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 Table of Contents  
REVIEW ARTICLE
Year : 2020  |  Volume : 8  |  Issue : 2  |  Page : 113-122

Diagnosis and treatment of basilar artery perforator aneurysm: A 20-year review with proposed treatment guidelines


1 Department of Neurosurgery, Manipal Hospital Whitefield, Bengaluru, Karnataka, India
2 Department of Neurosurgery, National Institute of Mental Health and Neurological Sciences, Bengaluru, Karnataka, India

Date of Submission16-Oct-2020
Date of Acceptance28-Nov-2020
Date of Web Publication3-Feb-2021

Correspondence Address:
Dr. Sibhi Ganapathy
Department of Neurosurgery, Manipal Hospital Whitefield, Bengaluru, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcvs.jcvs_26_20

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  Abstract 


Introduction: Aneurysms of the vertebrobasilar system comprise approximately 10%–15% of all intracranial aneurysms and most occur at the bifurcation of the basilar artery. Posterior circulation perforator artery aneurysms are sparsely reported in the literature. The natural history of these rare lesions remains unclear and their diagnosis and management are not well defined.
Materials and Methods: All case reports and case series from the past 20 years were analysed, and the results tabulated. Based on broad trends, guidelines were proposed for management.
Results: Forty-two cases from 22 case reports and case series were analysed. Most were managed endovascularly, with a complication rate approaching 43%. Observation was another popular treatment option with however a comparable morbidity of 42% only surgery proved to be better overall. Aneurysm size was inversely correlated with complication rate with smaller lesions more prone to rupture and complications. The nature of the perforating artery was also found to be a factor, where direct brain stem perforators from the upper two-third of the basilar artery were found to be difficult to treat both by surgery and endovascular methods, leading to significant failures and complications as compared to the wider circumflex perforating arteries.
Conclusion: Scarce published literature that addresses the limited understanding of the natural course of this entity lead to difficulties in proposing broad-based recommendations that are fail proof. Nevertheless, we hope this analysis of 20 years of data helps in shedding light on this difficult disease and its possible treatment options along with risks and outcomes.

Keywords: Basilar artery perforator aneurysm, endovascular coiling, flow diverter, microsurgical clipping, stenting, vessel trapping


How to cite this article:
Ganapathy S, Lingaraju T S. Diagnosis and treatment of basilar artery perforator aneurysm: A 20-year review with proposed treatment guidelines. J Cerebrovasc Sci 2020;8:113-22

How to cite this URL:
Ganapathy S, Lingaraju T S. Diagnosis and treatment of basilar artery perforator aneurysm: A 20-year review with proposed treatment guidelines. J Cerebrovasc Sci [serial online] 2020 [cited 2021 Oct 24];8:113-22. Available from: http://www.jcvs.com/text.asp?2020/8/2/113/308631




  Introduction Top


Intracranial aneurysms arising from the perforating branches of the basilar artery perforator aneurysm (BAPAs) are extremely rare. The initial description of these unusual location aneurysms was done by Ghogawala in 1996.[1] So far, very few published cases of ruptured BAPAs treated using endovascular techniques exist in literature. These ruptured aneurysms are not easily accessible for microvascular clipping/trapping but are very technically challenging to manage endovascularly. These technical difficulties are due to the retrobasilar location, tiny diameter of the perforators, and the small size of such aneurysms.[1] Successful endovascular coiling ALONE as primary and single mode of treatment is exceedingly rare with only a few articles of successful endovascular management published so far, the most recent being the publication of Gopal et al. reporting a case of coil-embolisation of a ruptured aneurysm arising from the intrapontine perforating artery in 2019.[1]

We present a review of all cases of BAPA aneurysms reported in the literature over the past 20 years and analyse the management of ruptured complex BAPA aneurysms, to reach treatment guidelines so that future generations do not have to reinvent the wheel in diagnosis and treatment.


  Materials and Methods Top


All case reports and series accessible from PubMed and Google Scholar from 200 to 2020 were accessed and investigated. The results were tabulated, and inferences were gleaned from the data collected. Based on the results obtained, broad treatment guidelines were proposed.


  Results Top


A total of 42 cases from 22 publications were tabulated and analysed for management protocols and difficulties faced [Table 1].
Table 1: Details of Documented Cases in Literature of Basilar Artery Perforator Aneurysms from 2000 to 2020

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Most aneurysms presented with high-grade subarachnoid bleeds which resulted in symptoms ranging from prostration to focal neurological deficits. Despite the acute nature of the presentation and the immediate application of cerebral angiography, only few were detected on the first angiogram. As per our data, only 28% (12) [Figure 1] of the patients had early detection of their aneurysm by the first angiogram. Possible reasons include, small calibre of the aneurysm, small calibre of the feeding vessel, possibility of thrombosis of either the aneurysm or the feeding vessel post-sentinel bleed or vasospasm of the feeding vessel causing the aneurysm not to fill on angiogram.
Figure 1: Percentage of detection of aneurysms on first angiogram. Nearly 63% weren't detected in the first angiogram

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Regardless, the lesion fills later on a second angiogram subsequently done either as routine practice or on further symptomatology precipitated by a second bleed. Most aneurysms were borne on perforators from either the upper or middle one-third of the basilar artery system (92% or 39 aneurysms) [Figure 2].
Figure 2: Distribution of Aneurysm incidence. Most Aneurysms arise from the direct brainstem perforators (93%) and a vast majority arise either from the upper 1/3rd or the middle 1/3rd of the basilar artery. Circumflex branches are rare and arise from the upper 2/3rd of the basilar trunk

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The perforators from which they arose can be classified as either intrapontine or intra-brainstem perforators or circumflex perforators. The intra-brain stem perforators are small short vessels that immediately exit the basilar trunk and head deep into the substance of the brainstem. Aneurysms arising from these vessels are small and positioned behind the basilar trunk making access difficult. Repeated angiograms are required to detect such aneurysms owing to the small calibre of vessel and aneurysm along with associated possibilities such as thrombosis or vasospasm. These aneurysms are difficult to access microsurgically and may require extreme dexterity in handling. Complications hence are common, leading to perforator brain stem infarcts and hemiplegia, which may or may not improve later with rehabilitation therapy. Circumflex perforators are longer and have a larger calibre. Therefore, they support larger more accessible aneurysms. The access being better, both surgery and endovascular therapy are attempted here (92% are direct perforators versus just two cases with circumflex perforators [Figure 3]).
Figure 3: The complication rates of the different treatment modalities. Endovascular treatment has a complication rate of 49% followed closely by observation (42%) and then by surgery (33%). The overall complication rate of this disease remains a staggeringly high 43%

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With regard to therapy, three possibilities exist which may be attempted either alone or as a combination protocol. The first is endovascular therapy. Endovascular treatment has been shown by both START and BRAT trials to be preferable for posterior circulation aneurysms. However, the modality has many options which may either tried in exclusion or in concert with other options. Of the 42 aneurysms treated, 21 were managed endovascularly. These included either coiling, stent-assisted coiling or flow diverter placement [Figure 4].
Figure 4: The comparisons of different modalities with their respective complications

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Flow diverters while being expensive are the best modality as they maintain the integrity of the vessel and reduce flow through the aneurysm. Long-term angiogram surveillance shows the complete obliteration of the aneurysms with minimal complications. Coiling is risky due to the possibility of rupture. Another important problem associated with endovascular management is the difficulty in negotiating hardware through the narrow vascular tree of the basilar system. Complications and stroke rates are higher than flow diverters but still acceptable [Figure 4].

Open surgery is advantageous as it allows the direct visualisation of the aneurysm. The techniques for access may vary with Orbitozygomatic approach through the Lilliquist membrane preferred for upper one-third basilar lesions and middle cranial fossa approach for middle one-third basilar aneurysms. Surgery is difficult due to the difficult access to the basilar region, as well as aneurysms located posteriorly to the artery wedged between the basilar artery and the brain stem substance, often leading to damage while clipping. Circumflex arteries perform better here with a smaller complication rate. If the perforator is visible yet small, the trapping the aneurysm by parent vessel ligation or clipping can also be contemplated. Such a modality will inevitably lead to long-term complications. Hence, care is to be taken in using this technique [Figure 4].

The last mode of therapy is neuro-observation or conservative therapy, where efforts are made to correct complications such as vasospasm and raised intracranial pressure, but little is done directly to treat the aneurysm per se long-term follow up for the aneurysms shows good resolution rates along with minimal risks in rebleeds in such small diameter aneurysms [Figure 4].

An interesting correlation can be made between aneurysm size and rebleed rate. The smaller the diameter implies a lower rate of rebleed, making observation a viable alternative for therapy [Figure 5]. There also appears to be a difference in behaviour between aneurysms that arise from the direct brain stem perforators and those that arise from the circumflex artery. Circumflex artery aneurysms are larger and more accessible. Hence, intervention is easier and usually more successful. Complications are also hence suitably lower. Direct brain stem perforator aneurysms are inaccessible, short, and have a small diameter making intervention difficult [Figure 6]. Observation (conservative management) is often more appropriate here with minimal risk of rebleeds and no complications otherwise.
Figure 5: A correlation between size of the aneurysm and complication. Here the larger the aneurysm, the more frequent the complication rates

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Figure 6: The correlation between perforater type and complication rate. All the complications (including endovascular failures) occurred in the direct brainstem perforator arteries (19# which is 100%)

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  Discussion Top


A total of 42 BAPA cases reported in literature for the past 20 years, and since their initial description in 1996 by Ghogawala et al., more have been tackled endovascularly [Table 1]. Till date, only eight cases of basilar perforators have been described in the literature with endovascular treatment by coiling or pipeline stent placement.[2] Basilar artery perforators have been stratified according to their location into caudal (2–5 in number with a diameter of 80–600 μm), middle (5–9 in number with diameter of 210–940 μm) and rostral perforators[2] 2 (1–5 in number with a diameter of 190–800 μm).[2],[3] The middle perforators of the basilar artery vary in number from five to nine and diameter ranging from 210 to 940 μm3.[3] These perforators originate directly from the basilar artery or from a common trunk together with the superolateral or inferolateral pontine artery.[3] Similarly, Rhoton observed that the distal 1 cm of the basilar artery is the origin of on average 8 perforating arteries usually arising from the posterior and lateral surface.[2],[3],[4] Thus, these vessels are tortuous, have variable anatomy, arise together and are critical for brain stem function, making them very difficult to approach and treat. It is self-explanatory that these arteries which supply the brain stem and mesencephalon must be preserved during intervention.[3],[4],[5]

Diagnosis of perforator aneurysm poses a serious challenge due to low flow in perforating arteries, which adequately explains the diagnostic difficulty in computed tomographic angiography (CTA) and even on initial catheter angiogram.[5] Careful assessment of conventional angiography in the delayed capillary and venous phases[4],[5] is required for analysis of perforator pathology. Typical intracranial saccular aneurysms fill during the arterial phase in contrast to perforator aneurysms which tend to fill in the capillary and venous phases due to the significantly smaller calibre of the parent artery.[5] This combined with very narrow aneurysm necks makes detection difficult. In general, small vessel aneurysms appear to be characterised by a rather reduced flow which may be due to the very narrow aneurysm necks.[5]

Slow flow through perforator aneurysms also predisposes them to intraluminal thrombus formation.[5] Another feature of these aneurysms is that the bleeding pattern in basilar trunk perforators (BTPs) is variable ranging from perimesencephalic, pre-pontine to even diffuse subarachnoid hemorrhage (SAH).[5]

Another difficulty is diagnosis owing to a variety of factors. Partial thrombosis can diminish the apparent size of an aneurysm, whereas complete thrombosis can make it angiographically occult.[5],[6] A basilar perforating aneurysm can be easily missed on CTA due to its small size, variable location, slow opacification and potential for intra-aneurysm thrombus.[5] Due to low blood flow within the parent vessel, these aneurysms can remain even angiographically occult for several days.[5],[6]

Finally, the small size of these lesions can predispose them to be overlooked. According to the available literature, these aneurysms usually measure <6 mm.[5],[6]

The above-mentioned factors highlight the necessity of repeat catheter angiography in patients with initially angiogram-negative SAH, although the proper timing of follow-up imaging studies remains poorly defined.[1] It has been reported that repeat angiograms can diagnose a cause of haemorrhage in 2% of cases.[6] Hence, care should be taken during the procedures to limit morbidity and mortality.

Direct coiling of BTP aneurysms is otherwise rarely possible because it requires catheterising exceedingly small-calibre perforators often arising at a straight angle from the basilar trunk.[6],[7] Moreover, the very small size of these aneurysms precludes safe coil placement.[6],[7] Therefore, Deshaies et al. in 2011 first performed the technique of telescoping stent for 3-mm basilar perforator after unsuccessful coil embolisation.[5],[6],[7] Flow diversion with overlapping stents as monotherapy has also recently been shown to be a successful endovascular technique for perforator aneurysms.[1] Onyx embolisation will almost certainly result in parent vessel obliteration as it is virtually impossible to restrict Onyx to only the small dome of a perforator aneurysm.[5],[6],[7],[18] Hence, embolisation is to be avoided in these dangerous lesions.

Aneurysms originating from small arteries may also be found on other cerebral vessels, for example lenticulostriate arteries.[7],[8] Such aneurysms may or may not be associated with arterial hypertension, and in most cases, the aetiology cannot be solved.[7],[8] Often these aneurysms are suggested to be caused by a play of environmental factors with hereditary diseases on congenital deficiencies of the vessel wall and cerebrovascular circulation which present sporadically as such.

We present the 20th documented case of a BAPA presenting with non-traumatic SAH and only the ninth case using an endovascular approach to treatment. Our review of the published cases to date, including our patient, is summarised in [Table 1].[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25] We were unable to identify any published cases of unruptured BAPAs.

Due to their small size and rarity and the lack of routine screening for intracranial aneurysms, the odds of identifying unruptured BAPAs are exceedingly low. This in case of an acute ruptured BAPA, there is uncertainty concerning the standard therapeutic management,[8],[9] owing to the scarcity of literature to effect a protocol. Most of these cases were approached microsurgically. The approach to the anatomic site is challenging both for clipping as well due to the retrobasilar location and tiny diameter of the perforators.[8],[9] It is also difficult to predict the haemorrhage rate from these lesions.[4] Hence, therapeutic attempts are risky and may fail.[8],[9]

Advances in endovascular therapy for perforating artery aneurysms available nowadays include improved imaging, improved microcatheter and microwire technology availability of delicate malleable microcatheters and coils and flow diverters have made endovascular therapy more acceptable. Given these considerations, stent placement and flow diverter placement are increasingly being considered, especially given growing experience, confidence and success with flow diversion techniques.[10],[11]

Nevertheless, surgery remains the only other option for treatment of ruptured BAPA aneurysms if endovascular treatment fails.[2] Consequently, the surgeon must decide if the risks of re-haemorrhage outweigh that of craniotomy and clipping.[11],[12] Operatively, perforating aneurysms provide the surgeon with several technical challenges.[12] It is difficult to obtain proximal control before securing the lesion, and it is clearly not possible to perform subpial dissection around the dome of the aneurysm to completely assess the anatomy of the lesion.[12],[13] One should also attempt to preserve all the other perforating vessels and avoid damage to the surrounding cranial nerves.[13],[14] The consequences such as vasospasm also remain severe as direct brainstem strokes are devastating for the patients.

Finally, the risks and benefits of observation versus various interventions must be carefully reviewed by a cerebrovascular team proficient in both endovascular therapies and open microsurgery. Some reports as suggested in [Table 1] show that, due to the small size of the aneurysm, spontaneous thrombosis and resolution are also seen. The danger of unpredictable natural history and devastating consequences of haemorrhage make observation a risky proposition at present until more data are available for study.

Based on the above data available, the following recommendations are proposed for BAPAs. The [Figure 7] illustrates our recommendations for treating such entities clearly.
Figure 7: Intervention protocol for basilar artery perforator aneurysm management

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  1. Circumflex artery aneurysms are to be managed through interventional therapy (either endovascular or open surgery)
  2. Aneurysms smaller than 1.5 mm are to be managed by observation alone
  3. Flow diverter placement is the best method for the management of these lesions. Coiling is the next best option
  4. Microsurgical clipping is best for circumflex artery aneurysms. Parent vessel ligation/trapping is the last option and is to be used only when all other options are untenable
  5. Associated complications such as arteriovenous malformations and the presence of multiple aneurysms need to be considered before deciding upon a modality of management
  6. Combinations of flow diverter, stent assisted coiling and glue injections can also be attempted, with similar complication and success rates to monotherapy
  7. Endovascular treatment failure is common and can be rectified by open microsurgery. Surgery in endovascular failure is uniformly successful with minimal complications. Thus, open microsurgery can function as a safety net for the disease in case of all other modalities failing.



  Conclusion Top


Aneurysms arising from the perforating branches of basilar artery are exceedingly rare vascular lesions. They are difficult to diagnose, often radiographically occult on initial CTA and angiography, and can also be extremely difficult to treat without risking significant morbidity. Based on our experience, endovascular treatment of these lesions has proved to be extremely challenging although successful coil embolisation and overlapping stent placement have been reported. From a literature review, microsurgical clipping although technically demanding has been shown to have a greater measure of success. Conservative management has demonstrated that, in some cases, spontaneous thrombosis and resolution may occur. However, since the natural history of BAPAs remains unknown, the management of these entities should be performed on an individual basis by a comprehensive cerebrovascular team.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Marinković SV, Gibo H. The surgical anatomy of the perforating branches of the basilar artery. Neurosurgery 1993;33:80-7.  Back to cited text no. 1
    
2.
Granja MF, Monteiro A, Agnoletto GJ, Jamal S, Sauvageau E, Aghaebrahim A, et al. A systematic review of non-trunk basilar perforator aneurysms: Is it worth chasing the small fish? J Neurointerv Surg 2020;12:412-16.  Back to cited text no. 2
    
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Buell TJ, Ding D, Raper DM, Chen CJ, Hixson HR, Crowley RW, et al. Posterior circulation perforator aneurysms: A proposed management algorithm. J Neurointerv Surg 2018;10:55-9.  Back to cited text no. 3
    
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Hamel W, Grzyska U, Westphal M, Kehler U. Surgical treatment of a basilar perforator aneurysm not accessible to endovascular treatment. Acta Neurochir (Wien) 2005;147:1283-6.  Back to cited text no. 4
    
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Sanchez-Mejia RO, Lawton MT. Distal aneurysms of basilar perforating and circumferential arteries. Report of three cases. J Neurosurg 2007;107:654-9.  Back to cited text no. 5
    
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Park SQ, Kwon OK, Kim SH, Oh CW, Han MH. Pre-mesencephalic subarachnoid hemorrhage: Rupture of tiny aneurysms of the basilar artery perforator. Acta Neurochir (Wien) 2009;151:1639-46.  Back to cited text no. 6
    
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Mathieson CS, Barlow P, Jenkins S, Hanzely Z. An unusual case of spontaneous subarachnoid haemorrhage-a ruptured aneurysm of a basilar perforator artery. Br J Neurosurg 2010;24:291-3.  Back to cited text no. 7
    
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Nyberg EM, Chaudry MI, Turk AS, Spiotta AM, Fiorella D, Turner RD. Report of two cases of a rare cause of subarachnoid hemorrhage including unusual presentation and an emerging and effective treatment option. J Neurointerv Surg 2013;5:e30.  Back to cited text no. 9
    
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Sahu CD, Ashpilaya A. Case series on perforator aneurysm: Endovascular stenting-a safe strategy. J Clin Interv Radiol ISVIR 2017;1:179-83.  Back to cited text no. 12
    
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Wu T, Wu Y, Chen A, Dai C, Zhu Q. Spontaneous subarachnoid hemorrhage caused by ruptured aneurysm of basilar trunk perforator. available at Research Square https://doi.org/10.21203/rs.3.rs-32783/v1 11 June 2020, PREPRINT (Version 1).  Back to cited text no. 13
    
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Sivakanthan S, Carlson AP, van Loveren H, Agazzi S. Surgical clipping of a basilar perforator artery aneurysm: A case of avoiding perforator sacrifice. J Neurol Surg A Cent Eur Neurosurg 2015;76:79-82.  Back to cited text no. 22
    
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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]
 
 
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