Skip to main content
SpringerLink
Log in

Post-Vagotomy Mechanical Characteristics and Structure of the Thoracic Aortic Wall

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

Abstract

This study assessed the long-term effect of vagotomy on the structure and passive mechanical characteristics of the thoracic aorta under a wide range of stresses in vitro. Eight healthy Landrace pigs underwent bilateral vagotomy distal to the origin of the recurrent laryngeal nerve, and 10 pigs were sham-operated. Three months post-surgery, the aorta was excised and specimens from the ascending aorta, arch, and descending thoracic aorta were subjected to histomorphometrical evaluation and uniaxial tensile-testing until failure. Elastic modulus-stress data were plotted and submitted to regression analysis. Structural remodeling after vagotomy was characterized as vascular growth in the ascending aorta and arch, and as thinning in the descending thoracic aorta. In the aortic segments of vagotomized animals, the area density of elastin and collagen was increased, but smooth muscle density was decreased. Similar differences in regression parameters and failure strength between groups were found in all aortic segments, indicating that the vessel wall was stiffer and stronger in vagotomized animals. In the clinical setting, disease states or drugs blocking the regulatory role of the vagi nerves on the aortic wall may have undesirable consequences on the mechanical performance of the thoracic aorta, and therefore on hemodynamic homeostasis.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Abbaud, F. M. Disturbances in Neurogenic Control of the Circulation. Baltimore: Williams and Wilkins, 1981.

  2. Adrian, R. H. Reviews in Physiology, Biochemistry and Pharmacology. New York: Springer-Verlag, 1978.

  3. Ahlgren, A. R., G. Sundkvist, P. Wollmer, B. Sonesson, and T. Lanne. Increased aortic stiffness in women with type I diabetes mellitus is associated with diabetes duration and autonomic nerve function. Diabet. Med. 16:291–297, 1999.

    Article  Google Scholar 

  4. Amenta, F., C. Cavallotti, F. Ferrante, and M. Zomparelli. The cholinergic innervation of the aorta. Acta Histochem. 66:197–203, 1980.

    Google Scholar 

  5. Angouras, D., D. P. Sokolis, T. Dosios, N. Kostomitsopoulos, H. Boudoulas, Gr. Skalkeas, and P. E. Karayannacos. Effect of impaired vasa vasorum flow on the structure and mechanics of the thoracic aorta: Implications for the pathogenesis of aortic dissection. Eur. J. Cardiothorac. Surg. 17:468–473, 2000.

    Article  Google Scholar 

  6. Aviado, D. Pharmacology of Ganglionic Transmission. New York: Springer-Verlag, 1979.

    Google Scholar 

  7. Baumbach, G. L., D. D. Heistad, and J. E. Siems. Effect of sympathetic nerves on composition and distensibility of cerebral arterioles in rats. J. Physiol. 416:123–140, 1989.

    Google Scholar 

  8. Bevan, R. D., and H. Tsuru. Functional and structural changes in the rabbit ear artery after sympathetic denervation. Circ. Res. 49:478–485, 1981.

    Google Scholar 

  9. Bhagot, B. Mode of Action of Autonomic Drugs. New York: Graceway, 1979.

    Google Scholar 

  10. Boudoulas, H., and C. F. Wooley. Aortic distensibility. Important in clinical medicine? Cardiol. Rev. 2:211–217, 1994.

    Google Scholar 

  11. Boudoulas, H., and C. F. Wooley. Aortic function. In: Functional Abnormalities of the Aorta, edited by H. Boudoulas, P. K. Toutouzas, and C. F. Wooley. New York: Futura, 1996, pp. 3–36.

  12. Boutouyrie, P., P. Lacolley, X. Girerd, L. Beck, M. Safar, and S. Laurent. Sympathetic activation decreases medium-size artery compliance in humans. Am. J. Physiol. 267:H1368–H1376, 1994.

    Google Scholar 

  13. Cheng, Z., T. L. Powley, J. S. Schwaber, and F. J. Doyle 3rd. A laser confocal microscopic study of vagal afferent innervation of rat aortic arch: Chemoreceptors as well as baroreceptors. J. Auton. Nerv. Syst. 67:1–14, 1997.

    Article  Google Scholar 

  14. Clark, J. M., and S. Glagov. Structural integration of the arterial wall. I. Relationships and attachments of medial smooth muscle cells in normally distended and hyperdistended aortas. Lab. Invest. 40:587–602, 1979.

    Google Scholar 

  15. Clark, J. M., and S. Glagov. Transmural organization of the arterial media. The lamellar unit revisited. Arteriosclerosis 5:19–34, 1985.

    Google Scholar 

  16. Cox, R. H. Mechanics of canine iliac artery smooth muscle in vitro. Am. J. Physiol. 230:H462–H470, 1976.

    Google Scholar 

  17. Cox, R. H. Passive mechanics and connective tissue composition of canine arteries. Am. J. Physiol. 234:H533–H541, 1978.

    Google Scholar 

  18. Dobrin, P. B., and T. Canfield. Elastase, collagenase, and the biaxial elastic properties of dog carotid artery. Am. J. Physiol. 237:H124–H131, 1984.

    Google Scholar 

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

    Google Scholar 

  20. Donald, D. E., and J. T. Shepherd. Autonomic regulation of the peripheral circulation. Annu. Rev. Physiol. 42:429–439, 1980.

    Article  Google Scholar 

  21. Ferrari, A. U. Age-related modifications in neural cardiovascular control. Aging (Milano) 4:183–195, 1992.

    Google Scholar 

  22. Ferrari, A. U. Modifications of the cardiovascular system with aging. Am. J. Geriatr. Cardiol. 11:30–33, 2002.

    MathSciNet  Google Scholar 

  23. Ferrari, A. U., A. Radaelli, and M. Centola. Invited review: Aging and the cardiovascular system. J. Appl. Physiol. 95:2591–2597, 2003.

    Google Scholar 

  24. Fronek, K., C. M. Bloor, D. Amiel, and M. Chvapil. Effect of long-term sympathectomy on the arterial wall in rabbits and rats. Exp. Mol. Pathol. 28:279–289, 1978.

    Article  Google Scholar 

  25. Fung, Y. C. Elasticity of soft tissues in simple elongation. Am. J. Physiol. 213:1532–1544, 1967.

    Google Scholar 

  26. Fung, Y. C. Biorheology of soft tissues. Biorheology 10:139–155, 1973.

    Google Scholar 

  27. Fung, Y. C. Description of internal deformation and forces. In: Biomechanics: Motion, Flow, Stress and Growth, edited by Y. C. Fung. New York: Springer-Verlag, 1990, pp. 353–381.

  28. Glagov, S., and H. Wolinsky. Physiology: Aortic wall as a ‘two phase’ material. Nature 199:606–608, 1963.

    Google Scholar 

  29. Gray, H., and H. V. Carter. Nervous system. In: Gray's Anatomy, edited by H. Gray and H. V. Carter. London: Magpie, 1993, pp. 509–514.

  30. Hayashi, K. Experimental approaches on measuring the mechanical properties and constitutive laws of arterial walls. J. Biomech. Eng. 115:481–488, 1993.

    Google Scholar 

  31. Hayashi, K., T. Washizu, N. Tsushima, R. J. Kirali, and Y. Nose. Mechanical properties of aortas and pulmonary arteries of calves implanted with cardiac prostheses. J. Biomech. 14:173–182, 1981.

    Article  Google Scholar 

  32. Humphrey, J. D. Cardiovascular Solid Mechanics: Cells, Tissues, and Organs, 1st ed. New York: Springer-Verlag, 2002, pp. 68–105.

  33. Lacolley, P., Y. Bezie, X. Girerd, P. Challande, A. Benetos, P. Boutouyrie, N. Ghodsi, B. Lucet, R. Azoui, and S. Laurent. Aortic distensibility and structural changes in sinoaortic-denervated rats. Hypertension 269:H407–H416, 1995.

    Google Scholar 

  34. Lacolley, P., E. Glaser, P. Challande, P. Boutouyrie, J. P. Mignot, M. Duriez, B. Levy, M. Safar, and S. Laurent. Structural changes and in situ aortic pressure-diameter relationship in long-term chemical-sympathectomized rats. Am. J. Physiol. 269:H407–H416, 1995.

    Google Scholar 

  35. Larson, E. W., and W. D. Edwards. Risk factors for aortic dissection: A necropsy study of 161 cases. Am. J. Cardiol. 53:849–855, 1984.

    Article  Google Scholar 

  36. Miao, C. Y., X. Tao, K. Gong, S. H. Zhang, Z. X. Chu, and F. Su. Arterial remodeling in chronic sinoaortic-denervated rats. J. Cardiovasc. Pharmacol. 37:6–15, 2001

    Article  Google Scholar 

  37. Mircoli L., A. A. Mangoni, C. Giannattasio, G. Mancia, and A. U. Ferrari. Heart-rate dependent stiffening of large arteries in intact and sympathectomized rats. Hypertension 32:735–739, 1999.

    Google Scholar 

  38. Pfeifer, M. A., C. R. Weinberg, D. Cook, J. D. Best, A. Reenan, and J. B. Halter. Differential changes of autonomic nervous system function with age in man. Am. J. Med. 75:249–258, 1983.

    Article  Google Scholar 

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

    Google Scholar 

  40. Sokolis, D. P., H. Boudoulas, and P. E. Karayannacos. Assessment of the aortic stress-strain relation in uniaxial tension. J. Biomech. 35:1213–1223, 2002.

    Article  Google Scholar 

  41. Sokolis, D. P., H. Boudoulas, N. Kavantzas, N. Kostomitsopoulos, H. Boudoulas, Gr. Skalkeas, and P. E. Karayannacos. A morphometric study of the structural characteristics of the aorta in pigs using an image analysis method. Anat. Histol. Embryol. 31:1–10, 2002.

    Google Scholar 

  42. Stefanadis, C., C. F. Wooley, C. A. Bush, A. J. Kolibash, and H. Boudoulas. Aortic distensibility abnormalities in coronary artery disease. Am. J. Cardiol. 59:1300–1304, 1987.

    Article  Google Scholar 

  43. Todd, M. E., and B. Gowen. Arterial wall and smooth muscle cell development in young Wistar rats and the effects of surgical denervation. Circ. Res. 69:438–446, 1991.

    Google Scholar 

  44. Wolinsky, H., and S. Glagov. Structural basis for the static mechanical properties of the aortic media. Circ. Res. 14:400–413, 1964.

    Google Scholar 

  45. Zar, J. H. Biostatistical Analysis, 3rd ed. New Jersey: Prentice-Hall, 1996.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Biomechanics, Foundation of Biomedical Research, Academy of Athens, Athens, Greece

    Dimitrios P. Sokolis

  2. Laboratory of Experimental Surgery and Surgical Research, School of Medicine, University of Athens, Athens, Greece

    Nikolaos Zarbis, Theodosios Dosios & Lilla Papadimitriou

  3. Center of Clinical Research, Foundation of Biomedical Research, Academy of Athens, Athens, Greece

    Harisios Boudoulas

  4. Center of Experimental Surgery, Foundation of Biomedical Research, Academy of Athens, Athens, Greece

    Vasiliki Papalouka & Panayotis E. Karayannacos

  5. 35, Lefkados Street, Athens, 15354, Greece

    Dimitrios P. Sokolis

Authors
  1. Dimitrios P. Sokolis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nikolaos Zarbis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Theodosios Dosios
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vasiliki Papalouka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lilla Papadimitriou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Harisios Boudoulas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Panayotis E. Karayannacos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dimitrios P. Sokolis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sokolis, D.P., Zarbis, N., Dosios, T. et al. Post-Vagotomy Mechanical Characteristics and Structure of the Thoracic Aortic Wall. Ann Biomed Eng 33, 1504–1516 (2005). https://doi.org/10.1007/s10439-005-7118-4

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-005-7118-4

Key Words

Search

Navigation