Abstract
Venous tortuosity is associated with multiple disease states and is often thought to be a consequence of venous hypertension and chronic venous disease. However, the underlying mechanisms of vein tortuosity are unclear. We hypothesized that increased pressure causes vein buckling that leads to a tortuous appearance. The specific aim of this study was to determine the critical buckling pressure of veins. We determined the buckling pressure of porcine jugular veins and measured the mechanical properties of these veins. Our results showed that the veins buckle when the transmural pressure exceeds a critical pressure that is strongly related to the axial stretch ratio in the veins. The critical pressures of the eight veins tested were 14.2 ± 5.4 and 26.4 ± 9.0 mmHg at axial stretch ratio 1.5 and 1.7, respectively. In conclusion, veins buckle into a tortuous shape at high lumen pressures or reduced axial stretch ratios. Our results are useful in understanding the development of venous tortuosity associated with varicose veins, venous valvular insufficiency, diabetic retinopathy, and vein grafts.
Similar content being viewed by others
References
Balaz, P., S. Rokosny, D. Klein, and M. Adamec. Aneurysmorrhaphy is an easy technique for arteriovenous fistula salvage. J. Vasc. Access 9(2):81–84, 2008.
Baumann, U. A., C. Marquis, C. Stoupis, T. A. Willenberg, J. Takala, and S. M. Jakob. Estimation of central venous pressure by ultrasound. Resuscitation 64(2):193–199, 2005.
Bergan, J. J., L. Pascarella, and G. W. Schmid-Schonbein. Pathogenesis of primary chronic venous disease: insights from animal models of venous hypertension. J. Vasc. Surg. 47(1):183–192, 2008.
Beris, A. E., P. N. Soucacos, and A. S. Touliatos. Experimental evaluation of the length of microvenous grafts under normal tension. Microsurgery 13(4):195–199, 1992.
Blankenship, J. C., J. A. Narke, and J. W. Roberts. Transluminal extraction catheter atherectomy in long saphenous vein grafts. Cathet. Cardiovasc. Diagn. 35(4):368–372, 1995.
Brown, W. R., D. M. Moody, V. R. Challa, C. R. Thore, and J. A. Anstrom. Venous collagenosis and arteriolar tortuosity in leukoaraiosis. J. Neurol. Sci. 203–204:159–163, 2002.
Canonico, S., C. Gallo, G. Paolisso, F. Pacifico, G. Signoriello, G. Sciaudone, N. Ferrara, V. Piegari, M. Varricchio, and F. Rengo. Prevalence of varicose veins in an Italian elderly population. Angiology 49(2):129–135, 1998.
Cheung, A. T., R. V. Perez, and P. C. Chen. Improvements in diabetic microangiopathy after successful simultaneous pancreas-kidney transplantation: a computer-assisted intravital microscopy study on the conjunctival microcirculation. Transplantation 68(7):927–932, 1999.
Cheung, A. T., A. R. Price, P. L. Duong, S. Ramanujam, J. Gut, E. C. Larkin, P. C. Chen, and D. M. Wilson. Microvascular abnormalities in pediatric diabetic patients. Microvasc. Res. 63(3):252–258, 2002.
Daniels, S. R., M. J. Lipman, M. J. Burke, and J. M. Loggie. The prevalence of retinal vascular abnormalities in children and adolescents with essential hypertension. Am. J. Ophthalmol. 111(2):205–208, 1991.
Dean, L. S., C. J. George, G. S. Roubin, E. D. Kennard, D. R. Holmes, Jr., S. B. King, 3rd, R. E. Vlietstra, J. W. Moses, D. Kereiakes, J. P. Carrozza, Jr., S. G. Ellis, J. R. Margolis, and K. M. Detre. Bailout and corrective use of Gianturco-Roubin flex stents after percutaneous transluminal coronary angioplasty: operator reports and angiographic core laboratory verification from the National Heart, Lung, and Blood Institute/New Approaches to Coronary Intervention Registry. J. Am. Coll. Cardiol. 29(5):934–940, 1997.
Ellis, S. G. Coronary lesions at increased risk. Am. Heart J. 130(3 Pt 2):643–646, 1995.
Field, M., K. MacNamara, G. Bailey, A. Jaipersad, R. H. Morgan, and A. D. Pherwani. Primary patency rates of AV fistulas and the effect of patient variables. J. Vasc. Access 9(1):45–50, 2008.
Fung, Y. C. Biomechanics: Mechanical Properties of Living Tissues (2nd ed.). New YorK: Springer Verlag, 1993.
Fung, Y. C. Biomechanics: Circulation, Chapter 4 (2nd ed.). New York: Springer, 1997.
Han, H. C. A biomechanical model of artery buckling. J. Biomech. 40(16):3672–3678, 2007.
Han, H. C. Nonlinear buckling of blood vessels: a theoretical study. J. Biomech. 41(12):2708–2713, 2008.
Han, H. C. Blood vessel buckling within soft surrounding tissue generates tortuosity. J. Biomech. 42(16):2797–2801, 2009.
Han, H. C., D. N. Ku, and R. P. Vito. Arterial wall adaptation under elevated longitudinal stretch in organ culture. Ann. Biomed. Eng. 31(4):403–411, 2003.
Han, H. C., L. Zhao, M. Huang, L. S. Hou, Y. T. Huang, and Z. B. Kuang. Postsurgical changes of the opening angle of canine autogenous vein graft. J. Biomech. Eng. 120(2):211–216, 1998.
Hughes, A. D., E. Martinez-Perez, A. S. Jabbar, A. Hassan, N. W. Witt, P. D. Mistry, N. Chapman, A. V. Stanton, G. Beevers, R. Pedrinelli, K. H. Parker, and S. A. Thom. Quantification of topological changes in retinal vascular architecture in essential and malignant hypertension. J. Hypertens. 24(5):889–894, 2006.
Hutchins, G. M., M. M. Miner, and B. H. Bulkley. Tortuosity as an index of the age and diameter increase of coronary collateral vessels in patients after acute myocardial infarction. Am. J. Cardiol. 41(2):210–215, 1978.
Jaggy, C., M. Lachat, D. Inderbitzin, B. Leskosek, D. Candinas, T. Burkhard, and M. Turina. Optimized veno-venous bypass with the affinity pump. ASAIO J. 47(1):56–59, 2001.
Jogiya, A., and C. Sandy. Mild optic nerve hypoplasia with retinal venous tortuosity in aarskog (facial-digital-genital) syndrome. Ophthalmic Genet. 26(3):139–141, 2005.
Kockx, M. M., M. W. Knaapen, H. E. Bortier, K. M. Cromheeke, O. Boutherin-Falson, and M. Finet. Vascular remodeling in varicose veins. Angiology 49(11):871–877, 1998.
Komsuoglu, B., O. Goldeli, K. Kulan, B. Cetinarslan, and S. S. Komsuoglu. Prevalence and risk factors of varicose veins in an elderly population. Gerontology 40(1):25–31, 1994.
Kylstra, J. A., T. Wierzbicki, M. L. Wolbarsht, M. B. Landers, 3rd, and E. Stefansson. The relationship between retinal vessel tortuosity, diameter, and transmural pressure. Graefes Arch. Clin. Exp. Ophthalmol. 224(5):477–480, 1986.
Lai, C. M., S. A. Dunlop, L. A. May, M. Gorbatov, M. Brankov, W. Y. Shen, N. Binz, Y. K. Lai, C. E. Graham, C. J. Barry, I. J. Constable, L. D. Beazley, and E. P. Rakoczy. Generation of transgenic mice with mild and severe retinal neovascularisation. Br. J. Ophthalmol. 89(7):911–916, 2005.
Liu, Q., D. Mirc, and B. M. Fu. Mechanical mechanisms of thrombosis in intact bent microvessels of rat mesentery. J. Biomech. 41(12):2726–2734, 2008.
Moody, D. M., W. R. Brown, V. R. Challa, H. S. Ghazi-Birry, and D. M. Reboussin. Cerebral microvascular alterations in aging, leukoaraiosis, and Alzheimer’s disease. Ann. N. Y. Acad. Sci. 826:103–116, 1997.
Oster, S. F., D. S. McLeod, T. Otsuji, M. F. Goldberg, and G. A. Lutty. Preliminary ocular histopathological observations on heterozygous NEMO-deficient mice. Exp. Eye Res. 88(3):613–616, 2009.
Owen, C. G., R. S. Newsom, A. R. Rudnicka, S. A. Barman, E. G. Woodward, and T. J. Ellis. Diabetes and the tortuosity of vessels of the bulbar conjunctiva. Ophthalmology 115(6):e27–e32, 2008.
Owens, C. D., F. J. Rybicki, N. Wake, A. Schanzer, D. Mitsouras, M. D. Gerhard-Herman, and M. S. Conte. Early remodeling of lower extremity vein grafts: inflammation influences biomechanical adaptation. J. Vasc. Surg. 47(6):1235–1242, 2008.
Pascarella, L., and G. W. Schmid Schonbein. Causes of telengiectasias, reticular veins, and varicose veins. Semin. Vasc. Surg. 18(1):2–4, 2005.
Pedley, T. J., and X. Y. Luo. Modelling flow and oscillations in collapsible tubes. Theoret. Comp. Fluid Dynamics 10:277–294, 1998.
Raffetto, J. D., and R. A. Khalil. Matrix metalloproteinases in venous tissue remodeling and varicose vein formation. Curr. Vasc. Pharmacol. 6(3):158–172, 2008.
Raffetto, J. D., and R. A. Khalil. Mechanisms of varicose vein formation: valve dysfunction and wall dilation. Phlebology 23(2):85–98, 2008.
Saaristo, A., T. Veikkola, B. Enholm, M. Hytonen, J. Arola, K. Pajusola, P. Turunen, M. Jeltsch, M. J. Karkkainen, D. Kerjaschki, H. Bueler, S. Yla-Herttuala, and K. Alitalo. Adenoviral VEGF-C overexpression induces blood vessel enlargement, tortuosity, and leakiness but no sprouting angiogenesis in the skin or mucous membranes. FASEB J. 16(9):1041–1049, 2002.
Schneider, P. R., J. Pribaz, and R. C. Russell. Microvenous graft length determination for arterial repair. Ann. Plast. Surg. 17(4):292–298, 1986.
Takase, S., L. Pascarella, J. J. Bergan, and G. W. Schmid-Schonbein. Hypertension-induced venous valve remodeling. J. Vasc. Surg. 39(6):1329–1334, 2004.
Tanaka, T. T., and Y. C. Fung. Elastic and inelastic properties of the canine aorta and their variation along the aortic tree. J. Biomech. 7(4):357–370, 1974.
Timoshenko, S. P., and J. M. Gere. Theory of Elastic Stability (2nd ed.). New York: McGraw-Hill, 1963.
Wakefield, T. W., D. D. Myers, and P. K. Henke. Mechanisms of venous thrombosis and resolution. Arterioscler. Thromb. Vasc. Biol. 28(3):387–391, 2008.
Wong, A. P., N. Nili, Z. S. Jackson, B. Qiang, H. Leong-Poi, R. Jaffe, E. Raanani, P. W. Connelly, J. D. Sparkes, and B. H. Strauss. Expansive remodeling in venous bypass grafts: novel implications for vein graft disease. Atherosclerosis 196(2):580–589, 2008.
Acknowledgments
This work was supported by a CAREER award # 0646646 and a REU supplement from the National Science Foundation. It was also partially supported by research grants from NSF (0602834), the Veterans Administration, and the National Institute of Health (HL074236 & HL095852). We thank Dr. Yong-Ung Lee and Miss Danika Hayman for their help in this study.
Author information
Authors and Affiliations
Corresponding author
Additional information
Associate Editor Jane Grande-Allen oversaw the review of this article.
Rights and permissions
About this article
Cite this article
Martinez, R., Fierro, C.A., Shireman, P.K. et al. Mechanical Buckling of Veins Under Internal Pressure. Ann Biomed Eng 38, 1345–1353 (2010). https://doi.org/10.1007/s10439-010-9929-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10439-010-9929-1