Advertisement

Prediction of Long Term Restenosis Risk After Surgery in the Carotid Bifurcation by Hemodynamic and Geometric Analysis

  • Maurizio Domanin
  • Diego Gallo
  • Christian Vergara
  • Pietro Biondetti
  • Laura V. Forzenigo
  • Umberto MorbiducciEmail author
Article

Abstract

This study explored the potential of hemodynamic disturbances and geometric features to predict long-term carotid restenosis after carotid endarterectomy (CEA). Thirteen CEA for carotid diameter stenosis > 70% were performed with patch graft (PG) angioplasty in nine cases, and primary closure (PC) in four cases. MRI acquisitions within one month after CEA were used for hemodynamic and geometric characterization. Personalized computational hemodynamic simulations quantified the exposure to low and oscillatory wall shear stress (WSS). Geometry was characterized in terms of flare (the expansion at the bulb) and tortuosity. At 60 months after CEA, Doppler ultrasound (DUS) was applied for restenosis detection and intima-media thickness determination. Larger flares were associated to larger exposure to low WSS (Pearson R2 values up to 0.38, P < 0.05). The two cases characterized by the highest flare and the largest low WSS exposure developed restenosis > 50% at 60 months. Linear regressions revealed associations of DUS observations of thickening with flare variables (up to R2 = 0.84, P < 0.001), and the exposure to low (but not oscillatory) WSS (R2 = 0.58, P < 0.05). Our findings suggest that arteriotomy repair should avoid a large widening of the carotid bulb, which is linked to restenosis via the generation of flow disturbances. Hemodynamics and geometry-based analyses hold potential for (1) preoperative planning, guiding the PG vs. PC clinical decision, and (2) stratifying long-term restenosis risk after CEA.

Keywords

Carotid endarterectomy Recurrent stenosis Computational fluid dynamics Wall shear stress Flare Tortuosity 

Abbreviations

CB

Carotid bulb

CCA

Common carotid artery

CEA

Carotid endarterectomy

CFD

Computational fluid dynamics

DUS

Doppler ultrasound

ECA

External carotid artery

ICA

Internal carotid artery

IMT

Intima-media thickness

LSA

Low shear area

OSA

Oscillatory shear area

OSI

Oscillatory shear index

PC

Primary closure

PG

Patch graft

PSV

Peak systolic velocity

TAWSS

Time-averaged wall shear stress

WSS

Wall shear stress

Notes

Acknowledgments

The Authors would like to thank the technical assistance of Paola Tasso and David Iommi, and the fruitful discussion with Prof. David A. Steinman.

Supplementary material

10439_2019_2201_MOESM1_ESM.pdf (551 kb)
Supplementary material 1 (PDF 550 kb)

References

  1. 1.
    Abdelhamid, M. F., M. L. Wall, and R. K. Vohra. Carotid artery pseudoaneurysm after carotid endarterectomy: case series and a review of the literature. Vasc. Endovasc. Surg. 43:571–577, 2009.CrossRefGoogle Scholar
  2. 2.
    AbuRahma A. F., P. Stone, S. Deem, L. S. Dean, T. Keiffer and E. Deem. Proposed duplex velocity criteria for carotid restenosis following carotid endarterectomy with patch closure. J. Vasc. Surg. 50: 286–291, 291 e281–282, 2009; discussion 291.Google Scholar
  3. 3.
    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.CrossRefGoogle Scholar
  4. 4.
    Archie, J. P. Geometric dimension changes with carotid endarterectomy reconstruction. J. Vasc. Surg. 25:488–498, 1997.CrossRefGoogle Scholar
  5. 5.
    Bandyk, D. F., H. W. Kaebnick, M. B. Adams, and J. B. Towne. Turbulence occurring after carotid bifurcation endarterectomy—a harbinger of residual and recurrent carotid stenosis. J. Vasc. Surg. 7:261–274, 1988.CrossRefGoogle Scholar
  6. 6.
    Bijari, P. B., L. Antiga, D. Gallo, B. A. Wasserman, and D. A. Steinman. Improved prediction of disturbed flow via hemodynamically-inspired geometric variables. J. Biomech. 45:1632–1637, 2012.CrossRefGoogle Scholar
  7. 7.
    Bijari, P. B., B. A. Wasserman, and D. A. Steinman. Carotid bifurcation geometry is an independent predictor of early wall thickening at the carotid bulb. Stroke 45:473–478, 2014.CrossRefGoogle Scholar
  8. 8.
    Brott, T. G., J. L. Halperin, S. Abbara, J. M. Bacharach, J. D. Barr, R. L. Bush, C. U. Cates, M. A. Creager, S. B. Fowler, G. Friday, V. S. Hertzberg, E. B. McIff, W. S. Moore, P. D. Panagos, T. S. Riles, R. H. Rosenwasser, and A. J. Taylor. ASA/ACCF/AHA/AANN/AANS/ACR/ASNR/CNS/SAIP/SCAI/SIR/SNIS/SVM/SVS guideline on the management of patients with extracranial carotid and vertebral artery disease: executive summary. A report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines, and the American Stroke Association, American Association of Neuroscience Nurses, American Association of Neurological Surgeons, American College of Radiology, American Society of Neuroradiology, Congress of Neurological Surgeons, Society of Atherosclerosis Imaging and Prevention, Society for Cardiovascular Angiography and Interventions, Society of Interventional Radiology, Society of NeuroInterventional Surgery, Society for Vascular Medicine, and Society for Vascular Surgery. Circulation 124:489–532, 2011.CrossRefGoogle Scholar
  9. 9.
    Domanin, M., D. Bissacco, D. Le Van, and C. Vergara. Computational fluid dynamic comparison between patch-based and primary closure techniques after carotid endarterectomy. J. Vasc. Surg. 67:887–897, 2018.CrossRefGoogle Scholar
  10. 10.
    Domanin, M., A. Buora, F. Scardulla, B. Guerciotti, L. Forzenigo, P. Biondetti, and C. Vergara. Computational fluid-dynamic analysis after carotid endarterectomy: patch graft versus direct suture closure. Ann. Vasc. Surg. 44:325–335, 2017.CrossRefGoogle Scholar
  11. 11.
    Formaggia, L., J. F. Gerbeau, F. Nobile, and A. Quarteroni. Numerical treatment of defective boundary conditions for the Navier-Stokes equations. Siam J. Numer. Anal. 40:376–401, 2002.CrossRefGoogle Scholar
  12. 12.
    Frericks, H., J. Kievit, J. M. van Baalen, and J. H. van Bockel. Carotid recurrent stenosis and risk of ipsilateral stroke: a systematic review of the literature. Stroke 29:244–250, 1998.CrossRefGoogle Scholar
  13. 13.
    Gallo, D., P. B. Bijari, U. Morbiducci, Y. Qiao, Y. J. Xie, M. Etesami, D. Habets, E. G. Lakatta, B. A. Wasserman, and D. A. Steinman. Segment-specific associations between local haemodynamic and imaging markers of early atherosclerosis at the carotid artery: an in vivo human study. J. R. Soc. Interface 15:20180352, 2018.CrossRefGoogle Scholar
  14. 14.
    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.CrossRefGoogle Scholar
  15. 15.
    Gallo, D., D. A. Steinman, and U. Morbiducci. An insight into the mechanistic role of the common carotid artery on the hemodynamics at the carotid bifurcation. Ann. Biomed. Eng. 43:68–81, 2015.CrossRefGoogle Scholar
  16. 16.
    Gallo, D., D. A. Steinman, and U. Morbiducci. Insights into the co-localization of magnitude-based versus direction-based indicators of disturbed shear at the carotid bifurcation. J. Biomech. 49:2413–2419, 2016.CrossRefGoogle Scholar
  17. 17.
    Gallo, D., O. Vardoulis, P. Monney, D. Piccini, P. Antiochos, J. Schwitter, N. Stergiopulos, and U. Morbiducci. Cardiovascular morphometry with high-resolution 3D magnetic resonance: first application to left ventricle diastolic dysfunction. Med. Eng. Phys. 47:64–71, 2017.CrossRefGoogle Scholar
  18. 18.
    Guerciotti, B., C. Vergara, L. Azzimonti, L. Forzenigo, A. Buora, P. Biondetti, and M. Domanin. Computational study of the fluid-dynamics in carotids before and after endarterectomy. J. Biomech. 49:26–38, 2016.CrossRefGoogle Scholar
  19. 19.
    Harloff, A., S. Berg, A. J. Barker, J. Schollhorn, M. Schumacher, C. Weiller, and M. Markl. Wall shear stress distribution at the carotid bifurcation: influence of eversion carotid endarterectomy. Eur. Radiol. 23:3361–3369, 2013.CrossRefGoogle Scholar
  20. 20.
    Hellings, W. E., F. L. Moll, J. P. de Vries, P. de Bruin, D. P. de Kleijn, and G. Pasterkamp. Histological characterization of restenotic carotid plaques in relation to recurrence interval and clinical presentation: a cohort study. Stroke 39:1029–1032, 2008.CrossRefGoogle Scholar
  21. 21.
    Heyer, E. J., R. Sharma, A. Rampersad, C. J. Winfree, W. J. Mack, R. A. Solomon, G. J. Todd, P. C. McCormick, J. G. McMurtry, D. O. Quest, Y. Stern, R. M. Lazar, and E. S. Connolly. A controlled prospective study of neuropsychological dysfunction following carotid endarterectomy. Arch. Neurol. 59:217–222, 2002.CrossRefGoogle Scholar
  22. 22.
    Imparato, A. M. The role of patch angioplasty after carotid endarterectomy. J. Vasc. Surg. 7:715–716, 1988.CrossRefGoogle Scholar
  23. 23.
    Jahromi, A. S., C. S. Cina, Y. Liu, and C. M. Clase. Sensitivity and specificity of color duplex ultrasound measurement in the estimation of internal carotid artery stenosis: a systematic review and meta-analysis. J. Vasc. Surg. 41:962–972, 2005.CrossRefGoogle Scholar
  24. 24.
    Kamenskiy, A. Computational fluid dynamic comparison between patch-based and primary closure techniques after carotid endarterectomy. J. Vasc. Surg. 67:897–898, 2018.CrossRefGoogle Scholar
  25. 25.
    Ku, D. N., D. P. Giddens, C. K. Zarins, and S. Glagov. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 5:293–302, 1985.CrossRefGoogle Scholar
  26. 26.
    Kumar, R., A. Batchelder, A. Saratzis, A. F. AbuRahma, P. Ringleb, B. K. Lal, J. L. Mas, M. Steinbauer, and A. R. Naylor. Restenosis after carotid interventions and its relationship with recurrent ipsilateral stroke: a systematic review and meta-analysis. Eur. J. Vasc. Endovasc. Surg. 53:766–775, 2017.CrossRefGoogle Scholar
  27. 27.
    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.CrossRefGoogle Scholar
  28. 28.
    Maertens, V., H. Maertens, M. Kint, C. Coucke, and Y. Blomme. Complication rate after carotid endarterectomy comparing patch angioplasty and primary closure. Ann. Vasc. Surg. 30:248–252, 2016.CrossRefGoogle Scholar
  29. 29.
    Malas, M., N. O. Glebova, S. E. Hughes, J. H. Voeks, U. Qazi, W. S. Moore, B. K. Lal, G. Howard, R. Llinas, and T. G. Brott. Effect of patching on reducing restenosis in the carotid revascularization endarterectomy versus stenting trial. Stroke 46:757–761, 2015.CrossRefGoogle Scholar
  30. 30.
    Morbiducci, U., D. Gallo, D. Massai, R. Ponzini, M. A. Deriu, L. Antiga, A. Redaelli, and F. M. Montevecchi. On the importance of blood rheology for bulk flow in hemodynamic models of the carotid bifurcation. J. Biomech. 44:2427–2438, 2011.CrossRefGoogle Scholar
  31. 31.
    Morbiducci, U., A. M. Kok, B. R. Kwak, P. H. Stone, D. A. Steinman, and J. J. Wentzel. Atherosclerosis at arterial bifurcations: evidence for the role of haemodynamics and geometry. Thromb. Haemost. 115:484–492, 2016.CrossRefGoogle Scholar
  32. 32.
    Naylor, A. R., J. B. Ricco, G. J. de Borst, S. Debus, J. de Haro, A. Halliday, G. Hamilton, J. Kakisis, S. Kakkos, S. Lepidi, H. S. Markus, D. J. McCabe, J. Roy, H. Sillesen, J. C. den van Berg, F. Vermassen, C. Esvs Guidelines, P. Kolh, N. Chakfe, R. J. Hinchliffe, I. Koncar, J. S. Lindholt, M. Vega de Ceniga, F. Verzini, R. Esvs Guideline, J. Archie, S. Bellmunt, A. Chaudhuri, M. Koelemay, A. K. Lindahl, F. Padberg, and M. Venermo. Editor’s choice—management of atherosclerotic carotid and vertebral artery disease: 2017 Clinical Practice Guidelines of the European Society for Vascular Surgery (ESVS). Eur. J. Vasc. Endovasc. Surg. 55:3–81, 2018.CrossRefGoogle Scholar
  33. 33.
    Ouriel, K., and R. M. Green. Clinical and technical factors influencing recurrent carotid stenosis and occlusion after endarterectomy. J. Vasc. Surg. 5:702–706, 1987.CrossRefGoogle Scholar
  34. 34.
    Pasterkamp, G., D. P. de Kleijn, and C. Borst. Arterial remodeling in atherosclerosis, restenosis and after alteration of blood flow: potential mechanisms and clinical implications. Cardiovasc. Res. 45:843–852, 2000.CrossRefGoogle Scholar
  35. 35.
    Phan, T. G., R. J. Beare, D. Jolley, G. Das, M. Ren, K. Wong, W. Chong, M. D. Sinnott, J. E. Hilton, and V. Srikanth. Carotid artery anatomy and geometry as risk factors for carotid atherosclerotic disease. Stroke 43:1596–1601, 2012.CrossRefGoogle Scholar
  36. 36.
    Rerkasem, K., and P. M. Rothwell. Systematic review of randomized controlled trials of patch angioplasty versus primary closure and different types of patch materials during carotid endarterectomy. Asian J. Surg. 34:32–40, 2011.CrossRefGoogle Scholar
  37. 37.
    Sangalli, L. M., P. Secchi, S. Vantini, and A. Veneziani. Efficient estimation of three-dimensional curves and their derivatives by free-knot regression splines, applied to the analysis of inner carotid artery centrelines. J. R. Stat. Soc. Ser. C 58:285–306, 2009.CrossRefGoogle Scholar
  38. 38.
    Taylor, C. A., and D. A. Steinman. Image-based modeling of blood flow and vessel wall dynamics: applications, methods and future directions: sixth international bio-fluid mechanics symposium and workshop, March 28-30, 2008 Pasadena, California. Ann. Biomed. Eng. 38:1188–1203, 2010.CrossRefGoogle Scholar
  39. 39.
    Timmins, L. H., D. S. Molony, P. Eshtehardi, M. C. McDaniel, J. N. Oshinski, D. P. Giddens, and H. Samady. Oscillatory wall shear stress is a dominant flow characteristic affecting lesion progression patterns and plaque vulnerability in patients with coronary artery disease. J. R. Soc. Interface 14:20160972, 2017.CrossRefGoogle Scholar
  40. 40.
    Veneziani, A., and C. Vergara. Flow rate defective boundary conditions in haemodynamics simulations. Int. J. Numer. Methods Fluids 47:803–816, 2005.CrossRefGoogle Scholar
  41. 41.
    Zenonos, G., N. Lin, A. Kim, J. E. Kim, L. Governale, and R. M. Friedlander. Carotid endarterectomy with primary closure: analysis of outcomes and review of the literature. Neurosurgery 70:646–654, 2012; (discussion 654-645).CrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2019

Authors and Affiliations

  1. 1.Department of Clinical Sciences and Community HealthUniversità di MilanoMilanItaly
  2. 2.Unità Operativa di Chirurgia VascolareFondazione I.R.C.C.S. Cà Granda Ospedale Maggiore PoliclinicoMilanItaly
  3. 3.PolitoBIOMed Lab, Department of Mechanical and Aerospace EngineeringPolitecnico di TorinoTurinItaly
  4. 4.Laboratory of Biological Structure Mechanics (LaBS), Dipartimento di Chimica, Materiali e Ingegneria Chimica “Giulio Natta”Politecnico di MilanoMilanItaly
  5. 5.Unità Operativa di RadiologiaFondazione I.R.C.C.S. Cà Granda Ospedale Maggiore PoliclinicoMilanItaly

Personalised recommendations