Skip to main content
SpringerLink
Log in

Association of Intraluminal Thrombus, Hemodynamic Forces, and Abdominal Aortic Aneurysm Expansion Using Longitudinal CT Images

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

Abstract

While hemodynamic forces and intraluminal thrombus (ILT) are believed to play important roles on abdominal aortic aneurysm (AAA), it has been suggested that hemodynamic forces and ILT also interact with each other, making it a complex problem. There is, however, a pressing need to understand relationships among three factors: hemodynamics, ILT accumulation, and AAA expansion for AAA prognosis. Hence this study used longitudinal computer tomography scans from 14 patients and analyzed the relationship between them. Hemodynamic forces, represented by wall shear stress (WSS), were obtained from computational fluid dynamics; ILT accumulation was described by ILT thickness distribution changes between consecutives scans, and ILT accumulation and AAA expansion rates were estimated from changes in ILT and AAA volume. Results showed that, while low WSS was observed at regions where ILT accumulated, the rate at which ILT accumulated occurred at the same rate as the aneurysm expansion. Comparison between AAAs with and without thrombus showed that aneurysm with ILT recorded lower values of WSS and higher values of AAA expansion than those without thrombus. Findings suggest that low WSS may promote ILT accumulation and submit the idea that by increasing WSS levels ILT accumulation may be prevented.

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

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9
Figure 10

Similar content being viewed by others

References

  1. Arzani, A., G.-Y. Suh, R. L. Dalman, and S. C. Shadden. A longitudinal comparison of hemodynamics and intraluminal thrombus deposition in abdominal aortic aneurysms. Am. J. Physiol.—Heart Circ. Physiol. 2014. doi:10.1152/ajpheart.00461.2014.

  2. Basciano, C., C. Kleinstreuer, S. Hyun, and E. A. Finol. A relation between near-wall particle-hemodynamics and onset of thrombus formation in abdominal aortic aneurysms. Ann. Biomed. Eng. 39:2010–2026, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Biasetti, J., T. C. Gasser, M. Auer, U. Hedin, and F. Labruto. Hemodynamics of the normal aorta compared to fusiform and saccular abdominal aortic aneurysms with emphasis on a potential thrombus formation mechanism. Ann. Biomed. Eng. 38:380–390, 2009.

    Article  Google Scholar 

  4. Bluestein, D., K. Dumont, M. De Beule, J. Ricotta, P. Impellizzeri, B. Verhegghe, and P. Verdonck. Intraluminal thrombus and risk of rupture in patient specific abdominal aortic aneurysm—FSI modelling. Comput. Methods Biomech. Biomed. Engin. 12:73–81, 2009.

    Article  PubMed  Google Scholar 

  5. Boussel, L., V. Rayz, C. McCulloch, A. Martin, G. Acevedo-Bolton, M. Lawton, R. Higashida, W. S. Smith, W. L. Young, and D. Saloner. Aneurysm growth occurs at region of low wall shear stress: patient-specific correlation of hemodynamics and growth in a longitudinal study. Stroke 39:2997, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Brady, A. R., S. G. Thompson, F. G. Fowkes, R. M. Greenhalgh, and J. T. Powell. Abdominal aortic aneurysm expansion risk factors and time intervals for surveillance. Circulation 110:16–21, 2004.

    Article  PubMed  Google Scholar 

  7. Chatzizisis, Y. S., A. U. Coskun, M. Jonas, E. R. Edelman, C. L. Feldman, and P. H. Stone. Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling. J. Am. Coll. Cardiol. 49:2379–2393, 2007.

    Article  CAS  PubMed  Google Scholar 

  8. Dalman, R. L. Oxidative stress and abdominal aneurysms: how aortic hemodynamic conditions may influence AAA disease. Cardiovasc. Surg. Lond. Engl. 11:417–419, 2003.

    Article  Google Scholar 

  9. Di Achille, P., G. Tellides, C. A. Figueroa, and J. D. Humphrey. A haemodynamic predictor of intraluminal thrombus formation in abdominal aortic aneurysms. Proc. R. Soc. Lond. Math. Phys. Eng. Sci. 470:20140163, 2014.

    Article  Google Scholar 

  10. Di Martino, E. S., A. Bohra, J. P. Vande Geest, N. Gupta, M. S. Makaroun, and D. A. Vorp. Biomechanical properties of ruptured versus electively repaired abdominal aortic aneurysm wall tissue. J. Vasc. Surg. 43:570–576, 2006.

    Article  PubMed  Google Scholar 

  11. Di Martino, E. S., S. Mantero, F. Inzoli, G. Melissano, D. Astore, R. Chiesa, and R. Fumero. Biomechanics of abdominal aortic aneurysm in the presence of endoluminal thrombus: experimental characterisation and structural static computational analysis. Eur. J. Vasc. Endovasc. Surg. 15:290–299, 1998.

    Article  PubMed  Google Scholar 

  12. Doyle, B. J., T. M. McGloughlin, E. G. Kavanagh, and P. R. Hoskins. From detection to rupture: a serial computational fluid dynamics case study of a rapidly expanding, patient-specific, ruptured abdominal aortic aneurysm. In: Computational Biomechanics for Medicine, edited by B. Doyle, K. Miller, A. Wittek, and P. M. F. Nielsen. New York: Springer, 2014, pp. 53–68.

    Chapter  Google Scholar 

  13. Dua, M. M., and R. L. Dalman. Hemodynamic influences on abdominal aortic aneurysm disease: application of biomechanics to aneurysm pathophysiology. Vascul. Pharmacol. 53:11–21, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Farsad, M., B. Zambrano, and S. Baek. Association of intraluminal thrombus, hemodynamic forces, and abdominal aortic aneurysm expansion using longitudinal CT images. In: Computational Biomechanics for Medicine. Berlin: Springer, 2015, pp. 13–23.

  15. Finol, E. A., and C. H. Amon. Flow-induced wall shear stress in abdominal aortic aneurysms: part I-steady flow hemodynamics. Comput. Methods Biomech. Biomed. Eng. 5:309–318, 2002.

    Article  Google Scholar 

  16. Finol, E. A., and C. H. Amon. Flow-induced wall shear stress in abdominal aortic aneurysms: part II-pulsatile flow hemodynamics. Comput. Methods Biomech. Biomed. Eng. 5:319–328, 2002.

    Article  Google Scholar 

  17. Folkesson, M., A. Silveira, P. Eriksson, and J. Swedenborg. Protease activity in the multi-layered intra-luminal thrombus of abdominal aortic aneurysms. Atherosclerosis 218:294–299, 2011.

    Article  CAS  PubMed  Google Scholar 

  18. Gaillard, E., P. Bergeron, and V. Deplano. Influence of wall compliance on hemodynamics in models of abdominal aortic aneurysm. J. Endovasc. Ther. 14:593–599, 2007.

    Article  PubMed  Google Scholar 

  19. Georgakarakos, E., C. V. Ioannou, S. Volanis, Y. Papaharilaou, J. Ekaterinaris, and A. N. Katsamouris. The influence of intraluminal thrombus on abdominal aortic aneurysm wall stress. Int. Angiol. 28:325–333, 2009.

    CAS  PubMed  Google Scholar 

  20. Gharahi, H., B. A. Zambrano, C. Lim, J. Choi, W. Lee, and S. Baek. On growth measurements of abdominal aortic aneurysms using maximally inscribed sphere. Med. Eng. Phys. 37:683–691, 2015.

    Article  CAS  PubMed  Google Scholar 

  21. Gijsen, F. J. H., F. N. van de Vosse, and J. D. Janssen. Wall shear stress in backward-facing step flow of a red blood cell suspension. Biorheology 35:263–279, 1998.

    Article  CAS  PubMed  Google Scholar 

  22. Gijsen, F. J., F. N. van de Vosse, and J. D. Janssen. The influence of the non-Newtonian properties of blood on the flow in large arteries: steady flow in a carotid bifurcation model. J. Biomech. 32:601–608, 1999.

    Article  CAS  PubMed  Google Scholar 

  23. Gimbrone, M. A., K. R. Anderson, J. N. Topper, et al. Special communication: the critical role of mechanical forces in blood vessel development, physiology and pathology. J. Vasc. Surg. 29:1104–1151, 1999.

    Article  PubMed  Google Scholar 

  24. Hans, S. S., O. Jareunpoon, M. Balasubramaniam, and G. B. Zelenock. Size and location of thrombus in intact and ruptured abdominal aortic aneurysms. J. Vasc. Surg. 41:584–588, 2005.

    Article  PubMed  Google Scholar 

  25. Hansen, K. B., A. Arzani, and S. C. Shadden. Mechanical platelet activation potential in abdominal aortic aneurysms. J. Biomech. Eng. 137:041005–041005, 2015.

    Article  PubMed  Google Scholar 

  26. Harter, L. P., B. H. Gross, P. W. Callen, and R. A. Barth. Ultrasonic evaluation of abdominal aortic thrombus. J. Ultrasound Med. 1:315–318, 1982.

    CAS  PubMed  Google Scholar 

  27. Humphrey, J. D. Vascular adaptation and mechanical homeostasis at tissue, cellular, and sub-cellular levels. Cell Biochem. Biophys. 50:53–78, 2008.

    Article  CAS  PubMed  Google Scholar 

  28. Kazi, M., J. Thyberg, P. Religa, J. Roy, P. Eriksson, U. Hedin, and J. Swedenborg. Influence of intraluminal thrombus on structural and cellular composition of abdominal aortic aneurysm wall. J. Vasc. Surg. 38:1283–1292, 2003.

    Article  PubMed  Google Scholar 

  29. Les, A. S., S. C. Shadden, C. A. Figueroa, J. M. Park, M. M. Tedesco, R. J. Herfkens, R. L. Dalman, and C. A. Taylor. Quantification of hemodynamics in abdominal aortic aneurysms during rest and exercise using magnetic resonance imaging and computational fluid dynamics. Ann. Biomed. Eng. 38:1288–1313, 2010.

    Article  PubMed  Google Scholar 

  30. Li, Z.-Y., J. U-King-Im, T. Y. Tang, E. Soh, T. C. See, and J. H. Gillard. Impact of calcification and intraluminal thrombus on the computed wall stresses of abdominal aortic aneurysm. J. Vasc. Surg. 47:928–935, 2008.

  31. Malek, A. M., S. L. Alper, and S. Izumo. Hemodynamic shear stress and its role in atherosclerosis. JAMA 282:2035–2042, 1999.

    Article  CAS  PubMed  Google Scholar 

  32. Mower, W. R., W. J. Quiñones, and S. S. Gambhir. Effect of intraluminal thrombus on abdominal aortic aneurysm wall stress. J. Vasc. Surg. 26:602–608, 1997.

  33. Nakahashi, T. K., K. Hoshina, P. S. Tsao, E. Sho, M. Sho, J. K. Karwowski, C. Yeh, R.-B. Yang, J. N. Topper, and R. L. Dalman. Flow loading induces macrophage antioxidative gene expression in experimental aneurysms. Arterioscler. Thromb. Vasc. Biol. 22:2017–2022, 2002.

    Article  CAS  PubMed  Google Scholar 

  34. Olufsen, M. S., C. S. Peskin, W. Y. Kim, E. M. Pedersen, A. Nadim, and J. Larsen. Numerical simulation and experimental validation of blood flow in arteries with structured-tree outflow conditions. Ann. Biomed. Eng. 28:1281–1299, 2000.

    Article  CAS  PubMed  Google Scholar 

  35. Raghavan, M. L., J. Kratzberg, E. M. Castro de Tolosa, M. M. Hanaoka, P. Walker, and E. S. da Silva. Regional distribution of wall thickness and failure properties of human abdominal aortic aneurysm. J. Biomech. 39:3010–3016, 2006.

  36. Raghavan, M. L., D. A. Vorp, M. P. Federle, M. S. Makaroun, and M. W. Webster. Wall stress distribution on three-dimensionally reconstructed models of human abdominal aortic aneurysm. J. Vasc. Surg. 31:760–769, 2000.

    Article  CAS  PubMed  Google Scholar 

  37. Salsac, A. V., S. R. Sparks, J. M. Chomaz, and J. C. Lasheras. Evolution of the wall shear stresses during the progressive enlargement of symmetric abdominal aortic aneurysms. J. Fluid Mech. 560:19–51, 2006.

    Article  Google Scholar 

  38. Schurink, G. W., J. M. van Baalen, M. J. Visser, and J. H. van Bockel. Thrombus within an aortic aneurysm does not reduce pressure on the aneurysmal wall. J. Vasc. Surg. 31:501–506, 2000.

    Article  CAS  PubMed  Google Scholar 

  39. Sheidaei, A., S. C. Hunley, S. Zeinali-Davarani, L. G. Raguin, and S. Baek. Simulation of abdominal aortic aneurysm growth with updating hemodynamic loads using a realistic geometry. Med. Eng. Phys. 33:80–88, 2011.

    Article  CAS  PubMed  Google Scholar 

  40. Shindo, S., H. Matsumoto, K. Kubota, A. Kojima, M. Matsumoto, K. Satoh, and Y. Ozaki. Is the size of an abdominal aortic aneurysm associated with coagulopathy? World J. Surg. 29:925–929, 2005.

    Article  PubMed  Google Scholar 

  41. Shum, J., E. S. DiMartino, A. Goldhamme, D. H. Goldman, L. C. Acker, G. Patel, J. H. Ng, G. Martufi, and E. A. Finol. Semiautomatic vessel wall detection and quantification of wall thickness in computed tomography images of human abdominal aortic aneurysms. Med. Phys. 37:638–648, 2010.

    Article  PubMed  Google Scholar 

  42. Silver, A. E., and J. A. Vita. Shear stress-mediated arterial remodeling in atherosclerosis too much of a good thing? Circulation 113:2787–2789, 2006.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Swedenborg, J., and P. Eriksson. The intraluminal thrombus as a source of proteolytic activity. Ann. N. Y. Acad. Sci. 1085:133–138, 2006.

    Article  CAS  PubMed  Google Scholar 

  44. Taylor, C. A., T. J. R. Hughes, and C. K. Zarins. Effect of exercise on hemodynamic conditions in the abdominal aorta. J. Vasc. Surg. 29:1077–1089, 1999.

    Article  CAS  PubMed  Google Scholar 

  45. Thubrikar, M. J., M. Labrosse, F. Robicsek, J. Al-Soudi, and B. Fowler. Mechanical properties of abdominal aortic aneurysm wall. J. Med. Eng. Technol. 25:133–142, 2001.

    Article  CAS  PubMed  Google Scholar 

  46. Thubrikar, M. J., F. Robicsek, M. Labrosse, V. Chervenkoff, and B. L. Fowler. Effect of thrombus on abdominal aortic aneurysm wall dilation and stress. J. Cardiovasc. Surg. (Torino) 44:67–77, 2003.

    CAS  Google Scholar 

  47. Vardulaki, K. A., T. C. Prevost, N. M. Walker, N. E. Day, A. B. Wilmink, C. R. Quick, H. A. Ashton, and R. A. Scott. Growth rates and risk of rupture of abdominal aortic aneurysms. Br. J. Surg. 85:1674–1680, 1998.

    Article  CAS  PubMed  Google Scholar 

  48. Vorp, D. A., W. J. Federspiel, and M. W. Webster. Does laminated intraluminal thrombus within abdominal aortic aneurysm cause anoxia of the aortic wall? J. Vasc. Surg. 23:540–541, 1996.

  49. Vorp, D. A., P. C. Lee, D. H. Wang, M. S. Makaroun, E. M. Nemoto, S. Ogawa, and M. W. Webster. Association of intraluminal thrombus in abdominal aortic aneurysm with local hypoxia and wall weakening. J. Vasc. Surg. 34:291–299, 2001.

    Article  CAS  PubMed  Google Scholar 

  50. Wang, D. H., M. S. Makaroun, M. W. Webster, and D. A. Vorp. Effect of intraluminal thrombus on wall stress in patient-specific models of abdominal aortic aneurysm. J. Vasc. Surg. 36:598–604, 2002.

    Article  PubMed  Google Scholar 

  51. Wilson, J. S., L. Virag, P. Di Achille, I. Karsaj, and J. D. Humphrey. Biochemomechanics of intraluminal thrombus in abdominal aortic aneurysms. J. Biomech. Eng. 135:021011, 2013.

    Article  CAS  PubMed  Google Scholar 

  52. Wood, N. B. Aspects of fluid dynamics applied to the larger arteries. J. Theor. Biol. 199:137–161, 1999.

    Article  CAS  PubMed  Google Scholar 

  53. Yu, S. C. M. Steady and pulsatile flow studies in abdominal aortic aneurysm models using particle image velocimetry. Int. J. Heat Fluid Flow 21:74–83, 2000.

    Article  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the support, in part, by the National Heart, Lung, and Blood Institute of the National Institutes of Health (R01HL115185 and R21HL113857) and National Science Foundation (CMMI-1150376). The contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH and NSF.

Author information

Authors and Affiliations

  1. Department of Mechanical Engineering, Michigan State University, 2555 Engineering Building, East Lansing, MI, 48824, USA

    Byron A. Zambrano, Hamidreza Gharahi, Farhad A. Jaberi, Jongeun Choi & Seungik Baek

  2. Department of Statistics and Probability, Michigan State University, 2555 Engineering Building, East Lansing, MI, 48824, USA

    ChaeYoung Lim

  3. Department of Electrical and Computer Engineering, Michigan State University, 2555 Engineering Building, East Lansing, MI, 48824, USA

    Jongeun Choi

  4. Department of Radiology, 101 Daehangno, Jongno-gu, Seoul, Korea

    Whal Lee

Authors
  1. Byron A. Zambrano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hamidreza Gharahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. ChaeYoung Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Farhad A. Jaberi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jongeun Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Whal Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Seungik Baek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Seungik Baek.

Additional information

Associate Editor Ender Finol 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

Zambrano, B.A., Gharahi, H., Lim, C. et al. Association of Intraluminal Thrombus, Hemodynamic Forces, and Abdominal Aortic Aneurysm Expansion Using Longitudinal CT Images. Ann Biomed Eng 44, 1502–1514 (2016). https://doi.org/10.1007/s10439-015-1461-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-015-1461-x

Keywords

Search

Navigation