Skip to main content
Log in

Sustained Axial Loading Lengthens Arteries in Organ Culture

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

Abstract

Although it has been recognized for many years that arteries in vivo exist under significant axial strain, studies of the adaptation of arteries to elevated axial strain have only recently been conducted. To determine the effects of sustained elevation of axial loading on arterial structure and function, axial stresses of 250 kPa or greater were applied to porcine common carotid arteries maintained in a perfusion organ culture system for 7 days at physiologic pressure and flow conditions. Our results demonstrated that axial stretch could lead to an increase in unloaded length that was proportional to the axial stretch ratio (stretched length divided by unloaded length) when the axial stretch ratio was above a threshold value of 2.14. Below this threshold, no significant length change occurred. Above this threshold, a significant increase in unloaded length (13 ± %,) and the number of smooth muscle cell nuclei (20 ± 7%) was observed. Permanent length change was associated with a significant decrease in axial stiffness, and the maximum elongation achieved was limited by rupture of the arterial wall. All tested arteries demonstrated good viability and strong vasomotor responses. These results show that arteries in organ culture can elongate under sustained axial loading.

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.

Similar content being viewed by others

References

  1. Bardy, N., G. J. Karillon, R. Merval, J. L. Samuel, and A. Tedgui. Differential effects of pressure and flow on DNA and protein synthesis and on fibronectin expression by arteries in a novel organ culture system. Circ. Res. 77:684–694, 1995.

    PubMed  Google Scholar 

  2. Bardy, N., R. Merval, J. Benessiano, J. L. Samuel, and A. Tedgui. Pressure and angiotensin II synergistically induce aortic fibronectin expression in organ culture model of rabbit aorta. Evidence for a pressure-induced tissue renin–angiotensin system. Circ. Res. 79:70–78, 1996.

    PubMed  Google Scholar 

  3. Bergsma, T. M., J. G. Grandjean, A. A. Voors, P. W. Boonstra, P. den Heyer, and T. Ebels. Low recurrence of angina pectoris after coronary artery bypass graft surgery with bilateral internal thoracic and right gastroepiploic arteries. Circulation 97:2402–2405, 1998.

    PubMed  Google Scholar 

  4. Birukov, K. G., S. Lehoux, A. A. Birukova, R. Merval, V. A. Tkachuk, and A. Tedgui. Increased pressure induces sustained protein kinase C-independent herbimycin A-sensitive activation of extracellular signal-related kinase 1/2 in the rabbit aorta in organ culture. Circ. Res. 81:895–903, 1997.

    PubMed  Google Scholar 

  5. Birukov, K. G., V. P. Shirinsky, O. V. Stepanova, V. A. Tkachuk, A. W. Hahn, T. J. Resink, and V. N. Smirnov. Stretch affects phenotype and proliferation of vascular smooth muscle cells. Mol. Cell. Biochem. 144:131–139, 1995.

    Article  PubMed  Google Scholar 

  6. Boonen, H. C., P. M. Schiffers, G. E. Fazzi, G. M. Janssen, M. J. Daemen, and J. G. De Mey. DNA synthesis in isolated arteries. Kinetics and structural consequences. Am. J. Physiol. 260:H210–H217, 1991.

    PubMed  Google Scholar 

  7. Clerin, V., J. W. Nichol, M. Petko, R. J. Myung, J. W. Gaynor, and K. J. Gooch. Tissue engineering of arteries by directed remodeling of intact arterial segments. Tissue Eng. 9(3):461–472, 2003.

    Article  PubMed  Google Scholar 

  8. Cohen, B. E., and A. Ruiz-Razura. Acute intraoperative arterial lengthening for closure of large vascular gaps. Plast. Reconstr. Surg. 90:463–468, 1992.

    PubMed  Google Scholar 

  9. Davis, N. P. Axial stretch as a means of lengthening arteries: An investigation in organ culture. PhD thesis, Georgia Institute of Technology, 2002.

  10. Eagle, K. A., R. A. Guyton, R. Davidoff, G. A. Ewy, J. Fonger, T. J. Gardner, J. P. Gott, H. C. Herrmann, R. A. Marlow, W. C. Nugent, G. T. O’Connor, T. A. Orszulak, R. E. Rieselbach, W. L. Winters, S. Yusuf, R. J. Gibbons, J. S. Alpert, K. A. Eagle, A. Garson Jr., G. Gregoratos, R. O. Russell, and S. C. Smith Jr. ACC/AHA Guidelines for Coronary Artery Bypass Graft Surgery: A Report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee to Revise the 1991 Guidelines for Coronary Artery Bypass Graft Surgery). American College of Cardiology/American Heart Association. J. Am. Coll. Cardiol. 34:1262–1347, 1999.

    Article  PubMed  Google Scholar 

  11. Fink, B., J. Singer, S. Braunstein, G. Schwinger, G. Schmielau, and W. Ruther. Behavior of blood vessels during lower-leg lengthening using the Ilizarov method. J. Pediatr. Orthop. 19:748–753, 1999.

    Article  PubMed  Google Scholar 

  12. Fu, G., Y. Zeng, Z. Xia, and J. Lee. Biorheological features of some soft tissues under a surgical tissue expansion procedure. Biorheology 34:281–293, 1997.

    Article  PubMed  Google Scholar 

  13. Garrett, W. M., and H. D. Guthrie. Detection of Bromodeoxyuridine in paraffin-embedded tissue sections using microwave antigen retieval is dependent on the mode of tissue fixation. Biochemica 1:17–20, 1998.

    Google Scholar 

  14. Han, H. C., and Y. C. Fung. Longitudinal strain of canine and porcine aortas. J. Biomech. 28:637–641, 1995.

    Article  PubMed  Google Scholar 

  15. Han, H. C., and D. N. Ku. Contractile responses in arteries subjected to hypertensive pressure in seven-day organ culture. Ann. Biomed. Eng. 29:467–475, 2001.

    Article  PubMed  Google Scholar 

  16. Han, H. C., D. N. Ku, and R. P. Vito. Arterial wall adaptation under elevated longitudinal stretch in organ culture. Ann. Biomed. Eng. 31:403–411, 2003.

    Article  PubMed  Google Scholar 

  17. Han, H. C., R. P. Vito, K. Michael, and D. N. Ku. Axial stretch increases cell proliferation in arteries in organ culture. Adv. Bioeng. ASME (BED) 48:63–64, 2000.

    Google Scholar 

  18. Huang, K., Y. Zeng, H. Xia, and C. Liu. Alterations in the biorheological features of some soft tissues after limb lengthening. Biorheology 35:355–363, 1998.

    Article  PubMed  Google Scholar 

  19. Humphrey, J. D. Mechanics of the arterial wall: Review and directions. Crit. Rev. Biomed. Eng. 23:1–162, 1995.

    PubMed  Google Scholar 

  20. Humphrey, J. D. Remodeling of a collagenous tissue at fixed lengths. J. Biomech. Eng. 121:591–597, 1999.

    PubMed  Google Scholar 

  21. Ilizarov, G. A. The tension–stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation. Clin. Orthop. 238:249–281, 1989.

    PubMed  Google Scholar 

  22. Ilizarov, G. A. The tension–stress effect on the genesis and growth of tissues: Part II. The influence of the rate and frequency of distraction. Clin. Orthop. 239:263–285, 1989.

    PubMed  Google Scholar 

  23. Ippolito, E., G. Peretti, M. Bellocci, P. Farsetti, C. Tudisco, R. Caterini, and C. De Martino. Histology and ultrastructure of arteries, veins, and peripheral nerves during limb lengthening. Clin. Orthop. 308:54–62, 1994.

    PubMed  Google Scholar 

  24. Jackson, Z. S., A. I. Gotlieb, and B. L. Langille. Wall tissue remodeling regulates longitudinal tension in arteries. Circ. Res. 90:918–925, 2002.

    PubMed  Google Scholar 

  25. Labadie, R. F., J. F. Antaki, J. L. Williams, S. Katyal, J. Ligush, S. C. Watkins, S. M. Pham, and H. S. Borovetz. Pulsatile perfusion system for ex vivo investigation of biochemical pathways in intact vascular tissue. Am. J. Physiol. 270:H760–H768, 1996.

    PubMed  Google Scholar 

  26. Langille, B. L. Remodeling of developing and mature arteries: Endothelium, smooth muscle, and matrix. J. Cardiovasc. Pharmacol. 21(S1):S11–S17, 1993.

    PubMed  Google Scholar 

  27. Learoyd, B. M., and M. G. Taylor. Alterations with age in the viscoelastic properties of human arterial walls. Circ. Res. 18:278–292, 1966.

    PubMed  Google Scholar 

  28. Ligush, J., Jr., R. F. Labadie, S. A. Berceli, J. B. Ochoa, and H. S. Borovetz. Evaluation of endothelium-derived nitric oxide mediated vasodilation utilizing ex vivo perfusion of an intact vessel. J. Surg. Res. 52:416–421, 1992.

    PubMed  Google Scholar 

  29. Matsumoto, T., and K. Hayashi. Mechanical and dimensional adaptation of rat aorta to hypertension. J. Biomech. Eng. 116:278–283, 1994.

    PubMed  Google Scholar 

  30. Matsumoto, T., E. Okumura, Y. Miura, and M. Sato. Mechanical and dimensional adaptation of rabbit carotid artery cultured in vitro. Med. Biol. Eng. Comput. 37:252–256, 1999.

    PubMed  Google Scholar 

  31. Merrilees, M. J., B. W. Beaumont, and L. J. Scott. Fluoroprobe quantification of viable and non-viable cells in human coronary and internal thoracic arteries sampled at autopsy. J. Vasc. Res. 32:371–377, 1995.

    PubMed  Google Scholar 

  32. Mitchell, G. M., J. J. McCann, I. W. Rogers, M. J. Hickey, W. A. Morrison, and B. M. O’Brien. A morphological study of the long-term repair process in experimentally stretched but unruptured arteries and veins. Br. J. Plast. Surg. 49:34–40, 1996.

    PubMed  Google Scholar 

  33. Mulvany, M. J. Control of vascular structure. Am. J. Med. 94:20S–23S, 1993.

    PubMed  Google Scholar 

  34. Pollman, M. J., T. Yamada, M. Horiuchi, and G. H. Gibbons. Vasoactive substances regulate vascular smooth muscle cell apoptosis. Countervailing influences of nitric oxide and angiotensin II. Circ. Res. 79:748–756, 1996.

    PubMed  Google Scholar 

  35. Ruiz-Razura, A., E. G. Layton Jr., J. L. Williams Jr., and B. E. Cohen. Clinical applications of acute intraoperative arterial elongation. J. Reconstr. Microsurg. 9:335–340, 1993.

    PubMed  Google Scholar 

  36. Stark, G. B., C. Hong, and J. W. Futrell. Rapid elongation of arteries and veins in rats with a tissue expander. Plast. Reconstr. Surg. 80:570–581, 1987.

    PubMed  Google Scholar 

  37. Sumpio, B. E., and A. J. Banes. Response of porcine aortic smooth muscle cells to cyclic tensional deformation in culture. J. Surg. Res. 44:696–701, 1988.

    PubMed  Google Scholar 

  38. Zarins, C. K., M. A. Zatina, D. P. Giddens, D. N. Ku, and S. Glagov. Shear stress regulation of artery lumen diameter in experimental atherogenesis. J. Vasc. Surg. 5:413–420, 1987.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. Peter Davis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Davis, N.P., Han, HC., Wayman, B. et al. Sustained Axial Loading Lengthens Arteries in Organ Culture. Ann Biomed Eng 33, 867–877 (2005). https://doi.org/10.1007/s10439-005-3488-x

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-005-3488-x

Keywords

Navigation