153–188.

    Google Scholar 

  22. Kochanek, P. M. Pediatric traumatic brain injury: quo vadis? Dev. Neurosci. 28:244–255, 2006.

    Article  CAS  PubMed  Google Scholar 

  23. Langfitt, T. W., W. D. Obrist, T. A. Gennarelli, M. J. O’Connor, and C. A. Weeme. Correlation of cerebral blood flow with outcome in head injured patients. Ann. Surg. 186:411–414, 1977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lee, R. M. K. W. Morphology of cerebral arteries. Pharmacol. Ther. 66:149–173, 1995.

    Article  CAS  PubMed  Google Scholar 

  25. Lindenberg, R., and E. Freytag. Morphology of brain lesions from blunt trauma in early infancy. Arch. Pathol. 87:298–305, 1969.

    CAS  PubMed  Google Scholar 

  26. Monson, K. L., N. M. Barbaro, and G. T. Manley. Biaxial response of passive human cerebral arteries. Ann. Biomed. Eng. 36:2028–2041, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Monson, K. L., W. Goldsmith, N. M. Barbaro, and G. T. Manley. Axial mechanical properties of fresh human cerebral blood vessels. J. Biomech. Eng. 125:288–294, 2003.

    Article  PubMed  Google Scholar 

  28. Monson, K. L., W. Goldsmith, N. M. Barbaro, and G. T. Manley. Significance of source and size in the mechanical response of human cerebral blood vessels. J. Biomech. 38:737–744, 2005.

    Article  PubMed  Google Scholar 

  29. Monson, K. L., V. Mathur, and D. A. Powell. Deformations and end effects in isolated blood vessel testing. J. Biomech. Eng. 133:011005, 2011.

    Article  PubMed  Google Scholar 

  30. Nagasawa, S., H. Handa, A. Okumura, Y. Naruo, K. Moritake, and K. Hayashi. Mechanical properties of human cerebral arteries. Part 1: effects of age and vascular smooth muscle activation. Surg. Neurol. 12:297–304, 1979.

    CAS  PubMed  Google Scholar 

  31. Pearce, W. J., A. D. Hull, D. M. Long, and L. D. Longo. Developmental changes in ovine cerebral artery composition and reactivity. Am. J. Physiol. 261:R458–R465, 1991.

    CAS  PubMed  Google Scholar 

  32. Roach, M. R. The static elastic properties of carotid arteries from fetal sheep. Can. J. Physiol. Pharmacol. 48:695–708, 1970.

    CAS  Google Scholar 

  33. Roach, M. R., and A. C. Burton. The reason for the shape of the distensibility curves of arteries. Can. J. Biochem. Physiol. 35:681–690, 1957.

    Article  CAS  PubMed  Google Scholar 

  34. Snoek, J. W., J. M. Minderhoud, and J. T. Wilmink. Delayed deterioration following mild head injury in children. Brain 107(Pt 1):15–36, 1984.

    Article  PubMed  Google Scholar 

  35. Stemper, B. D., N. Yoganandan, M. R. Stineman, T. A. Gennarelli, J. L. Baisden, and F. A. Pintar. Mechanics of fresh, refrigerated, and frozen arterial tissue. J Surg Res 139:236–242, 2007.

    Article  PubMed  Google Scholar 

  36. Svensson, R. B., H. Mulder, V. Kovanen, S. P. Magnusson, and Influence of Natural Cross-Links. Fracture mechanics of collagen fibrils: influence of natural cross-links. Biophys. J. 104:2476–2484, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Tian, L., Z. Wang, Y. Liu, J. C. Eickhoff, K. W. Eliceiri, and N. C. Chesler. Validation of an arterial constitutive model accounting for collagen content and crosslinking. Acta. Biomater. 31:276–287, 2016.

    Article  CAS  PubMed  Google Scholar 

  38. Udomphorn, Y., W. M. Armstead, and M. S. Vavilala. Cerebral blood flow and autoregulation after pediatric traumatic brain injury. Pediatr. Neurol. 38:225–234, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Unno, N., C. H. Wong, S. L. Jenkins, R. A. Wentworth, X.-Y. Ding, C. Li, S. S. Robertson, W. P. Smotherman, and P. W. Nathanielsz. Blood pressure and heart rate in the ovine fetus: ontogenic changes and effects of fetal adrenalectomy. Am. J. Physiol. 276:H248–H256, 1999.

    CAS  PubMed  Google Scholar 

  40. Van Loon, P., W. Klip, and E. L. Bradley. Length–force and volume–pressure relationships of arteries. Biorheology 14:181–201, 1977.

    PubMed  Google Scholar 

  41. Wagenseil, J. E., and R. P. Mecham. Vascular extracellular matrix and arterial mechanics. Physiol. Rev. 89:957–989, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Wang, Z., R. S. Lakes, J. C. Eickhoff, and N. C. Chesler. Effects of collagen deposition on passive and active mechanical properties of large pulmonary arteries in hypoxic pulmonary hypertension. Biomech. Model. Mechanobiol. 12:1115–1125, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Weizsacker, H. W., H. Lambert, and K. Pascale. Analysis of the passive mechanical properties of rat carotid arteries. J. Biomech. 16:703–715, 1983.

    Article  CAS  PubMed  Google Scholar 

  44. Zhang, L., J. Bae, W. N. Hardy, K. L. Monson, G. T. Manley, W. Goldsmith, K. H. Yang, and A. I. King. Computational study of the contribution of the vasculature on the dynamic response of the brain. Stapp. Car. Crash. J. 46:145–164, 2002.

    PubMed  Google Scholar 

Download references

Acknowledgments

Financial support was provided, in part, by the Primary Children’s Medical Center Foundation (PCMCF-ISA-KM-01-2012-02 to KLM) and by the National Institutes of Health (HL-110002 to KHA). The authors report no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kenneth L. Monson.

Additional information

Associate Editor Peter E. McHugh oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nye, K.S., Converse, M.I., Dahl, M.J. et al. Development of Mechanical and Failure Properties in Sheep Cerebral Arteries. Ann Biomed Eng 45, 1101–1110 (2017). https://doi.org/10.1007/s10439-016-1741-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-016-1741-0

Keywords

Navigation