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Original Article

Carotid rete mirabile associated with subarachnoid hemorrhage from intracranial aneurysm: A case report and systematic review

Interventional Neuroradiology 2015, Vol. 21(1) 55–60 ! The Author(s) 2015 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.15274/INR-2014-10107 ine.sagepub.com

Eric Homero Albuquerque Paschoal1, Vitor Nagai Yamaki1, Fernando Mendes Paschoal Ju´nior1, Ronie Leo Piske2, Manoel Jacobsen Teixeira3 and Edson Bor-Seng-Shu3

Abstract Carotid rete mirabile (CRM) is a rare physiological vascular network in humans that is most often found in Eastern populations. This paper describes a CRM associated with an aneurysmal subarachnoid hemorrhage (aSAH) and discusses the details of the patient’s treatment. A 28-year-old woman was admitted to our service with clinical signs and symptoms of a spontaneous aSAH. Computed tomography revealed a diffuse and extensive SAH (Fisher group IV), while an angiogram showed an abnormal collateral network in the right carotid system and a hypoplastic aspect to the internal carotid artery (ICA) on the same side. In addition, a saccular aneurysm with a diameter of 9.5 mm was present in the ophthalmic segment of the left ICA. This case is extremely uncommon. To avoid rebleeding in the patient, we successfully treated the patient by clipping the aneurysmal lesion. No procedure was performed for the CRM.

Keywords Cerebrovascular disorders, collateral circulation, subarachnoid hemorrhage, case report

Introduction Congenital artery collateral networks are rare in humans and frequently occur as a result of an embryonic abnormality in the formation of the native vessel. Lie defined agenesis as a complete failure of the organ to develop, aplasia as a lack of development, and hypoplasia as incomplete development. Evaluation of the skull base for the presence or absence of the carotid canal is required to distinguish aplasia from agenesis because the precursor of the internal carotid artery (ICA) is a prerequisite for the development of the carotid canal at five to six weeks.1 Carotid rete mirabile (CRM) is a transdural arterial network found in the cavernous portion of the ICA and is most often supplied by branches of the external carotid artery (ECA), particularly branches of the maxillary artery and ascending pharyngeal artery.2,3 CRM is a physiological communication between the external carotid and internal carotid systems in mammals such as pigs and sheep.4 These lower mammals have an incomplete circle of Willis that is frequently supplied by other branches of the ECA. During embryonic development, the ICA likely undergoes secondary atrophy, and as a result of this late regression, the CRM physiological network serves to replace the arterial supply to the circle of Willis.5

When considering the physiological formation of CRM in these animals, it helps to examine the physiopathology of this condition in humans, where CRM associated with developmental abnormalities of the ICA works as a pathway to compensate for deficient blood flow in the ICA.6 In other animals, these changes are required to facilitate heat exchange and regulate intracerebral blood pressure and flow, as a beneficial adaptation.7 CRM is a rare disorder that most frequently occurs in Asian populations. However, there are reports of the condition in Western patients.5 Patients with CRM exhibit a wide variety of clinical symptoms, from asymptomatic patients to patients presenting with headache, loss of balance, cognitive disturbances

1

Division of Neurosurgery, Hospital Ophir Loyola, Federal University of Para, Belem, Brazil 2 Division of Neuroradiology, Hospital Beneficeˆncia Portuguesa de Sa˜o Paulo, Sa˜o Paulo, Brazil 3 Division of Neurosurgery, Hospital das Clinicas, University of Sa˜o Paulo, Sa˜o Paulo, Brazil Corresponding author: Eric Homero Albuquerque Paschoal, Trav. Dom Romualdo de Seixas, 1164 apt 1601 CEP, 66055-200, Belem, PA, Brazil. Email: [email protected]

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Figure 1. A) Vessel angiogram demonstrating external and internal carotid arteries with a rete mirabile-type network compensating for segmental hypogenesis of the epidural horizontal segment of the right internal carotid artery (5th segment), promoting reconstitution of the distal siphon through collateral branches from the maxillary artery. This phase shows an early injection in the angiogram study at the right internal carotid artery. B) Late phase angiogram study demonstrating distal branches from the internal carotid artery.

caused by subarachnoid hemorrhage (SAH), intracerebral hemorrhage, or stroke.4,8,9 The association of intracranial aneurysm with rete mirabile is uncommon, but this association could be related to a number of symptoms. In some cases, intracranial aneurysms represent the source of bleeding in SAH events.10 This paper describes an uncommon case of CRM associated with an aneurysmal SAH (aSAH) and discusses the embryonic pathway of the disorder and the surgical strategy used to treat it.

Case Report The patient was a 28-year-old woman who suffered from a sudden and severe headache followed by meningismus and loss of consciousness, suggesting a spontaneous SAH episode. Neurological examination revealed a Hunt Hess scale (HHS) grade of 2 points, with amaurosis of the left eye but no other symptoms. Cranial computed tomography (CT) revealed an extensive and diffuse SAH (Fisher group IV) without expansion of the ventricular systems. An angiogram showed a hypoplastic shape of the right ICA at the emergence of the common carotid artery, which was associated with an anomalous vascular mesh on the cavernous segment of this artery (rete mirabile). A reconstitution at the point of the cavernous segment was made through collaterals from the internal maxillary artery (Figure 1). On the left ICA, a saccular aneurysm was detected that was 9.5 mm in diameter, with a neck measuring 4.2 mm. The aneurysm

Figure 2. Berry aneurysm located on the left side of the ophthalmic segment of the internal carotid artery over the upper surface of the arterial vessel.

topography was in the ophthalmic portion of the artery, with a compressive effect on the optic nerve. No vasospasm was observed among the other brain vessels (Figure 2). The patient did not present any risk factors such as tobacco use, alcohol ingestion, or advanced age, and there was no similar case in the patient’s family history. The selected treatment approach was a combined epidural and subdural direct microsurgical approach,

Paschoal et al.

Figure 3. Axial view of the skull base with CT demonstrating absence of the right carotid canal.

with partial removal of the anterior clinoid process, as proposed by Dolenc.11

Postoperative Course The patient was discharged without neurological deficit and did not present a recurrence of the symptoms during the first year. Postoperative transcranial Doppler ultrasonography was performed after ten days without emboli or arterial vasospasm signs. However, a high rate of cerebral blood flow was observed arising from the CRM in the right circulation. An angiogram was performed with no sign of intracranial aneurysm, and the CRM was preserved. A skull base CT was performed to search for carotid canal abnormalities. CT showed an absence of the right carotid canal (Figure 3), suggesting that the ICA involuted as part of normal embryonic development.

Discussion Arterial embryological collateral networks in humans are infrequent and tend to be observed in cases where there is hypoplasia, aplasia, or narrowing of the native vessels.6 When the ICA is absent from birth, collateral arteries develop to compensate for the absent segment. Most frequently, the middle and anterior cerebral arteries on the side of the absent vessel are supplied through the circle of Willis by the basilar artery and branches of the opposite ICA.12 However, collateral pathways may also develop between the external and internal carotid systems in such rare situations as CRM.12 The pathogenesis of ICA rete formation is unknown. The most widely accepted theory is late (fetal or perinatal) regression of the artery. If agenesis occurs as a primary deficit with the absence of the precursor vessel, then embryonic vessels (brachial and segmental arteries) become the source of the collateral

57 vascularization.5 If the carotid artery disappears through regression in a late period after its development, the embryonic vessel had already regressed, so there is no longer a source of recruitment for the collateral circulation, and a rete mirabile may form,3,5 ICA segmental agenesis follows the patterns of distal flow reconstitution of ICA by embryonic arteries. The cervical portion of ICA agenesis can be fed through the hyoid artery, through the ascending pharyngeal artery. Intracavernous ICA agenesis is usually fed via the primitive maxillary artery, through a complex parasellar rete that originates from internal maxillary artery branches.1,5,13 A signal trigger has been postulated because the cause of ICA or basilar artery delayed regression should be the same as what the cause of rete formation in both anterior and posterior circulations. Potential causes include a congenital defect supported by the absence of other cerebrovascular disorders, regular stenosis at the cavernous segment of the ICA, and in most cases, bilateral distribution.3,5 Among cases of CRM, bilateral CRM is more common than unilateral CRM. Both unilateral CRM and associated intracranial aneurysms are infrequently6 reported, particularly in Western populations.5 Our study revealed (via a Medline search) 35 reports of CRM, of which five (14.2%) were unilateral cases and seven (20%) were associated with intracranial aneurysm; most occurred in Asian populations (Table 1). The patient in this study is an extremely rare case of Western origin with unilateral involvement associated with a contralateral aneurysmal lesion. The clinical data available for these individuals are unclear. Nishimoto et al. found a considerable difference in the initial symptoms of patients with abnormal cerebrovascular networks, which could be related to age. In patients under 21 years of age, motor weakness of a limb was the most common manifestation, followed by seizures and visual changes. In patients over 20 years of age, SAH was the most common initial manifestation.8 Based on a literature review, we found that the initial symptom was most frequently SAH (34.2%), followed by incidental findings (20%), suggesting that cerebral perfusion is relatively well compensated by the carotid collateral network.4 Only seven individuals with different initial symptoms were younger than 21 years. However, in nearly 40% of the patients over 20 years of age, the clinical course began with SAH. Diagnosis of abnormal cerebrovascular networks is usually made due to incidental findings in asymptomatic patients.8 However, in these patients, CRM could be misdiagnosed on routine computed tomography angiography or magnetic resonance angiography. Alternatively, in patients with SAH and other symptoms, a careful evaluation of the imaging examinations could aid in the diagnosis of these abnormal networks. In this case report, CRM was associated with a carotid-ophthalmic artery aneurysm. The exact

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Interventional Neuroradiology 21(1)

Table 1. Reported Cases of Rete Mirabile. Authors

Year

Age/Sex

Symptoms

Associated lesions

Minagi and Newton Hawkins and Scott Rockett and Johnson Hately and Shapiro Jones and Wetzel Danziger et al. Koo and Newton Araki et al. Ito et al. Itoyama et al. Fuwa Hyogo et al. Karasawa et al. Kino et al. Kino et al. Nakaoka et al. Konno et al. Mahadevan et al. Yasuhara et al. Weon et al. Kim et al. Li et al. Herwadkar Henkes et al. Henkes et al. Castro et al.

1966 1967 1968 1969 1970 1972 1972 1986 1991 1993 1994 1996 1997 1999 1999 2000 2001 2004 2004 2005 2006 2006 2006 2007 2007 2009

43/M 37/M 40/M 10/F 43/M 39/F 20/M 55/F 43/F 40/M 13/F 37/F 17/F 28/M 60/F – 68/F 29/F 14/F 14/F 38/M 57/F 52/F 36/M 54/M 34/F

– CA – CA AVM – PXE PXE CA – Dieulafoy’s ulcer – – – – – – – PXE PHACE syndrome – – CA CA CA –

Sahin et al. Hong et al. Lee and Cha Aburto- Murrieta et al. Vasseur et al.

2010 2010 2011 2011 2011

32/F 45/F 28/M 26/F 38/F

Loss of balance SAH SAH Seizures/Headache – Ischemic stroke CCF Motor Weakness SAH Ischemic stroke Ischemic stroke SAH SAH SAH SAH – Loss of balance SAH – Visual changes – ICH SAH SAH SAH Visual changes/ Motor weakness – Headache – Seizures Visual changes

Del Zotto et al. Nagahata et al. Lin et al. Lu et al.

2012 2013 2013 2014

39/F 70/F 21/F 18/F

– SAH Facial paresthesia/ dizziness Headache

– – – – PXE/Chronic myocardial ischemia PXE CA – –

Uni/bilateral carotid involvement Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Unilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Unilateral Bilateral Bilateral Bilateral Bilateral Unilateral Unilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Unilateral Bilateral

SAH - subarachnoid hemorrhage; ICH - intracerebral hematoma; PXE - pseudoxanthoma elasticum; CA - cerebral aneurysm, AVM - arteriovenous malformation.

mechanism by which these diseases are associated is unclear, but this association may not be coincidental. We believe that the occurrence of the concomitant aneurysm is related to the symmetrical and segmental development of the ICA and transdural arteries. The signal responsible for the ICA agenesis and rete formation probably produces the same effect on the contralateral brain vessels, resulting in a greater ICA vulnerability to vascular disorders, such as intracranial aneurysms. These aneurysms are most likely related to an increased weakness of the arterial wall and are

further exposed to a higher shear stress due to the hemodynamic changes, consequently increasing their tendency to rupture. The management of a ruptured aneurysm associated with CRM is challenging for neurosurgeons. The surgical risk is higher than with common SAH because of the potential reduction in cerebral hemodynamic reserve, so attention should be concentrated on the pre- and postoperative vasospasm and the timing of surgery.10,14 In addition, the topography of the aneurysm includes a close relation with important structures,

Paschoal et al. including the optic nerve, optic chiasm, pituitary stalk, hypothalamus, ICA, and third cranial nerve.15 Patients who underwent conservative treatment usually had complications such as rebleeding of the aneurysm or ischemia.10 Some authors suggest that endovascular treatment is not possible because of the tortuous and fragile state of the rete vessels.3 When the aneurysm is contralateral to the rete mirabile, it does not seem to be an impediment, but it is important to consider the hemodynamic stress of this abnormality and the characteristics of the aneurysm. Our patient’s aneurysm presented in the neck, was larger than 4 mm, and had an unfavorable ‘‘dome/ neck’’ ratio (>1.5), which is a contraindication for coil embolization.16 Accordingly, for the treatment of this aneurysm, neuroendovascular reconstruction techniques such as Onyx, a flow diverter stent, or a stent with a coil had to be considered. However, all of these therapeutic choices require prophylactic antiplatelet therapy with salicylic acetyl acid and clopidogrel. This procedure has been shown to lead to substantial complications in the Amazon region, most likely due to the poor patient knowledge about the risks and functional limitations of this therapeutic task and the difficult follow-up of these patients from rural areas. Therefore, surgical treatment using the Dolenc11 technique was performed and achieved a successful clipping of the aneurysm, thereby reducing the mass effect under the optic cranial nerve. Funding This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Conflict of interest The authors declare no conflict of interest.

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