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Carotid Plaque Stiffness Measured with Supersonic Shear Imaging and Its Correlation with Serum Homocysteine Level in Ischemic Stroke Patients

  • Shang, Jing (Department of Ultrasound Medicine, The First Affiliated Hospital, Xi'an Jiaotong University) ;
  • Wang, Wen (Department of Radiology, Tangdu Hospital, Fourth Military Medical University) ;
  • Feng, Jun (Department of Neurology, Neurology, The First Affiliated Hospital, Xi'an Jiaotong University) ;
  • Luo, Guo-gang (Department of Neurology, Neurology, The First Affiliated Hospital, Xi'an Jiaotong University) ;
  • Dang, Ying (Department of Ultrasound Medicine, The First Affiliated Hospital, Xi'an Jiaotong University) ;
  • Sun, Jian (Department of Ultrasound Medicine, The First Affiliated Hospital, Xi'an Jiaotong University) ;
  • Yang, Yan-qiu (Department of Ultrasound Medicine, The First Affiliated Hospital, Xi'an Jiaotong University) ;
  • Ruan, Li-tao (Department of Ultrasound Medicine, The First Affiliated Hospital, Xi'an Jiaotong University)
  • Received : 2016.05.27
  • Accepted : 2016.12.24
  • Published : 2018.02.01

Abstract

Objective: To ascertain the feasibility of using shear wave velocity (SWV) in assessing the stiffness of carotid plaque by supersonic shear imaging (SSI) and explore preliminary clinical value for such evaluation. Materials and Methods: Supersonic shear imaging was performed in 142 patients with ischemic stroke, including 76 males and 66 females with mean age of 66 years (range, 45-80 years). The maximum, minimum, and mean values of SWV were measured for 129 carotid plaques. SWVs were compared between echolucent and echogenic plaques. Correlations between SWVs and serum homocysteine levels were investigated. Based on neurological symptom, the surrogate marker of vulnerable plaque (VP), binary logistic regression was performed and area under curve (AUC) of homocysteine only and homocysteine combing $SWV_{mean}$ was calculated respectively. Results: Echogenic plaques (n = 51) had higher SWVs than echolucent ones (n = 78) ($SWV_{min}$ 3.91 [3.24-4.17] m/s vs. 1.51 [1.04-1.94] m/s; $SWV_{mean}$, 4.29 [3.98-4.57] m/s vs. 2.09 [1.69-2.41] m/s; $SWV_{max}$, 4.67 [4.33-4.86] m/s vs. 2.62 [2.32-3.31] m/s all p values < 0.01). Pearson correlation analysis showed that stiffness of plaques was negatively correlated with homocysteine level. R values for $SWV_{min}$, $SWV_{mean}$, and $SWV_{max}$ were -0.205, -0.213, and -0.199, respectively. Binary logistic regression analysis showed that sex (p = 0.008), low-density lipoprotein (p = 0.015), triglycerides (p = 0.011), $SWV_{mean}$ (p = 0.004), and hyper-homocysteinemia (p = 0.010) were significantly associated with symptomatic ischemic stroke. Receiver operating characteristic curves revealed that $SWV_{mean}$ combing serum homocysteine level (AUC = 0.67) presented better diagnostic value than serum homocysteine only (AUC = 0.60) for symptomatic ischemic stroke. Conclusion: Supersonic shear imaging could be used to quantitatively evaluate stiffness of both echolucent and echogenic carotid plaques. More importantly, SWVs of plaques were not only correlated to serum homocysteine level, but also associated with symptomatic ischemic stroke, suggesting that SSI might be useful for understanding more about VP.

Keywords

Acknowledgement

Supported by : Natural Science Foundation of China

References

  1. Rothwell PM. Carotid artery disease and the risk of ischaemic stroke and coronary vascular events. Cerebrovasc Dis 2000;10 Suppl 5:21-33
  2. Mughal MM, Khan MK, DeMarco JK, Majid A, Shamoun F, Abela GS. Symptomatic and asymptomatic carotid artery plaque. Expert Rev Cardiovasc Ther 2011;9:1315-1330 https://doi.org/10.1586/erc.11.120
  3. Rothwell PM, Eliasziw M, Gutnikov SA, Fox AJ, Taylor DW, Mayberg MR, et al. Analysis of pooled data from the randomised controlled trials of endarterectomy for symptomatic carotid stenosis. Lancet 2003;361:107-116 https://doi.org/10.1016/S0140-6736(03)12228-3
  4. Halliday A, Harrison M, Hayter E, Kong X, Mansfield A, Marro J, et al. 10-year stroke prevention after successful carotid endarterectomy for asymptomatic stenosis (ACST-1): a multicentre randomised trial. Lancet 2010;376:1074-1084 https://doi.org/10.1016/S0140-6736(10)61197-X
  5. Moreno PR. Vulnerable plaque: definition, diagnosis, and treatment. Cardiol Clin 2010;28:1-30 https://doi.org/10.1016/j.ccl.2009.09.008
  6. Naghavi M, Libby P, Falk E, Casscells SW, Litovsky S, Rumberger J, et al. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part I. Circulation 2003;108:1664-1672 https://doi.org/10.1161/01.CIR.0000087480.94275.97
  7. Naghavi M, Libby P, Falk E, Casscells SW, Litovsky S, Rumberger J, et al. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part II. Circulation 2003;108:1772-1778 https://doi.org/10.1161/01.CIR.0000087481.55887.C9
  8. Takaya N, Yuan C, Chu B, Saam T, Underhill H, Cai J, et al. Association between carotid plaque characteristics and subsequent ischemic cerebrovascular events: a prospective assessment with MRI--initial results. Stroke 2006;37:818-823 https://doi.org/10.1161/01.STR.0000204638.91099.91
  9. Graebe M, Pedersen SF, Hojgaard L, Kjaer A, Sillesen H. 18FDG PET and ultrasound echolucency in carotid artery plaques. JACC Cardiovasc Imaging 2010;3:289-295 https://doi.org/10.1016/j.jcmg.2010.01.001
  10. Nissen SE, Yock P. Intravascular ultrasound: novel pathophysiological insights and current clinical applications. Circulation 2001;103:604-616 https://doi.org/10.1161/01.CIR.103.4.604
  11. Iezzi R, Petrone G, Ferrante A, Lauriola L, Vincenzoni C, la Torre MF, et al. The role of contrast-enhanced ultrasound (CEUS) in visualizing atherosclerotic carotid plaque vulnerability: which injection protocol? Which scanning technique? Eur J Radiol 2015;84:865-871 https://doi.org/10.1016/j.ejrad.2015.01.024
  12. Li ZY, Howarth SP, Tang T, Gillard JH. How critical is fibrous cap thickness to carotid plaque stability? A flow-plaque interaction model. Stroke 2006;37:1195-1199 https://doi.org/10.1161/01.STR.0000217331.61083.3b
  13. Selwaness M, van den Bouwhuijsen Q, Mattace-Raso FU, Verwoert GC, Hofman A, Franco OH, et al. Arterial stiffness is associated with carotid intraplaque hemorrhage in the general population: the Rotterdam study. Arterioscler Thromb Vasc Biol 2014;34:927-932 https://doi.org/10.1161/ATVBAHA.113.302603
  14. Bercoff J, Tanter M, Fink M. Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans Ultrason Ferroelectr Freq Control 2004;51:396-409 https://doi.org/10.1109/TUFFC.2004.1295425
  15. Tanter M, Bercoff J, Athanasiou A, Deffieux T, Gennisson JL, Montaldo G, et al. Quantitative assessment of breast lesion viscoelasticity: initial clinical results using supersonic shear imaging. Ultrasound Med Biol 2008;34:1373-1386 https://doi.org/10.1016/j.ultrasmedbio.2008.02.002
  16. Mitri FG, Urban MW, Fatemi M, Greenleaf JF. Shear wave dispersion ultrasonic vibrometry for measuring prostate shear stiffness and viscosity: an in vitro pilot study. IEEE Trans Biomed Eng 2011;58:235-242 https://doi.org/10.1109/TBME.2010.2053928
  17. Ramnarine KV, Garrard JW, Dexter K, Nduwayo S, Panerai RB, Robinson TG. Shear wave elastography assessment of carotid plaque stiffness: in vitro reproducibility study. Ultrasound Med Biol 2014;40:200-209 https://doi.org/10.1016/j.ultrasmedbio.2013.09.014
  18. Garrard JW, Ummur P, Nduwayo S, Kanber B, Hartshorne TC, West KP, et al. Shear wave elastography may be superior to greyscale median for the identification of carotid plaque vulnerability: a comparison with histology. Ultraschall Med 2015;36:386-390 https://doi.org/10.1055/s-0034-1399676
  19. Youk JH, Son EJ, Park AY, Kim JA. Shear-wave elastography for breast masses: local shear wave speed (m/sec) versus Young modulus (kPa). Ultrasonography 2014;33:34-39
  20. Garrard JW, Ramnarine K. Shear-wave elastography in carotid plaques: comparison with grayscale median and histological assessment in an interesting case. Ultraschall Med 2014;35:1-3 https://doi.org/10.1055/s-0034-1368830
  21. Ramnarine KV, Garrard JW, Kanber B, Nduwayo S, Hartshorne TC, Robinson TG. Shear wave elastography imaging of carotid plaques: feasible, reproducible and of clinical potential. Cardiovasc Ultrasound 2014;12:49 https://doi.org/10.1186/1476-7120-12-49
  22. Widman E, Maksuti E, Larsson D, Urban MW, Bjällmark A, Larsson M. Shear wave elastography plaque characterization with mechanical testing validation: a phantom study. Phys Med Biol 2015;60:3151-3174 https://doi.org/10.1088/0031-9155/60/8/3151
  23. Yang X, Zhou Y, Liu C, Gao X, Wang A, Guo Y, et al. Homocysteine and carotid plaque stability: a cross-sectional study in Chinese adults. PLoS One 2014;9:e94935 https://doi.org/10.1371/journal.pone.0094935
  24. Zhong C, Lv L, Liu C, Zhao L, Zhou M, Sun W, et al. High homocysteine and blood pressure related to poor outcome of acute ischemia stroke in Chinese population. PLoS One 2014;9:e107498 https://doi.org/10.1371/journal.pone.0107498
  25. Shi Z, Guan Y, Huo YR, Liu S, Zhang M, Lu H, et al. Elevated total homocysteine levels in acute ischemic stroke are associated with long-term mortality. Stroke 2015;46:2419-2425 https://doi.org/10.1161/STROKEAHA.115.009136
  26. Touboul PJ, Hennerici MG, Meairs S, Adams H, Amarenco P, Bornstein N, et al. Mannheim carotid intima-media thickness and plaque consensus (2004-2006-2011). An update on behalf of the advisory board of the 3rd, 4th and 5th watching the risk symposia, at the 13th, 15th and 20th European Stroke Conferences, Mannheim, Germany, 2004, Brussels, Belgium, 2006, and Hamburg, Germany, 2011. Cerebrovasc Dis 2012;34:290-296 https://doi.org/10.1159/000343145
  27. Kot BC, Zhang ZJ, Lee AW, Leung VY, Fu SN. Elastic modulus of muscle and tendon with shear wave ultrasound elastography: variations with different technical settings. PLoS One 2012;7:e44348 https://doi.org/10.1371/journal.pone.0044348
  28. Ueland PM, Refsum H, Stabler SP, Malinow MR, Andersson A, Allen RH. Total homocysteine in plasma or serum: methods and clinical applications. Clin Chem 1993;39:1764-1779
  29. Sarvazyan AP, Rudenko OV, Swanson SD, Fowlkes JB, Emelianov SY. Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics. Ultrasound Med Biol 1998;24:1419-1435 https://doi.org/10.1016/S0301-5629(98)00110-0
  30. Dahl JJ, Dumont DM, Allen JD, Miller EM, Trahey GE. Acoustic radiation force impulse imaging for noninvasive characterization of carotid artery atherosclerotic plaques: a feasibility study. Ultrasound Med Biol 2009;35:707-716 https://doi.org/10.1016/j.ultrasmedbio.2008.11.001
  31. Ji Y, Song B, Xu Y, Fang H, Wu J, Sun S, et al. Prognostic significance of homocysteine levels in acute ischemic stroke: a prospective cohort study. Curr Neurovasc Res 2015;12:334-340 https://doi.org/10.2174/1567202612666150807112205
  32. Boysen G, Brander T, Christensen H, Gideon R, Truelsen T. Homocysteine and risk of recurrent stroke. Stroke 2003;34:1258-1261 https://doi.org/10.1161/01.STR.0000069017.78624.37

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