Annals of Biomedical Engineering

, Volume 35, Issue 2, pp 285–291 | Cite as

Biomechanical Characterization of Internal Layer Subfailure in Blunt Arterial Injury

  • Brian D. Stemper
  • Narayan Yoganandan
  • Grant P. Sinson
  • Thomas A. Gennarelli
  • Michael R. Stineman
  • Frank A. Pintar
Article

Abstract

Blunt carotid artery injuries occur in 0.3% of blunt injured patients and may lead to devastating neurological consequences. However, arterial mechanics leading to internal layer subfailure have not been quantified. Twenty-two human carotid artery segments and 18 porcine thoracic aorta segments were opened to expose the intimal side and longitudinally distracted to failure. Porcine aortas were a geometrically accurate model of human carotid arteries. Internal layer subfailures were identified using videography and correlated with mechanical data. Ninety-three percent (93%) of vessels demonstrated subfailure prior to catastrophic failure. All subfailures occurred on the intimal surface. Initial subfailure occurred at 79% of the stress and 85% of the strain to catastrophic failure in younger porcine specimens, compared to 44% and 60%, respectively, in older human specimens. In most cases, multiple subfailures occurred prior to catastrophic failure. Due to limitations in human specimen quality (age, prior storage), young and fresh porcine aorta specimens are likely a more accurate model of clinical blunt carotid artery injuries. Present results indicate that vessels are acutely capable of maintaining physiologic function following initial subfailure. Delayed symptomatology commonly associated with blunt arterial injuries is explained by this mechanics-based and experimentally quantified onset of subcatastrophic failure.

Keywords

Endothelium Injury Mechanics Carotid artery Thoracic aorta 

Notes

Acknowledgments

This research was supported in part by the Department of Veterans Affairs Medical Research. The funding for this research has also been provided in part by an Australian Research Council linkage grant and by private parties, who have selected Dr. Kennerly Digges and FHWA/NHTSA National Crash Analysis Center at the George Washington University to be an independent solicitor of and funder for research in motor vehicle safety, and to be one of the peer reviewers for the research projects and reports. Neither of the private parties have determined the allocation of funds or had any influence on the content of this report.

References

  1. 1.
    Adham M., J. P. Gournier, J. P. Favre, et al. (1996) Mechanical characteristics of fresh and frozen human descending thoracic aorta. J. Surg. Res. 64(1):32–34PubMedCrossRefGoogle Scholar
  2. 2.
    Alimi Y., P. Di Mauro, L. Tomachot, et al. (1998) Bilateral dissection of the internal carotid artery at the base of the skull due to blunt trauma: incidence and severity. Ann. Vasc. Surg. 12(6):557–565PubMedCrossRefGoogle Scholar
  3. 3.
    Ballard J. L., T. J. Bunt, B. Fitzpatrick, et al. (1992) Bilateral traumatic internal carotid artery dissections: case report. J. Vasc. Surg. 15(2):431–435PubMedCrossRefGoogle Scholar
  4. 4.
    Batzdorf U., J. R. Bentson, H. I. Machleder (1979) Blunt trauma to the high cervical carotid artery. Neurosurgery 5(2):194–201CrossRefGoogle Scholar
  5. 5.
    Biffl W. L., E. E. Moore, R. K. Ryu, et al. (1998) The unrecognized epidemic of blunt carotid arterial injuries: early diagnosis improves neurologic outcome. Ann. Surg. 228(4):462–470PubMedCrossRefGoogle Scholar
  6. 6.
    Brossollet L. J., R. P. Vito (1997) The effects of cryopreservation on the biaxial mechanical properties of canine saphenous veins. J. Biomech. Eng. 119(1):1–5PubMedGoogle Scholar
  7. 7.
    Bujan J., G. Pascual, N. Garcia-Honduvilla, et al. (2000) Rapid thawing increases the fragility of the cryopreserved arterial wall. Eur. J. Vasc. Endovasc. Surg. 20(1):13–20PubMedCrossRefGoogle Scholar
  8. 8.
    Carmines D. V., J. H. McElhaney, R. Stack (1991) A piece-wise non-linear elastic stress expression of human and pig coronary arteries tested in vitro. J. Biomech. 24(10):899–906PubMedCrossRefGoogle Scholar
  9. 9.
    Carrillo E. H., D. L. Osborne, D. A. Spain, et al (1999) Blunt carotid artery injuries: difficulties with the diagnosis prior to neurologic event. J. Trauma 46(6):1120–1125PubMedGoogle Scholar
  10. 10.
    Cogbill T. H., E. E. Moore, M. Meissner, et al. (1994) The spectrum of blunt injury to the carotid artery: a multicenter perspective. J. Trauma 37(3):473–479PubMedGoogle Scholar
  11. 11.
    Cohuet G., P. Challande, M. Osborne-Pellegrin, et al. (2001) Mechanical strength of the isolated carotid artery in SHR. Hypertension 38(5):1167–1171PubMedCrossRefGoogle Scholar
  12. 12.
    Collins R., W. C. L. Hu (1972) Dynamic deformation experiments on aortic tissue. J. Biomech. 5(4):333–337PubMedCrossRefGoogle Scholar
  13. 13.
    Cothren C. C., E. E. Moore, W. L. Biffl, et al. (2004) Anticoagulation is the gold standard therapy for blunt carotid injuries to reduce stroke rate. Arch. Surg. 139(5):540–546PubMedCrossRefGoogle Scholar
  14. 14.
    Cox R. H. (1979) Regional, species, and age related variations in the mechanical properties of arteries. Biorheology 16(1&2):85–94PubMedGoogle Scholar
  15. 15.
    Cox R. H. (1974) Three-dimensional mechanics of arterial segments in vitro: methods. J. Appl. Physiol. 36(3):381–384PubMedGoogle Scholar
  16. 16.
    Crissey M. M., E. F. Bernstein (1974) Delayed presentation of carotid intimal tear following blunt craniocervical trauma. Surgery 75(4):543–549PubMedGoogle Scholar
  17. 17.
    Davis J. W., T. L. Holbrook, D. B. Hoyt, et al. (1990) Blunt carotid artery dissection: incidence, associated injuries, screening, and treatment. J. Trauma 30(12):1514–1517PubMedCrossRefGoogle Scholar
  18. 18.
    Fabian T. C., J. H. Patton, M. A. Croce, et al. (1996) Blunt carotid artery injury: importance of early diagnosis and anticoagulant therapy. Ann. Surg. 223(5):513–525PubMedCrossRefGoogle Scholar
  19. 19.
    Fanelli F., F. M. Salvatori, R. Ferrari, et al. (2004) Stent repair of bilateral post-traumatic dissections of the internal carotid artery. J. Endovasc. Ther. 11(4):517–521PubMedCrossRefGoogle Scholar
  20. 20.
    Gournier J. P., M. Adham, J. P. Favre, et al. (1993) Cryopreserved arterial homografts: preliminary study. Ann. Vasc. Surg. 7(6):503–511PubMedCrossRefGoogle Scholar
  21. 21.
    Gurdjian E. S., B. Audet, R. W. Sibayan, et al. (1971) Spasm of the extracranial internal carotid artery resulting from blunt trauma demonstrated by angiography. J. Neurosurg. 35(6):742–747PubMedGoogle Scholar
  22. 22.
    Hayashi K. (1993) Experimental approaches on measuring the mechanical properties and constitutive laws of arterial walls. J. Biomech. Eng. 115(4B):481–488PubMedGoogle Scholar
  23. 23.
    Krajewski L. P., N. R. Hertzer (1980) Blunt carotid artery trauma. Ann. Surg. 191(3):341–346PubMedCrossRefGoogle Scholar
  24. 24.
    Lacolley P., P. Challande, S. Boumaza, et al. (2001) Mechanical properties and structure of carotid arteries in mice lacking desmin. Cardiovasc. Res. 51(1):178–187PubMedCrossRefGoogle Scholar
  25. 25.
    Lawton R. W. (1955) Measurements on the elasticity and damping of isolated aortic strips in the dog. Circ. Res. 3(4):403–408PubMedGoogle Scholar
  26. 26.
    Lee M. C., R. C. Haut (1989) Insensitivity of tensile failure properties of human bridging veins to strain rate: implications in biomechanics of subdural hematoma. J. Biomech. 22(6/7):537–542PubMedCrossRefGoogle Scholar
  27. 27.
    Lee M. C., R. C. Haut (1992) Strain rate effects on tensile failure properties of the common carotid artery and jugular veins of ferrets. J. Biomech. 25(8):925–927PubMedCrossRefGoogle Scholar
  28. 28.
    L’Italien G. J., R. D. Maloney, W. M. Abbott (1979) The preservation of the mechanical properties of venous allografts by freezing. J. Surg. Res. 27(4):239–243PubMedCrossRefGoogle Scholar
  29. 29.
    Liu W. P., K. C. Ng, J. J. Hung (2005) Carotid artery injury with cerebral infarction following head and neck blunt trauma: report of a case. Yale J. Biol. Med. 78(3):151–156PubMedGoogle Scholar
  30. 30.
    Lowenhielm P. (1974) Dynamic properties of the parasagittal bridging veins. Z. Rechtsmed. 74(1):55–62PubMedCrossRefGoogle Scholar
  31. 31.
    Malek A. M., R. T. Higashida, C. C. Phatouros, et al. (2000) Endovascular management of extracranial carotid artery dissection achieved using stent angioplasty. AJNR Am. J. Neuroradiol. 21(7):1280–1292PubMedGoogle Scholar
  32. 32.
    Malin J. P., H. Becker, J. Abicht (1985) Bilateral traumatic extracranial aneurysms of the internal carotid artery with delayed brain infarction. J. Neurol. 232(5):314–317PubMedCrossRefGoogle Scholar
  33. 33.
    Martin R. F., J. Eldrup-Jorgensen, D. E. Clark, et al. (1991) Blunt trauma to the carotid arteries. J. Vasc. Surg. 14(6):789–795PubMedCrossRefGoogle Scholar
  34. 34.
    McKevitt E. C., A. W. Kirkpatrick, L. Vertesi, et al. (2002) Blunt vascular neck injuries: diagnosis and outcomes of extracranial vessel injury. J. Trauma 53(3):472–476PubMedGoogle Scholar
  35. 35.
    Miller P. R., T. C. Fabian, T. K. Bee, et al. (2001) Blunt cerebrovascular injuries: diagnosis and treatment. J. Trauma 51(2):279–285PubMedGoogle Scholar
  36. 36.
    Miller P. R., T. C. Fabian, M. A. Croce, et al. (2002) Prospective screening for blunt cerebrovascular injuries. Ann. Surg. 236(3):386–395PubMedCrossRefGoogle Scholar
  37. 37.
    Mitchell P., J. Jakubowski (2002) Failure testing cerebral arteries: are branch points weaker than unbranched vessels? Br. J. Neurosurg. 16(6):578–582PubMedCrossRefGoogle Scholar
  38. 38.
    Mohan D., J. W. Melvin (1982) Failure properties of passive human aortic tissue. I. Uniaxial tension tests. J. Biomech. 15(11):887–902PubMedCrossRefGoogle Scholar
  39. 39.
    Mokri B., D. G. Piepgras, O. W. Houser (1988) Traumatic dissections of the extracranial internal carotid artery. J. Neurosurg. 68(2):189–197PubMedCrossRefGoogle Scholar
  40. 40.
    Monson K. L., W. Goldsmith, N. M. Barbaro, et al. (2003) Axial mechanical properties of fresh human cerebral blood vessels. J. Biomech. Eng. 125(2):288–294PubMedCrossRefGoogle Scholar
  41. 41.
    Monson K. L., W. Goldsmith, N. M. Barbaro, et al. (2005) Significance of source and size in the mechanical response of human cerebral blood vessels. J. Biomech. 38(4):737–744PubMedCrossRefGoogle Scholar
  42. 42.
    Parikh A. A., F. A. Luchette, J. F. Valente, et al. (1997) Blunt carotid artery injuries. J. Am. Coll. Surg. 185(1):87–93Google Scholar
  43. 43.
    Perry M. O., W. H. Snyder, E. R. Thal (1980) Carotid artery injuries caused by blunt trauma. Ann. Surg. 192(1):74–77PubMedCrossRefGoogle Scholar
  44. 44.
    Prall J. A., K. E. Brega, D. M. Coldwell, et al. (1998) Incidence of unsuspected blunt carotid artery injury. Neurosurgery 42(3):495–499PubMedCrossRefGoogle Scholar
  45. 45.
    Pretre R., A. Reverdin, T. Kalonji, et al. (1994) Blunt carotid artery injury: difficult therapeutic approaches for an underrecognized entity. Surgery 115(3):375–381PubMedGoogle Scholar
  46. 46.
    Pukacki F., T. Jankowski, M. Gabriel, et al. (2000) The mechanical properties of fresh and cryopreserved arterial homografts. Eur. J. Vasc. Endovasc. Surg. 20(1):21–24PubMedCrossRefGoogle Scholar
  47. 47.
    Punjabi A. P., B. R. Plaisier, R. H. Haug, et al. (1997) Diagnosis and management of blunt carotid artery injury in oral and maxillofacial surgery. J. Oral. Maxillofac. Surg. 55(12):1388–1395PubMedCrossRefGoogle Scholar
  48. 48.
    Rosset E., A. Friggi, G. Novakovitch, et al. (1996) Effects of cryopreservation on the viscoelastic properties of human arteries. Ann. Vasc. Surg. 10(3):262–272PubMedCrossRefGoogle Scholar
  49. 49.
    Sauren A. A. H. J., M. C. van Hout, A. A. van Steenhoven, et al. (1983) The mechanical properties of porcine aortic valve tissue. J. Biomech. 16(5):327–337PubMedCrossRefGoogle Scholar
  50. 50.
    Scherman B. M., W. S. Tucker (1982) Bilateral traumatic thrombosis of the internal carotid arteries in the neck: a case report with review of literature. Neurosurgery. 10(6):751–753PubMedCrossRefGoogle Scholar
  51. 51.
    Showalter D., S. Durham, R. Sheppeck, et al. (1989) Cryopreserved venous homografts as vascular conduits in canine carotid arteries. Surgery. 106(4):652–659PubMedGoogle Scholar
  52. 52.
    Stemper B. D., M. R. Stineman, N. Yoganandan, et al. (2005) Subcatastrophic failure characteristics of the porcine descending aorta. Biomed. Sci. Instrum. 41:110–115PubMedGoogle Scholar
  53. 53.
    Stemper B. D., N. Yoganandan, and F. A. Pintar. Mechanics of arterial subfailure with increasing loading rates. J. Biomech. doi:10.1016/j.jbiomech.2006.07.005, in pressGoogle Scholar
  54. 54.
    Stemper B. D., N. Yoganandan, F. A. Pintar (2005) Methodology to study intimal failure mechanics in human internal carotid arteries. J. Biomech. 38(12):2491–2496PubMedCrossRefGoogle Scholar
  55. 55.
    Stemper B. D., N. Yoganandan, M. R. Stineman, et al. Mechanics of fresh, refrigerated, and frozen arterial tissue. J Surg Res. doi:10.1016/j.jss.2006.09.001, in pressGoogle Scholar
  56. 56.
    Stonebridge P. A., A. E. Clason, A. M. Jenkins (1990) Traumatic aneurysm of the extracranial internal carotid artery due to hyperextension of the neck. Eur. J. Vasc. Surg. 4(4):423–425PubMedCrossRefGoogle Scholar
  57. 57.
    Stringer W. L., D. L. Kelly (1980) Traumatic dissection of the extracranial internal carotid artery. Neurosurgery 6(2):123–130PubMedCrossRefGoogle Scholar
  58. 58.
    Tanaka T., Y. C. Fung (1974) Elastic and inelastic properties of the canine aorta and their variation along the aortic tree. J. Biomech. 7(4):357–370PubMedCrossRefGoogle Scholar
  59. 59.
    van Andel C. J., P. V. Pistecky, C. Borst (2003) Mechanical properties of porcine and human arteries: implications for coronary anastomotic connectors. Ann. Thorac. Surg. 76(1):58–65PubMedCrossRefGoogle Scholar
  60. 60.
    Wahl W. L., M. M. Brandt, G. Thompson, et al. (2002) Antiplatelet therapy: an alternative to heparin for blunt carotid injury. J. Trauma 52(5):896–901PubMedCrossRefGoogle Scholar
  61. 61.
    Wang P., Z. Shu, L. He, et al. (2006) The structural and cellular viability in cryopreserved rabbit carotid arteries. J. Surg. Res. 131(2):241–251PubMedCrossRefGoogle Scholar
  62. 62.
    Xie J., J. Zhou, Y. C. Fung (1995) Bending of blood vessel wall: stress–strain laws of the intima-media and adventitial layers. J. Biomech. Eng. 117(1):136–145PubMedGoogle Scholar
  63. 63.
    Zelenock G. B., A. Kazmers, W. M. Whitehouse, et al. (1982) Extracranial internal carotid artery dissections: noniatrogenic traumatic lesions. Arch. Surg. 117(4):425–432PubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2006

Authors and Affiliations

  • Brian D. Stemper
    • 1
    • 2
  • Narayan Yoganandan
    • 1
    • 2
  • Grant P. Sinson
    • 1
    • 2
  • Thomas A. Gennarelli
    • 1
    • 2
  • Michael R. Stineman
    • 1
    • 2
  • Frank A. Pintar
    • 1
    • 2
  1. 1.Department of NeurosurgeryMedical College of WisconsinMilwaukeeUSA
  2. 2.Department of Veterans Affairs Medical CenterMilwaukeeUSA

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