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Tortuosity of Coronary Bifurcation as a Potential Local Risk Factor for Atherosclerosis: CFD Steady State Study Based on In Vivo Dynamic CT Measurements

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Abstract

The purpose of the present study was to determine whether in vivo bifurcation geometric factors would permit prediction of the risk of atherosclerosis. It is worldwide accepted that low or oscillatory wall shear stress (WSS) is a robust hemodynamic factor in the development of atherosclerotic plaque and has a strong correlation with the local site of plaque deposition. However, it still remains unclear how coronary bifurcation geometries are correlated with such hemodynamic forces. Computational fluid dynamics simulations were performed on left main (LM) coronary bifurcation geometries derived from CT of eight patients without significant atherosclerosis. WSS amplitudes were accurately quantified at two high risk zones of atherosclerosis, namely at proximal left anterior descending artery (LAD) and at proximal left circumflex artery (LCx), and also at three high WSS concentration sites near the bifurcation. Statistical analysis was used to highlight relationships between WSS amplitudes calculated at these five zones of interest and various geometric factors. The tortuosity index of the LM-LAD segment appears to be an emergent geometric factor in determining the low WSS amplitude at proximal LAD. Strong correlations were found between the high WSS amplitudes calculated at the endothelial regions close to the flow divider. This study not only demonstrated that CT imaging studies of local risk factor for atherosclerosis could be clinically performed, but also showed that tortuosity of LM-LAD coronary branch could be used as a surrogate marker for the onset of atherosclerosis.

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Abbreviations

ARLAD/LM :

Area ratio = LAD2 section area divided by LM2 section area

ARLCx/LM :

Area ratio = LCx2 section area divided by LM2 section area

CFD:

Computational fluid dynamics

WSS:

Wall shear stress

High-WSSLAD :

Highest WSS amplitude at proximal LAD (region #4, Fig. 5)

High-WSSLCx :

Highest WSS amplitude at proximal LCx (region #3, Fig. 5)

High-WSSLM :

Highest WSS amplitude at the LM site of interest (region #1, Fig. 5)

LAD:

Left anterior descending artery

LCx:

Left circumflex artery

LM:

Left main artery

Low-WSSLAD :

Lowest WSS amplitude at proximal LAD (region #5, Fig. 5)

Low-WSSLCx :

Lowest WSS amplitude at proximal LCx (region #2, Fig. 5)

P bif :

Coronary bifurcation point

PLS:

Percentage luminal stenosis

TortuosityLAD-LCx :

Tortuosity of the LAD + LCx arterial segment near the bifurcation

TortuosityLM-LAD :

Tortuosity of the LM + LAD arterial segment near the bifurcation

TortuosityLM-LCx :

Tortuosity of the LM + LCx arterial segment near the bifurcation

\(\alpha _{\rm LM-LCx}\) :

Angle between LM and LCx branches (unit: °)

\(\alpha _{\rm LM-LAD}\) :

Angle between LM and LAD branches (unit: °)

α bif :

Bifurcation angle defined as the angle between LAD and LCx branches (unit: °)

References

  1. Caro, C.G., J. M. Fitz-Gerald, and R. C. Schroter. Arterial wall shear and distribution of early atheroma in man. Nature 223:1159–1160, 1969.

    Article  CAS  PubMed  Google Scholar 

  2. Caro, C. G., J. M. Fitz-Gerald, and R. C. Schroter. Atheroma and arterial wall shear. Observation, correlation and proposal of a shear dependent mass transfer mechanism for atherogenesis. Proc. R. Soc. Lond. B Biol. Sci. 177:109–159, 1971.

    Article  CAS  PubMed  Google Scholar 

  3. Chaichana, T., Z. Sun, and J. Jewkes. Computation of hemodynamics in the left coronary artery with variable angulations. J. Biomech. 44:1869–1878, 2011.

    Article  PubMed  Google Scholar 

  4. 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: molecular, cellular, and vascular behavior. J. Am. Coll. Cardiol. 49:2379–2393, 2007.

    Article  CAS  PubMed  Google Scholar 

  5. Cheng, C., D. Tempel, R. van Haperen, et al. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation 113:2744–2753, 2006.

    Article  PubMed  Google Scholar 

  6. Cheruvu, P. K., A. V. Finn, C. Gardner, et al. Frequency and distribution of thin-cap fibroatheroma and ruptured plaques in human coronary arteries: a pathologic study. J. Am. Coll. Cardiol. 50:940–949, 2007.

    Article  PubMed  Google Scholar 

  7. Del Corso, L., D. Moruzzo, B. Conte, M. Agelli, A. M. Romanelli, F. Pastine, M. Protti, F. Pentimone, and G. Baggiani. Tortuosity, kinking, and coiling of the carotid artery: expression of atherosclerosis or aging? Angiology 49:361–371, 1998.

    Article  PubMed  Google Scholar 

  8. Ethier, C. R., S. Prakash, D. A. Steinman, R. L. Leask, G. G. Couch, and M. Ojha. Steady flow separation patterns in a 45 degree junction. J. Fluid Mech. 411:1–38, 2000.

    Article  Google Scholar 

  9. Fayad, Z. A., V. Fuster, K. Nikolaou, and C. Becker. Computed tomography and magnetic resonance imaging for noninvasive coronary angiography and plaque imaging: current and potential future concepts. Circulation 106:2026–2034, 2002.

    Article  PubMed  Google Scholar 

  10. Fry, D. L. Acute vascular endothelial changes associated with increased blood velocity gradients. Circ. Res. 22:165–197, 1968.

    Article  CAS  PubMed  Google Scholar 

  11. Gijsen, F. J., J. J. Wentzel, A. Thury, et al. A new imaging technique to study 3-D plaque and shear stress distribution in human coronary artery bifurcations in vivo. J. Biomech. 40:2349–2357, 2007.

    Article  PubMed  Google Scholar 

  12. Gijsen, F. J., J. J. Wentzel, A. Thury, et al. Strain distribution over plaques in human coronary arteries relates to shear stress. Am. J. Physiol. Heart Circ. Physiol. 295:H1608–H1614, 2008.

    Article  CAS  PubMed  Google Scholar 

  13. Glagov, S., E. Weisenberg, C. K. Zarins, R. Stankunavicius, and G. J. Kolettis. Compensatory enlargement of human atherosclerotic coronary arteries. N. Engl. J. Med. 316:1371–1375, 1987.

    Article  CAS  PubMed  Google Scholar 

  14. Goubergrits, L., U. Kertzscher, B. Schoneberg, E. Wellnhofer, C. Petz, and H. C. Hege. CFD analysis in an anatomically realistic coronary artery model based on non-invasive 3D imaging: comparison of magnetic resonance imaging with computed tomography. Int. J. Cardiovasc. Imaging 24:411–421, 2008.

    Article  PubMed  Google Scholar 

  15. Han, H. C. Twisted blood vessels: symptoms, etiology and biomechanical mechanisms. J. Vasc. Res. 49:185–187, 2012.

    Article  PubMed Central  PubMed  Google Scholar 

  16. Hiroki, M., K. Miyashita, and M. Oda. Tortuosity of the white matter medullary arterioles is related to the severity of hypertension. Cerebrovasc. Dis. 13:242–250, 2002.

    Article  PubMed  Google Scholar 

  17. Huo, Y,, T. Wischgoll, and G. S. Kassab. Flow patterns in three-dimensional porcine epicardial coronary arterial tree. Am. J. Physiol. Heart Circ. Physiol. 293:H2959–H2970, 2007.

    Article  CAS  PubMed  Google Scholar 

  18. Jakob, M., D. Spasojevic, O. N. Krogmann, H. Wiher, R. Hug, and O. M. Hess. Tortuosity of coronary arteries in chronic pressure and volume overload. Cathet. Cardiovasc. Diagn. 38:25–31, 1996.

    Article  CAS  PubMed  Google Scholar 

  19. Johnson, K., P. Sharma, and J. Oshinski. Coronary artery flow measurement using navigator echo gated phase contrast magnetic resonance velocity mapping at 3.0 T. J. Biomech. 41:595–602, 2008.

    Article  PubMed Central  PubMed  Google Scholar 

  20. Johnston, B. M., P. R. Johnston, S. Corney, and D. Kilpatrick. Non-Newtonian blood flow in human right coronary arteries: steady state simulations. J. Biomech. 37:709–720, 2004.

    Article  PubMed  Google Scholar 

  21. Johnston BM, Johnston PR, Corney S, and Kilpatrick D. Non-Newtonian blood flow in human right coronary arteries: transient simulations. J. Biomech. 39:1116–1128, 2006.

    Article  PubMed  Google Scholar 

  22. Joshi, A. K., R. L. Leask, J. G. Myers, M. Ojha, J. Butany, and C. R. Ethier. Intimal thickness is not associated with wall shear stress patterns in the human right coronary artery. Arterioscler. Thromb. Vasc. Biol. 24:2408–2413, 2004.

    Article  CAS  PubMed  Google Scholar 

  23. Katouzian, A., S. Sathyanarayana, B. Baseri, E. E. Konofagou, and S. G. Carlier. Challenges in atherosclerotic plaque characterization with intravascular ultrasound (IVUS): from data collection to classification. IEEE Trans. Inf. Technol. Biomed. 12:315–327, 2008.

    Article  PubMed  Google Scholar 

  24. Kotys, M. S., D. A. Herzka, E. J. Vonken, et al. Profile order and time-dependent artifacts in contrast-enhanced coronary MR angiography at 3T: origin and prevention. Magn. Reson. Med. 62:292–299, 2009.

    Article  PubMed  Google Scholar 

  25. Kubo, T., T. Imanishi, S. Takarada, et al. Assessment of culprit lesion morphology in acute myocardial infarction: ability of optical coherence tomography compared with intravascular ultrasound and coronary angioscopy. J. Am. Coll. Cardiol. 50:933–939, 2007.

    Article  PubMed  Google Scholar 

  26. Lee, S. W., L. Antiga, J. D. Spence, and D. A. Steinman. Geometry of the carotid bifurcation predicts its exposure to disturbed flow. Stroke 39:2341–2347, 2008.

    Article  PubMed  Google Scholar 

  27. Lehoux, S., Y. Castier, and A. Tedgui. Molecular mechanisms of the vascular responses to haemodynamic forces. J. Intern. Med. 259:381–392, 2006.

    Article  CAS  PubMed  Google Scholar 

  28. MacLean, N. F., and M. R. Roach. Thickness, taper, and ellipticity in the aortoiliac bifurcation of patients aged 1 day to 76 years. Heart Vessels 13:95–101, 1998.

    Article  CAS  PubMed  Google Scholar 

  29. 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 

  30. Medina, A., J. Suarez de Lezo, and M. Pan. A new classification of coronary bifurcation lesions. Rev. Esp. Cardiol. 59(2):183–184, 2006.

    Article  PubMed  Google Scholar 

  31. Murray, C. D. The Physiological principle of minimum work: I. The vascular system and the cost of blood volume. Proc. Natl Acad. Sci. U.S.A. 12:207–214, 1926.

  32. Nissen, S. E., J. C. Gurley, C. L. Grines, D. C. Booth, R. McClure, M. Berk, C. Fischer, and A. N. DeMaria. Intravascular ultrasound assessment of lumen size and wall morphology in normal subjects and patients with coronary artery disease. Circulation 84(3):1087–99, 1991.

    Article  CAS  PubMed  Google Scholar 

  33. Ong, C. W., S. Dokos, B. T. Chan, E. Lim, A. Al Abed, N. A. B. Abu Osman, S. Kadiman, N. H. Lovell. Numerical investigation of the effect of cannula placement on thrombosis. Theor. Biol. Med. Model. 2013:10–35, 2013.

  34. Pancera, P., M. Ribul, B. Presciuttini, A. Lechi. Prevalence of carotid artery kinking in 590 consecutive subjects evaluated by echo-color Doppler. Is there a correlation with arterial hypertension? J. Intern. Med. 248:7–12, 2000.

    Article  CAS  PubMed  Google Scholar 

  35. Rioufol, G., M. Gilard, G. Finet, I. Ginon, J. Boschat, and X. Andre-Fouet. Evolution of spontaneous atherosclerotic plaque rupture with medical therapy: long-term follow-up with intravascular ultrasound. Circulation 110:2875–2880, 2004.

    Article  PubMed  Google Scholar 

  36. Sankaranarayanan, M., L. P. Chua, D. N. Ghista, and Tan, Y. S. Computational model of blood flow in the aorto-coronary bypass graft. Biomed. Online 4:1–14, 2005.

    Article  Google Scholar 

  37. Sanz, J., and Z. A. Fayad. Imaging of atherosclerotic cardiovascular disease. Nature 451:953–957, 2008.

    Article  CAS  PubMed  Google Scholar 

  38. Soulis, J. V., T. M. Farmakis, G. D. Giannoglou, and G. E. Louridas. Wall shear stress in normal left coronary artery tree. J. Biomech. 39:742–749, 2006.

    Article  PubMed  Google Scholar 

  39. Stone, P. H., A. U. Coskun, S. Kinlay, et al. Effect of endothelial shear stress on the progression of coronary artery disease, vascular remodeling, and in-stent restenosis in humans: in vivo 6-month follow-up study. Circulation 108:438–444, 2003.

    Article  PubMed  Google Scholar 

  40. Tearney, G. J., S. Waxman, M. Shishkov, et al. Three-dimensional coronary artery microscopy by intracoronary optical frequency domain imaging. JACC Cardiovasc. Imaging 1:752–761, 2008.

    Article  PubMed Central  PubMed  Google Scholar 

  41. Thomas, J. B., L. Antiga, S. L. Che, et al. Variation in the carotid bifurcation geometry of young versus older adults: implications for geometric risk of atherosclerosis. Stroke 36:2450–2456, 2005.

    Article  PubMed  Google Scholar 

  42. Thomas, J. B., J. S. Milner, and D. A. Steinman. On the influence of vessel planarity on local hemodynamics at the human carotid bifurcation. Biorheology 39:443–448, 2002.

    PubMed  Google Scholar 

  43. van Wyk, S., L. Prahl Wittberg, and L. Fuchs. Wall shear stress variations and unsteadiness of pulsatile blood-like flows in 90-degree bifurcations. Comput. Biol. Med. 43:1025–1036, 2013.

    Article  PubMed  Google Scholar 

  44. van Wyk, S., L. Prahl Wittberg, and L. Fuchs. Atherosclerotic indicators for blood-like fluids in 90-degree arterial-like bifurcations. Comput. Biol. Med. 50:56–69, 2014.

  45. Weibel, J., and W. S. Fields. Tortuosity, coiling, and kinking of the internal carotid artery. I. Etiology and radiographic anatomy. Neurology 15:7–18, 1965.

    CAS  Google Scholar 

  46. Wellnhofer, E., L. Goubergrits, U. Kertzscher, K. Affeld, and E. Fleck. Novel non-dimensional approach to comparison of wall shear stress distributions in coronary arteries of different groups of patients. Atherosclerosis 202:483–490, 2009.

    Article  CAS  PubMed  Google Scholar 

  47. Wellnhofer, E., J., U. Kertzscher, K. Affeld, E. Fleck, and L. Goubergrits. Non-dimensional modeling in flow simulation studies of coronary arteries including side-branches: a novel diagnostic tool in coronary artery disease. Atherosclerosis 216:277–282, 2011.

    Article  CAS  PubMed  Google Scholar 

  48. Zakaria, H., A. M. Robertson, and C. W. Kerber. A parametric model for studies of flow in arterial bifurcations. Ann. Biomed. Eng. 36:1515–1530, 2008.

    Article  PubMed  Google Scholar 

  49. Zeng, D., Z. Ding, M. H. Friedman, and C. R. Ethier. Effects of cardiac motion on right coronary artery hemodynamics. Ann. Biomed. Eng. 31:420–429, 2003.

    Article  PubMed  Google Scholar 

  50. Zhu, H., Z. Ding, R. N. Piana, T. R. Gehrig, and M. H. Friedman. Cataloguing the geometry of the human coronary arteries: a potential tool for predicting risk of coronary artery disease. Int. J. Cardiol. 135:43–52, 2009.

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

M. Malvè and M.A. Martínez are supported by the Spanish Ministry of Science and Technology through research project DPI-2010-20746-C03-01 and the Instituto de Salud Carlos III (ISCIII) through the CIBER-BBN initiative. This research was supported in part by an appointment (J. Ohayon) to the Senior Fellow Program at the National Institutes of Health (NIH). This program is administered by Oak Ridge Institute for Science and Education through an interagency agreement between the NIH and the U.S. Department of Energy.

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Authors and Affiliations

  1. Department of Mechanical Engineering, Energetics and Materials, Public University of Navarra, Campus Arrosadía, 31006, Pamplona, Spain

    M. Malvè

  2. Aragón Institute of Engineering Research, University of Zaragoza, Zaragoza, Spain

    M. Malvè & M. A. Martínez

  3. CIBER-BBN, Centro de Investigación en Red en Bioingeniería, Biomateriales y Nanomedicina, Madrid, Spain

    M. Malvè & M. A. Martínez

  4. Laboratory of Integrative Cardiovascular Imaging Science, National Institute of Diabetes Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, USA

    A. M. Gharib & R. Pettigrew

  5. Department of Mechanical Engineering, University of South Alabama, Mobile, AL, USA

    S. K. Yazdani

  6. Department of Hemodynamics and Interventional Cardiology, Hospices Civils de Lyon and Claude Bernard University Lyon 1, INSERM Unit 886, Lyon, France

    G. Finet

  7. Laboratory TIMC-DyCTiM, UJF, CNRS UMR 5525, In3S, Grenoble, France

    J. Ohayon

  8. Engineering School Polytech Annecy-Chambéry, University of Savoie, Chambéry, France

    J. Ohayon

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  1. M. Malvè
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Correspondence to M. Malvè or J. Ohayon.

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Associate Editor Umberto Morbiducci oversaw the review of this article.

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Malvè, M., Gharib, A.M., Yazdani, S.K. et al. Tortuosity of Coronary Bifurcation as a Potential Local Risk Factor for Atherosclerosis: CFD Steady State Study Based on In Vivo Dynamic CT Measurements. Ann Biomed Eng 43, 82–93 (2015). https://doi.org/10.1007/s10439-014-1056-y

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