Skip to main content
SpringerLink
Log in

Transitional Flow in the Venous Side of Patient-Specific Arteriovenous Fistulae for Hemodialysis

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

Abstract

Arteriovenous fistula (AVF) is the first choice for providing vascular access for hemodialysis patients, but maintaining its patency is challenging. AVF failure is primarily due to development of neointimal hyperplasia (NH) and subsequent stenosis. Using idealized models of AVF we previously suggested that reciprocating hemodynamic wall shear is implicated in vessel stenosis. The aim of the present study was to investigate local hemodynamics in patient-specific side-to-end AVF. We reconstructed realistic geometrical models of four AVFs from magnetic resonance images acquired in a previous clinical study. High-resolution computational fluid dynamics simulations using patient-specific blood rheology and flow boundary conditions were performed. We then characterized the flow field and categorized disturbed flow areas by means of established hemodynamic wall parameters. In all AVF, either in upper or lower arm location, we consistently observed transitional laminar to turbulent-like flow developing in the juxta-anastomotic vein and damping towards the venous outflow, but not in the proximal artery. High-frequency fluctuations of the velocity vectors in these areas result in eddies that induce similar oscillations of wall shear stress vector. This condition may importantly impair the physiological response of endothelial cells to blood flow and be responsible for NH formation in newly created AVF.

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

Similar content being viewed by others

References

  1. Al-Jaishi, A. A., M. J. Oliver, S. M. Thomas, C. E. Lok, J. C. Zhang, A. X. Garg, S. D. Kosa, R. R. Quinn, and L. M. Moist. Patency rates of the arteriovenous fistula for hemodialysis: a systematic review and meta-analysis. Am J Kidney Dis 63:464–478, 2014.

    Article  PubMed  Google Scholar 

  2. Antiga, L., M. Piccinelli, L. Botti, B. Ene-Iordache, A. Remuzzi, and D. A. Steinman. An image-based modeling framework for patient-specific computational hemodynamics. Med Biol Eng Comput 46:1097–1112, 2008.

    Article  PubMed  Google Scholar 

  3. Badero, O. J., M. O. Salifu, H. Wasse, and J. Work. Frequency of swing-segment stenosis in referred dialysis patients with angiographically documented lesions. Am J Kidney Dis 51:93–98, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bennett, S., M. S. Hammes, T. Blicharski, S. Watson, and B. Funaki. Characterization of the cephalic arch and location of stenosis. J Vasc Access 16:13–18, 2015.

    Article  PubMed  Google Scholar 

  5. Bode, A., A. Caroli, W. Huberts, N. Planken, L. Antiga, M. Bosboom, A. Remuzzi, and J. Tordoir. Clinical study protocol for the ARCH project—computational modeling for improvement of outcome after vascular access creation. J Vasc Access 12:369–376, 2011.

    Article  PubMed  Google Scholar 

  6. Bode, A. S., R. N. Planken, M. A. Merkx, F. M. van der Sande, L. Geerts, J. H. Tordoir, and T. Leiner. Feasibility of non-contrast-enhanced magnetic resonance angiography for imaging upper extremity vasculature prior to vascular access creation. Eur J Vasc Endovasc Surg 43:88–94, 2012.

    Article  CAS  PubMed  Google Scholar 

  7. Browne, L. D., M. T. Walsh, and P. Griffin. Experimental and numerical analysis of the bulk flow parameters within an arteriovenous fistula. Cardiovasc Eng Technol 6:450–462, 2015.

    Article  PubMed  Google Scholar 

  8. Caroli, A., S. Manini, L. Antiga, K. Passera, B. Ene-Iordache, S. Rota, G. Remuzzi, A. Bode, J. Leermakers, F. N. van de Vosse, R. Vanholder, M. Malovrh, J. Tordoir, and A. Remuzzi. Validation of a patient-specific hemodynamic computational model for surgical planning of vascular access in hemodialysis patients. Kidney Int 84:1237–1245, 2013.

    Article  PubMed  Google Scholar 

  9. Celik, I. B., U. Ghia, P. J. Roache, C. J. Freitas, H. Coleman, and P. E. Raad. Procedure for estimation and reporting of uncertainty due to discretization in CFD applications. J Fluids Eng 130:1–4, 2008.

    Google Scholar 

  10. Chiu, J. J., and S. Chien. Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol Rev 91:327–387, 2011.

    Article  PubMed  Google Scholar 

  11. Davies, P. F. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat Clin Pract Cardiovasc Med 6:16–26, 2009.

    Article  CAS  PubMed  Google Scholar 

  12. Davies, P. F., A. Remuzzi, E. J. Gordon, C. F. Dewey, Jr, and M. A. Gimbrone, Jr. Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc Natl Acad Sci USA 83:2114–2117, 1986.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Decorato, I., Z. Kharboutly, T. Vassallo, J. Penrose, C. Legallais, and A. V. Salsac. Numerical simulation of the fluid structure interactions in a compliant patient-specific arteriovenous fistula. Int J Numer Method Biomed Eng 30:143–159, 2014.

    Article  PubMed  Google Scholar 

  14. Ene-Iordache, B., L. Mosconi, L. Antiga, S. Bruno, A. Anghileri, G. Remuzzi, and A. Remuzzi. Radial artery remodeling in response to shear stress increase within arteriovenous fistula for hemodialysis access. Endothelium 10:95–102, 2003.

    Article  PubMed  Google Scholar 

  15. Ene-Iordache, B., and A. Remuzzi. Disturbed flow in radial-cephalic arteriovenous fistulae for haemodialysis: low and oscillating shear stress locates the sites of stenosis. Nephrol Dial Transplant 27:358–368, 2012.

    Article  PubMed  Google Scholar 

  16. Ene-Iordache, B., C. Semperboni, G. Dubini, and A. Remuzzi. Disturbed flow in a patient-specific arteriovenous fistula for hemodialysis: multidirectional and reciprocating near-wall flow patterns. J Biomech 48:2195–2200, 2015.

    Article  PubMed  Google Scholar 

  17. Fan, L., and T. Karino. Effect of a disturbed flow on proliferation of the cells of a hybrid vascular graft. Biorheology 47:31–38, 2010.

    PubMed  Google Scholar 

  18. Fillinger, M. F., E. R. Reinitz, R. A. Schwartz, D. E. Resetarits, A. M. Paskanik, and C. E. Bredenberg. Beneficial effects of banding on venous intimal-medial hyperplasia in arteriovenous loop grafts. Am J Surg 158:87–94, 1989.

    Article  CAS  PubMed  Google Scholar 

  19. Gallo, D., D. A. Steinman, P. B. Bijari, and U. Morbiducci. Helical flow in carotid bifurcation as surrogate marker of exposure to disturbed shear. J Biomech 45:2398–2404, 2012.

    Article  PubMed  Google Scholar 

  20. Gimbrone, Jr., M. A., and G. Garcia-Cardena. Vascular endothelium, hemodynamics, and the pathobiology of atherosclerosis. Cardiovasc Pathol 22:9–15, 2013.

    Article  CAS  PubMed  Google Scholar 

  21. He, X., and D. N. Ku. Pulsatile flow in the human left coronary artery bifurcation: average conditions. J Biomech Eng 118:74–82, 1996.

    Article  CAS  PubMed  Google Scholar 

  22. He, Y., C. M. Terry, C. Nguyen, S. A. Berceli, Y. T. Shiu, and A. K. Cheung. Serial analysis of lumen geometry and hemodynamics in human arteriovenous fistula for hemodialysis using magnetic resonance imaging and computational fluid dynamics. J Biomech 46:165–169, 2013.

    Article  PubMed  Google Scholar 

  23. Himburg, H. A., and M. H. Friedman. Correspondence of low mean shear and high harmonic content in the porcine iliac arteries. J Biomech Eng 128:852–856, 2006.

    Article  PubMed  Google Scholar 

  24. Jha, V., G. Garcia-Garcia, K. Iseki, Z. Li, S. Naicker, B. Plattner, R. Saran, A. Y. Wang, and C. W. Yang. Chronic kidney disease: global dimension and perspectives. Lancet 382:260–272, 2013.

    Article  PubMed  Google Scholar 

  25. Jia, L., L. Wang, F. Wei, H. Yu, H. Dong, B. Wang, Z. Lu, G. Sun, H. Chen, J. Meng, B. Li, R. Zhang, X. Bi, Z. Wang, H. Pang, and A. Jiang. Effects of wall shear stress in venous neointimal hyperplasia of arteriovenous fistulae. Nephrology (Carlton) 20:335–342, 2015.

    Article  Google Scholar 

  26. Khan, M. O., K. Valen-Sendstad, and D. A. Steinman. Narrowing the expertise gap for predicting intracranial aneurysm hemodynamics: impact of solver numerics versus mesh and time-step resolution. AJNR Am J Neuroradiol 36:1310–1316, 2015.

    Article  CAS  PubMed  Google Scholar 

  27. Lee, T., V. Chauhan, M. Krishnamoorthy, Y. Wang, L. Arend, M. J. Mistry, M. El-Khatib, R. Banerjee, R. Munda, and P. Roy-Chaudhury. Severe venous neointimal hyperplasia prior to dialysis access surgery. Nephrol Dial Transplant 26:2264–2270, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Lee, S. W., D. S. Smith, F. Loth, P. F. Fischer, and H. S. Bassiouny. Importance of flow division on transition to turbulence within an arteriovenous graft. J Biomech 40:981–992, 2007.

    Article  PubMed  Google Scholar 

  29. Leschziner, M. Statistical turbulence modelling for fluid dynamics—demystified: an introductory text for graduate engineering students. London: Imperial College Press, 2015.

    Book  Google Scholar 

  30. Lorensen, W. E., and H. E. Cline. Marching cubes: a high resolution 3D surface construction algorithm. Computer Graphics 21:163–169, 1987.

    Article  Google Scholar 

  31. Loth, F., P. F. Fischer, N. Arslan, C. D. Bertram, S. E. Lee, T. J. Royston, W. E. Shaalan, and H. S. Bassiouny. Transitional flow at the venous anastomosis of an arteriovenous graft: potential activation of the ERK1/2 mechanotransduction pathway. J Biomech Eng 125:49–61, 2003.

    Article  PubMed  Google Scholar 

  32. 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 

  33. Marie, Y., A. Guy, K. Tullett, H. Krishnan, R. G. Jones, and N. G. Inston. Patterns of blood flow as a predictor of maturation of arteriovenous fistula for haemodialysis. J Vasc Access 15:169–174, 2014.

    Article  PubMed  Google Scholar 

  34. McGah, P. M., D. F. Leotta, K. W. Beach, and A. Aliseda. Effects of wall distensibility in hemodynamic simulations of an arteriovenous fistula. Biomech Model Mechanobiol 13:679–695, 2014.

    Article  PubMed  Google Scholar 

  35. McGah, P. M., D. F. Leotta, K. W. Beach, R. Eugene Zierler, and A. Aliseda. Incomplete restoration of homeostatic shear stress within arteriovenous fistulae. J Biomech Eng 135:011005, 2013.

    Article  PubMed  Google Scholar 

  36. Mitra, A. K., D. M. Gangahar, and D. K. Agrawal. Cellular, molecular and immunological mechanisms in the pathophysiology of vein graft intimal hyperplasia. Immunol Cell Biol 84:115–124, 2006.

    Article  CAS  PubMed  Google Scholar 

  37. Moffatt, H. K., and A. Tsinober. Helicity in laminar and turbulent flow. Ann Rev Fluid Mech 24:281–312, 1992.

    Article  Google Scholar 

  38. Mohamied, Y., E. M. Rowland, E. L. Bailey, S. J. Sherwin, M. A. Schwartz, and P. D. Weinberg. Change of direction in the biomechanics of atherosclerosis. Ann Biomed Eng 43:16–25, 2015.

    Article  PubMed  Google Scholar 

  39. Morbiducci, U., R. Ponzini, D. Gallo, C. Bignardi, and G. Rizzo. Inflow boundary conditions for image-based computational hemodynamics: impact of idealized versus measured velocity profiles in the human aorta. J Biomech 46:102–109, 2013.

    Article  PubMed  Google Scholar 

  40. Morbiducci, U., R. Ponzini, M. Grigioni, and A. Redaelli. Helical flow as fluid dynamic signature for atherogenesis risk in aortocoronary bypass. A numeric study. J Biomech 40:519–534, 2007.

    Article  PubMed  Google Scholar 

  41. NKF, KDOQI. Clinical practice guidelines for vascular access. Am J Kidney Dis 48:S248–S273, 2006.

    Article  Google Scholar 

  42. Noris, M., M. Morigi, R. Donadelli, S. Aiello, M. Foppolo, M. Todeschini, S. Orisio, G. Remuzzi, and A. Remuzzi. Nitric oxide synthesis by cultured endothelial cells is modulated by flow conditions. Circ Res 76:536–543, 1995.

    Article  CAS  PubMed  Google Scholar 

  43. OpenFoam. The OpenFOAM Foundation. http://www.openfoam.org, 2014.

  44. Peiffer, V., S. J. Sherwin, and P. D. Weinberg. Computation in the rabbit aorta of a new metric—the transverse wall shear stress—to quantify the multidirectional character of disturbed blood flow. J Biomech 46:2651–2658, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Potter, C. M., M. H. Lundberg, L. S. Harrington, C. M. Warboys, T. D. Warner, R. E. Berson, A. V. Moshkov, J. Gorelik, P. D. Weinberg, and J. A. Mitchell. Role of shear stress in endothelial cell morphology and expression of cyclooxygenase isoforms. Arterioscler Thromb Vasc Biol 31:384–391, 2011.

    Article  CAS  PubMed  Google Scholar 

  46. Remuzzi, A., and B. Ene-Iordache. Novel paradigms for dialysis vascular access: upstream hemodynamics and vascular remodeling in dialysis access stenosis. Clin J Am Soc Nephrol 8:2186–2193, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Remuzzi, A., B. Ene-Iordache, L. Mosconi, S. Bruno, A. Anghileri, L. Antiga, and G. Remuzzi. Radial artery wall shear stress evaluation in patients with arteriovenous fistula for hemodialysis access. Biorheology 40:423–430, 2003.

    PubMed  Google Scholar 

  48. Roy-Chaudhury, P., Y. Wang, M. Krishnamoorthy, J. Zhang, R. Banerjee, R. Munda, S. Heffelfinger, and L. Arend. Cellular phenotypes in human stenotic lesions from haemodialysis vascular access. Nephrol Dial Transplant 24:2786–2791, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Sethian, J. A. Level set methods and marching cubes methods: evolving interfaces in computational geometry, fluid mechanics, computer vision and materials science, Vol. 3. Cambridge: Cambridge University Press, 1999.

    Google Scholar 

  50. Sigovan, M., V. Rayz, W. Gasper, H. F. Alley, C. D. Owens, and D. Saloner. Vascular remodeling in autogenous arterio-venous fistulas by MRI and CFD. Ann Biomed Eng 41:657–668, 2013.

    Article  PubMed  Google Scholar 

  51. Valen-Sendstad, K., M. Piccinelli, and D. A. Steinman. High-resolution computational fluid dynamics detects flow instabilities in the carotid siphon: implications for aneurysm initiation and rupture? J Biomech 47:3210–3216, 2014.

    Article  PubMed  Google Scholar 

  52. Van Canneyt, K., U. Morbiducci, S. Eloot, G. De Santis, P. Segers, and P. Verdonck. A computational exploration of helical arterio-venous graft designs. J Biomech 46:345–353, 2013.

    Article  PubMed  Google Scholar 

  53. Wang, C., B. M. Baker, C. S. Chen, and M. A. Schwartz. Endothelial cell sensing of flow direction. Arterioscler Thromb Vasc Biol 33:2130–2136, 2013.

    Article  CAS  PubMed  Google Scholar 

  54. Yamamoto, K., C. D. Protack, G. Kuwahara, M. Tsuneki, T. Hashimoto, M. R. Hall, R. Assi, K. E. Brownson, T. R. Foster, H. Bai, M. Wang, J. A. Madri, and A. Dardik. Disturbed shear stress reduces Klf2 expression in arterial-venous fistulae in vivo. Physiol Rep 3:e12348, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Yang, N., S. Deutsch, E. G. Paterson, and K. B. Manning. Numerical study of blood flow at the end-to-side anastomosis of a left ventricular assist device for adult patients. J Biomech Eng 131:111005, 2009.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Prof. Gabriele Dubini from Politecnico di Milano for helpful discussion. We acknowledge the ARCH Consortium colleagues for gaining the CE-MRA data during the clinical study (ARCH Project No. FP7-ICT-224390). Part of this study was presented at the 41st Annual ESAO Congress in Rome, Italy.

Author information

Author notes

    Authors and Affiliations

    1. Department of Biomedical Engineering, IRCCS - Istituto di Ricerche Farmacologiche “Mario Negri”, Via G.B. Camozzi, 3, 24020, Ranica, BG, Italy

      Michela Bozzetto, Bogdan Ene-Iordache & Andrea Remuzzi

    2. Department of Management, Information and Production and Engineering, University of Bergamo, Viale Marconi, 5, Dalmine, 24044, BG, Italy

      Andrea Remuzzi

    Authors
    1. Michela Bozzetto
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Bogdan Ene-Iordache
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Andrea Remuzzi
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Andrea Remuzzi.

    Additional information

    Associate Editor Ender Finol oversaw the review of this article.

    Michela Bozzetto and Bogdan Ene-Iordache contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (MP4 375 kb)

    Supplementary material 2 (PDF 1072 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Bozzetto, M., Ene-Iordache, B. & Remuzzi, A. Transitional Flow in the Venous Side of Patient-Specific Arteriovenous Fistulae for Hemodialysis. Ann Biomed Eng 44, 2388–2401 (2016). https://doi.org/10.1007/s10439-015-1525-y

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10439-015-1525-y

    Keywords

    Search

    Navigation