Asian Journal of Neurosurgery

ORIGINAL ARTICLE
Year
: 2016  |  Volume : 11  |  Issue : 3  |  Page : 240--254

The “focus on aneurysm” principle: Classification and surgical principles of management of concurrent arterial aneurysm with arteriovenous malformation causing intracranial hemorrhage


Vikas Jha1, Sanjay Behari1, Awadhesh K Jaiswal1, Kamlesh Singh Bhaisora1, Yogesh P Shende1, Rajendra V Phadke2,  
1 Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
2 Department of Radiology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India

Correspondence Address:
Dr. Sanjay Behari
Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow - 226 014, Uttar Pradesh
India

Abstract

Context: Concurrent arterial aneurysms (AAs) occurring in 2.7-16.7% patients harboring an arteriovenous malformation (AVM) aggravate the risk of intracranial hemorrhage. Aim: We evaluate the variations of aneurysms simultaneously coexisting with AVMs. A classification-based management strategy and an abbreviated nomenclature that describes their radiological features is also proposed. Setting: Tertiary care academic institute. Statistics: Test of significance applied to determine the factors causing rebleeding in the groups of patients with concurrent AVM and aneurysm and those with only AVMs. Subjects and Methods: Sixteen patients (5 with subarachnoid hemorrhage and 11 with intracerebral/intraventricular hemorrhage; 10 with low flow [LF] and 6 with high flow [HF] AVMs) underwent radiological assessment of Spetzler Martin (SM) grading and flow status of AA + AVM. Their modified Rankin's score (mRS) at admission was compared with their follow-up (F/U) score. Results: Pre-operative mRS was 0 in 5, 2 in 6, 3 in 1, 4 in 3 and 5 in 1; and, SM grade I in 5, II in 3, III in 3, IV in 4 and V in 1 patients, respectively. AA associated AVMs were classified as: (I) Flow-related proximal (n = 2); (II) flow-related distal (n = 3); (III) intranidal (n = 5); (IV) extra-intranidal (n = 2); (V) remote major ipsilateral (n = 1); (VI) remote major contralateral (n = 1); (VII) deep perforator related (n = 1); (VIII) superficial (n = 1); and (IX) distal (n = 0). Their treatment strategy included: Flow related AA, SM I-III LF AVM: aneurysm clipping with AVM excision; nidal-extranidal AA, SM I-III LF AVM: Excision or embolization of both AA + AVM; nidal-extranidal and perforator-related AA, SM IV-V HF AVM: Only endovascular embolization or radiosurgery. Surgical decision-making for remote AA took into account their ipsilateral/contralateral filling status and vessel dominance; and, for AA associated with SM III HF AVM, it varied in each patient based on diffuseness of AVM nidus, flow across arteriovenous fistula and eloquence of cortex. Follow up (F/U) (23.29 months; range: 1.5-69 months) mRS scores were 0 in 12, 2 in 2, 3 in 1 and 6 in 1 patients, respectively. Conclusions: Patients with intracranial AVMs should be screened for concurrent AAs. Further grading, management protocols and prognostication should particularly “focus on the aneurysm.”



How to cite this article:
Jha V, Behari S, Jaiswal AK, Bhaisora KS, Shende YP, Phadke RV. The “focus on aneurysm” principle: Classification and surgical principles of management of concurrent arterial aneurysm with arteriovenous malformation causing intracranial hemorrhage.Asian J Neurosurg 2016;11:240-254


How to cite this URL:
Jha V, Behari S, Jaiswal AK, Bhaisora KS, Shende YP, Phadke RV. The “focus on aneurysm” principle: Classification and surgical principles of management of concurrent arterial aneurysm with arteriovenous malformation causing intracranial hemorrhage. Asian J Neurosurg [serial online] 2016 [cited 2019 Dec 12 ];11:240-254
Available from: http://www.asianjns.org/text.asp?2016/11/3/240/145340


Full Text

 Introduction



Hemorrhage is a serious complication in approximately 50% of patients having an intracranial arteriovenous malformation (AVM).[1],[2] Concurrent arterial aneurysms (AAs), occurring in nearly 2.7-16.7% patients harboring an AVM, significantly increase the risk of hemorrhage.[3] In this situation, a non-invasive diagnostic evaluation utilizing either a computed tomography (CT) or magnetic resonance (MR) angiography often fails to pinpoint the precise source of the bleeding. No uniform classification system exists that qualifies the features of the aneurysm (such as size, direction of its neck or fundus, the proximity of the two entities and the dominance of parent vessel) and correlates it with the characteristics of the parent malformation. The association of aneurysms with AVMs also significantly influences treatment decisions and management protocols.

This study attempts to evaluate the variations of AAs coexisting with AVMs in patients who presented with either subarachnoid or intracerebral hemorrhage. It also attempts to formulate a treatment strategy for concurrent aneurysms with AVMs that incorporates both their individual management considerations as well as their relationship to one another and with the parent vessels.

 Subjects and Methods



Inclusion criteria

Sixteen patients presenting with subarachnoid hemorrhage (SAH), intracerebral hematoma or both and harboring a concurrent intracranial AA with AVM who underwent either surgery or an interventional procedure between January 2006 and December 2011 were included in this study. Their clinical presentation and timing from the onset of ictus/ first symptom were noted. The angioarchitecture of the aneurysm as well as the AVMs and their supporting arteries and the draining veins were assessed utilizing CT/MR angiogram as well as digital subtraction angiogram (DSA).

Classification of aneurysms

The aneurysms were classified into 9 categories depending upon their location relative to the coexisting AVM. This was based upon a modification of the classifications suggested by Redecop et al. and Cunha e Sa et al. [Table 1].[4],[5]Flow related proximal aneurysms were located on the proximal arteries that were specifically supplying the AVM and included the supraclinoid internal carotid artery (ICA) and the circle of Willis, the middle cerebral artery (MCA) until and including the primary bifurcation, the A1 segment of anterior cerebral artery (ACA) and the anterior communicating artery (A Comm A), or the vertebrobasilar trunk [Figure 1] and [Figure 2]. Flow related distal aneurysms were located on the arteries supplying the AVM and beyond the location of these major vessels but with a significant distance from the actual nidus of the AVM. Intranidal aneurysms were located within the AVM nidus and could be distinguished from arterial ectasias and venous aneurysms by their early filling during the arterial phase of the angiogram [Figure 3]. Intra- and extra nidal aneurysms included the simultaneous existence of both intranidal aneurysm and aneurysm in close proximity to the nidus of the AVMs [Figure 4]. The latter arose from arterial branches that formed one of the peripheral vessels of the conglomeration of the AVM nidus and could be easily distinguished from it on early arterial phase of angiography. In contrast to the flow related distal aneurysms that have the possibility of being at a considerable distance from the AVM, the intra and extranidal aneurysms were situated in and around the main nidus, respectively and were always surgically accessible along with the AVM nidus. Remote major ipsilateral aneurysms were situated on a major artery of circle of Willis unrelated to the AVM but were getting filled on ICA/vertebral injection ipsilateral to the side of AVM [Figure 5] and [Figure 6]. Remote major contralateral aneurysms were also situated on a major artery of the circle of Willis unrelated to the AVM but were getting filled on ICA/vertebral injection contralateral to the side from where the vessels that were supplying the AVM were filling [Figure 7]. Deep perforator related aneurysms were situated on deep perforator vessels proximal and ipsilateral to the side of AVM [Figure 8]. Superficial aneurysms were aneurysms arising from one of the abnormal unnamed arterial branches supplying the AVM and traversing superficially on the cortical surface. Finally, distal aneurysms were situated on the feeding artery beyond the location of the AVM.{Table 1}{Figure 1}{Figure 2}{Figure 3}{Figure 4}{Figure 5}{Figure 6}{Figure 7}{Figure 8}

Classification of AVMs

The AVMs were assigned Spetzler-Martin (SM) grade (by evaluating their size, number of draining veins and eloquence of the part of the brain they were situated in).[6] The classification of the AVMs (based upon the degree of arteriovenous shunt present) into a high flow (HF) and a low flow (LF) state was determined based upon the length of time required for venous filling to occur after arterial filling according to the criteria suggested by Brown et al.[7] Thus, HF AVMs had an almost simultaneous filling of their arteriovenous compartment; in the LF AVMs however, there was a considerable delay (more than 2 s) in the time to venous filling after the arterial filling was complete.

An abbreviated nomenclature for concurrent aneurysms with AVMs presenting with intracranial hemorrhage

The CT/MR imaging was studied to determine whether the aneurysm or the AVM had undergone hemorrhage. Following a detailed assessment of their radiological imaging and the four parameters [anatomical relation of aneurysm with AVM, SM grading, high/low flow status of the AVM and the origin of subarachnoid/intracerebral hemorrhage being from either aneurysm or AVM; [Table 1], these patients were assigned an abbreviated nomenclature that helped to determine their therapeutic intervention. The aneurysm (an) associated with the AVM was assigned a numerical value based upon its category given in [Table 1]. The AVM was also assigned a numerical value based upon the SM grade and, the “HF” or “LF” status based upon the prevalent high or low flow arteriovenous shunting, respectively, in them. The asterix designated whether the aneurysm or the AVM had been responsible for the intracranial hemorrhage. If the hemorrhage was not distinguishable as being from either the aneurysm or the AVM (especially in cases of nidal aneurysms), the asterix was assigned to both the aneurysm and the AVM category. If the hemorrhage was remote from the primary site of both the aneurysm or the AVM, the asterix was omitted. However, none of our patients had bleeding away from the site of the AVM and the aneurysm.

Therapeutic interventions

In this series, only patients associated with the simultaneous presence of AVM and aneurysm who presented with SAH/intracerebral hematoma were included. Evacuation of the clinically significant hematoma to relieve raised intracranial pressure, surgical clipping of the aneurysm (or occasionally, excision of the intra-nidal or extra-intra nidal aneurysm with the AVM), excision of the AVM, direct or staged embolization of the AVM and stereotactic radiosurgery were the therapeutic options available. The patients were assigned a modified Rankin's score (mRS) [Table 2][8],[9] and a Fisher's score (based upon the CT/MR image in the patients presenting with SAH) at admission and compared with the score at the last follow-up.{Table 2}

 Results



Demographic profile

The sixteen patients having the simultaneous presence of an intracranial aneurysm and AVM represented 2.56% of patients who had undergone surgical clipping for isolated intracranial aneurysms (n = 623); or 17.5% (n = 91) of patients who had undergone either surgical excision (n = 72) or therapeutic embolization (n = 29) for their isolated AVMs during the same time frame. Out of the later, 75 patients with an isolated AVMs had undergone an intracranial (subarachnoid or lobar) hemorrhage.

Clinical spectrum

The mean age of presentation in the series was 38.31 years (age range 12-60 years). The male:female ratio was 10:6. Their clinical presentation is summarized in [Table 3]. All of them presented with a sudden onset of symptoms (sudden headache with recurrent vomiting in 15 occasionally with neck stiffness or grand mal seizures and, sudden onset hemianopia in 1 patient) heralding the emergent development of either an intracerebral/intraventricular hematoma (n = 10) or SAH (n = 5). Transient loss of consciousness, alteration of sensorium, hemiparesis, ataxia and hemianopia were the associated clinical manifestations. Their mRS at admission was 0 in 5, 2 in 6, 3 in 1, 4 in 3 and 5 in 1 patients, respectively.[8],[9] The mean duration of presentation was 199.43 days but the range was extremely variable (2-190 days). Noteworthy was the fact that 9 out of the 16 patients presented for DSA and definitive treatment for their underlying aneurysm and AVM after a delay of 2 weeks or more following their initial ictus. One of them (patient 10) presented nearly 6 years after the first symptom appeared.{Table 3}

Radiological features

Five patients presented with SAH. The location of the bleed included interhemispheric fissure with gyrus rectus (n = 2), sylvian fissure, cistern magna or interpeduncular and suprasellar cistern (n = 1 each, respectively). Three of these 5 patients having SAH were in Fisher's grade IV with intraventricular extension of the hemorrhage and one each were in grade II and III, respectively. Eleven other patients presented with intracerebral hematoma that usually included surfacing hematomas in the frontal, temporo-occipital or posterior parietal regions and the infratentorial supracerebellar surface. Two of these patients, however, presented with deep seated hematomas in the basal ganglionic region and the caudate nucleus-lateral ventricular location; and, two others with a primary intraventricular hematoma [Table 4]. In 5 patients, aneurysmal rupture and in 2 patients, rupture of the AVM, caused the subarachnoid/intracerebral hemorrhage. In 9 patients, the concurrent AVM and aneurysm were in close proximity and so it was not possible to distinguish the etiology of hemorrhage. Six of these patients had an intranidal aneurysm and one each respectively, had an intra- and extranidal aneurysm, a deep seated perforator related aneurysm with AVM and an aneurysm on a superficial cortical branch in close proximity to the AVM.{Table 4}

The aneurysms associated with AVMs in the present series belonged to the following categories: (I) Flow related proximal [n = 2, [Figure 1] and [Figure 2]]; (II) flow related distal (n = 3); (III) intranidal [n = 5, [Figure 3], [Figure 9] and [Figure 10]; (IV) both extra- and intranidal [n = 2, [Figure 4]; (V) remote major ipsilateral [n = 1, [Figure 5] and [Figure 6]; (VI) remote major contralateral [n = 1, [Figure 7]; (VII) deep perforator related [n = 1, [Figure 8]; (VIII) superficial (n = 1); and (IX) distal (n = 0) [Table 1]. Apart from a single giant basilar top aneurysm, the rest were small to medium sized aneurysms. The aneurysms had a fairly widespread location on blood vessels of the circle of Willis or their branches, namely the A comm A (n = 3), MCA (n = 5), posterior cerebral artery (n = 4), distal ACA (n = 1), basilar bifurcation (n = 1), anterior inferior cerebellar artery (n = 1) and posterior inferior cerebellar artery (n = 1).{Figure 9}{Figure 10}

The AVMs were located in the frontal (n = 2), temporal/perisylvian (n = 5), parietal (n = 2), occipital (n = 2), basal ganglionic/lateral ventricular (n = 3); or cerebellar (n = 2) locations [Table 4]. Their SM grade was I in 5, II in 3, III in 3, IV in 4 and V in 1. Ten patients had a LF and six, a HF AVM [Table 1]. In 7 of these patients, the AVM was located in the eloquent cortex.

The procedures performed are summarized in [Table 5]. Clipping of the aneurysm and excision of the AVM was performed in 4 patients (Patient 1, 3, 4, and 7) and excision of both AVM and aneurysm in 2 patients (Patient 5 and 11). The procedure was staged and two separate craniotomies made in a patient who had ACA dominance and A Comm A aneurysm filling from the side contralateral to that harboring the frontal AVM [Patient 7, [Table 5], and [Figure 7]. Two patients with an intranidal HF AVM in deep seated basal ganglionic/intraventricular location and in SM grade 4 and 5 respectively [patients 8 and 12, [Figure 8] and [Figure 10] were only administered stereotacic radiosurgery. Five patients (4 with intranidal aneurysms [patients 9, 13, 14, 15] and one with aneurysm on superficial cortical branch supplying the AVM [patient 16]) underwent direct embolization of the AVM as well as the aneurysm. One patient each respectively, underwent clipping of the aneurysm and stereotactic radiosurgery of the AVM (Patient 2), and clipping of aneurysm with staged embolization of AVM (patient 6) [Table 5].{Table 5}

One patient who underwent excision of the AVM and clipping of the A Comm A aneurysm died due to development of post-operative extradural hematoma and septicemia. One patient had improved significantly in neurological status at discharge (modified Rankin's grade 2) and at first follow-up with resolution of the ganglionic hematoma and had been referred for stereotactic radiosurgery but was later on lost to long-term follow up. At follow-up ranging from 1.5 to 69 months (mean follow-up: 23.29 months), 12 patients had normalization of neurological disability (modified Rankin's grade 0), 2 were in grade 2 and 1 in grade 3, respectively [Table 5].[7],[8],[9] One other patient, following successful clipping of the A comm A aneurysm, is undergoing a staged embolization of the AVM with onyx glue [patient 6, [Figure 5] and [Figure 6]]. The patients were referred to another center for radiosurgery where the following protocol for radiosurgery was utilized. The radiation used for SM grade 4 and 5 was 17-20 Gy with follow-up every 6 months for the 1st year and then every year thereafter. A residual AVM usually warranted a repeat radiosurgery and/or microsurgery depending upon its accessibility and grade. A pre-radiosurgery embolization was also a part of the armamentarium for the multimodality strategy for these AVMs. The rationale for decision making due to the simultaneous presence of aneurysm with AVM is summarized in [Table 6].{Table 6}

 Discussion



Combined culpability of concurrent AVM and aneurysm

The simultaneous presence of an aneurysm with an AVM introduces several additional management dilemmas apart from those related to their individual natural histories. Firstly, aneurysms and AVMs are both prone to bleed; the presence of concurrent aneurysms either within the nidus, close to it or even remotely situated, increases the risk of hemorrhage associated with AVMs several folds.[2],[10],[11] An escalation in annual risk of 7% for intracranial hemorrhage in patients harboring unruptured AVMs with a concurrent AA compared with a 1.7% annual risk for patients with an AVM but without an aneurysm has been reported.[7] From the time of its diagnosis, a 9.8% hemorrhage rate of an AA is significantly higher than the 2-4% annual risk of hemorrhage associated with AVM alone.[5] Histology has also confirmed that these AAs are thin walled and devoid of elastic fibers or a thick muscular element. They are exposed to the same arterial pressures as arterial components of the AVM and are therefore prone to bleed.[12] Secondly, determining the etiology of the hemorrhage often becomes difficult.[5],[13] In 9 of our patients with an intranidal, intra- and extranidal, deep perforator related or superficial aneurysms, it was not possible to distinguish whether the aneurysm or the AVM had bled. Thirdly, aneurysms and AVMs may occur on remote vessels and may represent a coincidental phenomenon or may represent an underlying vascular anomaly, hemodynamic alteration, vasoactive stimuli or the action of growth factors, leading to vascular remodeling.[3],7,[14],[15],[16] The latter are conditions that may need to be identified and suitably modified to prevent recurrence. Fourthly, the rapidity of flow through the AVM and its SM grade would determine its resectibility. Institution of endovascular embolization or stereotactic radiosurgery as a primary or adjunctive therapy may often be necessary in higher grade AVMs with rapid fistulous connections.[12],[16] This would fail to concurrently take care of the associated small but potentially risky aneurysms without an adequate neck that are often associated with AVMs. Fifthly, appropriate management of the aneurysm would often depend upon its distance from the coexisting AVM and its anatomical characteristics. Finally, it is not clear if the two entities need to be managed simultaneously or separately and which of conditions should be addressed first? Initial elimination of the AVM may initiate hemodynamic alterations that may lead to regression of the associated aneurysm;[3],[17] conversely, AVM excision may increase the blood flow in feeding arteries and increase the risk of aneurysm rupture.[1]

The present classification

The traditional classification of concurrent AAs associated with AVMs proposing the categories of flow related aneurysms, nidal aneurysms and remote aneurysms has withstood the test of time and also has therapeutic and prognostic implications.[4],[5],[10],[12],[16],[18] While retaining the basic framework of the original classification, in this study, a more comprehensive sub-categorization has been offered that perhaps will cover all clinical variations of AAs coexisting with AVMs. It has been recognized that any management protocol for concurrent aneurysms with AVMs does not depend solely on the type of aneurysm present but also on whether the aneurysm or the AVM has bled [5] and the SM grade along with the flow status of the AVM.[6] A useful abbreviated nomenclature that succinctly summarizes the varying clinical situations in which intracranial AAs and AVMs coexist has also been included.

The rationale for our classification was based on the differences between groups with regard to the approach and feasibility of surgical obliteration of the aneurysms and AVMs. The flow related proximal aneurysms existed on major arteries of the circle of Willis while the flow related distal aneurysms were based on distal branches of circle of Willis that were supplying the AVM but at a distance from the nidus.[4],[5],[10],[18] Nidal aneurysms were situated within the AVM nidus while the extranidal aneurysms were situated on one of the peripheral nidal vessels with the aneurysm in close proximity but clearly distinguishable from the nidus of the AVM.[5] This differentiation would be necessary in a clinical scenario since it would often be possible to excise the intranidal and intra- and extranidal aneurysms along with the AVMs. Flow related aneurysms (whether proximal or distal), on the other hand, would usually require an additional focus on clipping/embolization of the aneurysm often utilizing a staged and/or separate approach for addressing the AVMs. Deep perforator related aneurysms may be associated with HF AVMs in eloquent regions of the brain and may not be suitable for surgical resection. A distal aneurysm uniquely occurs distal to the AVM on the feeding vessel while the superficial aneurysm occurs on one of the unnamed superficial cortical branches that has undergone a pathological dilatation and alteration of course to supply the AVM.[4]

Surgical planning for clipping of the aneurysm and excision of the AVM would also often be determined by the angiographic dominance of the circulation and the direction of fundus of the aneurysm. Thus, remote aneurysms could be divided into two categories: One where the aneurysm was being filled by the ipsilateral circulation harboring the AVM; and other, where the aneurysm was getting filled by the contralateral dominant circulation (so that the surgical approach would entail separate, staged craniotomies on either side to obliterate the two entities). This was well exemplified in our two patients with A Comm A aneurysms located on vessels remote from the feeding artery of the AVM (patients 6 and 7). In one of them, the circulation ipsilateral to, while in the other, the circulation contralateral to the side of the AVM was the dominant one and filling the aneurysm. The surgical approach, therefore, had to be tailored accordingly. It is also evident from this series that simultaneous decision making for the obliteration of AVMs would necessarily entail evaluating their flow status and SM grade. Thus, surgical excision in a LF SM grade I and II AVM would be preferable to endovascular obliteration; however, therapeutic embolization or stereotactic radiosurgery would be the more suitable option in SM grade IV and V, HF AVMs.

Emerging recommendations

Despite variations in management of individual patients in our series, some salient points emerged. Firstly, in SM grade I, II and III LF AVMs associated with flow related proximal or distal aneurysms that are surgically accessible through the same route as the coexisting AVM, surgical excision of the AVM with clipping of the aneurysm may be the most preferable option. If the AVMs and the aneurysms are not surgically accessible by the same route, a staged surgery using different corridors, endovascular embolization or surgery for the aneurysm and stereotactic radiosurgery for the AVM may be utilized. If the LF, grade I to III AVMs are associated with an intranidal or intra-extranidal aneurysm, then direct simultaneous excision of both the aneurysm and AVM may be performed. Decision making regarding flow related, intra- and intra-extranidal aneurysms associated with SM grade III, HF AVMs would, however, be variable and be based upon the eloquence of the cortex, their relative surgical accessibility, the diffuseness of the AVM and the rapidity of the arteriovenous fistula. Perhaps, therapeutic embolization of both; or, transarterial embolization of the aneurysm and steretotactic radiosurgery of the AVM would be the preferable option.

Surgical approach for remote ipsilateral or contralateral aneurysms associated with AVMs would need additional focus on the dominance of feeding vessels and the direction of fundus.

Finally, intranidal or intra-extranidal and deep perforator related aneurysms with a HF AVM in SM grade IV or V would not be considered for surgery and would solely require either therapeutic embolization or stereotactic radiosurgery or just observation.

Emphasis on surgical excision

In the present series, the role of surgery in facilitating immediate and definitive control of concurrent aneurysms with AVMS is emphasized.[4] However, wherever indicated, endovascular techniques or stereotactic radiosurgery were actively sought for their primary or adjunctive therapeutic potential.[13] Endovascular obliteration may induce thrombosis of aneurysms proximal to the AVM nidus as was observed in one of our patients (patient 9). It permits simultaneous access to flow related and remote aneurysms in conjunction with the AVM. Even staged partial embolization may help in eradicating the AVM nidus to prevent breakthrough bleeding.[12],[18],[19],[20] It may also help to overcome the steal phenomenon by improving the regional cerebral blood flow around the AVM.[12],[16],[21],[22]

We persisted with surgery in some of the cases due to several reasons. The AVMs associated with AAs were often having a LF; and, the aneurysm may be within or in close proximity to the AVM nidus. Tortuous arteries and multiple nidi of the AVM as well as small and multiple aneurysms within or around the AVM may often preclude its complete obliteration utilizing the endovascular route. HF arteriovenous fistulae may increase the risk of distal embolism of the embolic material with its potential to obstruct end arteries of the brain. Both staged therapeutic embolization and primary radiosurgery are relatively expensive and require a long latency period to effect thrombosis of the AVM during which there is a continued risk of hemorrhage from the unobliterated nidus. Larger AVMs are less likely to completely thrombose with stereotacic radiosurgery also.[12]

The “focus on the aneurysm” principle

The present study clearly demonstrates that in contrast to the population that harbors an AVM alone, AVM with AA is much more common in older patients and is rare in children. In support of this finding, Lasjuanias et al. in their study observed that only 8% of patients less than 25 years presented with AAs, while 37% of patients between 25 and 50 years had an aneurysm associated with an AVM.[2],[10] The presence of a concurrent aneurysm with the AVM, therefore, indicates an alteration in both the population characteristics as well as in the etiopathogenesis of the intracranial hemorrhage.

The simultaneous presence of an aneurysm with AVM often leads to a significant modification in the surgical planning. Aneurysms within or close to the AVM nidus may be too small to be clipped or coiled and may also not be obliterated utilizing endovascular technique or stereotacic radiosurgery. Aneurysms situated at a distance from the AVM, or even remotely (including those present contralaterally), may require additional/staged surgical or endovascular approaches.

The presence of AVM causing hemorrhage is not treated with the same degree of urgency as accorded to cases with aneurysmal SAH. This was aptly exemplified in our study where 9 out of the 16 patients harboring both an aneurysm and AVM were referred for DSA or MR/CT angiography and definitive treatment after a delay of 2 weeks or more following their initial ictus. This was despite the fact that the initial CT scan clearly pointed toward the presence of an AVM either due to the appearance of characteristic serpiginous vessel hyperdensities or due to the pattern of the lobar bleed. The emergent situation arising due to the simultaneous presence of an aneurysm and AVM with additional risk of hemorrhage is almost never considered under these circumstances and routine protocol is instituted for investigation and management of the suspected AVM. This study highlights that In the patients in whom an AVM is suspected as the primary cause of intracranial hemorrhage, special efforts must be undertaken to identify concurrent aneurysms. Further grading, institution of management protocols and prognostication should particularly “focus on the aneurysms.”

Limitations of the study

The personal evaluating outcome were not blinded to the treatment administered and were participating in the care of the patients. While we were fortunate to include patients representing most of the categories of aneurysms with AVMs in the series, one of the groups (group IX: distal) went unrepresented. The patients included in this series were those who were admitted for surgical or endovascular obliteration of the aneurysm with AVM due to the presence of intracranial hemorrhage. Therefore, all of them underwent an interventional or surgical procedure and none of them were followed without treatment.

Outcome assessment in a larger number of patients would have added further credence to the validity of our classification in predicting recommendations for management of patients having concurrent aneurysms with AVMs. Finally, the protocols of management were not always consistent and varied between individual patients. A prospective assessment of the proposed grading with rigid treatment protocols would perhaps sanctify standard of care in these patients.

 Conclusions



While encountering AVMs with intracerebral hemorrhage, special efforts must be undertaken to identify concurrent aneurysms. A comprehensive subcategorization of concurrent aneurysms as well as an abbreviated nomenclature has been offered that perhaps will cover all clinical variations of AAs coexisting with AVMs. A management protocol for concurrent aneurysms with AVMs has been proposed that depends on the type of aneurysm present, on whether the aneurysm or the AVM has bled and, the SM grade and the flow status of the AVM.

References

1Batjer H, Suss RA, Samson D. Intracranial arteriovenous malformations associated with aneurysms. Neurosurgery 1986;18:29-35.
2Hoffman C, Riina HA, Stieg P, Allen B, Gobin YP, Santillan A, et al. Associated aneurysms in pediatric arteriovenous malformations and the implications for treatment. Neurosurgery 2011;69:315-22.
3Deruty R, Mottolese C, Soustiel JF, Pelissou-Guyotat I. Association of cerebral arteriovenous malformation and cerebral aneurysm. Diagnosis and management. Acta Neurochir (Wien) 1990;107:133-9.
4Cunha e Sa MJ, Stein BM, Solomon RA, McCormick PC. The treatment of associated intracranial aneurysms and arteriovenous malformations. J Neurosurg 1992;77:853-9.
5Redekop G, TerBrugge K, Montanera W, Willinsky R. Arterial aneurysms associated with cerebral arteriovenous malformations: Classification, incidence, and risk of hemorrhage. J Neurosurg 1998;89:539-46.
6Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg 1986;65:476-83.
7Brown RD Jr, Wiebers DO, Forbes GS. Unruptured intracranial aneurysms and arteriovenous malformations: Frequency of intracranial hemorrhage and relationship of lesions. J Neurosurg 1990;73:859-63.
8Bonita R, Beaglehole R. Recovery of motor function after stroke. Stroke 1988;19:1497-500.
9Rankin J. Cerebral vascular accidents in patients over the age of 60. II. Prognosis. Scott Med J 1957;2:200-15.
10Lasjaunias P, Piske R, Terbrugge K, Willinsky R. Cerebral arteriovenous malformations (C. AVM) and associated arterial aneurysms (AA). Analysis of 101 C. AVM cases, with 37 AA in 23 patients. Acta Neurochir (Wien) 1988;91:29-36.
11Stapf C, Mohr JP, Pile-Spellman J, Sciacca RR, Hartmann A, Schumacher HC, et al. Concurrent arterial aneurysms in brain arteriovenous malformations with haemorrhagic presentation. J Neurol Neurosurg Psychiatry 2002;73:294-8.
12Marks MP, Lane B, Steinberg GK, Chang PJ. Hemorrhage in intracerebral arteriovenous malformations: Angiographic determinants. Radiology 1990;176:807-13.
13Meisel HJ, Mansmann U, Alvarez H, Rodesch G, Brock M, Lasjaunias P. Cerebral arteriovenous malformations and associated aneurysms: Analysis of 305 cases from a series of 662 patients. Neurosurgery 2000;46:793-800.
14Boyd-Wilson JS. The association of cerebral angiomas with intracranial aneurysms. J Neurol Neurosurg Psychiatry 1959;22:218-23.
15Suzuki J, Onuma T. Intracranial aneurysms associated with arteriovenous malformations. J Neurosurg 1979;50:742-6.
16Marks MP, Lane B, Steinberg GK, Snipes GJ. Intranidal aneurysms in cerebral arteriovenous malformations: Evaluation and endovascular treatment. Radiology 1992;183:355-60.
17Yasargil MG. AVM of the brain. History, embryology, pathological consideration, hemodynamics, diagnostic studies, microsurgical anatomy. In: Yasargil MG, editor. Microneurosurgery. Vol. IIIA. Stuttgart: Thieme Verlag; 1987. p. 57-62.
18Perata HJ, Tomsick TA, Tew JM Jr. Feeding artery pedicle aneurysms: Association with parenchymal hemorrhage and arteriovenous malformation in the brain. J Neurosurg 1994;80:631-4.
19Perret G, Nishioka H. Report on the cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Section VI. Arteriovenous malformations. An analysis of 545 cases of cranio-cerebral arteriovenous malformations and fistulae reported to the cooperative study. J Neurosurg 1966;25:467-90.
20Piotin M, Ross IB, Weill A, Kothimbakam R, Moret J. Intracranial arterial aneurysms associated with arteriovenous malformations: Endovascular treatment. Radiology 2001;220:506-13.
21Thompson RC, Steinberg GK, Levy RP, Marks MP. The management of patients with arteriovenous malformations and associated intracranial aneurysms. Neurosurgery 1998;43:202-11.
22Turjman F, Massoud TF, Viñuela F, Sayre JW, Guglielmi G, Duckwiler G. Aneurysms related to cerebral arteriovenous malformations: Superselective angiographic assessment in 58 patients. AJNR Am J Neuroradiol 1994;15:1601-5.