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Abstract
While the trend for endovascular therapy of posterior circulation aneurysms is permeating, cerebrovascular bypass remains essential in the armamentarium for complex lesions not amendable to these techniques. This review discusses the microsurgical anatomy of the posterior fossa intracranial circulation, as well as the techniques and outcomes related to cerebrovascular bypass.
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Introduction
The estimated prevalence of unruptured intracranial aneurysms (IA) in the general population varies widely and has been reported generally as between 1% and 3%.1–3 Attempts to predict rupture risk help to guide clinical care and treatment recommendations. When it does occur, subarachnoid hemorrhage from ruptured IA affects approximately 30 000 individuals in the USA annually with a high morbidity and mortality resulting in death in 50% of patients and functional impairment in more than 40% of survivors.4 5
Treatment for IA involves exclusion of the aneurysm from the intracranial circulation in the setting of saccular aneurysms or vascular reconstruction in the setting of fusiform aneurysms. Historically, microsurgical aneurysm clip obliteration has been the most common modality for the treatment of IA. This is sometimes combined with complex microsurgical revascularization techniques to ensure adequate cerebral perfusion and aneurysm obliteration.6–8 Recent studies have demonstrated that endovascular embolization with coil materials also represents a safe and effective treatment option.9–11 Intracranial stents have been employed to assist in the delivery of these embolization materials.12–14 Additionally, high viscosity liquid embolization agents have been used effectively, particularly in the treatment of distal posterior circulation IA.15 While the treatment of IA of the posterior fossa is complex, individual characteristics such as morphology and location, age and practitioner experience must be taken into consideration. Here we review the anatomical considerations, techniques and outcomes related to cerebral revascularization in the treatment of posterior fossa IA.
Methods
A PubMed search was performed to identify studies reporting patients treated with cerebrovascular bypass for the treatment of IA located in the posterior fossa. The terms ‘aneurysm’, ‘intracranial’ and ‘surgery’ were combined with the limitations of ‘English’ and ‘Human’. Manuscripts were then selected that reported the outcomes of cerebrovascular bypass involving the vertebral artery (VA), posterior inferior cerebellar artery (PICA), anterior inferior cerebellar artery (AICA), superior cerebellar artery (SCA) or the posterior cerebral artery (PCA). For each study, the number of patients and IA were identified. Details regarding the IA itself were recorded, such as aneurysm morphology (saccular or fusiform) and location. The primary treatment modality and the specific revascularization technique used were recorded. Outcomes such as graft patency, as well as perioperative morbidity and mortality, were identified. The average length of follow-up was calculated in months.
Anatomical considerations
Aneurysms of the posterior circulation comprise approximately 15% of all IA.16 17 Such lesions are located below the level of the tentorium and arise on the VA, the basilar artery (BA) or their branches up to the BA bifurcation.16 A subset are considered complex and may require revascularization procedures as part of treatment. Aneurysms within the posterior fossa are difficult to reach surgically and are located in close proximity to critical structures, such as the brainstem and cranial nerves. Their treatment is further complicated by variations in arterial distributions that make it difficult to predict the vessels that perfuse specific regions.18 Furthermore, the occlusion of certain segments may be clinically silent whereas sacrifice of other segments of the posterior circulation may result in neurological deficit or death due to brainstem or cerebellar infarction. Thus an intimate understanding of the anatomy of the posterior circulation anatomy and its relationship to surrounding structures is required for the surgical treatment of posterior fossa aneurysms. For complex aneurysms requiring revascularization, additional knowledge of the collateral circulation and brainstem perforators is needed for decisions regarding vessel sacrifice and bypass technique. The four major recipient vessels involved in cerebral revascularization of the posterior fossa are the PICA, AICA, SCA and PCA.19
Posterior inferior cerebellar artery
Of the cerebellar arteries, the PICA follows the most variable and tortuous course.20 PICA aneurysms make up approximately one-fifth of all IA, with an estimated incidence ranging from 0.5% to 3%.21 Two-thirds of PICA aneurysms arise at the VA-PICA junction, usually above the PICA origin, and point superiorly. The rest arise in peripheral segments and are known as distal PICA aneurysms.22
The PICA is divided into five segments based on its relationship to the medulla and cerebellum. The names of the segments, along with the aneurysm incidence for each segment, are as follows: anterior medullary (8%); lateral medullary (18%); tonsillomedullary (16%); telovelotonsillar (34%); and cortical (24%).22 23 The anterior medullary segment begins at the origin of the PICA at the VA and extends posteriorly to the inferior olivary prominence. Next, the lateral meduallary segment extends to the origins of the glossopharyngeal, vagus and accessory rootlets, and the tonsillomedullary segment extends medially across the posterior aspect of the medulla to the mid-level of the medial surface of the tonsil. The tonsillomedullary segment passes between the lower margin of the tonsil and the medulla and then turns rostrally, thereby creating a caudal loop, which is one of the largest distal vessels in the cerebellar arteries.23 The telovelotonsillar segment extends to the cortical surface of the cerebellum and ends between the tonsil and vermis on one side and the hemisphere on the other side. This segment may form a loop with a convex rostral curve, known as the cranial loop.23 Lastly, the cortical segment extends to the cerebellar vermis and hemisphere.22
For complex PICA aneurysms, segmental anatomy dictates the treatment approach, as certain segments give off perforating branches, thereby precluding vessel sacrifice. The anterior and lateral medullary segments, or proximal segments, contribute to the blood supply of the brainstem, whereas the supply by the tonsillomedullary segment, or transitional segment, is variable. The telovelotonsillar and cortical segments, or distal segments, do not supply the brainstem. Therefore, distal segments may be sacrificed without neurological compromise, as the leptomeningeal communicators, SCA and AICA are sources of collateral circulation.24 In general, bypass strategies are considered for aneurysms involving the proximal three segments, and sacrifice of distal vessels is considered safe without revascularization.19
Anterior inferior cerebellar artery
The AICA is the least likely of the major arteries of the posterior circulation to be affected by an aneurysm.25 AICA aneurysms account for less than 2% of all IA, and such aneurysms are more common proximally than distally.26
The AICA arises in cerebellopontine angle, commonly from the lower third portion of the BA, with a single, duplicate or triplicate origin in 72%, 26% or 2% of patients, respectively.27 The AICA is divided into three segments based on its relationship to the vestibulocochlear complex. The segments include the following: premeatal, or proximal segment, which extends from the origin of the AICA to the seventh and eighth cranial nerve complex; meatal segment, which gives off the internal auditory artery, recurrent perforating arteries and subarcuate artery; and the postmeatal, or distal segment, which is distal to the seventh and eighth cranial nerve complex. As the vessel approaches the eighth cranial nerve, it commonly bifurcates into rostral and caudal branches, with distal aneurysms occurring more commonly on the rostral branch.28 The AICA goes on to supply the cerebellum and merges with branches from the SCA or PICA.
Early in the course of the AICA, small perforators supply the brainstem; however, the distal branch of the AICA, distal to the internal auditory artery, can be occluded without neurological compromise.29 For lesions distal to branches coursing to the brainstem, trapping and aneurysm resection are viable options that do not require bypass.25
Superior cerebellar artery
The SCA is the most constant of the cerebellar arteries. Aneurysms arising from the distal portion of the SCA account for only 0.2% of all intracranial aneurysms.30 The SCA commonly arises from the BA, below the oculomotor nerve, and is divided into four segments. The SCA segments include the following: anterior pontomesencephalic, which begins at the origin of the SCA and extends to the anterolateral margin of the brainstem; lateral pontomesencephalic, which extends caudally to the lateral pons and then continues to the anterior cerebellomesencephalic fissue; cerebellomesencephalic, which courses through the cerebellomesencephalic fissure and gives rise to branches penetrating branches; and cortical, which gives rise to branches that pass under the tentorium.23 The distal portion passing below the tentorium is the most rostral of the infratentorial arteries. Alternatively, the SCA may be divided into a cisternal segment, consisting of anterior pontine, ambient, and quadrigmeninal segments, and a cortical segment, consisting of marginal, hemispheric, and verminan branches.30 Distal SCA aneurysms occur approximately with equal likelihood in the cisternal and cortical segments. SCA occlusion is well tolerated, likely because of collateral circulation supplied by the PICA and AICA.31 Anastomoses are especially common between the SCA and AICA.18
Posterior cerebral artery
Aneurysms of the PCA account for 0.7% to 2.3% of all intracranial aneurysms and most commonly arise from the anterior portion of the PCA.32 PCA aneurysms may form larger or dissecting-type aneurysms. The PCA arises as the terminal branch of the bifurcation of the proximal basilar and it is joined by the posterior communicating artery (PCOM) at the lateral margin of the interpeduncular cistern.23 The PCA encircles the brainstem and continues on to the posterior cerebral hemispheres. The PCA is divided into four segments, which include the following: P1 segment, or precommunicating segment, which is proximal to the PCOM artery; P2 segment, which extends from the PCOM artery to the entry point of the PCA into the quadrigeminal cistern; P3 segment, or quadrigeminal segment, which begins at the posterior midbrain and courses through the quadrigmeninal cistern; and P4 segment, which begins at the anterior limit of the calcarine fissure, after the origin of the parietooccipital and calcarine arteries. The P2 segment is subdivided into an anterior and posterior part.33 The anterior portion passes through the crural cistern and the posterior portion passes through the ambient cistern.
The PCA gives rise to three types of branches, which include the following: central perforating branches to the diencephalon and midbrain, which are divided into the direct and circumflex perforating arteries and include the thalamoperforating, peduncular perforating and thalamogeniculate arteries; ventricular branches to the choroid plexus and walls of the lateral and third ventricles and include the lateral and medial posterior choroidal arteries; and cerebral branches to the cerebral cortex and the splenium of the corpus collosum and include the inferior temporal group of branches.23 The inferior temporal group is divided into the anterior, middle, posterior and common temporal branches and the parietooccipital, calcarine and splenial branches. The long and short cirucumflex, thalamoperforating and medial posterior choroidal arteries arise predominantly from the P1 segment, and the other PCA branches commonly arise from the P2 or P3 segment.23 Anastomosis with donor vessels usually is performed at the anterior half of the P2 segment because it is essentially free of perforating vessels.46 The PCA receives collateral flow from the leptomeningeal collaterals. Additionally, when the P1 segment of the PCA or upper basilar is occluded, the PCOM artery commonly provides adequate flow.
Preoperative workup
Typically, detailed imaging of the cerebral vasculature is obtained when an IA is suspected or discovered. For complex aneurysms situated in the posterior intracranial circulation, an angiogram is performed to reveal detailed anatomy as well as dynamic characteristics of cerebral blood flow. This technique can be supplemented by transcranial Doppler studies and quantitative MR angiography.48 49 Some patients may undergo a balloon test occlusion to determine the suitability for permanent vessel sacrifice as a means of aneurysm obliteration.50 However, there are many situations where occlusion of the parent vessel or dissecting aneurysm is not possible, such as when the PICA originates from a dissecting aneurysm or when the contralateral VA provides inadequate collateral blood flow to the distal basilar circulation. For situations such as these, the utility of cerebrovascular revascularization is indisputable.
Techniques
Cerebrovascular bypass is an uncommon procedure associated with high morbidity and mortality rates. This procedure is typically reserved for high volume cerebrovascular centers where patient volume has been associated with fewer complications.51 Techniques associated with bypass in the posterior fossa are variations on a theme: they provide a means to exclude the offending aneurysm from the circulation while preserving blood flow to vital brain parenchyma. This can be accomplished in two broad categories: intracranial to intracranial bypass52 53 and extracranial to intracranial bypass. Permutations of these include in situ37 41 and transposition anastomotic techniques.54 Both arterial and venous grafts have been used with success.54–57 Ancillary measures, such as intraoperative blood flow determination and hypothermic arrest, have been used to improve the efficacy of this high risk procedure.58 59
Outcomes
Our literature search yielded 14 studies of patients undergoing revascularization procedures as part of treatment for complex aneurysms of the posterior fossa (table 1). Eight studies exclusively examined patients with bypass for posterior fossa aneurysms whereas relevant data were extracted from the remaining six studies, which included patients with vertebrobasilar insufficiency and anterior circulation aneurysms, in addition to patients with posterior circulation aneurysms. Only data on posterior fossa revascularization for complex aneurysms were collected.
Studies of patients undergoing revascularization procedures as part of treatment for complex aneurysms of the posterior fossa
Among the 74 patients, 34 were male (46%), 20 were female (27%) and the gender was unable to be extracted for the remaining 19 patients (26%). The mean reported age was 51.8±8.2 years and ranged from 5 to 77 years. The mean follow-up period was 15.6±13.3 months and ranged from 0.1 to 147 months.
Seventy-five aneurysms were treated in 74 patients. The location and frequency of posterior fossa aneurysms varied as follows: low or mid-BA (13 patients; 17%), BA apex or bifurcation (eight patients; 11%), AICA (one patients; 1%), VA-PICA junction (17 patients; 23%), PICA (13 patients; 17%), VA-BA junction (six patients; 8%) and VA (17 patient, 23%) (table 2). Among the treated aneurysms, 23 were fusiform, 22 were dissecting and 17 were giant (>2.5 cm).
Aneurysm location
Revascularization procedures included PICA-PICA anastomosis (19 patients; 25%), AICA-PICA side to side anastomosis (one patient; 1%), PICA reimplantation into AICA (one patient; 1%), PICA reimplantation into VA (one patient; 1%), ophthalmic artery-PICA (seven patients; 9%), superficial temporal artery-PICA (nine patients; 12%), superficial temporal artery-SCA (three patients; 4%), external carotid artery-SCA, external carotid artery-SCA, internal carotid artery-BA or VA-VA bypass with saphenous vein graft (22 patients; 29%), VA-PICA bypass with radial artery interposition graft (two patients; 3%) and external carotid artery-PCA, VA-PCA or middle cerebral artery-PCA bypass with radial artery interposition graft (10 patients; 13%) (table 3). The recipient vessel of the revascularization procedures included the PICA (41 patients; 55%), PCA (22 patients; 29%), SCA (five patients; 7%) or VA (five patients; 7%), AICA (one patient; 1%) and BA (one patient; 1%). In 48 patients, bypass was followed by proximal occlusion or aneurysm trapping, primarily by clipping, although endovascular coiling was used in at least three patients.
Bypass performed
Surgical approaches were reported in 37% of cases and included far lateral (five patients), subtemporal (three patients), retrosigmoid (one patient), lateral suboccipital (one patient), far lateral suboccipital (one patient), extreme lateral (five patients), transpetrosal (six patients), transpetrosal and extreme lateral (two patients) and frontotemporal-orbitozygomatic (four patients). Overall graft patency rate was 95% at the most recent follow-up, with 10 studies reporting 100% patency rates.
Methods of outcome assessment varied between studies. For studies using the Glasgow Outcome Scale (GOS) (n=4, 11 patients), five patients (45%) had GOS of 5, three patients (27%) had GOS of 4 and one patient (9%) had GOS <4. The perioperative mortality rate was 15%, with eight studies reporting no deaths. Causes of mortality included sepsis (three patients; 4%), brainstem infarction (two patients; 3%), subarachnoid hemorrhage (one patient; 1%), BA occlusion (four patients; 5%) and pulmonary embolism (one patient; 1%). The all-cause mortality rate was 19%. Perioperative complications included stroke, cranial nerve deficit (VI, VIII, X), seizure, locked-in syndrome, partial lateral medullary syndrome, ataxia, hemiparesis, subdural hematoma, conductive hearing loss, CSF leak and subdural hygroma. Non-neurological complications included pneumonia, myopathy of the quadriceps and wound infection (table 4).
Complications
Conclusion and future directions
Complex IA of the posterior circulation requiring cerebrovascular bypass are challenging entities. In our review of the literature, a periprocedural mortality rate of 15% underscores the difficulty in treating these lesions. With the introduction of flow diverting endovascular stents, it is likely that many IA previously excluded from endovascular treatment may now be treated with this emerging modality.60–63 Further refinements in microsurgical technique are likely to focus on intraoperative flow assessment with quantitative indocyanine green angiography,64 non-occlusive anastomotic technique,65 determination of optimum graft material and periprocedural care.
References
Footnotes
BPW and JMP contributed equally to this manuscript.
Competing interests None.
Provenance and peer review Commissioned; not externally peer reviewed.