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Imaging detection of cerebral artery fenestrations and their clinical correlation with cerebrovascular diseases
Clinical Imaging 62 (2020) 57–62
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Clinical Imaging journal homepage: www.elsevier.com/locate/clinimag
Neuroradiology
Imaging detection of cerebral artery fenestrations and their clinical correlation with cerebrovascular diseases
T
Xuan Wu1, Xinyuan Chen1, Jiting Zhu, Qunlin Chen, Zhiwen Li, Aiyu Lin
⁎
Department of Neurology, the First Affiliated Hospital of Fujian Medical University, Fuzhou, Fujian, China
ARTICLE INFO
ABSTRACT
Keywords: Cerebral artery Fenestration Vascular malformations Aneurysm Cerebral infarction
Objectives: Cerebral artery fenestrations detected incidentally during computed tomographic angiography (CTA) or magnetic resonance angiography (MRA) are reported to be associated with aneurysmal dilatation, which may cause cerebrovascular diseases, arteriovenous malformations, or, rarely, ischemic symptoms. Methods: We retrospectively analyzed CTA and MRA of patients with cerebral artery fenestration examined between January 2014 and December 2017. The location, shape, and other associated vascular diseases were described. Results: Two hundred eleven cerebral artery fenestrations were found in 208 patients for a detection rate of 1.13% (208/18,360). Basilar artery fenestrations were most common, accounting for 50.2% (106/211). The fenestration was < 5 mm in 115 patients (54.5%), 5–10 mm in 63 (29.9%), and ≥10 mm in 33 (15.6%). Fortyone patients had other vascular malformations, including 29 aneurysms. Except for one aneurysm, which was at the site of the fenestration, all other aneurysms were separate from the fenestrations. 26 patients had cerebral infarctions; among them, 11 had cerebral infarctions in the blood supply area of the arterial fenestration. Conclusions: Cerebral artery fenestration is an uncommon finding at cerebral imaging, but mostly affects the basilar artery. Cerebral artery fenestrations could be associated with cerebrovascular diseases and malformations, but the present study could not evaluate the cause-to-effect relationship.
1. Introduction Fenestration of a cerebral artery refers to a division of the lumen of an artery, resulting in two distinct endothelium-lined channels [1]. The first report of a fenestration in the cerebrovascular system was found in the vertebral artery during an autopsy in 1866, and most have been discovered only through cadaveric dissection thereafter [2]. Nowadays, cerebral artery fenestrations are reported with an incidence of 0.03% to 1% during angiographic studies [3]. The true incidence of fenestration in the cerebral artery is difficult to define, as it is greatly dependent on the type of fenestration and different modalities of detection. The detection of cerebral fenestration is much higher during autopsy compared to angiography, which is because most fenestrations are too thin to be visible in angiograms [4]. Based on their morphology and size, fenestrations are differentiated into four variants: slit-like shape, convex-lens-like shape, duplicated artery, and other irregular shape fenestrations. Slit-like fenestrations are much smaller and with inconspicuous openings, whereas the convex-lens-like shape appears long and with a wide opening [5]. The duplication variant refers to the total
duplication of an artery [6]. The irregularly shaped fenestrations are other shapes that cannot be included in the first three categories. Fenestrations of the cerebral arteries can appear in all its branches, but they are most commonly reported in the anterior communicating artery (ACoA) [7], the vertebrobasilar system [8,9], the anterior cerebral artery (ACA) [10], the middle cerebral artery (MCA) [11–14], and the posterior cerebral artery [15]. Among all cerebral artery fenestrations, basilar artery (BA) fenestrations are the most frequently observed. Some studies suggested a relationship between cerebral artery fenestration and congenital cerebrovascular malformations such as intracerebral aneurysm [1], [16–18] moyamoya disease [19], and intracranial arteriovenous malformation [20]. Many cases reported previously indicate that cerebral artery fenestration may be related to cerebral infarction [12,16,21,22] and transient ischemic attack [23]. Fenestrations of the middle cerebral artery are more frequently reported with cerebral aneurysm at its proximal end and are rarely associated with cerebral arteriovenous malformations or ischemic symptoms [14]. Nevertheless, cerebral artery fenestrations are still poorly understood. Therefore, we analyzed the computed tomographic angiography
Corresponding author at: Department of Neurology, the First Affiliated Hospital of Fujian Medical University, Fuzhou, Fujian 350005, China. E-mail address: [email protected] (A. Lin). 1 These authors contributed equally to this work. ⁎
https://doi.org/10.1016/j.clinimag.2020.01.012 Received 22 April 2019; Received in revised form 10 January 2020; Accepted 13 January 2020 0899-7071/ © 2020 Elsevier Inc. All rights reserved.
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Fig. 1. Angiogram showing four different types of cerebral artery fenestrations based on size and morphology. (A) Slit-like fenestration in the basilar artery with an aneurysm located at the ACOA. (B) A small convex-lens-like fenestration was seen in the right ACA. (C) A completely duplicated right ACA. (D) Bilateral irregular fenestration in the VA.
(CTA) and magnetic resonance angiography (MRA) data of patients diagnosed with cerebral artery fenestration between January 2014 and December 2017. The purpose of this study was to examine the location and characteristic configuration of cerebral artery fenestrations and to delineate their association with cerebrovascular diseases and malformations.
1.3 mm. For Siemens 3.0-T Magnetom Verio System, RT was set at 22 ms and ET at 3.6 ms. The imaging data were carefully analyzed by one experienced radiologist along with an attending neurologist. When discrepancies occurred as to whether a fenestration was present or what the morphology was, these were resolved by discussion and also by acquiring external opinion with other expert clinicians. The demographic information of the patients were collected and analyzed and included patients' sex, age, clinical symptoms, diagnosis, the location and morphology of fenestrations, and the other associated vascular diseases. The clinical features of different cerebrovascular diseases and malformations related to the imaging finding of the cerebral arterial fenestrations in patients with cerebral infarctions were analyzed and classified according to the National Institutes of Health Stroke Scale (NIHSS) and Trial of Org 10172 in Acute Stroke Treatment (TOAST) criteria. TOAST is a well-established system for the etiological classification of ischemic stroke, using different categories of stroke diagnoses, e.g., large-artery atherosclerosis, small-artery occlusion, cardioembolism stroke, stroke of other determined cause, and stroke of undetermined cause [24]. BA fenestrations were classified into four categories according to their relation with the location of the origin of the anterior inferior cerebellar artery (AICA): type I, the fenestration is located proximal to the AICA or absence of AICA; type II, bilateral AICAs symmetrically originating from the fenestrated trunks; type III, a unilateral AICA
2. Methods 2.1. Patients This study was approved by the ethics committee. Between January 2014 and December 2017, a total of 18,360 cerebral CTA or MRA covering the intracranial vessels were performed among both inpatients and outpatients in our hospital. The patients whose image findings were compatible with cerebral artery fenestrations were included. The imaging report system was searched for the word “fenestration”. If patients had more than one image, only the most recent images were analyzed. CT angiography was performed using a 320-row dynamic volume scanner (Toshiba Aquilion One), with 1.0-mm section thickness, 100 kV, and 250 mA. MR angiography was performed using a 1.5-T TOSHIBA EXCELART vantage or a Siemens 3.0-T Magnetom Verio System. For TOSHIBA EXCELART vantage, repetition time (RT) was 30 ms, and echo time (ET) was 6.8 ms. Angiogram parameters were set with a field of view at 19 × 19 cm and original slice thickness at 58
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vascular risk factors, all other cases had at least one vascular risk factor such as hypertension, diabetes mellitus, and dyslipidemia. The median follow-up was 13.5 months. Except for one infarction patient who was lost to follow-up, no acute stroke or transient ischemic attack occurred in the 11 patients who had 7 to 30 months (median, 18.1 months) antiplatelet and statin therapy after they were diagnosed as cerebral infarction.
originating from one side of the fenestrated trunk; and type IV, the fenestration is located distal to the AICA [4]. The clinical characteristics of patients with the location of cerebral infarctions in the blood supply area of the arterial fenestration were subjected to thorough analysis based on their risk factors. A routine follow-up was performed on patients reported with infarctions for a period of 30 months through outpatient follow-up after hospitalization or through direct telephonic contact with the patient's relatives.
4. Discussion
3. Results
Cerebral artery fenestrations detected incidentally during angiography are reported to be associated with aneurysmal dilatation, which may cause cerebrovascular diseases, arteriovenous malformations, or, rarely, ischemic symptoms. Therefore, this study aimed to analyze the characteristics of cerebral artery fenestrations and to correlate the clinical features of patients with cerebrovascular diseases and malformations. The results suggest that cerebral artery fenestrations are associated with cerebrovascular diseases and malformations. BA fenestrations were found to be the most common form. In this small retrospective study, among the 26 patients with cerebral infarction, 11 had cerebral infarctions in the blood supply area of the arterial fenestration, but they were without any cerebral infarction or transient ischemic attack during follow-up. The detection rate of cerebral vascular fenestration in the present study was 1.13%. This is about half the frequency reported by Cooke et al. [25] and Gao et al. [5]. Differences between studies could be due to the study populations and the methods used to identify the patients. In addition, there is the possibility that DSA is more sensitive to fenestrations than MRA and CTA, but this will have to be examined more closely. Among the fenestrations found in the present study, BA fenestrations were the most common, accounting for 50.2% (106/211) of the fenestrations. The frequency of BA fenestration in our study was 0.58% (106/18,360), which was similar to the frequency reported by Sanders et al. (0.31%) [1], but lower than the frequencies reported by Uchino et al. (1.7%) [6] and Gao et al. (2.33%) [5]. We found a case with bilateral fenestration in the VA, and another with three fenestrations in the left VA. Fenestrations of intracranial arteries and their association with cerebral aneurysms have been described in previous studies [1,16,17, [26],27]. In this study, 41 patients were reported with other vascular malformations, including 29 aneurysms (13.7%). This rate is low compared with the study by Cooke et al. [25], in which 60.5% of the patients with fenestrations had at least one aneurysm, and compared with van Rooij et al. [27], with 31%. Of note, the overall frequency of aneurysm observed in the present and previous studies (14%–61%) is much higher than in the original population (1–2%) [28], hinting toward an association between fenestrations and aneurysms. Among them, except one aneurysm at the site of the fenestration, all other 28 aneurysms were separate from the fenestrations. This does not mean that those 28 aneurysms are completely unrelated to the fenestrations
Two hundred eleven (211) cerebral artery fenestrations were found in 208 patients (frequency of 1.13%, 208/18,360). One hundred twelve (112) were male, and 96 were female; the male:female ratio was 1:0.86. Age at imaging ranged from 5 to 89 years (median, 52.5 years). Most of these patients were suspected of having intracranial tumors or cerebrovascular diseases. Of the 211 fenestrations, the most common type of fenestration (n = 106) was BA fenestration. The incidence of BA fenestration was 0.58% (106/18,360). The BA fenestrations were classified as: type I, 44 cases; type II, 26 cases; type III, 31 cases (of which 8 cases had only one anterior inferior cerebellar artery and originated from the fenestrations); and type IV, 5 cases. Of these fenestrations, 131 were of a slitlike configuration (Fig. 1A), while 72 had a convex-lens-like in shape (Fig. 1B), four were duplications of arteries (Fig. 1C), and four showed irregular morphology (Fig. 1D). The location and shape of the fenestrated vessels are shown in Table 1. Forty-one patients had other vascular malformations: 29 with aneurysms, three with moyamoya disease (Fig. 2A), four with venous malformations, four with arteriovenous fistulas, and six with cavernous hemangiomas (Table 2). The frequency of aneurysms was 13.9% (29/ 208). There was only one aneurysm at the site of a fenestration in the vertebral artery (Fig. 2B). All other aneurysms were separate from the fenestrations. Eleven patients presented with subarachnoid hemorrhage (SAH), seven patients had aneurysms, two patients had moyamoya disease, and two had no other malformation except the fenestration. Digital subtraction angiography (DSA) was performed in all cases of aneurysms for confirmation. Twenty-six patients had cerebral infarctions, of which 11 patients had cerebral infarctions in the blood supply area of the arterial fenestration because the arterial fenestration was precisely located in the blood supply area subjected to infarct. All of these 11 patients underwent CTA or MRA when they had cerebral infarctions in order to confirm that the cause of infarction could be related, at least anatomically, to the fenestrations. Patients with BA fenestrations had a higher incidence of cerebral infarctions in the blood supply area of the arterial fenestration than those with other arterial fenestrations (10 in 106 vs. 1 in 102, P = 0.01). The clinical features of cerebral infarctions in the blood supply area of the arterial fenestration patients are described in Table 3. Except for one patient (No.6) without any traditional Table 1 Shape and differential location of cerebral artery fenestrations among the patients Location
Shape
Length Number (%)
Slit-like Convex-lens-like Duplication Irregular < 5 mm 5–10 mm ≥10 mm
Number (%)
ACA
MCA
PCA
ACOA
VA
BA
ICA
24 17 2 0 23 17 3 43 (20.4)
5 0 0 0 4 1 0 5 (2.4)
2 1 0 0 2 1 0 3 (1.4)
6 1 0 0 7 0 0 7 (3.3)
10 30 2 4 8 14 24 46 (21.8)
83 23 0 0 71 29 6 106 (50.2)
1 0 0 0 0 1 0 1 (0.5)
131 (62.1) 72 (34.1) 4 (1.9) 4 (1.9) 115 (54.5) 63 (29.9) 33 (15.6) 211
ACA: anterior cerebral artery, MCA: middle cerebral artery, PCA: posterior cerebral artery, ACOA: anterior communicating artery, VA: vertebral artery, BA: basilar artery, ICA: internal carotid artery. 59
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Fig. 2. Angiogram showing different locations of cerebral artery fenestrations and their clinical correlation with cerebrovascular diseases and malformations. (A) CTA revealed a fenestration in the right VA and arterial collateral vessels at the base of the brain, indicating the clinical criteria of moyamoya disease. (B) A fenestration was seen with aneurysm superimposed over the left VA. (C) Three fenestrations could be seen in the left VA.
because the aneurysms could have been secondary to blood flow diversion. Unfortunately, this was a retrospective study of already diagnosed cases, and more refined measurements of hemodynamics were not available. In the study by Cooke et al. [25], there was no difference in the rates of arachnoid hemorrhage between the patients with related vs. unrelated aneurysm. There were seven patients who presented with SAH among the patients with fenestrations and aneurysms. Moreover, we also found two patients with SAH in whom the fenestration was the only malformation. Bożek et al. [29] and Gao et al. [5] reported two patients in whom the fenestration was the only malformation that coexisted with SAH. Nevertheless, because of the limited number of described cases in this study and the literature, it is difficult to explain whether the fenestration was the cause for SAH. Compared with the study by Cooke et al. [25], the present study presented the morphology of the fenestrations in addition to their location. Such morphological classification has been suggested by Uchino et al. [6], who divided the BA fenestrations into three types according to vascular morphology: slit-like shape, convex-lens-like shape, and duplication. We referred to their method for classification and found that there was a fourth type with irregular morphology, which was only found in the VA. Nevertheless, the clinical significance of this fourth type of fenestration in the VA and of the other types of fenestration require further study. In the BA, the type of fenestration (slit-like vs.
convex-lens-like) seems to be related to the origin of the anterior inferior cerebral artery (AICA), namely that the AICA has a predisposition to originate from a convex-lens-like fenestration [5]. Since the endothelium-lined septum increases the risk of thrombus formation in the fenestration [30], pontine and cerebellar infarction may develop if the AICA arises from a fenestrated segment of the BA [9]. Twenty-six (12.3%) patients had cerebral infarctions, and 11 of them (42.3%) had cerebral infarctions in the blood supply area of the arterial fenestration. This frequency of ischemic stroke is higher than in the general population [31], suggesting a possible involvement of fenestrations in ischemic stroke, but the present study was not designed to determine causality between fenestration and stroke. Importantly, only one stroke patient in the present had fenestration without any other risk factor for stroke, while all other patients had at least one additional risk factor. Therefore, additional studies are necessary to determine the exact relationship between stroke and fenestrations. Some cases of cerebral artery fenestration in patients with cerebral ischemia have been previously reported [12,16,21–23,32]. Jeong et al. [12] have reported five patients with MCA fenestration who had arteryrelevant cerebral infarction or ischemia. They determined that the atherothrombotic process could be initiated because of the local hemodynamics in an arterial branching site, progressing toward the proximal edge of the fenestration. The lateral wall of the smaller limb of the fenestration could be more easily affected. One of our patients 60
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Fig. 3. A 47-year-old man with left cerebellum and brain stem infarction. (A) Diffusion-weighted MRI revealed an area of reduced diffusivity in the left cerebellum and brain stem. (B) Magnetic resonance angiography revealed a small fenestration in the basilar artery. (C, D, and E) High-resolution MRI of the brain showing a small fenestration in the basilar artery, and the coronal plane images showing that the basilar artery was divided into two lumens with unstable plaque seen in the arteries. (F) Axial images showing the enhancing plaque.
Our study was limited because of its retrospective nature and because of the small sample size. In addition, because of the imaging protocols, other vascular malformations such as venous malformation, arteriovenous fistula, and intracranial hemangioma could not be displayed in the same images as the arterial fenestrations. In addition, since it is a retrospective study, and since the radiologists were not specifically looking for fenestrations when they read the images, it is highly possible that many patients were not included in this study. Hence, a multicenter study with a large number of patients could provide more definite data about the cerebrovascular diseases, location, morphology, and configuration of cerebral artery fenestrations.
Table 2 Frequency of other vascular malformations among 208 patients with fenestration Vascular malformations
Number
Frequency among patients with fenestration (n = 208)
Aneurysm Moyamoya disease Venous malformations Arteriovenous fistulas Cavernous hemangiomas Aneurysm+arteriovenous fistulas Aneurysm+venous malformations Aneurysm+cavernous hemangiomas+venous malformations Venous malformations+cavernous hemangiomas Total
26 3 1 3 4 1 1 1
12.5% 1.4% 0.5% 1.4% 1.9% 0.5% 0.5% 0.5%
1
0.5%
41
19.7%
5. Conclusions In conclusion, cerebral artery fenestrations are associated with cerebrovascular diseases and malformations. Basilar artery fenestrations were found to be the most common form. Fenestrations can be differentiated into four variants: slit-like shape, convex-lens-like shape, duplicated artery, and other irregular shape fenestrations, slit, and convex-lens-like being by far the most common types in the present study. In this small retrospective study, among the 26 patients with cerebral infarction, 11 had cerebral infarctions in the blood supply area of the arterial fenestration, but they were without any cerebral infarction or transient ischemic attack during follow-up. Importantly, the present study revealed that a cerebral infarction occurred in the blood supply area of the arterial fenestration of 42% of the patients with
(No.8) was subjected to high-resolution MRI of the brain to study the detailed structure of the fenestration, which revealed that the left smaller vessel had more obvious arteriosclerotic signs. All of the patients reported by Jeong et al. [12] had more than one vascular risk factor, including hypertension, diabetes mellitus, dyslipidemia, and smoking. On the other hand, one of our cases (No.6) did not show any traditional vascular risk factors or etiology of cryptogenic stroke. 61
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Table 3 Demographic and clinical characteristics of patients with the location of cerebral infarctions in the blood supply area of the arterial fenestration. Case
Age, y
Sex
Site of fenestration
Infarction location
Risk factors
NIHSS
TOAST
1 2 3 4 5 6 7 8 9 10 11
77 55 83 61 53 36 72 47 69 65 59
F M M M F M F M F M F
BA BA Right, ACA BA BA BA BA BA (Fig. 3) BA BA BA
Pons Medulla oblongata Right parietal lobe Cerebellum, medulla oblongata Midbrain Cerebellum Pons Cerebellum, pons Cerebellum Right parietal lobe, occipital lobe, basal ganglia Cerebellum
HTN, dyslipidemia Dyslipidemia HTN, dyslipidemia HTN, DM, dyslipidemia HTN, DM NA HTN, DM, dyslipidemia HTN, dyslipidemia HTN, IGT, dyslipidemia HTN, DM, dyslipidemia HTN
8 2 3 6 5 1 1 12 1 3 2
LAA LAA LAA LAA LAA SUD LAA LAA LAA LAA LAA
HTN; hypertension, DM; diabetes mellitus, IGT; impaired glucose toleration, NA; Not applicable, NIHSS; National Institutes of Health Stroke scale, LAA; large-artery atherosclerosis, TOAST; Trial of Org 10,172 Acute Stroke Treatment, SUD; Stroke of undetermined etiology.
stroke, but the present study could not evaluate the cause-to-effect relationship. A large multicenter study could be ideal to derive more conclusive evidence of diseases associated with cerebral artery fenestration.
cerebral ischemia. J Neurol Sci 2008;275:181–4. [13] Uchino A, Kato A, Takase Y, Kudo S. Middle cerebral artery variations detected by magnetic resonance angiography. Eur Radiol 2000;10:560–3. [14] Uchino A, Takase Y, Nomiyama K, Egashira R, Kudo S. Fenestration of the middle cerebral artery detected by MR angiography. Magn Reson Med 2006;5:51. [15] Hacein-Bey L, Muszynski C, Varelas P. Saccular aneurysm associated with posterior cerebral artery fenestration manifesting as a subarachnoid hemorrhage in a child. AJNR Am J Neuroradiol 2002;23:1291–4. [16] Chen YY, Chang FC, Hu HH, Chao AC. Fenestration of the supraclinoid internal carotid artery associated with aneurysm and ischemic stroke. Surg Neurol 2007;68(Suppl. 1):S60–3. (discussion S3). [17] Kanematsu M, Satoh K, Nakajima N, Hamazaki F, Nagahiro S. Ruptured aneurysm arising from a basilar artery fenestration and associated with a persistent primitive hypoglossal artery. Case report and review of the literature. J Neurosurg 2004;101:532–5. [18] Patel MA, Caplan JM, Yang W, Colby GP, Coon AL, Tamargo RJ, et al. Arterial fenestrations and their association with cerebral aneurysms. J Clin Neurosci 2014;21:2184–8. [19] Voros E, Kiss M, Hanko J, Nagy E. Moyamoya with arterial anomalies: relevance to pathogenesis. Neuroradiology 1997;39:852–6. [20] Orru E, Wyse E, Pearl MS. Fenestration of the supraclinoid internal carotid artery in a patient with a concomitant intracranial arteriovenous malformation. Bmj Case Rep 2015;2015:289. [21] Gold JJ, Crawford JR. An unusual cause of pediatric stroke secondary to congenital basilar artery fenestration. Case Rep Crit Care 2013;2013:627972. [22] Bernard TJ, Mull BR, Handler MH, Harned RK, Filley CM, Kumpe DA, et al. An 18year-old man with fenestrated vertebral arteries, recurrent stroke and successful angiographic coiling. J Neurol Sci 2007;260:279–82. [23] Pleş H, Kimball D, Miclăuş GD, Iacob N, Kimball H, Matusz P, et al. Fenestration of the middle cerebral artery in a patient who presented with transient ischemic attack. Romanian journal of morphology and embryology = Revue roumaine de morphologie et embryologie 2015;56:861–5. [24] Adams Jr. HP, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of org 10172 in acute stroke treatment. Stroke 1993;24:35–41. [25] Cooke DL, Stout CE, Kim WT, Kansagra AP, Yu JP, Gu A, et al. Cerebral arterial fenestrations. Interv Neuroradiol 2014;20:261–74. [26] Tanaka S, Tokimura H, Makiuchi T, Nagayama T, Takasaki K, Tomosugi T, et al. Clinical presentation and treatment of aneurysms associated with basilar artery fenestration. J Clin Neurosci 2012;19:394–401. [27] van Rooij SB, Bechan RS, Peluso JP, Sluzewski M, van Rooij WJ. Fenestrations of intracranial arteries. AJNR Am J Neuroradiol 2015;36:1167–70. [28] Brown Jr. RD, Broderick JP. Unruptured intracranial aneurysms: epidemiology, natural history, management options, and familial screening. Lancet Neurol 2014;13:393–404. [29] Paweł B, Joanna P-K, Ewa K, Anna Z-Z. Detection of cerebral artery fenestrations by computed tomography angiography. Neurol Neurochir Pol 2012;46:239–44. [30] Berry 3rd AD, Kepes JJ, Wetzel MD. Segmental duplication of the basilar artery with thrombosis. Stroke 1988;19:256–60. [31] Rosamond W, Flegal K, Furie K, Go A, Greenlund K, Haase N, et al. Heart disease and stroke statistics–2008 update: a report from the American Heart Association statistics committee and stroke statistics subcommittee. Circulation 2008;117:e25–146. [32] Kloska SP, Schlegel PM, Strater R, Niederstadt TU. Causality of pediatric brainstem infarction and basilar artery fenestration? Pediatr Neurol 2006;35:436–8.
Acknowledgments None. Funding This work was supported by Startup Fund for scientific research, Fujian Medical University (grant number: 2017XQ1090) and by Fujian Youth Education Research Project (grant number: JT180191). Declaration of competing interest The authors report no declarations of interest. References [1] Sanders WP, Sorek PA, Mehta BA. Fenestration of intracranial arteries with special attention to associated aneurysms and other anomalies. AJNR Am J Neuroradiol 1993;14:675–80. [2] Uchino A, Saito N, Takahashi M, Okano N, Tanisaka M. Variations of the posterior cerebral artery diagnosed by MR angiography at 3 tesla. Neuroradiology 2016;58:141–6. [3] Sim KB, Lee CS, Park JC, Huh JS. Cerebral aneurysm in the long fenestration at the middle portion of m1 segment. J Korean Neurosurg Soc 2010;48:434–7. [4] Tanaka M, Kikuchi Y, Ouchi T. Neuroradiological analysis of 23 cases of basilar artery fenestration based on 2280 cases of MR angiographies. Interv Neuroradiol 2006;12:39–44. [5] Gao LY, Guo X, Zhou JJ, Zhang Q, Fu J, Chen WJ, et al. Basilar artery fenestration detected with CT angiography. Eur Radiol 2013;23:2861–7. [6] Uchino A, Kato A, Takase Y, Kudo S. Basilar artery fenestrations detected by MR angiography. Radiat Med 2001;19:71. [7] Gabriel Z, Eisha C, Liu CY, Giannotta SL. Fenestrated aneurysm clips in the surgical management of anterior communicating artery aneurysms: operative techniques and strategy. Clinical article Neurosurgical Focus 2009;26:E7. [8] Tasker AD, Byrne JV. Basilar artery fenestration in association with aneurysms of the posterior cerebral circulation. Neuroradiology 1997;39:185–9. [9] Uchino A, Okada Y, Kozawa E, Nishi N, Mizukoshi W, Inoue K, et al. Fenestrations of the intracranial vertebrobasilar system diagnosed by MR angiography. Neuroradiology 2012;54:445–50. [10] Wong GKC, Wang K, Yu SCH, Poon WS. A rare anatomical variant: median anterior cerebral artery fenestration associated with an azygous infra-optic anterior cerebral artery. J Clin Neurosci 2010;17:1434–6. [11] Gailloud P, Albayram S, Fasel JH, Beauchamp NJ, Murphy KJ. Angiographic and embryologic considerations in five cases of middle cerebral artery fenestration. AJNR Am J Neuroradiol 2002;23:585–7. [12] Jeong SK, Kwak HS, Cho YI. Middle cerebral artery fenestration in patients with
62
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Clinical Imaging journal homepage: www.elsevier.com/locate/clinimag
Neuroradiology
Imaging detection of cerebral artery fenestrations and their clinical correlation with cerebrovascular diseases
T
Xuan Wu1, Xinyuan Chen1, Jiting Zhu, Qunlin Chen, Zhiwen Li, Aiyu Lin
⁎
Department of Neurology, the First Affiliated Hospital of Fujian Medical University, Fuzhou, Fujian, China
ARTICLE INFO
ABSTRACT
Keywords: Cerebral artery Fenestration Vascular malformations Aneurysm Cerebral infarction
Objectives: Cerebral artery fenestrations detected incidentally during computed tomographic angiography (CTA) or magnetic resonance angiography (MRA) are reported to be associated with aneurysmal dilatation, which may cause cerebrovascular diseases, arteriovenous malformations, or, rarely, ischemic symptoms. Methods: We retrospectively analyzed CTA and MRA of patients with cerebral artery fenestration examined between January 2014 and December 2017. The location, shape, and other associated vascular diseases were described. Results: Two hundred eleven cerebral artery fenestrations were found in 208 patients for a detection rate of 1.13% (208/18,360). Basilar artery fenestrations were most common, accounting for 50.2% (106/211). The fenestration was < 5 mm in 115 patients (54.5%), 5–10 mm in 63 (29.9%), and ≥10 mm in 33 (15.6%). Fortyone patients had other vascular malformations, including 29 aneurysms. Except for one aneurysm, which was at the site of the fenestration, all other aneurysms were separate from the fenestrations. 26 patients had cerebral infarctions; among them, 11 had cerebral infarctions in the blood supply area of the arterial fenestration. Conclusions: Cerebral artery fenestration is an uncommon finding at cerebral imaging, but mostly affects the basilar artery. Cerebral artery fenestrations could be associated with cerebrovascular diseases and malformations, but the present study could not evaluate the cause-to-effect relationship.
1. Introduction Fenestration of a cerebral artery refers to a division of the lumen of an artery, resulting in two distinct endothelium-lined channels [1]. The first report of a fenestration in the cerebrovascular system was found in the vertebral artery during an autopsy in 1866, and most have been discovered only through cadaveric dissection thereafter [2]. Nowadays, cerebral artery fenestrations are reported with an incidence of 0.03% to 1% during angiographic studies [3]. The true incidence of fenestration in the cerebral artery is difficult to define, as it is greatly dependent on the type of fenestration and different modalities of detection. The detection of cerebral fenestration is much higher during autopsy compared to angiography, which is because most fenestrations are too thin to be visible in angiograms [4]. Based on their morphology and size, fenestrations are differentiated into four variants: slit-like shape, convex-lens-like shape, duplicated artery, and other irregular shape fenestrations. Slit-like fenestrations are much smaller and with inconspicuous openings, whereas the convex-lens-like shape appears long and with a wide opening [5]. The duplication variant refers to the total
duplication of an artery [6]. The irregularly shaped fenestrations are other shapes that cannot be included in the first three categories. Fenestrations of the cerebral arteries can appear in all its branches, but they are most commonly reported in the anterior communicating artery (ACoA) [7], the vertebrobasilar system [8,9], the anterior cerebral artery (ACA) [10], the middle cerebral artery (MCA) [11–14], and the posterior cerebral artery [15]. Among all cerebral artery fenestrations, basilar artery (BA) fenestrations are the most frequently observed. Some studies suggested a relationship between cerebral artery fenestration and congenital cerebrovascular malformations such as intracerebral aneurysm [1], [16–18] moyamoya disease [19], and intracranial arteriovenous malformation [20]. Many cases reported previously indicate that cerebral artery fenestration may be related to cerebral infarction [12,16,21,22] and transient ischemic attack [23]. Fenestrations of the middle cerebral artery are more frequently reported with cerebral aneurysm at its proximal end and are rarely associated with cerebral arteriovenous malformations or ischemic symptoms [14]. Nevertheless, cerebral artery fenestrations are still poorly understood. Therefore, we analyzed the computed tomographic angiography
Corresponding author at: Department of Neurology, the First Affiliated Hospital of Fujian Medical University, Fuzhou, Fujian 350005, China. E-mail address: [email protected] (A. Lin). 1 These authors contributed equally to this work. ⁎
https://doi.org/10.1016/j.clinimag.2020.01.012 Received 22 April 2019; Received in revised form 10 January 2020; Accepted 13 January 2020 0899-7071/ © 2020 Elsevier Inc. All rights reserved.
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Fig. 1. Angiogram showing four different types of cerebral artery fenestrations based on size and morphology. (A) Slit-like fenestration in the basilar artery with an aneurysm located at the ACOA. (B) A small convex-lens-like fenestration was seen in the right ACA. (C) A completely duplicated right ACA. (D) Bilateral irregular fenestration in the VA.
(CTA) and magnetic resonance angiography (MRA) data of patients diagnosed with cerebral artery fenestration between January 2014 and December 2017. The purpose of this study was to examine the location and characteristic configuration of cerebral artery fenestrations and to delineate their association with cerebrovascular diseases and malformations.
1.3 mm. For Siemens 3.0-T Magnetom Verio System, RT was set at 22 ms and ET at 3.6 ms. The imaging data were carefully analyzed by one experienced radiologist along with an attending neurologist. When discrepancies occurred as to whether a fenestration was present or what the morphology was, these were resolved by discussion and also by acquiring external opinion with other expert clinicians. The demographic information of the patients were collected and analyzed and included patients' sex, age, clinical symptoms, diagnosis, the location and morphology of fenestrations, and the other associated vascular diseases. The clinical features of different cerebrovascular diseases and malformations related to the imaging finding of the cerebral arterial fenestrations in patients with cerebral infarctions were analyzed and classified according to the National Institutes of Health Stroke Scale (NIHSS) and Trial of Org 10172 in Acute Stroke Treatment (TOAST) criteria. TOAST is a well-established system for the etiological classification of ischemic stroke, using different categories of stroke diagnoses, e.g., large-artery atherosclerosis, small-artery occlusion, cardioembolism stroke, stroke of other determined cause, and stroke of undetermined cause [24]. BA fenestrations were classified into four categories according to their relation with the location of the origin of the anterior inferior cerebellar artery (AICA): type I, the fenestration is located proximal to the AICA or absence of AICA; type II, bilateral AICAs symmetrically originating from the fenestrated trunks; type III, a unilateral AICA
2. Methods 2.1. Patients This study was approved by the ethics committee. Between January 2014 and December 2017, a total of 18,360 cerebral CTA or MRA covering the intracranial vessels were performed among both inpatients and outpatients in our hospital. The patients whose image findings were compatible with cerebral artery fenestrations were included. The imaging report system was searched for the word “fenestration”. If patients had more than one image, only the most recent images were analyzed. CT angiography was performed using a 320-row dynamic volume scanner (Toshiba Aquilion One), with 1.0-mm section thickness, 100 kV, and 250 mA. MR angiography was performed using a 1.5-T TOSHIBA EXCELART vantage or a Siemens 3.0-T Magnetom Verio System. For TOSHIBA EXCELART vantage, repetition time (RT) was 30 ms, and echo time (ET) was 6.8 ms. Angiogram parameters were set with a field of view at 19 × 19 cm and original slice thickness at 58
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vascular risk factors, all other cases had at least one vascular risk factor such as hypertension, diabetes mellitus, and dyslipidemia. The median follow-up was 13.5 months. Except for one infarction patient who was lost to follow-up, no acute stroke or transient ischemic attack occurred in the 11 patients who had 7 to 30 months (median, 18.1 months) antiplatelet and statin therapy after they were diagnosed as cerebral infarction.
originating from one side of the fenestrated trunk; and type IV, the fenestration is located distal to the AICA [4]. The clinical characteristics of patients with the location of cerebral infarctions in the blood supply area of the arterial fenestration were subjected to thorough analysis based on their risk factors. A routine follow-up was performed on patients reported with infarctions for a period of 30 months through outpatient follow-up after hospitalization or through direct telephonic contact with the patient's relatives.
4. Discussion
3. Results
Cerebral artery fenestrations detected incidentally during angiography are reported to be associated with aneurysmal dilatation, which may cause cerebrovascular diseases, arteriovenous malformations, or, rarely, ischemic symptoms. Therefore, this study aimed to analyze the characteristics of cerebral artery fenestrations and to correlate the clinical features of patients with cerebrovascular diseases and malformations. The results suggest that cerebral artery fenestrations are associated with cerebrovascular diseases and malformations. BA fenestrations were found to be the most common form. In this small retrospective study, among the 26 patients with cerebral infarction, 11 had cerebral infarctions in the blood supply area of the arterial fenestration, but they were without any cerebral infarction or transient ischemic attack during follow-up. The detection rate of cerebral vascular fenestration in the present study was 1.13%. This is about half the frequency reported by Cooke et al. [25] and Gao et al. [5]. Differences between studies could be due to the study populations and the methods used to identify the patients. In addition, there is the possibility that DSA is more sensitive to fenestrations than MRA and CTA, but this will have to be examined more closely. Among the fenestrations found in the present study, BA fenestrations were the most common, accounting for 50.2% (106/211) of the fenestrations. The frequency of BA fenestration in our study was 0.58% (106/18,360), which was similar to the frequency reported by Sanders et al. (0.31%) [1], but lower than the frequencies reported by Uchino et al. (1.7%) [6] and Gao et al. (2.33%) [5]. We found a case with bilateral fenestration in the VA, and another with three fenestrations in the left VA. Fenestrations of intracranial arteries and their association with cerebral aneurysms have been described in previous studies [1,16,17, [26],27]. In this study, 41 patients were reported with other vascular malformations, including 29 aneurysms (13.7%). This rate is low compared with the study by Cooke et al. [25], in which 60.5% of the patients with fenestrations had at least one aneurysm, and compared with van Rooij et al. [27], with 31%. Of note, the overall frequency of aneurysm observed in the present and previous studies (14%–61%) is much higher than in the original population (1–2%) [28], hinting toward an association between fenestrations and aneurysms. Among them, except one aneurysm at the site of the fenestration, all other 28 aneurysms were separate from the fenestrations. This does not mean that those 28 aneurysms are completely unrelated to the fenestrations
Two hundred eleven (211) cerebral artery fenestrations were found in 208 patients (frequency of 1.13%, 208/18,360). One hundred twelve (112) were male, and 96 were female; the male:female ratio was 1:0.86. Age at imaging ranged from 5 to 89 years (median, 52.5 years). Most of these patients were suspected of having intracranial tumors or cerebrovascular diseases. Of the 211 fenestrations, the most common type of fenestration (n = 106) was BA fenestration. The incidence of BA fenestration was 0.58% (106/18,360). The BA fenestrations were classified as: type I, 44 cases; type II, 26 cases; type III, 31 cases (of which 8 cases had only one anterior inferior cerebellar artery and originated from the fenestrations); and type IV, 5 cases. Of these fenestrations, 131 were of a slitlike configuration (Fig. 1A), while 72 had a convex-lens-like in shape (Fig. 1B), four were duplications of arteries (Fig. 1C), and four showed irregular morphology (Fig. 1D). The location and shape of the fenestrated vessels are shown in Table 1. Forty-one patients had other vascular malformations: 29 with aneurysms, three with moyamoya disease (Fig. 2A), four with venous malformations, four with arteriovenous fistulas, and six with cavernous hemangiomas (Table 2). The frequency of aneurysms was 13.9% (29/ 208). There was only one aneurysm at the site of a fenestration in the vertebral artery (Fig. 2B). All other aneurysms were separate from the fenestrations. Eleven patients presented with subarachnoid hemorrhage (SAH), seven patients had aneurysms, two patients had moyamoya disease, and two had no other malformation except the fenestration. Digital subtraction angiography (DSA) was performed in all cases of aneurysms for confirmation. Twenty-six patients had cerebral infarctions, of which 11 patients had cerebral infarctions in the blood supply area of the arterial fenestration because the arterial fenestration was precisely located in the blood supply area subjected to infarct. All of these 11 patients underwent CTA or MRA when they had cerebral infarctions in order to confirm that the cause of infarction could be related, at least anatomically, to the fenestrations. Patients with BA fenestrations had a higher incidence of cerebral infarctions in the blood supply area of the arterial fenestration than those with other arterial fenestrations (10 in 106 vs. 1 in 102, P = 0.01). The clinical features of cerebral infarctions in the blood supply area of the arterial fenestration patients are described in Table 3. Except for one patient (No.6) without any traditional Table 1 Shape and differential location of cerebral artery fenestrations among the patients Location
Shape
Length Number (%)
Slit-like Convex-lens-like Duplication Irregular < 5 mm 5–10 mm ≥10 mm
Number (%)
ACA
MCA
PCA
ACOA
VA
BA
ICA
24 17 2 0 23 17 3 43 (20.4)
5 0 0 0 4 1 0 5 (2.4)
2 1 0 0 2 1 0 3 (1.4)
6 1 0 0 7 0 0 7 (3.3)
10 30 2 4 8 14 24 46 (21.8)
83 23 0 0 71 29 6 106 (50.2)
1 0 0 0 0 1 0 1 (0.5)
131 (62.1) 72 (34.1) 4 (1.9) 4 (1.9) 115 (54.5) 63 (29.9) 33 (15.6) 211
ACA: anterior cerebral artery, MCA: middle cerebral artery, PCA: posterior cerebral artery, ACOA: anterior communicating artery, VA: vertebral artery, BA: basilar artery, ICA: internal carotid artery. 59
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Fig. 2. Angiogram showing different locations of cerebral artery fenestrations and their clinical correlation with cerebrovascular diseases and malformations. (A) CTA revealed a fenestration in the right VA and arterial collateral vessels at the base of the brain, indicating the clinical criteria of moyamoya disease. (B) A fenestration was seen with aneurysm superimposed over the left VA. (C) Three fenestrations could be seen in the left VA.
because the aneurysms could have been secondary to blood flow diversion. Unfortunately, this was a retrospective study of already diagnosed cases, and more refined measurements of hemodynamics were not available. In the study by Cooke et al. [25], there was no difference in the rates of arachnoid hemorrhage between the patients with related vs. unrelated aneurysm. There were seven patients who presented with SAH among the patients with fenestrations and aneurysms. Moreover, we also found two patients with SAH in whom the fenestration was the only malformation. Bożek et al. [29] and Gao et al. [5] reported two patients in whom the fenestration was the only malformation that coexisted with SAH. Nevertheless, because of the limited number of described cases in this study and the literature, it is difficult to explain whether the fenestration was the cause for SAH. Compared with the study by Cooke et al. [25], the present study presented the morphology of the fenestrations in addition to their location. Such morphological classification has been suggested by Uchino et al. [6], who divided the BA fenestrations into three types according to vascular morphology: slit-like shape, convex-lens-like shape, and duplication. We referred to their method for classification and found that there was a fourth type with irregular morphology, which was only found in the VA. Nevertheless, the clinical significance of this fourth type of fenestration in the VA and of the other types of fenestration require further study. In the BA, the type of fenestration (slit-like vs.
convex-lens-like) seems to be related to the origin of the anterior inferior cerebral artery (AICA), namely that the AICA has a predisposition to originate from a convex-lens-like fenestration [5]. Since the endothelium-lined septum increases the risk of thrombus formation in the fenestration [30], pontine and cerebellar infarction may develop if the AICA arises from a fenestrated segment of the BA [9]. Twenty-six (12.3%) patients had cerebral infarctions, and 11 of them (42.3%) had cerebral infarctions in the blood supply area of the arterial fenestration. This frequency of ischemic stroke is higher than in the general population [31], suggesting a possible involvement of fenestrations in ischemic stroke, but the present study was not designed to determine causality between fenestration and stroke. Importantly, only one stroke patient in the present had fenestration without any other risk factor for stroke, while all other patients had at least one additional risk factor. Therefore, additional studies are necessary to determine the exact relationship between stroke and fenestrations. Some cases of cerebral artery fenestration in patients with cerebral ischemia have been previously reported [12,16,21–23,32]. Jeong et al. [12] have reported five patients with MCA fenestration who had arteryrelevant cerebral infarction or ischemia. They determined that the atherothrombotic process could be initiated because of the local hemodynamics in an arterial branching site, progressing toward the proximal edge of the fenestration. The lateral wall of the smaller limb of the fenestration could be more easily affected. One of our patients 60
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Fig. 3. A 47-year-old man with left cerebellum and brain stem infarction. (A) Diffusion-weighted MRI revealed an area of reduced diffusivity in the left cerebellum and brain stem. (B) Magnetic resonance angiography revealed a small fenestration in the basilar artery. (C, D, and E) High-resolution MRI of the brain showing a small fenestration in the basilar artery, and the coronal plane images showing that the basilar artery was divided into two lumens with unstable plaque seen in the arteries. (F) Axial images showing the enhancing plaque.
Our study was limited because of its retrospective nature and because of the small sample size. In addition, because of the imaging protocols, other vascular malformations such as venous malformation, arteriovenous fistula, and intracranial hemangioma could not be displayed in the same images as the arterial fenestrations. In addition, since it is a retrospective study, and since the radiologists were not specifically looking for fenestrations when they read the images, it is highly possible that many patients were not included in this study. Hence, a multicenter study with a large number of patients could provide more definite data about the cerebrovascular diseases, location, morphology, and configuration of cerebral artery fenestrations.
Table 2 Frequency of other vascular malformations among 208 patients with fenestration Vascular malformations
Number
Frequency among patients with fenestration (n = 208)
Aneurysm Moyamoya disease Venous malformations Arteriovenous fistulas Cavernous hemangiomas Aneurysm+arteriovenous fistulas Aneurysm+venous malformations Aneurysm+cavernous hemangiomas+venous malformations Venous malformations+cavernous hemangiomas Total
26 3 1 3 4 1 1 1
12.5% 1.4% 0.5% 1.4% 1.9% 0.5% 0.5% 0.5%
1
0.5%
41
19.7%
5. Conclusions In conclusion, cerebral artery fenestrations are associated with cerebrovascular diseases and malformations. Basilar artery fenestrations were found to be the most common form. Fenestrations can be differentiated into four variants: slit-like shape, convex-lens-like shape, duplicated artery, and other irregular shape fenestrations, slit, and convex-lens-like being by far the most common types in the present study. In this small retrospective study, among the 26 patients with cerebral infarction, 11 had cerebral infarctions in the blood supply area of the arterial fenestration, but they were without any cerebral infarction or transient ischemic attack during follow-up. Importantly, the present study revealed that a cerebral infarction occurred in the blood supply area of the arterial fenestration of 42% of the patients with
(No.8) was subjected to high-resolution MRI of the brain to study the detailed structure of the fenestration, which revealed that the left smaller vessel had more obvious arteriosclerotic signs. All of the patients reported by Jeong et al. [12] had more than one vascular risk factor, including hypertension, diabetes mellitus, dyslipidemia, and smoking. On the other hand, one of our cases (No.6) did not show any traditional vascular risk factors or etiology of cryptogenic stroke. 61
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Table 3 Demographic and clinical characteristics of patients with the location of cerebral infarctions in the blood supply area of the arterial fenestration. Case
Age, y
Sex
Site of fenestration
Infarction location
Risk factors
NIHSS
TOAST
1 2 3 4 5 6 7 8 9 10 11
77 55 83 61 53 36 72 47 69 65 59
F M M M F M F M F M F
BA BA Right, ACA BA BA BA BA BA (Fig. 3) BA BA BA
Pons Medulla oblongata Right parietal lobe Cerebellum, medulla oblongata Midbrain Cerebellum Pons Cerebellum, pons Cerebellum Right parietal lobe, occipital lobe, basal ganglia Cerebellum
HTN, dyslipidemia Dyslipidemia HTN, dyslipidemia HTN, DM, dyslipidemia HTN, DM NA HTN, DM, dyslipidemia HTN, dyslipidemia HTN, IGT, dyslipidemia HTN, DM, dyslipidemia HTN
8 2 3 6 5 1 1 12 1 3 2
LAA LAA LAA LAA LAA SUD LAA LAA LAA LAA LAA
HTN; hypertension, DM; diabetes mellitus, IGT; impaired glucose toleration, NA; Not applicable, NIHSS; National Institutes of Health Stroke scale, LAA; large-artery atherosclerosis, TOAST; Trial of Org 10,172 Acute Stroke Treatment, SUD; Stroke of undetermined etiology.
stroke, but the present study could not evaluate the cause-to-effect relationship. A large multicenter study could be ideal to derive more conclusive evidence of diseases associated with cerebral artery fenestration.
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