|Year : 2020 | Volume
| Issue : 2 | Page : 87-95
Multiple flow-related intracranial aneurysms in the setting of contralateral carotid occlusion: Coincidence or association?
Cassidy Werner, Mansour Mathkour, Tyler Scullen, Erin Mccormack, Aaron S Dumont, Peter S Amenta
Department of Neurosurgery, Tulane Medical Center, New Orleans, LA, USA
|Date of Submission||12-Jan-2020|
|Date of Acceptance||26-May-2020|
|Date of Web Publication||26-Jun-2020|
Dr. Peter S Amenta
Department of Neurosurgery, Tulane Medical Center, 1415 Tulane Ave, New Orleans, LA 70112
Source of Support: None, Conflict of Interest: None
The prevalence of intracranial aneurysms (IAs) is higher in patients with internal carotid artery (ICA) stenosis, likely due to alterations in intracranial hemodynamics. Severe stenosis or occlusion of one ICA may result in increased demand and altered hemodynamics in the contralateral ICA, thus increasing the risk of contralateral IA formation. In this article, we discuss a relevant case and a comprehensive literature review as it pertains to the association of ICA stenosis and IA. Our patient was a 50-year-old female with a chronic asymptomatic right ICA occlusion who presented with diffuse subarachnoid hemorrhage. Emergent angiography revealed left-sided A1-A2 junction, paraclinoid, left middle cerebral artery (MCA) bifurcation, and left anterior temporal artery aneurysms. Brisk filling of the right anterior circulation through the anterior communicating artery was also identified, signifying increased demand on the left ICA circulation. Complete obliteration of all aneurysms was achieved with coil embolization and clipping. For our literature review, we searched the PubMed and EMBASE databases for case reports and case series, as well as references in previously published review articles that described patients with concurrent aneurysms and ICA stenosis. We selected articles that provided adequate information about the case presentations to compare aneurysm and patient characteristics. Our review revealed a higher number of patients with multiple aneurysms contralateral (25%) to rather than ipsilateral to (6%), the ICA stenosis. We discuss the pathogenesis and management of multiple flow-related IA in the context of the existing literature related to concurrent ICA stenosis and IA.
Keywords: Carotid stenosis, endovascular, flow-related aneurysm, intracranial aneurysm, neurosurgery, subarachnoid hemorrhage
|How to cite this article:|
Werner C, Mathkour M, Scullen T, Mccormack E, Dumont AS, Amenta PS. Multiple flow-related intracranial aneurysms in the setting of contralateral carotid occlusion: Coincidence or association?. Brain Circ 2020;6:87-95
|How to cite this URL:|
Werner C, Mathkour M, Scullen T, Mccormack E, Dumont AS, Amenta PS. Multiple flow-related intracranial aneurysms in the setting of contralateral carotid occlusion: Coincidence or association?. Brain Circ [serial online] 2020 [cited 2023 May 31];6:87-95. Available from: http://www.braincirculation.org/text.asp?2020/6/2/87/287731
| Introduction|| |
Approximately 2.8% of the general population harbors an unruptured intracranial aneurysm (IA). IA rupture results in subarachnoid hemorrhage (SAH), which carries a 30-day mortality rate of 45% and moderate-to-severe neurologic disability in 30%–50% of survivors., The incidence of aneurysmal SAH ranges from 6 to 16/100,000 individuals depending on the country.,,, IAs have also been shown to be associated with conditions that alter intracranial blood flow, such as arteriovenous malformations, collateral circulation from persistent fetal arteries, moyamoya disease and other vasculopathies, and atherosclerotic arterial stenosis or occlusion.,,,
In this article, we present a patient with SAH who was found to have multiple left-sided anterior circulation IA and a chronic right ICA occlusion. We conducted a comprehensive literature review pertaining to the association of ICA stenosis and IA. The management of this complex clinical scenario is discussed, and the contribution of ICA stenosis-induced hemodynamic influences on IA formation is reviewed.
| Case Report|| |
A 50-year-old female with a past medical history significant for smoking, hypertension, and a chronic asymptomatic right ICA occlusion presented with a Hunt Hess grade III, Fisher grade III SAH [Figure 1]a. Angiography revealed a left 8 mm × 5 mm A1-A2 junction aneurysm, a 3 mm × 2 mm left paraclinoid aneurysm, a 3 mm × 3.5 mm left middle cerebral artery (MCA) bifurcation aneurysm with an excrescence, and a 2.7 mm left anterior temporal artery aneurysm [Figure 1]. Brisk filling of the right anterior circulation through the anterior communicating (ACOM) artery was also identified, signifying increased demand on the left ICA circulation.
|Figure 1: (a) Noncontrast axial head computed tomography demonstrating diffuse subarachnoid hemorrhage. (b) Left internal carotid anteroposterior (AP) injection showing left-sided 8 mm × 5 mm A1-A2 junction aneurysm, 3 mm × 2 mm left paraclinoid aneurysm, 3 mm × 3.5 mm middle cerebral artery bifurcation aneurysm with an excrescence, and a 2.7 mm left anterior temporal artery aneurysm (arrows). Note the large anterior communicating artery (ACOM), through which the right anterior circulation is supplied. (b and c) Left internal carotid AP injections demonstrate filling of the right anterior circulation through the ACOM complex|
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Due to the diffuse blood pattern, definitive confirmation of which aneurysm ruptured was not possible, however, the large size of the A1-A2 junction aneurysm and excrescence on the MCA bifurcation aneurysm made one of these the most likely culprit [Figure 2]. Complete obliteration of the A1-A2 junction, paraclinoid, and MCA bifurcation aneurysms was achieved with coil embolization. The left anterior temporal aneurysm was left untreated in the acute setting due to its small size, regular shape, and low likelihood of being the ruptured aneurysm. The patient was unable to be weaned from an external ventricular drain and a ventriculoperitoneal shunt was ultimately placed. The patient was discharged neurologically intact on postbleed day 15 to an inpatient rehabilitation facility. The anterior temporal artery aneurysm was obliterated with clipping 6 weeks following the hemorrhage. Postoperative angiogram at that time demonstrated stable complete obliteration of the coiled aneurysms [Figure 3] and [Figure 4]. The patient made a complete recovery and is living independently. All aneurysms remained completely occluded on 8-month follow-up angiography.
|Figure 2: Left anterior oblique injection better demonstrating the left middle cerebral artery bifurcation aneurysm with dome excrescence|
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|Figure 3: (a) Final left anterior oblique injection demonstrating complete obliteration of the left A1A2 junction (blue arrow), paraclinoid (green arrow), and middle cerebral artery bifurcation (yellow arrow) aneurysms|
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|Figure 4: (a) Angiogram post left anterior temporal artery aneurysm clipping performed 6 weeks following initial presentation. Left anterior oblique injection demonstrating stable complete obliteration of the left A1A2 junction (blue arrow), paraclinoid (green arrow), and middle cerebral artery bifurcation (yellow arrow) aneurysms. The left anterior temporal artery aneurysm has been obliterated by clipping (red arrow)|
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| Literature Review Methods and Results|| |
For this report, we searched the PubMed and EMBASE databases for all case reports, case series, and references in previously published reviews regarding patients with concurrent aneurysms and ICA stenosis. To the best of our knowledge, we have included all available instances of coexistent IA and carotid artery stenosis in our analysis [Table 1].,,,,,,,,,,,,,,,,,,,,,,, Because some of the individual patient records did not include all useful data (e.g., age and gender), the total number of patients is different for each category, and thus, the data are presented as percentages. In addition, aneurysm sizes that were presented as a range were not included in the calculations of means. The published cases of patients with multiple aneurysms all contralateral to the side of major ICA stenosis are presented in [Table 2], and cases with multiple aneurysms all ipsilateral or bilateral to the side of major ICA stenosis are presented in [Table 3].,,,,,,,, In addition, we have collected the available data from case studies that only listed the average values for their cohorts instead of data from individual patients.,,,,,, These studies have not been compiled into a table because of insufficient data regarding the location of the aneurysms.
|Table 1: Statistical comparison of patients with single and multiple aneurysms from published individual cases|
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|Table 2: Cases from the literature of patients with multiple aneurysms all contralateral to major carotid stenosis|
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|Table 3: Cases from literature of patients with multiple aneurysms either all ipsilateral or bilateral to major carotid stenosis|
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We found a total of 150 relevant patient reports in the literature. Of those, 134 (89.3%) had a single aneurysm and 16 (10.7%) had multiple aneurysms. Sixteen patients with multiple aneurysms had a total of 37 aneurysms: 12 patients had two aneurysms, three patients had three aneurysms, and one patient had four aneurysms. For both groups (a single aneurysm and multiple aneurysms), there were more female than male patients. Most of the aneurysms were located in the anterior cerebral circulation for patients with a single aneurysm (102/132, 77.2%) and for patients with multiple aneurysms (27/37, 73.0%). The most common aneurysm location for each group was the MCA and the second most common location for each group was the posterior communicating artery (PCOM).
Of the reports that listed laterality of both the aneurysm and the stenosis, most (72.6%) of the patients with a single aneurysm had IA ipsilateral to the ICA stenosis. Most patients with multiple aneurysms had aneurysms both ipsilateral and contralateral (69%) to the carotid stenosis; however, more patients (25%) had all of their aneurysms on the contralateral side than on the ipsilateral side (6%), as was the case with our patient. The proportion of patients that presented with symptoms attributed to the aneurysm (SAH, visual field defects, headache, paresis, and paresthesia) was higher for patients with multiple aneurysms (25.0%) than for patients with a single aneurysm (18.0%).
None of the patients with ICA stenosis and multiple aneurysms all contralateral to the side of major stenosis presented with aneurysmal rupture. Of the four patients, only one was treated (clipping). No recurrence or rupture of the aneurysm was reported in that patient upon follow-up. Of the 12 patients with ICA stenosis and multiple aneurysms ipsilateral or bilateral to the side of major stenosis, three of them presented with SAH from a ruptured aneurysm. Two of these patients initially presented with SAH and both patients were treated with aneurysm clipping. No follow-up data are available. The third patient did not initially present with rupture but suffered a fatal aneurysmal SAH 7 months after an initial presentation of left hemiparesis and the discovery of two unruptured IA that were left untreated. Of the 21 aneurysms in the nine other patients, six were clipped and one was coiled. For the cases with available data, none of these treated aneurysms showed the recurrence or rupture at follow-up.
A study by Kappelle et al. reported that nine out of ninety patients with ICA stenosis and concomitant IA had multiple aneurysms (10%), which is similar to our findings in the pooled literature data. They reported a slightly higher number of patients with ipsilateral aneurysms (56.6%) than patients with contralateral aneurysms (43.4%). However, because the data on the individual aneurysm locations is unavailable, we are unable to determine the number of patients with all ipsilateral and all contralateral aneurysms. A study conducted in South Korea by Cho et al. reported a high rate of patients with multiple aneurysms (29.1%) and more contralateral aneurysms (52.6%) than ipsilateral aneurysms, but they also did not report the laterality of all their patients' aneurysms. In both of those studies and in four additional similar studies,,,,, there were no reported cases of SAH due to an untreated aneurysm in patients with single or multiple aneurysms.
| Discussion|| |
Our patient presented with multiple left-sided IAs and chronic asymptomatic right ICA occlusion. In comparison to the compiled data from the literature, she is 23 years younger than the average age of a patient presenting with multiple aneurysms (all contralateral) in the setting of carotid stenosis, possibly due to her risk factors of chronic hypertension and cigarette smoking. The only reported cases of aneurysmal SAH in patients with multiple aneurysms and coexistent ICA stenosis were of patients with ipsilateral aneurysms, making her case unique. Her MCA aneurysm matched with the most common location found in the data, whereas her paraclinoid and anterior temporal artery aneurysms were not as commonly found among other patients. Most patients in the literature with multiple aneurysms had IA both ipsilateral and contralateral (69%) to the ICA stenosis; however, more patients (25%) had all of their aneurysms on the contralateral side than on the ipsilateral side (6%), as was the case with our patient.
| Hemodynamic Stress and Aneurysm Genesis|| |
Initiation of IA development, growth, and eventual rupture is a complex process that is influenced by multiple genetic and environmental factors. Chronic hypertension, binge drinking, and cigarette smoking are all well-defined contributors to IA pathogenesis and the inflammatory cascade represents a potential common endpoint through which these environmental stimuli lead to IA genesis.,, Hemodynamic stress along vessel walls drives vascular remodeling, which is the end result of inflammation, endothelial dysfunction, and vascular smooth muscle cell (VSMC) phenotypic changes. Increased shear stress along a vessel wall is a known activator of the inflammatory response.,,, IA most commonly form at vessel branch points, where hemodynamic stress is greatest. In addition, the strong link between IA and environmental stimuli known to disrupt vascular integrity (smoking and hypertension) highlights the contribution of abnormal blood flow and shear stress in IA formation. Endothelial cells, which serve as the interface between blood flow and the vessel wall, are key contributors to this process. The apical and basal surfaces of endothelial cells display multiple mechanical sensors, including, ion channels, integrins, cell adhesion molecules, and G protein-coupled receptors.,,, These sensors respond to the mechanical stimuli of shear, stretch, and flow by altering their physical structure and initiating biologic signaling through mechanotransduction.,,
VSMCs represent the primary cellular component of the tunica media and maintain vessel wall integrity. Under normal physiologic conditions, the cells remain in a nonmotile contractile state and allow the vessel wall to adapt to changes in blood pressure. In the setting of increased hemodynamic stress, the endothelium and VSMCs partake in complex and cyclical cascade of events that lead to disruption of the tunica media and extracellular matrix., VSMCs transition from the contractile phenotype to a secretory phenotype that is defined by gain in motility, a loss of markers of contractility, and expression of proinflammatory cytokines and matrix metalloproteinases.,,,,, Histologic examination of IA walls, which demonstrates erratic migration and apoptosis of VSMCs, provides evidence of this phenotypic change. Aneurysm growth is defined by additional degradation of the tunica media and cellular loss.,, The walls of ruptured IA more frequently demonstrate hypocellular and hyalinized walls when compared to unruptured IA.,
| Internal Carotid Artery Stenosis and Intracranial Aneurysm Formation|| |
Yang et al. reported a 6.3% prevalence of carotid stenosis and coexistent IA, which is more than twice the prevalence of incidentally found IA in the general population. This value includes IA both ipsilateral and contralateral to the ICA stenosis. Although the exact mechanisms underlying IA formation in the setting of ICA stenosis have yet to be fully defined, it is postulated that hemodynamic changes in the intracranial vasculature heavily influence IA development. For IA ipsilateral to the stenosis, at least initially, autoregulation distal to the stenotic ICA likely leads to increased blood flow, increased blood flow velocity, and greater wall stress in the intracranial vasculature. As the stenosis progresses, flow to the intracranial circulation may decrease, or stop, in cases of complete occlusion. Examination of flow rate through a stenotic vessel has been demonstrated to remain stable, until the stenosis reaches 75%, at which point a significant reduction is observed. Severe ICA stenosis (75%–99%) results in a 35% reduction in blood flow through the artery, whereas occlusion also leads to a 14% flow reduction in the ipsilateral MCA. This may explain the reported higher number of patients with multiple contralateral aneurysms than with multiple ipsilateral aneurysms (5 to one including this case report). In addition, the eventual significant drop in flow through the stenosis likely also contributes to the finding that IA ipsilateral to ICA stenosis are of a mean smaller size than those IA located contralateral to ICA stenosis.
In those IA contralateral to the ICA stenosis, it is likely that the increased metabolic demand on the nonstenotic vessel increases blood flow, stretch, and hemodynamic stress distal to the nonstenotic vessel. Furthermore, these hemodynamic stresses are likely greatest at the sites of collateralization between the circulations (ACOM and PCOM). A recent quantitative magnetic resonance angiography study to assess hemodynamic changes that may lead to IA showed higher wall shear stress and flow velocity across vessels that provide collateral blood supply in the setting of ICA occlusion, namely the ACOM and PCOM. Additional studies have reported larger aneurysm sizes on the side contralateral to a stenotic ICA. Our patient presented with an asymptomatic chronic right ICA occlusion and a large ACOM through which the entire right anterior circulation was fed by the left ICA. The left A1-A2 junction was also the site of the patient's largest aneurysm.
Our patient also had two IA arising from the left MCA, which we believe to be secondary to increased flow and hemodynamic stress through the parent vessel. Based on the downstream location of the MCA from the ICA, increased demand on the ICA contralateral to the stenosis is transmitted to the ipsilateral MCA and in turn, would translate into conditions conducive to MCA IA formation.
IA in the setting of concomitant posterior circulation artery occlusion are less common than aneurysms in the setting of anterior circulation occlusion for a number of reasons. First, in general, posterior circulation IA are significantly less common, accounting for only approximately 10%–15% of all IA. Second, occlusion of a single vertebral artery reduces the overall flow through the posterior circulation. Increased flow through the contralateral vertebral artery could result in conditions suitable for IA formation along that vessel; however, contrary to the intracranial ICA, there is only a single large caliber branch, the posterior inferior cerebellar artery (PICA). Overall PICA IA is rare, and there are multiple variations in its caliber, origin, and angioarchitecture. Finally, severe posterior circulation atherosclerosis and stenosis are associated with a higher mortality rate and may not allow adequate time for the chronic hemodynamic changes that lead to aneurysm formation.
One situation in which posterior circulation aneurysms are likely formed due to increased blood flow is moyamoya disease, where chronic anterior circulation occlusion leads to increased demand through the posterior circulation. A review of published cases demonstrated a higher incidence of posterior circulation aneurysms (50%–60%) in moyamoya patients than in the normal population.
| Management Considerations in Our Patient|| |
Our patient presented with a Hunt Hess grade III Fisher grade III SAH and was found to have multiple left-sided IA. Due to the diffuse blood pattern, identification of the ruptured IA was difficult; however, the large A1-A2 junction and MCA bifurcation aneurysm with an excrescence were felt to be the most likely rupture source. The left anterior temporal and paraclinoid aneurysms were of a small size and regular shape.
The A1-A2 junction, MCA bifurcation, and paraclinoid aneurysms were all narrow-necked and suitable candidates for obliteration with either clipping or coiling. The left anterior temporal aneurysm was small, of wide-neck morphology, incorporated the M1 trunk and left anterior temporal artery, and was deemed a better candidate for clipping. Coiling was chosen for the A1-A2 junction, MCA bifurcation, and paraclinoid aneurysms for multiple reasons. First, the patient presented with a high-grade hemorrhage, hydrocephalus requiring an external ventricular drain, and significant cerebral edema. Endovascular treatment allowed for rapid occlusion of all three aneurysms without the need for extensive Sylvian fissure dissection and brain retraction. Second, the left-sided location of all the aneurysms would have forced dissection of the dominant left frontal and temporal lobes. Third, treatment of the paraclinoid aneurysm would have required a clinoidectomy and neck dissection to gain proximal control of the left internal carotid artery. Temporary occlusion of the left internal carotid artery would result in hypoperfusion of both hemispheres due to the occluded right ICA. Finally, the A1-A2 junction aneurysm was the largest and possibly the aneurysm most likely to have ruptured. In the event that temporary clipping of the left A1 segment would be required, the entire right hemisphere would be deprived of blood flow through the ACOM complex.
All aneurysms were obliterated, and the patient made a complete recovery, yet we do acknowledge that coiling of flow-related aneurysms could be subject to criticism. Although the literature tends to demonstrate improved clinical outcomes with coiling,, multiple studies have shown superior durability of clipping when compared to coiling. In part, recurrence of coiled IA is caused by continuous blood flow compacting the coil mass within the dome. Certainly, the exaggerated hemodynamic parameters that led to the formation of our patient's IA, would likely contribute to an increased risk of recurrence. On short-term follow-up angiography, all aneurysms remain completely obliterated with no evidence of residual or recurrence. Follow-up angiography at 8 months showed persistent complete occlusion of all treated aneurysms. The patient will require routine long-term serial imaging to identify the potential recurrence.
The management of patients presenting with multiple IA in the setting of ICA stenosis should be considered on a case-by-case basis. As shown by our review of the literature, the risk of rupture in untreated patients is not greatly increased when the patient has more than one IA (3.5%; 10%). The difference can be explained by the larger mean size of aneurysms in our sample of patients with multiple aneurysms (5.9 mm and 7.5 mm), as larger IA carry a higher risk of rupture. Prophylactic management should likely depend on risk factors for aneurysmal rupture other than the number of aneurysms, such as size, age, morphology, and intracranial location.
| Conclusion|| |
We present a patient with a chronic asymptomatic right ICA occlusion and aneurysmal SAH, who was found to have multiple, likely flow-related, left-sided anterior circulation aneurysms. All aneurysms were obliterated with a combination of endovascular and microsurgical techniques, and the patient made a complete recovery. A review of published case reports/studies of patients with concurrent ICA stenosis and IA revealed a higher number of patients with multiple aneurysms contralateral (25%) to, rather than ipsilateral to (6%), the ICA stenosis. We discuss these findings in relation to the available data pertaining to hemodynamics and IA formation. Ruptured IA in the setting of concomitant significant ICA stenosis or occlusion represents a challenging clinical scenario that is further complicated by the presence of multiple IA. An understanding of IA pathogenesis, cerebral hemodynamics, and available treatment options are critical to successful patient management.
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The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
Vlak MH, Algra A, Brandenburg R, Rinkel GJ. Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: A systematic review and meta-analysis. Lancet Neurol 2011;10:626-36.
Bederson JB, Awad IA, Wiebers DO, Piepgras D, Haley Jr EC, Brott T, et al
. Recommendations for the management of patients with unruptured intracranial aneurysms: A statement for healthcare professionals from the Stroke Council of the American Heart Association. Stroke 2011;31:2742-50.
Johnston SC, Selvin S, Gress DR. The burden, trends, and demographics of mortality from subarachnoid hemorrhage. Neurology 1998;50:1413-8.
Etminan N, Brown RD Jr., Beseoglu K, Juvela S, Raymond J, Morita A, et al
. The unruptured intracranial aneurysm treatment score: A multidisciplinary consensus. Neurology 2018;85:881-9.
Lin N, Cahill KS, Frerichs KU, Friedlander RM, Claus EB. Treatment of ruptured and unruptured cerebral aneurysms in the USA: A paradigm shift. J Neurointerv Surg 2018;10:i69-i76.
Thompson RC, Steinberg GK, Levy RP, Marks MP. The management of patients with arteriovenous malformations and associated intracranial aneurysms. Neurosurgery 1998;43:202-11.
Touze E, Oppenheim C, Trystram D, Nokam G, Pasquini M, Alamowitch S, et al
. Fibromuscular dysplasia of cervical and intracranial arteries. Int J Stroke 2010;5:296-305.
Varvari I, Bos EM, Dinkelaar W, van Es AC, Can A, Hunfeld M, et al
. Fatal subarachnoid hemorrhage from an aneurysm of a persistent primitive hypoglossal artery: Case series and literature overview. World Neurosurg 2018;117:285-91.
Zhang L, Xu K, Zhang Y, Wang X, Yu J. Treatment strategies for aneurysms associated with moyamoya disease. Int J Med Sci 2015;12:234-42.
Adams HP Jr. Carotid stenosis and coexisting ipsilateral intracranial aneurysm. A problem in management. Arch Neurol 1977;34:515-6.
Badruddin A, Teleb MS, Abraham MG, Taqi MA, Zaidat OO. Safety and feasibility of simultaneous ipsilateral proximal carotid artery stenting and cerebral aneurysm coiling. Front Neurol 2010;1:120.
Ballotta E, Da Giau G, Manara R, Baracchini C. Extracranial severe carotid stenosis and incidental intracranial aneurysms. Ann Vasc Surg 2006;20:5-8.
Borkon MJ, Hoang H, Rockman C, Mussa F, Cayne NS, Riles T, et al
. Concomitant unruptured intracranial aneurysms and carotid artery stenosis: An institutional review of patients undergoing carotid revascularization. Ann Vasc Surg 2014;28:102-7.
Denton IC Jr., Gutmann L. Surgical treatment of symptomatic carotid stenosis and asymptomatic ipsilateral intracranial aneurysm. Case report. J Neurosurg 1973;38:662-5.
Detry O, Defraigne JO, Desiron Q, Martin D, Born J, Hans P, et al
. Sequential Successful surgical management of extracranial internal carotid stenosis and ipsilateral intracranial aneurysm. Vasc Surg 1997;31:179-85.
Espinosa G, Dzieciuchowicz L, Grochowicz L. Endovascular treatment of carotid stenosis associated with incidental intracranial aneurysm. Ann Vasc Surg 2009;23:688.e1-5.
Iwata T, Mori T, Tajiri H. Successful staged endovascular treatment of a symptomatic cervical carotid bifurcation stenosis coupled with a coincidental unruptured cerebral aneurysm in the carotid distal segment. AJNR Am J Neuroradiol 2008;29:1948-50.
Kajiwara H, Kodama T, Itoyama Y, Matsukado Y, Fukumura A. Surgical treatment of the symptomatic carotid stenosis associated with unruptured ipsilateral intracranial aneurysm. Case report. Neurol Med Chir (Tokyo) 1984;24:815-20.
Kann BR, Matsumoto T, Kerstein MD. Safety of carotid endarterectomy associated with small intracranial aneurysms. South Med J 1997;90:1213-6.
Ladowski JS, Webster MW, Yonas HO, Steed DL. Carotid endarterectomy in patients with asymptomatic intracranial aneurysm. Ann Surg 1984;200:70-3.
León JI, Aramendía LC, Marco FB, Suárez JC. Concomitant endovascular treatment of concomitant extracranial carotid stenosis and intracranial aneurysm. Our experience. Interv Neuroradiol 2009;15:53-9.
McConkey PP, Kien ND. Cerebral protection with thiopentone during combined carotid endarterectomy and clipping of intracranial aneurysm. Anaesth Intensive Care 2002;30:219-22.
Navaneethan SD, Kannan VS, Osowo A, Shrivastava R, Singh S. Concomitant intracranial aneurysm and carotid artery stenosis: A therapeutic dilemma. South Med J 2006;99:757-8.
Orecchia PM, Clagett GP, Youkey JR, Brigham RA, Fisher DF, Fry RF, et al
. Management of patients with symptomatic extracranial carotid artery disease and incidental intracranial berry aneurysm. J Vasc Surg 1985;2:158-64.
Pappadà G, Fiori L, Marina R, Vaiani S, Gaini SM. Management of symptomatic carotid stenoses with coincidental intracranial aneurysms. Acta Neurochir (Wien) 1996;138:1386-90.
Portnoy HD, Avellanosa A. Carotid aneurysm and contralateral carotid stenosis with successful surgical treatment of both lesions; case report. J Neurosurg 1970;32:476-82.
Riphagen JH, Bernsen HJ. Rupture of an intracerebral aneurysm after carotid endarterectomy: A case report. Acta Neurol Belg 2009;109:314-6.
Shoumaker RD, Avant WS, Cohen GH. Coincidental multiple asymptomatic intracranial aneurysms and symptomatic carotid stenosis. Stroke 1976;7:504-6.
Stern J, Whelan M, Brisman R, Correll JW. Management of extracranial carotid stenosis and intracranial aneurysms. J Neurosurg 1979;51:147-50.
Suh BY, Yun WS, Kwun WH. Carotid artery revascularization in patients with concomitant carotid artery stenosis and asymptomatic unruptured intracranial artery aneurysm. Ann Vasc Surg 2011;25:651-5.
Thyrion FZ, Azzaretti A, Di Maria F, Saluzzo CM, Quaretti P, Rodolico G, et al
. Double stenting procedure and coil embolization in a patient with carotid stenosis and incidental ipsilateral intracranial aneurysm. A case report and dosimetric evaluation. Neuroradiol J 2007;20:318-26.
Wasnick JD, Conlay LA. Induced hypertension for cerebral aneurysm surgery in a patient with carotid occlusive disease. Anesth Analg 1990;70:331-3.
Carvi YN, Haas E, Hollerhage HG. Unruptured large intracranial aneurysms in patients with transient cerebral ischemic episodes. Neurosurg Rev 2003;26:215-20.
Cho YD, Jung KH, Roh JK, Kang HS, Han MH, Lim JW. Characteristics of intracranial aneurysms associated with extracranial carotid artery disease in South Korea. Clin Neurol Neurosurg 2013;115:1677-81.
Héman LM, Jongen LM, van der Worp HB, Rinkel GJ, Hendrikse J. Incidental intracranial aneurysms in patients with internal carotid artery stenosis: A CT angiography study and a metaanalysis. Stroke 2009;40:1341-6.
Kappelle LJ, Eliasziw M, Fox AJ, Barnett HJ. Small, unruptured intracranial aneurysms and management of symptomatic carotid artery stenosis. North American Symptomatic Carotid Endarterectomy Trial Group. Neurology 2000;55:307-9.
Liang Y, Wang J, Li B. Symptomatic carotid artery stenosis complicated with unruptured intracranial aneurysms. Chin J Geriatr Heart Brain Vessel Dis 2015;17:21-4.
Yang X, Lu J, Wang J, Wang L, Qi P, Hu S, et al
. A clinical study and meta-analysis of carotid stenosis with coexistent intracranial aneurysms. J Clin Neurosci 2018;52:41-9.
Yang W, Rong X, Braileanu M, Jiang B, Garzon-Muvdi T, Caplan JM, et al
. Is carotid revascularization safe for patients with concomitant carotid stenosis and intracranial aneurysms? World Neurosurg 2016;93:11-8.
Yeung BK, Danielpour M, Matsumura JS, Ailawadi G, Batjer H, Yao JS. Incidental asymptomatic cerebral aneurysms in patients with extracranial cerebrovascular disease: Is this a case against carotid endarterectomy without arteriography? Cardiovasc Surg 2000;8:513-8.
Turjman AS, Turjman F, Edelman ER. Role of fluid dynamics and inflammation in intracranial aneurysm formation. Circulation 2014;129:373-82.
Frösen J, Tulamo R, Paetau A, Laaksamo E, Korja M, Laakso A, et al
. Saccular intracranial aneurysm: Pathology and mechanisms. Acta Neuropathol 2012;123:773-86.
Ronkainen A, Hernesniemi J, Ryynanen M. Familial subarachnoid hemorrhage in east Finland, 1977-1990. Neurosurg 1993;33:787-96.
Schievink WI, Schaid DJ, Michels VV, Piepgras DG. Familial aneurysmal subarachnoid hemorrhage: A community-based study. J Neurosurg 1995;83:426-9.
Penn DL, Komotar RJ, Connolly ES. Hemodynamic mechanisms underlying cerebral aneurysm pathogenesis. J Clin Neurosci 2011;18:1435-8.
Chien S. Effects of disturbed flow on endothelial cells. Ann Biomed Eng 2008;36:554-62.
Nagel T, Resnick N, Dewey CF Jr., Gimbrone MA Jr. Vascular endothelial cells respond to spatial gradients in fluid shear stress by enhanced activation of transcription factors. Arterioscler Thromb Vasc Biol 1999;19:1825-34.
Pepper MS, Ferrara N, Orci L, Montesano R. Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro
. Biochem Biophys Res Commun 1992;189:824-31.
Tardy Y, Resnick N, Nagel T, Gimbrone MA Jr., Dewey CF Jr. Shear stress gradients remodel endothelial monolayersin vitro
via a cell proliferation-migration-loss cycle. Arterioscler Thromb Vasc Biol 1997;17:3102-6.
Chachisvilis M, Zhang YL, Frangos JA. G protein-coupled receptors sense fluid shear stress in endothelial cells. Proc Natl Acad Sci (USA) 2006;103:15463-8.
Olesen SP, Clapham DE, Davies PF. Haemodynamic shear stress activates a K+current in vascular endothelial cells. Nature 1988;331:168-70.
Tzima E, del Pozo MA, Shattil SJ, Chien S, Schwartz MA. Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. Embo J 2011;20:4639-47.
Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, et al
. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 2005;437:426-31.
Burridge K, Chrzanowska-Wodnicka M. Focal adhesions, contractility, and signaling. Annu Rev Cell Dev Biol 1996;12:463-518.
Takeichi M. The cadherins: Cell-cell adhesion molecules controlling animal morphogenesis. Development 1988;102:639-55.
Wang N, Tytell JD, Ingber DE. Mechanotransduction at a distance: Mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 2009;10:75-82.
Aoki T, Kataoka H, Ishibashi R, Nozaki K, Morishita R, Hashimoto N. Reduced collagen biosynthesis is the hallmark of cerebral aneurysm: Contribution of interleukin-1beta and nuclear factor-kappaB. Arterioscler Thromb Vasc Biol 2009;29:1080-6.
Chiu JJ, Chen LJ, Chang SF, Lee PL, Lee CI, Tsai MC, et al
. Shear stress inhibits smooth muscle cell-induced inflammatory gene expression in endothelial cells: Role of NF-kappaB. Arterioscler Thromb Vasc Biol 2005;25:963-9.
Aoki T, Kataoka H, Morimoto M, Nozaki K, Hashimoto N. Macrophage-derived matrix metalloproteinase-2 and -9 promote the progression of cerebral aneurysms in rats. Stroke 2007;38:162-9.
Aoki T, Kataoka H, Moriwaki T, Nozaki K, Hashimoto N. Role of TIMP-1 and TIMP-2 in the progression of cerebral aneurysms. Stroke 2007;38:2337-45.
Kolega J, Gao L, Mandelbaum M, Mocco J, Siddiqui AH, Natarajan SK, et al
. Cellular and molecular responses of the basilar terminus to hemodynamics during intracranial aneurysm initiation in a rabbit model. J Vasc Res 2011; 48:429-442.
Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 2004;84:767-801.
Nakajima N, Nagahiro S, Sano T, Satomi J, Satoh K. Phenotypic modulation of smooth muscle cells in human cerebral aneurysmal walls. Acta Neuropathol 2000;100:475-80.
Hazama F, Hashimoto N. An animal model of cerebral aneurysms. Neuropathol Appl Neurobiol 1987;13:77-90.
Meng H, Metaxa E, Gao L, Liaw N, Natarajan SK, Swartz DD, et al
. Progressive aneurysm development following hemodynamic insult. J Neurosurg 2011;114:1095-103.
Frösen J, Piippo A, Paetau A, Kangasniemi M, Niemelä M, Hernesniemi J, et al
. Remodeling of saccular cerebral artery aneurysm wall is associated with rupture: Histological analysis of 24 unruptured and 42 ruptured cases. Stroke 2004;35:2287-93.
Kataoka K, Taneda M, Asai T, Kinoshita A, Ito M, Kuroda R. Structural fragility and inflammatory response of ruptured cerebral aneurysms. A comparative study between ruptured and unruptured cerebral aneurysms. Stroke 1999;30:1396-401.
Doberenz C, Paulus W, Reimers CD, Eicke BM. Volume flow rate evaluation in patients with obstructive arteriosclerotic disease. Cerebrovasc Dis 2004;18:312-7.
Alastruey J, Parker KH, Peiro J, Byrd SM, Sherwin SJ. Modelling the circle of Willis to assess the effects of anatomical variations and occlusions on cerebral flows. J Biomech 2004;40:1794-805.
Shakur SF, Alaraj A, Mendoza-Elias N, Osama M, Charbel FT. Hemodynamic characteristics associated with cerebral aneurysm formation in patients with carotid occlusion. J Neurosurg 2018;130:917-22.
Jou LD, Shaltoni HM, Morsi H, Mawad ME. Hemodynamic relationship between intracranial aneurysm and carotid stenosis: Review of clinical cases and numerical analyses. Neurol Res 2010;32:1083-9.
Zarrinkoob L, Wåhlin A, Ambarki K, Birgander R, Eklund A, Malm J. Blood flow lateralization and collateral compensatory mechanisms in patients with carotid artery stenosis. Stroke 2019;50:1081-8.
Datar S, Lanzino G, Rabinstein AA. An unusually benign course of extensive posterior circulation occlusion. J Stroke Cerebrovasc Dis 2015;24:e165-8.
Wijdicks EF, Scott JP. Outcome in patients with acute basilar artery occlusion requiring mechanical ventilation. Stroke 1996;27:1301-3.
Furtado SV, Medress ZA, Teo M, Steinberg GK. Pathogenesis of aneurysms on major vessels in moyamoya disease and management outcome. J Clin Neurosci 2019;61:219-24.
Li H, Pan R, Wang H, Rong X, Yin Z, Milgrom DP, et al
. Clipping versus coiling for ruptured intracranial aneurysms: A systematic review and meta-analysis. Stroke 2013;44:29-37.
Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, et al
. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: A randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet 2005;366:809-17.
Molyneux AJ, Birks J, Clarke A, Sneade M, Kerr RS. The durability of endovascular coiling versus neurosurgical clipping of ruptured cerebral aneurysms: 18 year follow-up of the UK cohort of the International Subarachnoid Aneurysm Trial (ISAT). Lancet 2015;385:691-7.
Cognard C, Weill A, Spelle L, Piotin M, Castaings L, Rey A, et al
. Long-term angiographic follow-up of 169 intracranial berry aneurysms occluded with detachable coils. Radiology 1999;212:348-56.
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3]