Use of Cerebral Revascularization Techniques in the Endovascular Era. Is it Still a Useful Technique?
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Cerebral revascularization (CR) was a revolutionary surgical technique first introduced by Professor Yasargil in 1967 in the treatment of cerebral ischemia’s case. In the following decades, its use was subjected to several modifications and implementations, to the point that its purpose has been expanded to other several cerebrovascular diseases. In the more recent years, its use was strongly reduced because of the advancement of the endovascular techniques, which have been showed to bring a significant number of benefits and avoid the most common surgical complications; not last, these endovascular techniques reduces in a significant way the recovery length and gives an effective treatment for those patients who were not suitable for traditional surgery. In this review, the authors search the literature to analyze the cases in which such techniques is still of use for the treatment of neurovascular diseases. CR is still a useful technique in the treatment of several pathologies, among which are moyamoya disease, complex intracranial aneurysms, and skull base tumors. A good neurosurgeon should be able to master both surgical and neurovascular approach. The teaching of CR seem to be even harder since the few cases suitable to this approaches are sometimes not enough to allow a resident or a young neurosurgeon to gain experience. CR remains an important tool in neurosurgeons’ armamentarium. In this review, authors analyze the role of the cerebral revascularization techniques in the contemporary era and study the pathologies for which it can be used, in particular, moyamoya disease, complex intracranial aneurysms, and skull base tumors.
KeywordsCerebral revascularization Moyamoya disease Complex intracranial aneurysms Skull base tumors
Superficial temporal artery
Internal carotid artery
Middle cerebral artery
Transient ischemic attack
Gross total resection
When it was firstly introduced in 1967 by Professor Gazi Yasargil, cerebral revascularization (CR) was considered an outstanding surgical innovation . The first attempt of CR consisted in a bypass using the superficial temporal artery (STA) as donor and the middle cerebral artery (MCA) as recipient vessel in a case of cerebral ischemia.
From there, this technique was subjected to a great evolution and improvement, up to the point that it can now be defined as one of the most influential technique in vascular neurosurgery . Even though it remains a well-known surgical technique in the vascular field, its performance remained very limited due to the high level of specialty needed and to the limited indications, since the beginning of the endovascular era, thanks to which patients expect almost the same clinical results, have a faster recovery and present a lower rate of complications [3, 4].
The enthusiasm for the technique, that quite rapidly spread all over the world, was suddenly reduced by a mainstay randomized trial, published in 1985, about the extracranial–intracranial (EC-IC) bypass trial and Carotid Occlusion Surgery Study trial which rejected the idea that the EC-IC anastomosis could prevent ischemia in atherosclerotic patients [5, 6]. Consequently, the usefulness of this kind of anastomosis in carotid diseases remained a topic of discussion [5, 6].
Another concern about the use of CR is given by the optimal timing to perform such technique. Moreover, also the real benefits of the technique are under revision, since authors started to see if the STA is sufficient to restore the hemodynamic properties of the patients . In these modern days, the use of bypass surgery for occlusive vascular disease has greatly reduced. It should be also noticed that the trials [5, 8, 9] were criticized for not being able to define the subset of patients with poor collateral circulation for whom cerebral bypass surgery will be of great benefit. Another factor that should be considered in the assessment of a patient with an occlusive disease is the presence of autoregulation failure, causing an alteration of blood supply and perfusion [6, 10].
Even though it received several critics, the trials showed that the surgical approach, consisting in the cerebral revascularization, causes an improved hemodynamics without perioperative stroke and a low risk of recurrent stroke . The advantages related to the hemodynamics properties were largely appreciated; however, surgical complications make the physicians to prefer medical therapies which did not any major complications. CR, however, remains still an affordable option for the small group of patients which are refractory or are not suitable to the pharmacological therapy .
The aim of CR is to increase or replace the blood flow to the brain provided by one cerebral artery. Even though, it was mainly thought for ischemic cases, the concept behind it of flow augmentation can be applied to several cerebral pathologies not related to ischemia, like rare neurovascular diseases, complex aneurysms, and difficult skull base tumors [11, 12, 13].
It has been defined as a intracranial arteriopathy commonly denoted by bilateral stenosis of the internal carotid arteries (ICAs) and middle cerebral arteries (MCAs), which are responsible for transient ischemic attacks (TIAs) or strokes [14, 15].
The word “Moyamoya” has a Japanese origin, meaning “puff of smoke”, because, at the imaging exams, the newly formed vessels aiming to compensate the stenosis obstruction resemble puff of smokes. Moyamoya angiopathy has different clinical history: it may have a slow progression with few and rare events or a very rapid one, characterized by a quick neurological decline. It has been reported that patients underwent a medical treatment have a poorer prognosis: it is known that 40 to 82% of patients in a gap of 5 years are subjected to another stroke [16, 17]; in the same gap of time, patients affected by moyamoya syndrome (unilateral disease), progress up to moyamoya disease (bilateral disease). Instead, patients underwent surgical treatment (cerebral revascularization) had a far better prognosis [18, 19, 20, 21].
There are different methods to perform cerebral revascularization. Traditionally, the 2 main approaches are defined as direct and indirect anastomotic procedure. In the first case, the surgeon can use the STA, the occipital artery (OA), or even the middle meningeal artery (MMA) as donor vessels; the recipient vessel can be the MCA, the anterior cerebral artery (ACA), or the posterior cerebral artery (PCA) as recipient . The indirect revascularization, instead, aims to exploit the angiogenetic potential of the tissue used (which can be a muscle, like the temporalis muscle), putting it on the region affected by the ischemia, making it a more suitable option for the pediatric population .
Even though these are the most common used approaches, several others have been described, like the so called encephalo-duro-arterio-synangiosis (EDAS), which is quite similar to the indirect approach: it consists in laying a branch of vessels on the ischemic regions, waiting until its angiogenetic potential creates a new functioning vessel . Advantages of direct revascularization procedures are several; among them, we should remember that, at the cost of few possible complication, it restores quite immediately the blood flow in the region affected, assuring also a long term result. While performing the direct procedure, it should be kept in mind that the anastomosis will enlarge in around half of the cases, increasing the risks of rupture . As any surgical procedure, it presents also potential disadvantages, which neurosurgeons should consider in the treatment plan; among them, they should be worried about the technical difficulties (particularly the young neurosurgeons) related to the creation of submillimeter anastomoses and cross-clamping of recipient vessels, but also other complications more related to the surgery itself, like strokes and hyperperfusion syndrome [21, 24, 25, 26, 27].
A large series of 450 patients affected by moyamoya disease  and treated almost all of them (91%) with CR, showed a rate of 5.5% of hemorrhage in the 5 years following the surgery. In front of such a low rate of hemorrhage, 71% of the patient had a functional improvement, which was recorded in a quick gap of time (1 month) . Regarding the so called indirect revascularization procedures, it is showed in the literature that they have the benefit of generally shorter operative times, due to the less complicated technical challenges, which is pay by a longer time of functional improvement [15, 24, 25, 26]. In fact, the main disadvantage is the delay of weeks to months for new vessel formation; the formation of new collateral vessels, in fact, required 3 to 4 months to develop . An increased risk of stroke has also been noticed [26, 27].
Complex Intracranial Aneurysms
Complex intracranial aneurysms (CIAs) is a broad term used to define all those aneurysm which are difficult to treat, under a surgical point of view, because of their dimensions (giant aneurysms), the difficulty related to their access in the operating room or because they have complicated wall structure, which are more prone to complications. Clinical presentation of a cerebral aneurysm can be vague. The most common symptom at presentation is headache. It is possible, however, to encounter other sign of cerebro-vascular lesions, such as transient ischemic attacks (TIAs), cranial nerve palsies but also altered mental status and several other symptoms suggestive of mass effect. It is also common that even these aneurysms are casually encountered during the treatment of other disease .
Due to the great range of tools of the endovascular operating rooms and the improvements in their approaches, also here there is a reduction for indication to the CR. Endovascular treatments are nowadays the cornerstone therapy for almost all the posterior circulation aneurysms, since they are more difficult to reach through a traditional surgical approach. The new endovascular devices not only present less complications, because of the avoidance of the surgery itself, but also because it does not involve the sacrifice of any healthy vessel [23, 29, 30]. Still, the more traditional cerebral revascularization has its own primary role in case in which the lesion is judge to be not suitable for the endovascular treatment. Several studies about the use of flow diverters in the treatment of lesions in the posterior circulations are defined to be not sufficiently satisfactory; this is why neurosurgeons are still not prone to strongly recommend them; in particular, these studies worry the scientific community because of the elevated recurrence rate, in particular in the subsert of giant aneurysms [31, 32, 33].
There is also another main reason, for which physicians could choose the surgical approach; there is in fact a group of patients which, for a wide range of motivations are not able to undergo an antiplatelet therapy, a mandatory procedure for stent placement . Due to the limitations presented in the use of endovascular approaches and the impossibility to surgically clip certain complex aneurysms, the Hunterian ligation, which is still a widely performed technique that can be easily performed without significant technical challenges or surgical planning, can be used in some limited cases. It should be noticed, however, that surgical occlusion of the ICA for the management of aneurysms was associated with infarction in around 40% of patients .
There was an attempt to use Baloon test occlusion test (BTO) to assess its safety in the occlusion of cerebral vessels . The results, however, were not homogenous and reassuring as thought. Several type of complications has been reported, like dissections and embolic complications . Following studies have focused their attention on the use of BTO on ICA, reporting elevated rates of strokes (from 1.5 up to 4.8%), accompanied by more worrying data about immediate (10–12%) and delayed ischemia (1.4%) . Beside the risk of ischemia, the neurosurgeon should also worry about the risks related to the removal of a vessels. A study has showed that there is a 10% chance that patients undergoing Hunterian ligation develops de novo aneurysms in their collateral circulation .
Although recent advances in 3D angiography and new algorithms allowed an easier determination of the “clippability” of the aneurysms [33, 37, 38], the intraoperative exploration remains up to now the safest way to determine the best approach: if, while performing the intraoperative evaluation, the surgeon decide that the clip is not the best option for the patient, there is a wide range of option among which he could decide, like an occlusion or the trapping with a bypass . The type of bypass performed in the treatment of complex aneurysms, which could be high-flow or low-flow, depends on several factors, among which the experience of the neurosurgeons with the microanastomosis, the location and the dimensions of the aneurysms itself.
It has been proposed by some neurosurgeons that the use of intraoperative blood flow measurements to define how much flow augmentation is needed to obtain a satisfactory results, while others have proposed to try to define the chance of getting a good result by assessing the collateral flow through an angiography [38, 40, 41]. In case collateral circulation is not enough or flow rate is lower than expected, the neurosurgeon can decide to perform a low-flow bypass such as an STA-MCA. It can also happen that, for several reasons, such as a physiological hypoplasia, in the absence of collaterals, a high-flow bypass should be chosen [38, 41, 42]. A simple “trick” to determine which kind of bypass should be preferred consists in performing a gentle compression on the carotid artery, at the level of the neck, in order to assess the presence of collaterals [38, 41, 42]. For what regard success rates, several studies report high levels of satisfactory results, ranging from 50 to 93% [38, 41, 42, 43].
Lastly, it should be noticed that it results quite hard to compare realistically different series of patients across different eras, which were characterized by different approaches and technologies. In the present endovascular era, patients are preferentially treated through a microsurgical approach only when and if the endovascular treatment has failed, or when they have been deemed poor candidates for endovascular therapy.
Skull Base Tumors
Even though it is not of major use, it is important to remember that CR has also been used in the treatment of difficult skull base tumors . Despite the limited number in which CR is needed in the oncological field, the indications are various: a CR should be performed where the sacrifice of a vessel is needed to perform the complete resection of the tumor lesion, or in case in which the neurosurgeon suspect a high risk of intraoperative vessel injury [11, 13].
There are meningiomas that encased and narrowed ICA or vertebral artery that frequently invade arterial wall, as it has been reported from the histological exam . In case there are no enough collaterals, it should be avoided to perform a gross total resection (GTR), sacrificing the vessels encased; in these cases, a subtotal resection (STR) should be preferred, followed then by a radiosurgical treatment. In some tumors, like chordomas and chondrosarcomas, due to their consistence, the neurosurgeon has the chance to try to dissect them from the vessel and then try to continue with a GTR .
It has been observed that, after the performance of cerebral revascularization for skull base tumor removal, a high number of focal stenosis (up to 20%) and/or occlusion develops over a long-term follow-up . These occlusions usually happen in conjunction with an important enlargement of collateral vessels, according to Poiseuille law . These characteristics can be caused by several factors, such as not optimal hemodynamic factors (low blood pressure or longer graft vessels). Few words should be spent on local bypasses, also known as in situ side-to-side anastomosis, re-implantation, re-anastomosis; since they showed a long term patency rate near to 100%, they do not require a donor graft and show a better outcome, from the cosmetical point of view [12, 13].
After analyzing the cases where cerebral revascularization techniques could be used, we should conclude by saying that bypass surgical techniques, whether direct EC/IC or IC/IC bypass or indirect via EDAS approach, will continue to have an important role in the treatment of several neurosurgical pathologies.
Although the admirable advances showed in the recent years in endovascular, medical and radiation therapies [45, 46], there is a limited number of patients respectively affected by complex aneurysms, atherosclerotic occlusive disease, and skull base tumors which should undergo, as primary treatment, to bypass procedures. Thus, it is important that the surgeons, mainly the young generation, continue to improve their bypass technique using laboratory training in order to have this skill in their surgical armamentarium for the cases they will encounter.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethical Approval and Informed Consent
The present study does not need any approval for the ethical committee, nor a signed Informed consent from patients.
- 5.Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. The EC/IC Bypass Study Group. N Engl J Med 313:1191–1200, 1985. https://doi.org/10.1056/NEJM198511073131904
- 6.Powers WJ, Clarke WR, Grubb RL Jr, Videen TO, Adams HP Jr, Derdeyn CP. COSS investigators: extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the carotid occlusion surgery study randomized trial. JAMA. 2011;306:1983–92. https://doi.org/10.1001/jama.2011.1610.CrossRefPubMedPubMedCentralGoogle Scholar
- 8.Extracranial to intracranial bypass and the prevention of stroke. Lancet 2:1401–1402, 1985. https://www.ncbi.nlm.nih.gov/pubmed/?term=Extracranial+to+intracranial+bypass+and+the+prevention+of+stroke+and+lancet
- 9.The EC/IC Bypass Study group. The International Cooperative Study of Extracranial/Intracranial Arterial Anastomosis (EC/IC Bypass Study): methodology and entry characteristics. Stroke 16: 397–406, 1985. https://www.ncbi.nlm.nih.gov/pubmed/?term=The+EC%2FIC+Bypass+Study+group.+The+International+Cooperative+Study+of+Extracranial%2FIntracranial+Arterial+Anastomosis+(EC%2FIC+Bypass+Study)%3A+methodology+and+entry+characteristics.
- 11.Lawton MT, Spetzler RF. Internal carotid artery sacrifice for radical resection of skull base tumors. Skull Base Surg. 1996;6:119–23 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1656574/.CrossRefGoogle Scholar
- 13.Sekhar LN, Natarajan SK, Ellenbogen RG, Ghodke B. Cerebral revascularization for ischemia, aneurysms, and cranial base tumors. Neurosurgery. 2008;62(Suppl 3):1373–410. https://doi.org/10.1227/01.neu.0000333803.97703.c6.CrossRefPubMedGoogle Scholar
- 14.Abla AA, Gandhoke G, Clark JC, Oppenlander ME, Velat GJ, Zabramski JM, et al. Surgical outcomes for moyamoya angiopathy at barrow neurological institute with comparison of adult indirect encephaloduroarteriosynangiosis bypass, adult direct superficial temporal artery-to-middle cerebral artery bypass, and pediatric bypass: 154 revascularization surgeries in 140 affected hemispheres. Neurosurgery. 2013;73:430–9. https://doi.org/10.1227/NEU.0000000000000017.CrossRefPubMedGoogle Scholar
- 16.Hallemeier CL, Rich KM, Grubb RL Jr, et al. Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke. 2006;37(6):1490–6. https://doi.org/10.1161/01.STR.0000221787.70503.ca.CrossRefPubMedGoogle Scholar
- 17.Shirane R, Yoshida Y, Takahashi T, Yoshimoto T. Assessment of encephalo-galeomyo- synangiosis with dural pedicle insertion in childhood moyamoya disease: characteristics of cerebral blood flow and oxygen metabolism. Clin Neurol Neurosurg. 1997;99(suppl 2):S79–85 https://www.ncbi.nlm.nih.gov/pubmed/?term=Assessment+of+encephalo-galeomyo-+synangiosis+with+dural+pedicle+insertion+in+childhood+moyamoya+disease%3A+characteristics+of+cerebral+blood+flow+and+oxygen+metabolism.CrossRefGoogle Scholar
- 23.Molyneux A, Kerr R, Stratton I, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360(9342):1267–74 https://www.ncbi.nlm.nih.gov/pubmed/12414200.CrossRefGoogle Scholar
- 31.Parkinson RJ, Eddleman CS, Batjer HH, Bendok BR. Giant intracranial aneurysms: endovascular challenges. Neurosurgery. 2008;62(6 suppl 3):1336–45. https://doi.org/10.1227/01.neu.0000333798.67209.1f.CrossRefPubMedGoogle Scholar
- 32.Peluso JP, van Rooij WJ, Sluzewski M, Beute GN. Coiling of basilar tip aneurysms: results in 154 consecutive patients with emphasis on recurrent haemorrhage and re-treatment during mid- and long-term follow-up. J Neurol Neurosurg Psychiatry. 2008;79(6):706–11. https://doi.org/10.1136/jnnp.2007.127480.CrossRefPubMedGoogle Scholar
- 33.Jahromi BS, Mocco J, Bang JA, et al. Clinical and angiographic outcome after endovascular management of giant intracranial aneurysms. Neurosurgery. 2008;63(4):662–74. https://doi.org/10.1227/01.NEU.0000325497.79690.4C.CrossRefPubMedGoogle Scholar
- 35.Polevaya NV, Kalani MY, Steinberg GK, Tse VC. The transition from Hunterian ligation to intracranial aneurysm clips: a historical perspective. Neurosurg Focus. 2006;20(6):E3 https://www.ncbi.nlm.nih.gov/pubmed/?term=The+transition+from+Hunterian+ligation+to+intracranial+aneurysm+clips%3A+a+historical+perspective.CrossRefGoogle Scholar
- 36.Torigai T, Mase M, Ohno T, et al. Usefulness of dual and fully automated measurements of cerebral blood flow during balloon occlusion test of the internal carotid artery. J Stroke Cerebrovasc Dis. 2013;22(3):197–204. https://doi.org/10.1016/j.jstrokecerebrovasdis.2011.07.015.CrossRefPubMedGoogle Scholar
- 37.Jabbour P, Chalouhi N, Tjoumakaris S, et al. The pipeline embolization device: learning curve and predictors of complications and aneurysm obliteration. Neurosurgery. 2013;73(1):113–20. https://doi.org/10.1227/01.neu.0000429844.06955.39.CrossRefPubMedGoogle Scholar
- 44.Kalani MY, Kalb S, Martirosyan NL, Lettieri SC, Spetzler RF, Porter RW, et al. Cerebral revascularization and carotid artery resection at the skull base for treatment of advanced head and neck malignancies. J Neurosurg. 2013;118:637–42. https://doi.org/10.3171/2012.9.JNS12332.CrossRefPubMedGoogle Scholar
- 45.Sorenson TJ, Zaed I, Rangel-Castilla L, Lanzino G. Endovascular occlusion of epidural spinal dural arteriovenous fistula: 2-dimensional operative video. Oper Neurosurg (Hagerstown). 2018 Dec 1;15(6):726. https://doi.org/10.1093/ons/opy031.Noabstractavailable.CrossRefGoogle Scholar