Skip to main content
Top
Published in: European Radiology 2/2019

01-02-2019 | Vascular-Interventional

The role of wall shear stress in the parent artery as an independent variable in the formation status of anterior communicating artery aneurysms

Authors: Xin Zhang, Zhi-Qiang Yao, Tamrakar Karuna, Xu-Ying He, Xue-Min Wang, Xi-Feng Li, Wen-Chao Liu, Ran Li, Shen-Quan Guo, Yun-Chang Chen, Gan-Cheng Li, Chuan-Zhi Duan

Published in: European Radiology | Issue 2/2019

Login to get access

Abstract

Objectives

The study aimed to determine which hemodynamic parameters independently characterize anterior communicating artery (AcomA) aneurysm formation and explore the threshold of wall shear stress (WSS) of the parent artery to better illustrate the correlation between the magnitude of WSS and AcomA aneurysm formation.

Methods

Eighty-one patients with AcomA aneurysms and 118 patients without intracranial aneurysms (control population), as confirmed by digital subtraction angiography (DSA) from January 2014 to May 2017, were included in this cross-sectional study. Three-dimensional-DSA was performed to evaluate the morphologic characteristics of AcomA aneurysms. Local hemodynamic parameters were obtained using transcranial color-coded duplex (TCCD). Multivariate logistic regression and a two-piecewise linear regression model were used to determine which hemodynamic parameters are independent predictors of AcomA aneurysm formation and identify the threshold effect of WSS of the parent artery with respect to AcomA aneurysm formation.

Results

Univariate analyses showed that the WSS (p < 0.0001), angle between the A1 and A2 segments of the anterior cerebral artery (ACA) (p < 0.001), hypertension (grade II) (p = 0.007), fasting blood glucose (FBG; > 6.0 mmol/L) (p = 0.005), and dominant A1 (p < 0.001) were the significant parameters. Multivariate analyses showed a significant association between WSS of the parent artery and AcomA aneurysm formation (p = 0.0001). WSS of the parent artery (7.8-12.3 dyne/cm2) had a significant association between WSS and aneurysm formation (HR 2.0, 95% CI 1.3-2.8, p < 0.001).

Conclusions

WSS ranging between 7.8 and 12.3 dyne/cm2 independently characterizes AcomA aneurysm formation. With each additional unit of WSS, there was a one-fold increase in the risk of AcomA aneurysm formation.

Key Points

• Multivariate analyses and a two-piecewise linear regression model were used to evaluate the risk factors for AcomA aneurysm formation and the threshold effect of WSS on AcomA aneurysm formation.
• WSS ranging between 7.8 and 12.3 dyne/cm 2 was shown to be a reliable hemodynamic parameter in the formation of AcomA aneurysms. The probability of AcomA aneurysm formation increased one-fold for each additional unit of WSS.
• An ultrasound-based TCCD technique is a simple and accessible noninvasive method for detecting WSS in vivo; thus, it can be applied as a screening tool for evaluating the probability of aneurysm formation in primary care facilities and community hospitals because of the relatively low resource intensity.
Literature
1.
go back to reference Horiuchi T, Tanaka Y, Hongo K (2005) Surgical treatment for aneurysmal subarachnoid hemorrhage in the 8th and 9th decades of life. Neurosurgery 56:469–475 discussion 469-475CrossRef Horiuchi T, Tanaka Y, Hongo K (2005) Surgical treatment for aneurysmal subarachnoid hemorrhage in the 8th and 9th decades of life. Neurosurgery 56:469–475 discussion 469-475CrossRef
2.
go back to reference Leipzig TJ, Morgan J, Horner TG, Payner T, Redelman K, Johnson CS (2005) Analysis of intraoperative rupture in the surgical treatment of 1694 saccular aneurysms. Neurosurgery 56:455–468 discussion 455-468CrossRef Leipzig TJ, Morgan J, Horner TG, Payner T, Redelman K, Johnson CS (2005) Analysis of intraoperative rupture in the surgical treatment of 1694 saccular aneurysms. Neurosurgery 56:455–468 discussion 455-468CrossRef
3.
go back to reference Qiu T, Jin G, Xing H, Lu H (2017) Association between hemodynamics, morphology, and rupture risk of intracranial aneurysms: a computational fluid modeling study. Neurol Sci 38:1009–1018CrossRef Qiu T, Jin G, Xing H, Lu H (2017) Association between hemodynamics, morphology, and rupture risk of intracranial aneurysms: a computational fluid modeling study. Neurol Sci 38:1009–1018CrossRef
4.
go back to reference Meng H, Tutino VM, Xiang J, Siddiqui A (2014) High WSS or low WSS? Complex interactions of hemodynamics with intracranial aneurysm initiation, growth, and rupture: toward a unifying hypothesis. AJNR Am J Neuroradiol 35:1254–1262CrossRef Meng H, Tutino VM, Xiang J, Siddiqui A (2014) High WSS or low WSS? Complex interactions of hemodynamics with intracranial aneurysm initiation, growth, and rupture: toward a unifying hypothesis. AJNR Am J Neuroradiol 35:1254–1262CrossRef
5.
go back to reference Karmonik C, Yen C, Grossman RG, Klucznik R, Benndorf G (2009) Intra-aneurysmal flow patterns and wall shear stresses calculated with computational flow dynamics in an anterior communicating artery aneurysm depend on knowledge of patient-specific inflow rates. Acta Neurochir (Wien) 151:479–485 discussion 485CrossRef Karmonik C, Yen C, Grossman RG, Klucznik R, Benndorf G (2009) Intra-aneurysmal flow patterns and wall shear stresses calculated with computational flow dynamics in an anterior communicating artery aneurysm depend on knowledge of patient-specific inflow rates. Acta Neurochir (Wien) 151:479–485 discussion 485CrossRef
6.
go back to reference Malek AM, Alper SL, Izumo S (1999) Hemodynamic shear stress and its role in atherosclerosis. JAMA 282:2035–2042CrossRef Malek AM, Alper SL, Izumo S (1999) Hemodynamic shear stress and its role in atherosclerosis. JAMA 282:2035–2042CrossRef
7.
go back to reference Meng H, Wang Z, Hoi Y et al (2007) Complex hemodynamics at the apex of an arterial bifurcation induces vascular remodeling resembling cerebral aneurysm initiation. Stroke 38:1924–1931CrossRef Meng H, Wang Z, Hoi Y et al (2007) Complex hemodynamics at the apex of an arterial bifurcation induces vascular remodeling resembling cerebral aneurysm initiation. Stroke 38:1924–1931CrossRef
8.
go back to reference Can A, Du R (2016) Association of hemodynamic factors with intracranial aneurysm formation and rupture: systematic review and meta-analysis. Neurosurgery 78:510–520CrossRef Can A, Du R (2016) Association of hemodynamic factors with intracranial aneurysm formation and rupture: systematic review and meta-analysis. Neurosurgery 78:510–520CrossRef
9.
go back to reference Skodvin TØ, Evju Ø, Helland CA, Isaksen JG (2017) Rupture prediction of intracranial aneurysms: a nationwide matched case-control study of hemodynamics at the time of diagnosis. J Neurosurg:1–7 Skodvin TØ, Evju Ø, Helland CA, Isaksen JG (2017) Rupture prediction of intracranial aneurysms: a nationwide matched case-control study of hemodynamics at the time of diagnosis. J Neurosurg:1–7
10.
go back to reference Fukazawa K, Ishida F, Umeda Y et al (2015) Using computational fluid dynamics analysis to characterize local hemodynamic features of middle cerebral artery aneurysm rupture points. World Neurosurg 83:80–86CrossRef Fukazawa K, Ishida F, Umeda Y et al (2015) Using computational fluid dynamics analysis to characterize local hemodynamic features of middle cerebral artery aneurysm rupture points. World Neurosurg 83:80–86CrossRef
11.
go back to reference Kaspera W, Ładziński P, Larysz P et al (2014) Morphological, hemodynamic, and clinical independent risk factors for anterior communicating artery aneurysms. Stroke 45:2906–2911CrossRef Kaspera W, Ładziński P, Larysz P et al (2014) Morphological, hemodynamic, and clinical independent risk factors for anterior communicating artery aneurysms. Stroke 45:2906–2911CrossRef
12.
go back to reference Ye J, Zheng P, Hassan M, Jiang S, Zheng J (2017) Relationship of the angle between the A1 and A2 segments of the anterior cerebral artery with formation and rupture of anterior communicating artery aneurysm. J Neurol Sci 375:170–174CrossRef Ye J, Zheng P, Hassan M, Jiang S, Zheng J (2017) Relationship of the angle between the A1 and A2 segments of the anterior cerebral artery with formation and rupture of anterior communicating artery aneurysm. J Neurol Sci 375:170–174CrossRef
13.
go back to reference Krejza J, Mariak Z, Walecki J, Szydlik P, Lewko J, Ustymowicz A (1999) Transcranial color Doppler sonography of basal cerebral arteries in 182 healthy subjects: age and sex variability and normal reference values for blood flow parameters. AJR Am J Roentgenol 172:213–218CrossRef Krejza J, Mariak Z, Walecki J, Szydlik P, Lewko J, Ustymowicz A (1999) Transcranial color Doppler sonography of basal cerebral arteries in 182 healthy subjects: age and sex variability and normal reference values for blood flow parameters. AJR Am J Roentgenol 172:213–218CrossRef
14.
go back to reference Irace C, Carallo C, De Franceschi MS et al (2012) Human common carotid wall shear stress as a function of age and gender: a 12-year follow-up study. Age (Dordr) 34:1553–1562CrossRef Irace C, Carallo C, De Franceschi MS et al (2012) Human common carotid wall shear stress as a function of age and gender: a 12-year follow-up study. Age (Dordr) 34:1553–1562CrossRef
15.
go back to reference Stolz E, Kaps M, Kern A, Dorndorf W (1999) Frontal bone windows for transcranial color-coded duplex sonography. Stroke 30:814–820CrossRef Stolz E, Kaps M, Kern A, Dorndorf W (1999) Frontal bone windows for transcranial color-coded duplex sonography. Stroke 30:814–820CrossRef
16.
go back to reference Velcheva I, Antonova N, Damianov P, Dimitrov N (2010) Common carotid artery hemodynamic factors in patients with cerebral infarctions. Clin Hemorheol Microcirc 45:233–238 Velcheva I, Antonova N, Damianov P, Dimitrov N (2010) Common carotid artery hemodynamic factors in patients with cerebral infarctions. Clin Hemorheol Microcirc 45:233–238
17.
go back to reference Carallo C, Irace C, Pujia A et al (1999) Evaluation of common carotid hemodynamic forces. Relations with wall thickening. Hypertension 34:217–221CrossRef Carallo C, Irace C, Pujia A et al (1999) Evaluation of common carotid hemodynamic forces. Relations with wall thickening. Hypertension 34:217–221CrossRef
18.
go back to reference Longo M, Granata F, Racchiusa S et al (2017) Role of hemodynamic forces in unruptured intracranial aneurysms: an overview of a complex scenario. World Neurosurg 105:632–642CrossRef Longo M, Granata F, Racchiusa S et al (2017) Role of hemodynamic forces in unruptured intracranial aneurysms: an overview of a complex scenario. World Neurosurg 105:632–642CrossRef
19.
go back to reference Kawaguchi T, Nishimura S, Kanamori M et al (2012) Distinctive flow pattern of wall shear stress and oscillatory shear index: similarity and dissimilarity in ruptured and unruptured cerebral aneurysm blebs. J Neurosurg 117:774–780CrossRef Kawaguchi T, Nishimura S, Kanamori M et al (2012) Distinctive flow pattern of wall shear stress and oscillatory shear index: similarity and dissimilarity in ruptured and unruptured cerebral aneurysm blebs. J Neurosurg 117:774–780CrossRef
20.
go back to reference Liu J, Xiang J, Zhang Y et al (2014) Morphologic and hemodynamic analysis of paraclinoid aneurysms: ruptured versus unruptured. J Neurointerv Surg 6:658–663CrossRef Liu J, Xiang J, Zhang Y et al (2014) Morphologic and hemodynamic analysis of paraclinoid aneurysms: ruptured versus unruptured. J Neurointerv Surg 6:658–663CrossRef
21.
go back to reference Shojima M, Oshima M, Takagi K et al (2004) Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms. Stroke 35:2500–2505CrossRef Shojima M, Oshima M, Takagi K et al (2004) Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms. Stroke 35:2500–2505CrossRef
22.
go back to reference Sugiyama S, Meng H, Funamoto K et al (2012) Hemodynamic analysis of growing intracranial aneurysms arising from a posterior inferior cerebellar artery. World Neurosurg 78:462–468CrossRef Sugiyama S, Meng H, Funamoto K et al (2012) Hemodynamic analysis of growing intracranial aneurysms arising from a posterior inferior cerebellar artery. World Neurosurg 78:462–468CrossRef
23.
go back to reference Chien A, Tateshima S, Sayre J, Castro M, Cebral J, Viñuela F (2009) Patient-specific hemodynamic analysis of small internal carotid artery-ophthalmic artery aneurysms. Surg Neurol 72:444–450 discussion 450CrossRef Chien A, Tateshima S, Sayre J, Castro M, Cebral J, Viñuela F (2009) Patient-specific hemodynamic analysis of small internal carotid artery-ophthalmic artery aneurysms. Surg Neurol 72:444–450 discussion 450CrossRef
24.
go back to reference Frösen J (2016) Flow dynamics of aneurysm growth and rupture: challenges for the development of computational flow dynamics as a diagnostic tool to detect rupture-prone aneurysms. Acta Neurochir Suppl 123:89–95CrossRef Frösen J (2016) Flow dynamics of aneurysm growth and rupture: challenges for the development of computational flow dynamics as a diagnostic tool to detect rupture-prone aneurysms. Acta Neurochir Suppl 123:89–95CrossRef
25.
go back to reference Cheng C, Helderman F, Tempel D et al (2007) Large variations in absolute wall shear stress levels within one species and between species. Atherosclerosis 195:225–235CrossRef Cheng C, Helderman F, Tempel D et al (2007) Large variations in absolute wall shear stress levels within one species and between species. Atherosclerosis 195:225–235CrossRef
26.
go back to reference Galizia MS, Barker A, Liao Y et al (2014) Wall morphology, blood flow and wall shear stress: MR findings in patients with peripheral artery disease. Eur Radiol 24:850–856CrossRef Galizia MS, Barker A, Liao Y et al (2014) Wall morphology, blood flow and wall shear stress: MR findings in patients with peripheral artery disease. Eur Radiol 24:850–856CrossRef
27.
go back to reference Gnasso A, Carallo C, Irace C et al (1996) Association between intima-media thickness and wall shear stress in common carotid arteries in healthy male subjects. Circulation 94:3257–3262CrossRef Gnasso A, Carallo C, Irace C et al (1996) Association between intima-media thickness and wall shear stress in common carotid arteries in healthy male subjects. Circulation 94:3257–3262CrossRef
28.
go back to reference Samijo SK, Barkhuysen R, Willigers JM et al (2002) Wall shear stress assessment in the common carotid artery of end-stage renal failure patients. Nephron 92:557–563CrossRef Samijo SK, Barkhuysen R, Willigers JM et al (2002) Wall shear stress assessment in the common carotid artery of end-stage renal failure patients. Nephron 92:557–563CrossRef
29.
go back to reference Katritsis D, Kaiktsis L, Chaniotis A, Pantos J, Efstathopoulos EP, Marmarelis V (2007) Wall shear stress: theoretical considerations and methods of measurement. Prog Cardiovasc Dis 49:307–329CrossRef Katritsis D, Kaiktsis L, Chaniotis A, Pantos J, Efstathopoulos EP, Marmarelis V (2007) Wall shear stress: theoretical considerations and methods of measurement. Prog Cardiovasc Dis 49:307–329CrossRef
30.
go back to reference Liu Z, Zhao Y, Wang X et al (2016) Low carotid artery wall shear stress is independently associated with brain white-matter hyperintensities and cognitive impairment in older patients. Atherosclerosis 247:78–86CrossRef Liu Z, Zhao Y, Wang X et al (2016) Low carotid artery wall shear stress is independently associated with brain white-matter hyperintensities and cognitive impairment in older patients. Atherosclerosis 247:78–86CrossRef
31.
go back to reference Sui B, Gao P, Lin Y, Gao B, Liu L, An J (2008) Assessment of wall shear stress in the common carotid artery of healthy subjects using 3.0-tesla magnetic resonance. Acta Radiol 49:442–449CrossRef Sui B, Gao P, Lin Y, Gao B, Liu L, An J (2008) Assessment of wall shear stress in the common carotid artery of healthy subjects using 3.0-tesla magnetic resonance. Acta Radiol 49:442–449CrossRef
32.
go back to reference Mynard JP, Wasserman BA, Steinman DA (2013) Errors in the estimation of wall shear stress by maximum Doppler velocity. Atherosclerosis 227:259–266CrossRef Mynard JP, Wasserman BA, Steinman DA (2013) Errors in the estimation of wall shear stress by maximum Doppler velocity. Atherosclerosis 227:259–266CrossRef
33.
go back to reference Nixon AM, Gunel M, Sumpio BE (2010) The critical role of hemodynamics in the development of cerebral vascular disease. J Neurosurg 112:1240–1253CrossRef Nixon AM, Gunel M, Sumpio BE (2010) The critical role of hemodynamics in the development of cerebral vascular disease. J Neurosurg 112:1240–1253CrossRef
34.
go back to reference Shakur SF, Alaraj A, Mendoza-Elias N, Osama M, Charbel FT (2018) Hemodynamic characteristics associated with cerebral aneurysm formation in patients with carotid occlusion. J Neurosurg :1-6 Shakur SF, Alaraj A, Mendoza-Elias N, Osama M, Charbel FT (2018) Hemodynamic characteristics associated with cerebral aneurysm formation in patients with carotid occlusion. J Neurosurg :1-6
35.
go back to reference Jing L, Zhong J, Liu J et al (2016) Hemodynamic effect of flow diverter and coils in treatment of large and giant intracranial aneurysms. World Neurosurg 89:199–207CrossRef Jing L, Zhong J, Liu J et al (2016) Hemodynamic effect of flow diverter and coils in treatment of large and giant intracranial aneurysms. World Neurosurg 89:199–207CrossRef
36.
go back to reference Box FM, van der Grond J, de Craen AJ et al (2007) Pravastatin decreases wall shear stress and blood velocity in the internal carotid artery without affecting flow volume: results from the PROSPER MRI study. Stroke 38:1374–1376CrossRef Box FM, van der Grond J, de Craen AJ et al (2007) Pravastatin decreases wall shear stress and blood velocity in the internal carotid artery without affecting flow volume: results from the PROSPER MRI study. Stroke 38:1374–1376CrossRef
37.
go back to reference Box FM, van der Geest RJ, Rutten MC, Reiber JH (2005) The influence of flow, vessel diameter, and non-Newtonian blood viscosity on the wall shear stress in a carotid bifurcation model for unsteady flow. Invest Radiol 40:277–294CrossRef Box FM, van der Geest RJ, Rutten MC, Reiber JH (2005) The influence of flow, vessel diameter, and non-Newtonian blood viscosity on the wall shear stress in a carotid bifurcation model for unsteady flow. Invest Radiol 40:277–294CrossRef
38.
go back to reference Dormandy JA (1974) Medical and engineering problems of blood viscosity. Biomed Eng 9:284–289 Dormandy JA (1974) Medical and engineering problems of blood viscosity. Biomed Eng 9:284–289
Metadata
Title
The role of wall shear stress in the parent artery as an independent variable in the formation status of anterior communicating artery aneurysms
Authors
Xin Zhang
Zhi-Qiang Yao
Tamrakar Karuna
Xu-Ying He
Xue-Min Wang
Xi-Feng Li
Wen-Chao Liu
Ran Li
Shen-Quan Guo
Yun-Chang Chen
Gan-Cheng Li
Chuan-Zhi Duan
Publication date
01-02-2019
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 2/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5624-7

Other articles of this Issue 2/2019

European Radiology 2/2019 Go to the issue