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Low Wall Shear Stress Is Associated with Saphenous Vein Graft Stenosis in Patients with Coronary Artery Bypass Grafting

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Abstract

Biomechanical forces may play a key role in saphenous vein graft (SVG) disease after coronary artery bypass graft (CABG) surgery. Computed tomography angiography (CTA) of 430 post-CABG patients were evaluated and 15 patients were identified with both stenosed and healthy SVGs for paired analysis. The stenosis was virtually removed, and detailed 3D models were reconstructed to perform patient-specific computational fluid dynamic (CFD) simulations. Models were processed to compute anatomic parameters, and hemodynamic parameters such as local and vessel-averaged wall shear stress (WSS), normalized WSS (WSS*), low shear area (LSA), oscillatory shear index (OSI), and flow rate. WSS* was significantly lower in pre-diseased SVG segments compared to corresponding control segments without disease (1.22 vs. 1.73, p = 0.012) and the area under the ROC curve was 0.71. No differences were observed in vessel-averaged anatomic or hemodynamic parameters between pre-stenosed and control whole SVGs. There are currently no clinically available tools to predict SVG failure post-CABG. CFD modeling has the potential to identify high-risk CABG patients who may benefit from more aggressive medical therapy and closer surveillance.

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References

  1. D’Agostino, R. S., Jacobs, J. P., Badhwar, V., et al. (2019). The Society of Thoracic Surgeons Adult Cardiac Surgery Database: 2019 update on outcomes and quality. The Annals of Thoracic Surgery, 107(1), 24–32. https://doi.org/10.1016/j.athoracsur.2018.10.004.

    Article  PubMed  Google Scholar 

  2. Goldman, S., Zadina, K., Moritz, T., et al. (2004). Long-term patency of saphenous vein and left internal mammary artery grafts after coronary artery bypass surgery. Journal of the American College of Cardiology, 44(11), 2149–2156. https://doi.org/10.1016/j.jacc.2004.08.064.

    Article  PubMed  Google Scholar 

  3. Hess, C. N., Lopes, R. D., Gibson, C. M., et al. (2014). Saphenous vein graft failure after coronary artery bypass surgery insights from PREVENT IV. Circulation., 130(17), 1445–1451. https://doi.org/10.1161/CIRCULATIONAHA.113.008193.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Weintraub, W. S., Jones, E. L., Morris, D. C., King, S. B., Guyton, R. A., & Graver, J. M. (1997). Outcome of reoperative coronary bypass surgery versus coronary angioplasty after previous bypass surgery. Circulation., 95(4), 868–877. https://doi.org/10.1161/01.CIR.95.4.868.

    Article  CAS  PubMed  Google Scholar 

  5. De Vries, M. R., Simons, K. H., Jukema, J. W., Braun, J., & Quax, P. H. A. (2016). Vein graft failure: from pathophysiology to clinical outcomes. Nature Reviews Cardiology, 13(8), 451–470. https://doi.org/10.1038/nrcardio.2016.76.

    Article  CAS  PubMed  Google Scholar 

  6. Malek, A., Alpher, S., & Izumo, S. (1999). Hemodynamic shear stress and its role in atherosclerosis. Journal of American Medical Association, 282(21), 2035–2042.

    Article  CAS  Google Scholar 

  7. Markl, M., Frydrychowicz, A., Kozerke, S., Hope, M., & Wieben, O. (2012). 4D flow MRI. Journal of Magnetic Resonance Imaging, 36, 1015–1036. https://doi.org/10.1002/jmri.23632.

    Article  PubMed  Google Scholar 

  8. Morris, P. D., Narracott, A., Von Tengg-Kobligk, H., et al. (2016). Computational fluid dynamics modelling in cardiovascular medicine. Heart, 102(1), 18–28. https://doi.org/10.1136/heartjnl-2015-308044.

    Article  PubMed  Google Scholar 

  9. Lu, M. T., Ferencik, M., Roberts, R. S., et al. (2017). Noninvasive FFR derived from coronary CT angiography—management and outcomes in the PROMISE trial. JACC: Cardiovascular Imaging, 10(11), 1350–1358. https://doi.org/10.1016/j.jcmg.2016.11.024.

    Article  PubMed  Google Scholar 

  10. Packard, R. R. S., Li, D., Budoff, M. J., & Karlsberg, R. P. (2017). Fractional flow reserve by computerized tomography and subsequent coronary revascularization. European Heart Journal Cardiovascular Imaging, 18(2), 145–152. https://doi.org/10.1093/ehjci/jew148.

    Article  PubMed  Google Scholar 

  11. Sankaran, S., Moghadam, M. E., Kahn, A. M., Tseng, E. E., Guccione, J. M., & Marsden, A. L. (2012). Patient-specific multiscale modeling of blood flow for coronary artery bypass graft surgery. Annals of Biomedical Engineering, 40(10), 2228–2242. https://doi.org/10.1007/s10439-012-0579-3.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Tran, J. S., Schiavazzi, D. E., Ramachandra, A. B., Kahn, A. M., & Marsden, A. L. (2016). Automated tuning for parameter identification and uncertainty quantification in multi-scale coronary simulations. Computers and Fluids, 142, 128–138. https://doi.org/10.1016/j.compfluid.2016.05.015.

    Article  PubMed  Google Scholar 

  13. Ramachandra, A. B., Kahn, A. M., & Marsden, A. L. (2016). Patient-specific simulations reveal significant differences in mechanical stimuli in venous and arterial coronary grafts. Journal of Cardiovascular Translational Research, 9(4), 279–290. https://doi.org/10.1007/s12265-016-9706-0.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Gaudino, M., Antoniades, C., Benedetto, U., et al. (2017). Mechanisms, consequences, and prevention of coronary graft failure. Circulation, 136(18), 1749–1764. https://doi.org/10.1161/CIRCULATIONAHA.117.027597.

    Article  PubMed  Google Scholar 

  15. Podesser, B. K., Neumann, F., Neumann, M., Schreiner, W., Wollenek, G., & Mallinger, R. (1998). Outer radius-wall thickness ratio, a postmortem quantitative histology in human coronary arteries. Acta Anatomica (Basel), 163(2), 63–68.

    Article  CAS  Google Scholar 

  16. Johnson, K., Sharma, P., & Oshinski, J. (2008). Coronary artery flow measurement using navigator echo gated phase contrast magnetic resonance velocity mapping at 3.0 T. Journal of Biomechanics, 41(3), 595–602. https://doi.org/10.1016/j.jbiomech.2007.10.010.

    Article  PubMed  Google Scholar 

  17. Zamir, M., Sinclair, P., & Wonnacott, T. H. (1992). Relation between diameter and flow in major branches of the arch of the aorta. Journal of Biomechanics, 25(11), 1303–1310. https://doi.org/10.1016/0021-9290(92)90285-9.

    Article  CAS  PubMed  Google Scholar 

  18. Changizi, M. A., & Cherniak, C. (2000). Modeling the large-scale geometry of human coronary arteries. Canadian Journal of Physiology and Pharmacology, 78(8), 603–611.

    Article  CAS  Google Scholar 

  19. Zhao, X., Liu, Y., Li, L., Wang, W., Xie, J., & Zhao, Z. (2016). Hemodynamics of the string phenomenon in the internal thoracic artery grafted to the left anterior descending artery with moderate stenosis. Journal of Biomechanics, 49(7), 983–991. https://doi.org/10.1016/j.jbiomech.2015.11.044.

    Article  PubMed  Google Scholar 

  20. Zhao, Z., Mao, B., Liu, Y., Yang, H., & Chen, Y. (2018). The study of the graft hemodynamics with different instant patency in coronary artery bypassing grafting. Computer Modeling in Engineering and Sciences, 116(2), 229–245. https://doi.org/10.31614/cmes.2018.04192.

    Article  Google Scholar 

  21. Dur, O., Coskun, S. T., Coskun, K. O., Frakes, D., Kara, L. B., & Pekkan, K. (2011). Computer-aided patient-specific coronary artery graft design improvements using CFD coupled shape optimizer. Cardiovascular Engineering and Technology, 2(1), 35–47. https://doi.org/10.1007/s13239-010-0029-z.

    Article  PubMed  Google Scholar 

  22. Meirson, T., Orion, E., Di Mario, C., et al. (2015). Flow patterns in externally stented saphenous vein grafts and development of intimal hyperplasia. The Journal of Thoracic and Cardiovascular Surgery, 150(4), 871–878. https://doi.org/10.1016/j.jtcvs.2015.04.061.

    Article  PubMed  Google Scholar 

  23. Fan, T., Feng, Y., Feng, F., et al. (2017). A comparison of postoperative morphometric and hemodynamic changes between saphenous vein and left internal mammary artery grafts. Physiological Reports, 5(21), 1–12. https://doi.org/10.14814/phy2.13487.

    Article  Google Scholar 

  24. Ballarin, F., Faggiano, E., Manzoni, A., et al. (2017). Numerical modeling of hemodynamics scenarios of patient-specific coronary artery bypass grafts. Biomechanics and Modeling in Mechanobiology, 16(4), 1373–1399.

  25. Khan, M., Valen-Sendstad, K., & Steinman, D. (2015). Narrowing the expertise gap for predicting intracranial aneurysm hemodynamics: impact of solver numerics versus mesh and time-step resolution. AJNR. American Journal of Neuroradiology, 36, 1310–1316. https://doi.org/10.3174/ajnr.A4263.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Xiang, J., Natarajan, S., Tremmel, M., et al. (2011). Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke, 42(1), 144–152. https://doi.org/10.1161/STROKEAHA.110.592923.

    Article  PubMed  Google Scholar 

  27. Khan, M. O., Arana, V. T., Rubbert, C., et al. (2020). Association between aneurysm hemodynamics and wall enhancement on 3D vessel wall MRI. Journal of Neurosurgery, 1–11. https://doi.org/10.3171/2019.10.JNS191251.

  28. Koszegi, Z., Kiss, B., Sipos, D., et al. (2018). Comparing the shear stress in degenerated and intact venous grafts from the same patients. European Heart Journal, 39(Suppl_1), ehy565–eP2695.

    Google Scholar 

  29. Akasaka, T., Yoshikawa, J., Yoshida, K., et al. (1995). Flow capacity of internal mammary artery grafts: Early restriction and later improvement assessed by Doppler guide wire. Comparison with saphenous vein grafts. Journal of the American College of Cardiology, 25(3), 640–647. https://doi.org/10.1016/0735-1097(94)00448-Y.

    Article  CAS  PubMed  Google Scholar 

  30. Shimizu, T., Ito, S., Kikuchi, Y., et al. (2004). Arterial conduit shear stress following bypass grafting for intermediate coronary artery stenosis: a comparative study with saphenous vein grafts. European Journal of Cardio-Thoracic Surgery, 25(4), 578–584. https://doi.org/10.1016/j.ejcts.2003.12.039.

    Article  PubMed  Google Scholar 

  31. Ramachandra, A., Kahn, A., & Marsden, A. (2016). Patient-specific simulations reveal significant differences in mechanical stimuli in venous and arterial coronary grafts. Journal of Cardiovascular Translational Research, 9(4), 279–290. https://doi.org/10.1007/s12265-016-9706-0.

  32. Ku, D., Giddens, D., Zarins, C., & Glagov, S. (1985). Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis., 5(3), 293–302. https://doi.org/10.1161/01.ATV.5.3.293.

    Article  CAS  PubMed  Google Scholar 

  33. Hozumi, T., Yoshikawa, J., Yoshida, K., et al. (1996). Use of intravascular ultrasound for in vivo assessment of changes in intimal thickness of angiographically normal saphenous vein grafts one year after aortocoronary bypass surgery. Heart., 76(4), 317–320. https://doi.org/10.1136/hrt.76.4.317.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Motwani, J., & Topol, E. (1998). Aortocoronary saphenous vein graft disease. Pathogenesis, predisposition, and prevention. Circulation., 97(9), 916–931. https://doi.org/10.4324/9781315731964-2.

    Article  CAS  PubMed  Google Scholar 

  35. Khan M, Valen-Sendstad K, Steinman D. Direct numerical simulation of laminar-turbulent transition in a non-axisymmetric stenosis model for Newtonian vs. shear-thinning non-Newtonian rheologies. Flow Turbul Combust. 2018.

  36. Chatzizisis, Y. S., Jonas, M., Coskun, A. U., et al. (2008). Prediction of the localization of high-risk coronary atherosclerotic plaques on the basis of low endothelial shear stress: an intravascular ultrasound and histopathology natural history study. Circulation., 117(8), 993–1002. https://doi.org/10.1161/CIRCULATIONAHA.107.695254.

    Article  PubMed  Google Scholar 

  37. Ramachandra, A. B., Humphrey, J. D., & Marsden, A. L. (2017). Gradual loading ameliorates maladaptation in computational simulations of vein graft growth and remodelling. Journal of the Royal Society Interface, 14(130), 20160995.

  38. Shah, P. J., Gordon, I., Fuller, J., et al. (2003). Factors affecting saphenous vein graft patency: clinical and angiographic study in 1402 symptomatic patients operated on between 1977 and 1999. The Journal of Thoracic and Cardiovascular Surgery, 126(6), 1972–1977. https://doi.org/10.1016/S0022-5223(03)01276-5.

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors wish to thank Derrick Laurel from the 3D and Quantitative Imaging Laboratory for his help in constructing models from CTA data, and Dr. Jin Long at the Quantitative Science Unit at the Stanford University School of Medicine for his help in statistical analysis.

Funding

This work was supported by NIH grant (NIH R01- RHL123689A), NSF CAREER Award OCI-1150184 to A. L. M., and a Burroughs Wellcome Fund Career Award at the Scientific Interface to A. L. M. Computational resources were provided by a grant to A. L. M (TG-CTS130034) through the Extreme Science and Engineering Discovery Environment (XSEDE). R.R.S.P. is supported by VA Merit BX004558. M. O. K. acknowledges funding support from the Natural Sciences and Engineering Research Council of Canada.

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Authors and Affiliations

  1. Department of Pediatrics, Stanford University School of Medicine, Stanford, CA, USA

    Muhammad Owais Khan & Alison L. Marsden

  2. Institute for Computational and Mathematical Engineering, Stanford University, Stanford, CA, USA

    Muhammad Owais Khan & Alison L. Marsden

  3. Department of Mechanical Engineering, California State University Fullerton, Fullerton, CA, USA

    Justin S. Tran

  4. Department of Cardiovascular Medicine, Stanford University School of Medicine, Stanford, CA, USA

    Han Zhu

  5. Department of Cardiothoracic Surgery, Stanford University School of Medicine, Stanford, CA, USA

    Jack Boyd

  6. Department of Medicine, University of California Los Angeles, Los Angeles, CA, USA

    René R. Sevag Packard

  7. Cardiovascular Medical Group of Southern California, Beverly Hills, CA, USA

    Ronald P. Karlsberg

  8. Division of Cardiovascular Medicine, University of California San Diego, La Jolla, CA, USA

    Andrew M. Kahn

  9. Department of Bioengineering, Stanford University, Stanford, CA, USA

    Alison L. Marsden

  10. Stanford Cardiovascular Institute, Stanford University, Stanford, CA, USA

    Alison L. Marsden

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  1. Muhammad Owais Khan
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Correspondence to Andrew M. Kahn or Alison L. Marsden.

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Human Subjects/Informed Consent Statement

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000 (5). Informed consent was obtained from all patients for being included in the study. No animal studies were carried out by the authors for this article. Patient recruitment and access to non-invasive clinical data (computer tomographic (CT) images, echocardiography data) was carried out according to protocols approved by the Stanford University Institutional Review Board.

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Khan, M.O., Tran, J.S., Zhu, H. et al. Low Wall Shear Stress Is Associated with Saphenous Vein Graft Stenosis in Patients with Coronary Artery Bypass Grafting. J. of Cardiovasc. Trans. Res. 14, 770–781 (2021). https://doi.org/10.1007/s12265-020-09982-7

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  • DOI: https://doi.org/10.1007/s12265-020-09982-7

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