Extracranial-intracranial Anastomosis Research Articles

Functional Arterial Anatomy of the Cranial Base

Two main vascular routes supply the brain, internal carotid arteries (ICAs) and vertebral arteries. The external carotid artery (ECA) mainly supplies the skin, muscle, and skull; thus, neurointerventionalists should be aware of ECA‐ICA, ECA‐vertebral artery, and extracranial–intracranial anastomoses. These anastomoses are not newly formed but are arteries that are remnants of developmental processes. During development, the ICA has anastomoses with the original ECA at the first and second pharyngeal arches, and carotid‐basilar anastomoses exist between the ICA and vertebral artery/basilar artery. Advances in neurointerventional technology are increasingly expanding the indications for transarterial embolization in the ECA territory. To avoid embolic complications to the brain and cranial nerve palsy, knowledge and understanding of such extracranial–intracranial anastomosis are crucial for neurointerventionalists interested in neurovascular diseases. The arterial contributions to these anastomoses are mainly the branches of the maxillary artery, ascending pharyngeal artery (extracranial), ophthalmic artery, and branches of the ICA (intracranial). Knowledge of the embryological processes is essential for understanding the routes and patterns of these anastomoses. This review discusses ECA development, the ICA segmental concept and functional anatomy of the extracranial‐intracranial anastomoses in the orbit, cavernous sinus, petrosal bone, and posterior fossa from an embryological point of view.

Indirect Revascularization Surgery for Chronic Ischemia in Moyamoya Disease

Indirect revascularization is a surgical procedure to reduce cerebral ischemia, using subcutaneous tissues or dura mater supplied by extracranial arteries as grafts. The perfusion pressure gradient between the cortex and the graft, if present, induces arteriogenesis and develops extracranial-intracranial anastomoses to supply blood flow to the cerebral cortex underneath the graft. Therefore, it is essential to perform the craniotomy over the site of the cerebral ischemia to induce functional anastomoses. The details of the indirect revascularization procedure vary among institutes in terms of the grafts used(skin arteries, such as the superficial temporal artery; temporal muscle, galea, or pericranium), dura mater incisions(removal and replacement with the grafts, linear incision, or multiple small incisions), and the location and size of the craniotomy. Indirect revascularization is especially effective in patients with moyamoya disease because the pathophysiology of the disease itself is related to intracranial to extracranial carotid system conversion. Generally, indirect revascularization was considered ineffective in patients with atherosclerotic steno-occlusive cerebrovascular disease; however, recent clinical trials suggested that it may also be effective in these patients. If a future clinical trial demonstrates a positive outcome, indirect revascularization may become a possible treatment for atherosclerotic patients.

Endovascular Management of Intracranial Dural AVFs: Transvenous Approach.

In this third review article on the endovascular management of intracranial dural AVFs, we discuss transvenous embolization approaches. Transvenous embolization is increasingly popular and now the first-line approach for ventral dural AVFs involving the cavernous sinus and hypoglossal canal. In addition, transvenous embolization is increasingly used in lateral epidural dural AVFs in high-risk locations such as the petrous and ethmoid regions. The advantage of transvenous embolization in these locations is the ability to retrogradely embolize the draining vein and fistula while reducing the risk of ischemic cranial neuropathy or brain parenchymal infarction commonly feared from a transarterial approach. By means of coils ± ethylene-vinyl alcohol copolymer, transvenous embolization can achieve angiographic cure rates of 80%-90% in ventral locations. Potential complications include transient cranial neuropathy, neurologic deterioration due to venous outflow obstruction, and perforation while navigating pial veins. Transvenous embolization should be considered when dural AVFs arise in proximity to the vasa nervosum or extracranial-intracranial anastomoses.

Role of the ophthalmic artery in the endovascular treatment for intracranial vascular diseases.

The ophthalmic artery (OA) is a crucial artery. Centered at the OA, there are numerous extracranial-intracranial anastomoses. The OA and its collaterals can be involved in some intracranial vascular diseases. So, it is very important to understand its specific anatomy, variation, and role in different neurovascular diseases. The OA has various anomalies both in the origin and collateral circulation. When performing endovascular treatment (EVT), the OA may suffer unexpected embolization through the numerous dangerous anastomoses. In case of a dural arteriovenous fistula or brain arteriovenous malformation mainly fed by the OA, the OA can be the passage of EVT, during which the central retinal artery could be injured. During interventional recanalization of steno-occlusive diseases of the internal carotid artery, dissection at the cavernous segment could progress to the OA segment and occlude the origin of OA. Under the circumstance of moyamoya disease, the OA can provide collateral flow to the anterior cerebral artery. When performing EVT for OA aneurysm concurrent with moyamoya disease, the parent OA should be preserved. After placement of a flow-diverting device for ophthalmic ICA aneurysm, the covered OA could experience spontaneous occlusion, leading to visual disturbance. Hence, the OA is an extremely important artery in the EVT for intracranial vascular diseases. In this article, we would extensively review the related literature to increase our understanding of the role of OA in intracranial vascular diseases. In addition, some illustrative cases would also be provided.

Dangerous Extracranial-Intracranial Anastomoses: What the Interventionalist Must Know.

The extracranial and intracranial circulations are richly interconnected at numerous locations, a functional connectivity which underlies their impressive capacity for adaptive plasticity in the setting of vasoocclusive disease. While evolutionarily beneficial, these connections can also result in inadvertent communication with the intracranial circulation during embolization of extracranial vessels, potentially resulting in stroke or cranial nerve palsy. While these anastomoses are always present to a certain extent, flow through them occurs under predictable circumstances, and thus embolization of the extracranial vasculature can be performed safely when knowledge of functional anatomy is combined with adherence to basic principles. Herein, we will review the anatomy of known extracranial-intracranial anastomoses and strategies for avoidance of unwanted intracranial embolization. We will also review the vascular supply to cranial nerves most at risk during common neurointerventional procedures, as well as blood supply to mucosal structures.

Arterial Anatomy of the Parasellar Area.

The arterial anatomy of the parasellar area is complex in that it deals with extracranial-intracranial anastomosis and supply to various cranial nerves in a small area. Pathologies such as hypervascular tumors and shunts are not uncommon and require good knowledge of anatomy in planning the treatment. In this article, the basic anatomy of the arterial supply in this region is discussed, covering the origins, territories, relation to the cranial nerves, and the connections among different systems.

Different ophthalmic artery origins: Embryology and clinical significance

This retrospective study gives a summary of ophthalmic artery (OA) variations to serve as guidelines for surgical interventionists and trainees. Pubmed and Medline searches were conducted. The OA usually arises intradurally (superomedial, anteromedial, or rarely superolateral) from the internal carotid artery (ICA). Rare extradural origin (primitive dorsal OA) (PDOA) remnant and extremely rare interdural origin (primitive ventral OA) (PVOA) remnant are of significance when sectioning the dural ring. Rarely, a persistent PDOA with ICA origin, or a PDOA remnant with inferolateral trunk origin, enters the orbit via the superior orbital fissure (SOF) for sole or partial orbital supply. Extremely rare, the PDOA and PVOA persist and form double OAs that arise from the ICA and run via the SOF and optic foramen. Occasionally, the OA arises from the middle meningeal artery (MMA), when both the PDOA and VDOA regress and enter the orbit via the SOF. Sole orbital supply via the external carotid artery (ECA), i.e. meningo-ophthalmic artery and/or MMA branches, or dual OAs (ECA and ICA origins) may occur. Other rare OA origins include anterior or posterior communicating artery; anterior or middle cerebral artery; basilar artery; posterior inferior cerebellar artery; and the carotid bifurcation. Primitive arteries (persistent or remnant), and/or abnormal anastomoses play pivotal roles in manifestations of OA variations. Of clinical importance are orbital collateral routes and dangerous extracranial-intracranial anastomoses. Awareness of OA origins and collateral routes is imperative for transarterial embolizations or infusion chemotherapy in the ECA territory to prevent visual complications.

Change in brain perfusion after extracranial–intracranial bypass surgery detected using the mean transit time of computed tomography perfusion

BackgroundCerebral perfusion can be evaluated using a computed tomography (CT) scan by intravenous bolus injection of contrast media. The purpose of this study was to investigate the value of CT perfusion (CTP) in follow-up of extracranial–intracranial (EC-IC) bypass surgery. MethodsWe retrospectively reviewed pre- and postoperative CTP studies in 14 patients who received EC-IC bypass surgery because of cerebral arterial occlusion or stenosis. Brain areas showing prolongation of the mean transit time (MTT) were automatically identified and quantitatively measured. ResultsAll 14 patients showed MTT prolongation in the preoperative CTP study. In 13 patients, a reduction in brain volume with MTT prolongation was noted during postoperative CTP. These 13 patients had a patent EC-IC anastomosis, and 42 ± 21% of the brain area with MTT prolongation returned to normal MTT during CTP 7 ± 4 days (range 2–13 days) after surgery. On clinical follow up of 41 ± 16 months (range 14–60 months), no stroke or transient ischemic attack was noted after bypass surgery in these 13 patients. The brain volume with MTT prolongation did not decrease in just one patient whose EC-IC anastomosis was not patent, and the patient suffered a minor stroke during surgery. ConclusionQuantitative results for the brain area with MTT prolongation were positively correlated with improvement in brain perfusion shown on MTT, EC-IC bypass patency, and patient outcome.

132 Urgent EC-IC Bypass for Symptomatic Atherosclerotic Ischemic Stroke

INTRODUCTION: Previous studies have shown that extracranial-intracranial (EC-IC) bypass surgery has no preventive effect of subsequent ipsilateral ischemic stroke in patients with symptomatic atherosclerotic internal carotid occlusion and hemodynamic cerebral ischemia. However, few studies have assessed whether an urgent EC-IC bypass surgery is an effective treatment for main trunk stenosis or occlusion in acute stage. METHODS: The authors retrospectively reviewed 58 consecutive patients who underwent urgent EC-IC bypass for symptomatic stenosis or occlusion at internal carotid artery or middle cerebral artery between January 2003 and December 2011. Clinical characteristics and neuroimagings were evaluated and analyzed. RESULTS: Based on preoperative angiogram, the responsible lesions were internal carotid artery in 19 (32.8%) patients and middle cerebral artery in 39 (67.2%). No hemorrhagic complication occurred. Sixty-nine percent of patients showed an improvement of neurological function after surgery and 74.1% of patients had favorable outcome. Unfavorable outcome was associated with insufficient collateral flow and new infarction after bypass surgery. CONCLUSION: Although EC-IC anastomosis for acute ischemic stroke is still debatable, it may be a good option for medication-resistance stenoocclusive disease.

Cerebral Protection During Retrograde Carotid Artery Stenting for Proximal Carotid Artery Stenosis-Technical Note-

Carotid artery stenting for carotid bifurcation stenosis usually uses the transfemoral approach. However, in patients with proximal common carotid artery (CCA) stenosis, the guiding catheter is difficult to introduce into the narrow origin of the CCA without risking cerebral embolization before activation of the protection device. A technique of cerebral protection by internal carotid artery (ICA) clamping with or without simultaneous external carotid artery (ECA) clamping was used to treat patients with proximal CCA stenosis by the retrograde direct carotid approach. The carotid bifurcation was surgically exposed and retrograde catheterization was performed to approach the stenosis. The ICA was clamped during angioplasty and stenting to avoid cerebral embolization. The ECA was clamped simultaneously if any extracranial-intracranial anastomosis was present. None of five patients treated with this technique experienced ischemic complications attributable to this technique.

The history of neurosurgical procedures for moyamoya disease

Almost 50 years of research on moyamoya disease (1957-2006) has led to the development of a variety of surgical and medical options for its management in affected patients. Some of these options have been abandoned, others have served as the basis for the development of better procedures, and many are still in use today. Investigators studying moyamoya disease during this period have concluded that the best treatment is planned after studying each patient's presenting symptoms and angiographic pattern. The surgical procedures proposed for the treatment of moyamoya disease can be classified into three categories: direct arterial bypasses, indirect arterial bypasses, and other methods. Direct bypass methods that have been proposed are vein grafts and extracranial-intracranial anastomosis (superficial temporal artery-middle cerebral artery [STA-MCA] anastomosis and occipital artery-MCA anastomosis). Indirect techniques that have been proposed are the following: 1) encephaloduroarteriosynangiosis; 2) encephalomyosynangiosis; 3) encephalomyoarteriosynangiosis; 4) multiple cranial bur holes; and 5) transplantation of omentum. Other options such as cervical carotid sympathectomy and superior cervical ganglionectomy have also been proposed. In this paper the authors describe the history of the development of surgical techniques for treating moyamoya disease.

The significance of the extracranial-intracranial anastomoses of carotid system in occlusion of internal carotid artery

The existence of collateral circulation in patients with impaired intracranial circulation was studied. We analysed angiograms of 35 patients of the Neurology Clinic of Clinical Centre in Sarajevo with occlusion of internal carotid artery. In majority cases collateral circulation was not established. In patients with occlusion of internal carotid artery, extracranial-intracranial anastomoses were established in some cases, with results of surviving and patients recovery. Collateral circulation based on blood vessels which are formed in the early stages of fetal life. Some embryonal arteries undergo an involution process, while the other part of blood vessels stay unfunctional during life, until cerebrovascular disease appearence, when it comes to their activation. Establishing of the collateral circulation in post-occlusiv status depend on great number of factors: number of anastomoses, their calibre,velocity of occlusion and complete vascular status of patients.

Surgical management of complex middle cerebral artery aneurysms.

Complex middle cerebral artery (MCA) aneurysms are defined in this review as aneurysms larger than 20 mm, arising from the MCA bifurcation, and requiring unusual surgical approaches for their obliteration. The direct surgical approaches to complex MCA aneurysms can be divided into five techniques: 1) direct clipping, 2) trapping, 3) trapping and extracranial-intracranial anastomosis, 4) excision and end-to-end anastomosis, and 5) external wrapping. The pertinent surgical anatomy, preoperative preparation, intraoperative procedures, operative approaches, and potential complications will be reviewed.

Anaesthesia for cerebrovascular surgery

Cerebrovascular surgery includes clipping of aneurysms, excision of arteriovenous malformations (AVM), carotid endarterectomy and extracranial-intracranial anastomosis. Anaesthesia for clipping of cerebral aneurysms aims to minimise the chances of rupture of the aneurysm whilst maintaining adequate cerebral perfusion. Ischaemic deficits occurring postoperatively should be actively treated by raising the cerebral perfusion pressure which may require hypervolaemic, hypertensive haemodilution. Induced hypotension is now generally avoided and profound hypothermia only used in the management of giant aneurysms. In patients with arteriovenous malformations cerebral vasospasm is not a problem so controlled hypotension can usefully be employed to reduce blood loss, which may be considerable, and prevent or treat hyperperfusion and oedema of the surrounding brain following obliteration of the AVM. Carotid endarterectomy is usually performed on patients with significant intercurrent disease, and manoeuvres aimed at optimising cerebral perfusion may have detrimental effects on a diseased heart, so compromise is required. Various methods are used to monitor cerebral perfusion during cross-clamping and the procedure may be performed under local anaesthesia to allow continuous monitoring of neurological function. Extracranial-intracranial anastomosis requires careful anaesthetic management but the operation is presently out of favour.

Stroke Prevention by Surgery for Symptomatic Disease in Carotid Territory

The benefit of surgical procedures in preventing stroke is of concern to physicians, surgeons, and all health-care providers. The multicenter randomized trial has been applied in evaluating these strategies. Extracranial-intracranial anastomosis has failed to measure up to this rigid form of scientific scrutiny and the reasons for the demise of this procedure are reviewed. By contrast, for symptomatic disease of the internal carotid artery, patients with very severe stenosis are better treated by endarterectomy than with medical care alone. The ongoing North American Symptomatic Carotid Endarterectomy Trial (NASCET) is reviewed and the compelling reasons to continue the trial for patients with moderate disease are outlined.

Management of giant intracranial ICA aneurysms with combined extracranial-intracranial anastomosis and endovascular occlusion

Nine patients with giant internal carotid artery (ICA) aneurysms (greater than 2.5 cm in diameter) were subjected to a combined extracranial-intracranial (EC-IC) bypass procedure and endovascular ICA occlusion during 1987 and 1988. The procedures were performed under one anesthetic. In all cases the collateral circulation had been judged insufficient on the basis of a strict preoperative testing protocol including: cerebral panangiography, electroencephalography, somatosensory potential recording, and cerebral blood flow monitoring during manual compression of the ICA in the neck. There were four intracavernous ICA aneurysms, four carotid-ophthalmic artery aneurysms, and one supraclinoid ICA aneurysm. All patients showed symptoms and signs of compression of the surrounding nervous structures. In the five cases of intradural lesions, the artery was occluded at the level of the aneurysm neck, so the ophthalmic artery had to be occluded. There was, nevertheless, no case of worsening of vision following surgery, and all nine patients showed significant improvement following the combined procedure. A combined EC-IC bypass procedure and endovascular ICA occlusion allows for immediate verification of the surgical results and appears to be a worthwhile method for treating giant intracranial aneurysms.

Natural and surgically imposed anastomoses of the circle of Willis.

The efficacy of the circle of Willis as a flow equalizer is well known. Most cerebral macrovasculatures also contain other natural anastomoses which are activated in times of stenotic stress. For the past several decades, neurosurgeons have surgically augmented the cerebral network with additional vessels which further increase the flow of blood to a defrauded region of the brain. It is desirable to know quantitatively what role these anastomoses play in the delivery of blood. Apart from computer simulation, such knowledge remains out of reach to the medical community but with modern simulation techniques, a wealth of information can be made available. This paper presents both time-dependent and period-averaged results of a detailed study of cerebral anastomoses. Four different models of the macrovasculature in the circle of Willis vicinity have been developed, two of which contain an extracranial-intracranial (EC-IC) anastomosis. Five cases were developed to show how the amount of blood flow is related to the sizes of the anastomoses. Since the EC-IC bypass is only marginally beneficial in those patients whose cerebral circulations are well-equipped with naturally occurring anastomotic vessels, procedures should be developed to screen for their presence or absence. The fluid mechanics associated with the EC-IC bypass operation dictate a beneficial result. Since the surgical procedures fail to consistently show reduction in risk even when good grafts have been made, there is an enigma in the study group results.

Surgical alternatives in the treatment of cavernous sinus aneurysms.

Direct surgery on aneurysms in the cavernous sinus is a formidable technical procedure. The intimate relationship of the intracavernous carotid artery to the venous structures and to the cranial nerves make surgical access difficult at best. Thirty-two of 356 aneurysm patients presented with symptomatic aneurysms originating from the intracavernous internal carotid artery. Twenty-one patients had aneurysms contained entirely within the cavernous sinus, and in 11 others the aneurysms arose within the cavernous sinus and extended into the subarachnoid space. Of the purely intracavernous aneurysms there were five small aneurysms (less than 25 mm) and 16 giant (greater than or equal to 25 mm) aneurysms. Fifteen patients with purely intracavernous lesions had a superior orbital fissure syndrome, and six had a variety of other symptoms. Of 11 patients with subarachnoid extension, five had a subarachnoid hemorrhage (Grade I or II), five had ipsilateral visual loss, and one had periorbital pain. The aneurysms were treated as follows: Group 1 received progressive ligation of the internal carotid artery in the neck with a Selverstone clamp and a surface superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis (purely intracavernous in nine, and with subarachnoid extension in one); Group 2 underwent trapping of the internal carotid artery and a deep STA-MCA anastomosis (purely intracavernous in seven); and Group 3 had direct clipping of the aneurysm (purely intracavernous in five, and with subarachnoid extension in 10). The cavernous sinus was entered directly through its roof by a pterional craniotomy with radical removal of the optic canal, lesser sphenoid wing, and lateral and superior orbital walls. Proximal control of the internal carotid artery was obtained through a cervical incision. Two patients in Group 1 developed transient neurological deficits, which resolved. Two patients in Group 2 developed a cerebral infarction, one of whom died; in both of these patients, the anastomosis was completed after the internal carotid artery occlusion. Two patients in Group 3 progressed from marked visual loss to blindness of the same side, and one developed an intraventricular hemorrhage during induction of anesthesia and died without surgery. It is proposed that a direct approach to symptomatic aneurysms in the cavernous sinus is the best initial alternative. When this approach is not feasible, a trapping procedure preceded by a high-flow extracranial-intracranial anastomosis may be considered. Although the authors have been able to clip aneurysms of various sizes, this has not been possible in all patients. Further work is needed in this area.

Changes in Cerebral Hemodynamics after Extracranial-intracranial Bypass

A group of 25 patients with patent extracranial-intracranial anastomoses were followed for 18 months in an effort to determine the long-term effects on regional cerebral blood flow (rCBF). The 133Xe inhalation method was used to measure rCBF. In patients whose preoperative mean rCBF (mCBF) on the affected side was low, i.e., less than 40 ml/100 gm/min, or who had internal carotid artery occlusion (ICO) or middle cerebral artery occlusion (MCO), mCBF on the affected side increased postoperatively. In patients with high preoperative mCBF rates on the affected side, i.e., 40 ml/100 gm/min or more, or internal carotid artery stenosis (ICS) or middle cerebral artery stenosis (MCS), mCBF on the affected side did not change after bypass. Postoperatively, the hemispheric difference in mCBF between the anastomosed and opposite sides was small in cases with ICO or MCO and negligible in patients with ICS or MCS, relative to the preoperative values. The rCBF significantly increased in the frontal, precentral, and superior temporal areas in patients with ICO, MCO, or low preoperative mCBF rates on the affected side.

???Giant pneumoaneurysm??? after combined internal carotid artery occlusion and extracranial-intracranial anastomosis

???Giant pneumoaneurysm??? after combined internal carotid artery occlusion and extracranial-intracranial anastomosis