Case Report
Disappearance of a Ruptured Distal FloweRelated Aneurysm after Arteriovenous Malformation Nidal Embolization Lucy He1, Junwei Gao2, Ajith J. Thomas3, Matthew R. Fusco3, Christopher S. Ogilvy3
Key words Arteriovenous malformation - Endovascular treatment - Flow-related aneurysm - Intraventricular hemorrhage -
Abbreviations and Acronyms ACA: Anterior cerebral artery AVM: Arteriovenous malformation DSA: Digital subtraction angiography EDAS: Encephaloduroarteriosynangiosis IVH: Intraventricular hemorrhage MCA: Middle cerebral artery STA: Superficial temporal artery From the 1Department of Neurosurgery, Vanderbilt University Medical Center, Nashville, Tennessee, USA; 2Department of Neurosurgery, Lanzhou University Second Hospital, Lanzhou, Gansu, China; and 3Neurosurgery Service, Brain Aneurysm Institute, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA To whom correspondence should be addressed: Christopher S. Ogilvy, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.05.065
Aneurysms associated with arteriovenous malformations (AVMs) are well represented in the literature. Their exact etiology is poorly understood, but likely global hemodynamic changes coupled with vascular wall pathology play into their formation. Flow-related and intranidal aneurysms, in particular, appear to have an increased risk for hemorrhagic presentation. Treatment strategies for these aneurysms are particularly challenging. We report the case of an AVMassociated aneurysm causing intraventricular hemorrhage that disappeared after embolization of unrelated, distal feeding pedicles to the nidus, at a site distant from the aneurysm. We also review the literature with regards to these so-called “disappearing aneurysms” in the context of AVMs and other vascular pathologies.
aneurysm causing intraventricular hemorrhage that disappeared after subsequent embolization of the nidus from pedicles not directly feeding the aneurysm. We also review the literature with regards to these so-called “disappearing aneurysms” in the context of AVMs and other vascular pathologies.
Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
Intraventricular hemorrhage associated with arteriovenous malformations (AVMs) has been reported previously in the literature and can be a presenting symptom secondary to direct AVM hemorrhage into the ventricle or secondary to ruptures of aneurysms associated with AVMs (17, 22). Aneurysms associated with AVMs are classified depending on their relationship to the AVM nidus and/or feeder vessels (10, 11, 14). They are considered weak points within the vessel wall that increase the risk of intracranial hemorrhage. Hemodynamic changes, such as increased blood flow or changes in intravascular pressure, are associated with rupture of these AVM-associated aneurysms. Treatment strategies for these aneurysms are particularly challenging (25). Here, we report the case of an AVM-associated
CASE REPORT A 57-year-old female with a known diagnosis of a large left parietal AVM presented with acute onset of headache, nausea, and photophobia. Noncontrasted computed tomography head imaging demonstrated intraventricular hemorrhage (IVH), left greater than right, without evidence of subarachnoid hemorrhage (Figure 1A). The patient’s initial diagnosis occurred more than 30 years prior, a time when there were no endovascular treatment options. Open treatment options were thought too morbid given the size of the lesion and its proximity to the postecentral gyrus and visual cortex. The patient was last seen by the senior author 10 years before her current hospital presentation and had been routinely followed by her outpatient neurologist. The patient also had a history of seizure disorder well controlled with a single agent. She had no known history of hemorrhage from this AVM.
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The day after admission, the patient underwent digital subtraction angiography (DSA), which demonstrated a 5.4 cm 5.2 cm 5.8 cm AVM within the left posterior parietal lobe with predominant feeders from the left anterior cerebral artery (ACA), middle cerebral artery (MCA), and posterior cerebral artery (PCA) with marked dilation of the ACA and MCA feeders in particular (Figure 2). There was predominant drainage via the superior sagittal sinus and Labeé vein with a smaller portion of venous outflow from the deep venous system. Functional magnetic resonance imaging demonstrated that motor and speech areas were anterior to the nidus, and there was no involvement of the occipital lobe. Given these findings, the patient was deemed to have a SpetzlerMartin grade III AVM (21). The patient was monitored for development of hydrocephalus and ultimately discharged to inpatient rehabilitation 10 days after presentation. Discussion in our institution’s neurovascular conference recommended staged embolization treatment followed by surgical resection. Two weeks after discharge, while awaiting her first staged embolization, the patient re-presented with acute-onset severe headache. Repeat computed tomography imaging again demonstrated acute IVH, this time confined to the left ventricle (Figure 1B). DSA demonstrated similar
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DISCUSSION
Figure 1. Axial-view, noncontrasted computed tomography (CT) head images from the patient. (A) Initial presentation with bilateral intraventricular hemorrhage (IVH), more in the left than right ventricle. The patient was medically managed and observed for signs of hydrocephalus. Her last CT before discharge showed resolution of the IVH. (B) Two weeks after discharge, the patient re-presented with acute-onset headache and hadleft-only acute IVH.
arterial flow patterns when compared with prior angiography. On 3D-DSA, a 5-mm anterior choroidal artery aneurysm, anatomically near the atria of the left ventricle, was found. Careful review of this second DSA showed dysplastic features of the left anterior choroidal artery that provided small pedicle feeders to the AVM. The aneurysm was located distally on the left anterior choroidal artery, some distance from the vessel origin off the MCA. On review of the patient’s first DSA, this aneurysm was previously present but smaller and partially obscured, likely secondary to thrombosis (Figure 2). The periventricular location of this aneurysm was likely the source of the patient’s recurrent IVH. Despite providing feeders to the AVM nidus, this left anterior choroidal artery was diminutive in caliber with a tortuous course. There was concern that any attempts to access the vessel and potentially treat this distal aneurysm would lead to vessel dissection or perforation and devastating associated stroke. Thus the decision was made to target the AVM nidus instead. The patient subsequently underwent AVM embolization of a distal M3 branch
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supplying the pre-Rolandic region with Onyx-18 (ev3, Plymouth, Minnesota, USA) resulting in approximately 40% reduction in nidus size. Three days later, a follow-up DSA was performed to further delineate the distal left anterior choroidal aneurysm with possible treatment. Multiple magnified views of the area of interest failed to demonstrate continued presence of this aneurysm (Figure 3). The patient was ultimately discharged to inpatient rehabilitation 2 weeks after her second IVH. Two months later, second-stage Onyx embolization was undertaken via left MCA posterior branch feeders, resulting in another 10%e20% reduction in nidus size. Multiple views of the distal left anterior choroidal artery again did not demonstrate presence of the previously seen aneurysm. A third-stage Onyx embolization was undertaken almost 6 months after the initial hemorrhage and again did not demonstrate evidence of this aneurysm. The aneurysm has remained resolved without direct treatment of the aneurysm. The patient is currently anticipated to undergo craniotomy for AVM resection.
The incidence of AVM-associated aneurysms has been quoted in the literature as ranging from 2.7%e51.5% (10, 11, 15, 20, 22). Our internal review over the past 18 months for AVMs undergoing DSA indicates an associated aneurysm rate of 13%; 71% of these aneurysms were type II Perata et al. (14) and type IIa Redekop et al (19), and the remainder were type III Perata et al. (14) and type IIb Redekop et al (19). None were like our currently described aneurysm. None of our aneurysms regressed with direct AVM nidal treatment as the primary treatment (internal unpublished data). It is hypothesized that hemodynamic stress secondary to the high-flow nature of AVMs likely causes continual damage to the endothelia of blood vessels, leading to aneurysm formation, and over time these weakened blood vessels have a propensity to rupture (1, 7, 10, 16, 25). To our knowledge, this is the first reported case of resolution of ruptured AVM-associated aneurysm after treatment of nidus from unrelated, distant arterial feeders. Classification Systems Various classification systems exist to characterize AVM-associated aneurysms, though a definitive system is still lacking given the uncertainty regarding the actual etiology of these aneurysms (10, 11, 14, 19). The first was proposed by Lasjaunias et al., who described 3 types of AVMassociated aneurysms: 1) distal or intralesional, 2) proximal aneurysms directly on vessels supplying the AVM, and 3) remote or dysplastic aneurysms unrelated to inflow vessels. Further refinement of this classification separates whether “flow related” aneurysms originated from vessels off the circle of Willis that directly supplied the AVM or originated more distally in the feeding pedicle (Table 1) (14, 19). Our patient’s aneurysm is difficult to classify on the basis of the existing systems as the anterior choroidal in our patient arose off the ICA/MCA junction, the MCA was a feeder vessel to the AVM, but the anterior choroidal was not a feeder to the AVM. It is not entirely “unrelated” to the AVM according to the classification systems; however, it is not truly a “distal pedicle” aneurysm, either. It shares features
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Figure 2. Anterior-posterior (AP) view digital subtraction angiography (DSA) injections from the left internal carotid artery (ICA) (left panels) and slightly oblique view 3D-DSA (right panels). Note the increased diameter of the entirety of the left middle cerebral artery (MCA) from the M1 portion through to the distal branches feeding the AVM nidus. There is an infundibulum at the origin of the anterior temporal artery seen. The caliber of the left anterior choroidal artery (arrows), despite arising from this dilated left MCA, did not show significant increase in size. (A-C) DSA from the patient’s initial presentation with IVH shows the small left anterior choroidal artery aneurysm (*) that is best seen on the 3D-DSA (B) and lateral projection (C). On the lateral projection, the aneurysm is seen as a double density. (D-F) Stage I embolization after the patient re-presented with acute headache and IVH. Note the left anterior choroidal artery aneurysm (*) is much better visualized both on traditional DSA (D), 3D-DSA (E), and lateral projections (F).
similar to the type III Perata et al. classification or type IIb based on the Redekop et al. classification, but both systems incompletely categorize this aneurysm. The lack of consistently used classification system for aneurysm-associated AVMs is noted in the sometimes conflicting results from papers looking at hemorrhage in this population. Meisel et al. classified aneurysms as simply intranidal (IN) or proximal (PROX)—defined only as arising off a feeding artery—and failed to find an increased risk of hemorrhage in patients with AVM alone versus those with
INs or PROXs (11). They did find that INs had a higher risk of rebleeding. Looking at only feeding vessel aneurysms, excluding intranidal and noneflowrelated aneurysms, Kim et al. found increased rates of hemorrhage in the aneurysm group compared with the AVMonly group (8). In subgroup analysis, both studies were consistent in their findings that there was a greater association with hemorrhage and distal flowerelated aneurysms, though not statistically significant (8, 11). In the studies using the more detailed classification systems, consistent results favor that flow-related
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and/or intranidal aneurysms are associated with an increased risk of hemorrhage (5, 14, 19, 22). These studies conclude that distal flowerelated aneurysms, in particular, present a significant risk factor for hemorrhage. Interestingly, it would appear that the source of hemorrhage is equally divided between the aneurysm and AVM itself (5, 19). Treatment Practices There remains controversy with regards to whether all AVM-associated aneurysms should be treated and, if so, the exact timing of aneurysm treatment relative to
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Figure 3. Anterior-posterior view digital subtraction angiography (DSA) (A) and oblique view 3D-DSA (B) from the patient’s follow-up angiography 3 days after stage I embolization. Note that there is no further persistence of the previously seen distal left anterior choroidal artery (*). This result persisted when the patient returned for her stage II embolization 2 months later (not shown). We hypothesize that even with partial AVM nidus, this caused enough hemodynamic change in the proximal MCA that was transmitted to the left anterior choroidal artery, leading to complete aneurysm regression.
AVM treatment (5, 15, 23, 25). Current trends would favor treatment of ruptured aneurysms given their higher likelihood of rerupture (5, 15, 22, 25). Endovascular treatment with coil embolization of larger feeding pedicle aneurysms or liquid embolic treatment of more distal aneurysms have been well reported in the literature with good efficacy and safety
Table 1. Arteriovenous Malformation (AVM)-Associated Aneurysm Classification Systems. Lasjaunias et al. (10)
Perata Redekop et al. et al. (14) (19)
Unrelated to AVM
Type III
Type I
Type I
Proximal vessel, flow related
Type II
Type II
Type IIa
Distal vessel, flow related
Type I
Type III
Type IIb
Intranidal
Type I
Type IV
Type III
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profile (6, 11, 15, 25). Given the complex high-flow hemodynamics of AVMs and the relative anatomic relationships of the aneurysm to nidus, it is generally difficult to concurrently treat both pathologies in the same setting, even endovascularly (25). For unruptured aneurysms, there is a paucity of definitive guidelines for prophylactic aneurysm treatment (5, 19, 25). Regression of aneurysms associated with AVM nidal treatment has been previously described (5, 18, 19, 23). Of the distal aneurysms that resolved, embolization was undertaken on feeder pedicles associated or in close proximity to the aneurysm, but none of the proximal flowrelated aneurysms regressed with treatment (5, 14, 19). It is postulated that obliterative treatment of the AVM eventually decreased overall blood flow through feeder vessels, thereby decreasing intravascular pressure and reducing the vessel wall stress, allowing for vessel remodeling and leading to aneurysm resolution (8, 14, 18, 19). In one study, at least 50% nidal reduction was necessary for distal flowe related aneurysm regression (19). None of
these studies indicated whether the aneurysm or AVM was the source for hemorrhage. Our case of a deep perforator, flowrelated aneurysm completely regressing after only partial embolization of an AVM feeder unrelated to the aneurysm vessel has not been described. We hypothesize that this spontaneous resolution was likely secondary to changes in flow dynamics after AVM embolization arising from the left MCA. The patient had a significantly enlarged left MCA secondary to the AVM with increased blood flow even through the proximal M1 segment as seen on DSA (Figure 2). This likely also increased the blood flow through the left anterior choroidal artery, and as the vessel naturally tapers more distally, this distal segment could not compensate for the increased blood flow or intravascular pressure, thus leading to formation of the aneurysm. During the first embolization, an estimated 40% of the nidal volume was obliterated, which should reduce the blood flow through the proximal left MCA and by proxy through the left anterior choroidal artery (4). Flow-Related Aneurysm Formation in Moyamoya A similar phenomenon of deep perforator artery aneurysm formation and resolution in the setting of hemodynamic changes after circulatory bypass has been reported in the moyamoya disease (MMD) literature (2, 9, 12, 13). The incidence of aneurysm formation in MMD has been reported as being between 3% and 14% (3, 12, 24). It is believed that aneurysm formation in MMD is related to both hemodynamic stress and pathologic vessel architecture. Deep perforator collateral branch aneurysms account for 44% of MMD-associated aneurysms (2). It is hypothesized that high flows in these collateral vessels occur secondary to lack of flow through the internal carotid arteries, and this increased flow combined with a lack of robust muscular layer in these smaller vessels makes them prone to aneurysmal formation. Amin-Hanjani et al. summarized the available case reports for deep perforator aneurysm resolution after superficial temporal artery (STA)-MCA bypass, with or without encephaloduroarteriosynangiosis
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(EDAS), in MMD patients. The postulated mechanism was secondary to reduction in hemodynamic stress of the deep perforator vessels with revascularization through the bypass and/or EDAS procedure. Imaging confirmed resolution occurred as early as 1 month post procedure (9), though the average was after 6 months. It is not clear if aneurysm resolution could have occurred at a time point earlier than 1 month because there was no set criteria for when repeat DSA was undertaken in the reported cases. The exact etiology of distal flowerelated aneurysms is not well understood. However, resolution of this type of aneurysm in our patient and others with AVM nidal treatment along with the MMD data lends credit to the theory that global hemodynamic disturbances are causative. Alleviation of increased intravascular pressure, in the form of AVM nidal treatment or bypass in the setting of MMD, relieves significant stress on these more distal vessels and can lead to aneurysm resolution. This mechanism may differ from the formation of other proximal or noneflow-related aneurysms and explain why AVM treatment seems to have little effect on their regression (5, 14, 19). Our case of aneurysm regression highlights the dynamic nature of AVMs and global hemodynamic changes that can occur with nidal treatment. We highlight that in cases of ruptured AVM-associated aneurysms arising off small distal arterial feeders, treatment of unrelated main pedicle feeders can bring about changes in vessel stresses that can cause aneurysm regression. This may be particularly important in cases of acute hemorrhage where endovascular treatment is considered high risk due to small vessel caliber or tortuosity. Our lone case is not enough to make definitive conclusions about cause and effect of nidal treatment and regression of this aneurysm. It is possible that this aneurysm would regress spontaneously and that the timing of embolization was merely coincidental. In situations where direct treatment of the ruptured aneurysm associated with an AVM is too high risk, it is reasonable to attempt AVM nidal treatment first, followed by short-term DSA (within 1e2 weeks) to assess for changes in the aneurysm. If there is continued aneurysm filling, then risk/benefit regarding
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treatment of the aneurysm can be considered versus continued observation or AVM nidal treatment. CONCLUSION Aneurysm formation in the context of AVM disease still lacks a clear etiology and may be caused by multiple mechanisms given the differences in how these aneurysms respond to nidal treatment. We present a case of distal flowerelated artery aneurysm formation, a source of recurrent IVH, which spontaneously resolved after partial embolization of the AVM nidus via distant pedicle feeders. Our lone patient cannot be used to draw cause and effect relationships, and the conclusion that these aneurysms can regress with nidal treatment alone is anecdotal. We postulate that there are gross hemodynamic changes associated with AVMs that place particular stress on the distal areas of arterial feeders and predispose to aneurysm formation and/or rupture. Although primary treatment of ruptured distal flowerelated aneurysms is recommended, our case demonstrates that even when this cannot safely be done, primary treatment of the AVM may offer concurrent treatment of the at-risk aneurysm. REFERENCES 1. Akabane A, Jokura H, Ogasawara K, Takahashi K, Sugai K, Ogawa A, Yoshimoto T: Rapid development of an intranidal aneurysm with perifocal brain edema in an unruptured cerebral arteriovenous malformation. J Neurosurg 97 (6):1436-1440, 2002. 2. Amin-Hanjani S, Goodin S, Charbel FT, Alaraj A: Resolution of bilateral moyamoya associated collateral vessel aneurysms: Rationale for endovascular versus surgical intervention. Surg Neurol Int 5 (Suppl 4):S155-S160, 2014. 3. Borota L, Marinkovic S, Bajic R, Kovacevic M: Intracranial aneurysms associated with moyamoya disease. Neurol Med Chir (Tokyo) 36 (12):860-864, 1996. 4. Chuang YM, Guo W, Lin CP: Appraising the plasticity of the circle of Willis: a model of hemodynamic modulation in cerebral arteriovenous malformations. Eur Neurol 63:295-301, 2010. 5. Flores BC, Klinger DR, Rickert KL, Barnett SL, Welch BG, White JA, Batjer HH, Samson DS: Management of intracranial aneurysms associated with arteriovenous malformations. Neurosurg Focus 37:E11, 2014. 6. Garcia-Monaco R, Rodesch G, Alvarez H, Iizuka Y, Hui F, Lasjaunias P: Pseudoaneurysms within ruptured intracranial arteriovenous malformations:
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diagnosis and early endovascular management. AJNR Am J Neuroradiol 14:315-321, 1993. 7. Hodozuka A, Sako K, Yonemasu Y, Suzuki N, Fujita T, Ohgami S: Spontaneous disappearance of aneurysm after total removal of accompanying intracranial arteriovenous malformation. Case report. Neurol Med Chir (Tokyo) 31:966-971, 1991. 8. Kim EJ, Halim AX, Dowd CF, Lawton MT, Singh V, Bennett J, Young WL: The relationship of coexisting extranidal aneurysms to intracranial hemorrhage in patients harboring brain arteriovenous malformations. Neurosurgery 54: 1349-1357; discussion 1357-1358, 2004. 9. Kuroda S, Houkin K, Kamiyama H, Abe H: Effects of surgical revascularization on peripheral artery aneurysms in moyamoya disease: report of three cases. Neurosurgery 49 (2):463-467; discussion 467-468, 2001. 10. Lasjaunias 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) 91:29-36, 1988. 11. Meisel 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 46:793-800; discussion 800-802, 2000. 12. Ni W, Xu F, Xu B, Liao Y, Gu Y, Song D: Disappearance of aneurysms associated with moyamoya disease after STA-MCA anastomosis with encephaloduro myosynangiosis. J Clin Neurosci 19 (3): 485-487, 2012. 13. Otawara Y, Ogasawara K, Seki K, Kibe M, Kubo Y, Ogawa A: Intracerebral hemorrhage after prophylactic revascularization in a patient with adult moyamoya disease. Surg Neurol 68:335-337; discussion 337, 2007. 14. Perata HJ, Tomsick TA, Tew JM: Feeding artery pedicle aneurysms: association with parenchymal hemorrhage and arteriovenous malformation in the brain. J Neurosurg 80:631-634, 1994. 15. Piotin M, Ross IB, Weill A, Kothimbakam R, Moret J: Intracranial arterial aneurysms associated with arteriovenous malformations: endovascular treatment. Radiology 220:506-513, 2001. 16. Platz J, Berkefeld J, Singer OC, Wolff R, Seifert V, Konczalla J, Güresir E: Frequency, risk of hemorrhage and treatment considerations for cerebral arteriovenous malformations with associated aneurysms. Acta Neurochir (Wien) 156:2025-2034, 2014. 17. Pollock GA, Shaibani A, Awad I, Batjer HH, Bendok BR: Intraventricular hemorrhage secondary to intranidal aneurysm rupture-successful management by arteriovenous malformation embolization followed by intraventricular tissue plasminogen activator: case report. Neurosurgery 68:E581-E586; discussion E586, 2011. 18. Poon WL, Alvarez H, Lasjaunias P: Secondary spontaneous thrombosis of a giant aneurysm located dstally on a feeding artery after embolization of an associated arteriovenous malformation. Interv Neuroradiol 9:367-372, 2003.
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19. Redekop G, TerBrugge K, Montanera W, Willinsky R: Arterial aneurysms associated with cerebral arteriovenous malformations: classification, incidence, and risk of hemorrhage. J Neurosurg 89:539-546, 1998. 20. Sakata Y, Aoki H, Higashi K, Tsue M: Simultaneous occurrence of intracranial aneurysm and arteriovenous malformation. Nihon Geka Hokan Arch Für Jpn Chir 37:242-247, 1968.
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malformations with haemorrhagic presentation. J Neurol Neurosurg Psychiatry 73:294-298, 2002. 23. Stiefel MF, Al-Okaili R, Weigele JB, Hurst RW: De novo aneurysm formation and regression after brain arteriovenous malformation embolization: case report. Surg Neurol 67 (1):99-101; discussion 101, 2007.
21. Spetzler RF, Martin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:476-483, 1986.
24. Yeon JY, Kim JS, Hong SC: Incidental major artery aneurysms in patients with non-hemorrhagic moyamoya disease. Acta Neurochir (Wien) 153 (6):1263-1270, 2011.
22. Stapf C, Mohr JP, Pile-Spellman J, Sciacca RR, Hartmann A, Schumacher HC, Mast H: Concurrent arterial aneurysms in brain arteriovenous
25. Yu JL, Yang S, Luo Q, Wang HL, Wang B, Qu YY, Xu K: Endovascular treatment of intracranial ruptured aneurysms associated with arteriovenous
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malformations: a clinical analysis of 14 hemorrhagic cases. Interv Neuroradiol 17:78-86, 2011.
Conflict of interest statement: All authors affirm that they have no conflicts of interest. Received 24 February 2015; accepted 28 May 2015 Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.05.065 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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Disappearance of a Ruptured Distal FloweRelated Aneurysm after Arteriovenous Malformation Nidal Embolization Lucy He1, Junwei Gao2, Ajith J. Thomas3, Matthew R. Fusco3, Christopher S. Ogilvy3
Key words Arteriovenous malformation - Endovascular treatment - Flow-related aneurysm - Intraventricular hemorrhage -
Abbreviations and Acronyms ACA: Anterior cerebral artery AVM: Arteriovenous malformation DSA: Digital subtraction angiography EDAS: Encephaloduroarteriosynangiosis IVH: Intraventricular hemorrhage MCA: Middle cerebral artery STA: Superficial temporal artery From the 1Department of Neurosurgery, Vanderbilt University Medical Center, Nashville, Tennessee, USA; 2Department of Neurosurgery, Lanzhou University Second Hospital, Lanzhou, Gansu, China; and 3Neurosurgery Service, Brain Aneurysm Institute, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA To whom correspondence should be addressed: Christopher S. Ogilvy, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.05.065
Aneurysms associated with arteriovenous malformations (AVMs) are well represented in the literature. Their exact etiology is poorly understood, but likely global hemodynamic changes coupled with vascular wall pathology play into their formation. Flow-related and intranidal aneurysms, in particular, appear to have an increased risk for hemorrhagic presentation. Treatment strategies for these aneurysms are particularly challenging. We report the case of an AVMassociated aneurysm causing intraventricular hemorrhage that disappeared after embolization of unrelated, distal feeding pedicles to the nidus, at a site distant from the aneurysm. We also review the literature with regards to these so-called “disappearing aneurysms” in the context of AVMs and other vascular pathologies.
aneurysm causing intraventricular hemorrhage that disappeared after subsequent embolization of the nidus from pedicles not directly feeding the aneurysm. We also review the literature with regards to these so-called “disappearing aneurysms” in the context of AVMs and other vascular pathologies.
Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
Intraventricular hemorrhage associated with arteriovenous malformations (AVMs) has been reported previously in the literature and can be a presenting symptom secondary to direct AVM hemorrhage into the ventricle or secondary to ruptures of aneurysms associated with AVMs (17, 22). Aneurysms associated with AVMs are classified depending on their relationship to the AVM nidus and/or feeder vessels (10, 11, 14). They are considered weak points within the vessel wall that increase the risk of intracranial hemorrhage. Hemodynamic changes, such as increased blood flow or changes in intravascular pressure, are associated with rupture of these AVM-associated aneurysms. Treatment strategies for these aneurysms are particularly challenging (25). Here, we report the case of an AVM-associated
CASE REPORT A 57-year-old female with a known diagnosis of a large left parietal AVM presented with acute onset of headache, nausea, and photophobia. Noncontrasted computed tomography head imaging demonstrated intraventricular hemorrhage (IVH), left greater than right, without evidence of subarachnoid hemorrhage (Figure 1A). The patient’s initial diagnosis occurred more than 30 years prior, a time when there were no endovascular treatment options. Open treatment options were thought too morbid given the size of the lesion and its proximity to the postecentral gyrus and visual cortex. The patient was last seen by the senior author 10 years before her current hospital presentation and had been routinely followed by her outpatient neurologist. The patient also had a history of seizure disorder well controlled with a single agent. She had no known history of hemorrhage from this AVM.
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The day after admission, the patient underwent digital subtraction angiography (DSA), which demonstrated a 5.4 cm 5.2 cm 5.8 cm AVM within the left posterior parietal lobe with predominant feeders from the left anterior cerebral artery (ACA), middle cerebral artery (MCA), and posterior cerebral artery (PCA) with marked dilation of the ACA and MCA feeders in particular (Figure 2). There was predominant drainage via the superior sagittal sinus and Labeé vein with a smaller portion of venous outflow from the deep venous system. Functional magnetic resonance imaging demonstrated that motor and speech areas were anterior to the nidus, and there was no involvement of the occipital lobe. Given these findings, the patient was deemed to have a SpetzlerMartin grade III AVM (21). The patient was monitored for development of hydrocephalus and ultimately discharged to inpatient rehabilitation 10 days after presentation. Discussion in our institution’s neurovascular conference recommended staged embolization treatment followed by surgical resection. Two weeks after discharge, while awaiting her first staged embolization, the patient re-presented with acute-onset severe headache. Repeat computed tomography imaging again demonstrated acute IVH, this time confined to the left ventricle (Figure 1B). DSA demonstrated similar
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DISCUSSION
Figure 1. Axial-view, noncontrasted computed tomography (CT) head images from the patient. (A) Initial presentation with bilateral intraventricular hemorrhage (IVH), more in the left than right ventricle. The patient was medically managed and observed for signs of hydrocephalus. Her last CT before discharge showed resolution of the IVH. (B) Two weeks after discharge, the patient re-presented with acute-onset headache and hadleft-only acute IVH.
arterial flow patterns when compared with prior angiography. On 3D-DSA, a 5-mm anterior choroidal artery aneurysm, anatomically near the atria of the left ventricle, was found. Careful review of this second DSA showed dysplastic features of the left anterior choroidal artery that provided small pedicle feeders to the AVM. The aneurysm was located distally on the left anterior choroidal artery, some distance from the vessel origin off the MCA. On review of the patient’s first DSA, this aneurysm was previously present but smaller and partially obscured, likely secondary to thrombosis (Figure 2). The periventricular location of this aneurysm was likely the source of the patient’s recurrent IVH. Despite providing feeders to the AVM nidus, this left anterior choroidal artery was diminutive in caliber with a tortuous course. There was concern that any attempts to access the vessel and potentially treat this distal aneurysm would lead to vessel dissection or perforation and devastating associated stroke. Thus the decision was made to target the AVM nidus instead. The patient subsequently underwent AVM embolization of a distal M3 branch
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supplying the pre-Rolandic region with Onyx-18 (ev3, Plymouth, Minnesota, USA) resulting in approximately 40% reduction in nidus size. Three days later, a follow-up DSA was performed to further delineate the distal left anterior choroidal aneurysm with possible treatment. Multiple magnified views of the area of interest failed to demonstrate continued presence of this aneurysm (Figure 3). The patient was ultimately discharged to inpatient rehabilitation 2 weeks after her second IVH. Two months later, second-stage Onyx embolization was undertaken via left MCA posterior branch feeders, resulting in another 10%e20% reduction in nidus size. Multiple views of the distal left anterior choroidal artery again did not demonstrate presence of the previously seen aneurysm. A third-stage Onyx embolization was undertaken almost 6 months after the initial hemorrhage and again did not demonstrate evidence of this aneurysm. The aneurysm has remained resolved without direct treatment of the aneurysm. The patient is currently anticipated to undergo craniotomy for AVM resection.
The incidence of AVM-associated aneurysms has been quoted in the literature as ranging from 2.7%e51.5% (10, 11, 15, 20, 22). Our internal review over the past 18 months for AVMs undergoing DSA indicates an associated aneurysm rate of 13%; 71% of these aneurysms were type II Perata et al. (14) and type IIa Redekop et al (19), and the remainder were type III Perata et al. (14) and type IIb Redekop et al (19). None were like our currently described aneurysm. None of our aneurysms regressed with direct AVM nidal treatment as the primary treatment (internal unpublished data). It is hypothesized that hemodynamic stress secondary to the high-flow nature of AVMs likely causes continual damage to the endothelia of blood vessels, leading to aneurysm formation, and over time these weakened blood vessels have a propensity to rupture (1, 7, 10, 16, 25). To our knowledge, this is the first reported case of resolution of ruptured AVM-associated aneurysm after treatment of nidus from unrelated, distant arterial feeders. Classification Systems Various classification systems exist to characterize AVM-associated aneurysms, though a definitive system is still lacking given the uncertainty regarding the actual etiology of these aneurysms (10, 11, 14, 19). The first was proposed by Lasjaunias et al., who described 3 types of AVMassociated aneurysms: 1) distal or intralesional, 2) proximal aneurysms directly on vessels supplying the AVM, and 3) remote or dysplastic aneurysms unrelated to inflow vessels. Further refinement of this classification separates whether “flow related” aneurysms originated from vessels off the circle of Willis that directly supplied the AVM or originated more distally in the feeding pedicle (Table 1) (14, 19). Our patient’s aneurysm is difficult to classify on the basis of the existing systems as the anterior choroidal in our patient arose off the ICA/MCA junction, the MCA was a feeder vessel to the AVM, but the anterior choroidal was not a feeder to the AVM. It is not entirely “unrelated” to the AVM according to the classification systems; however, it is not truly a “distal pedicle” aneurysm, either. It shares features
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Figure 2. Anterior-posterior (AP) view digital subtraction angiography (DSA) injections from the left internal carotid artery (ICA) (left panels) and slightly oblique view 3D-DSA (right panels). Note the increased diameter of the entirety of the left middle cerebral artery (MCA) from the M1 portion through to the distal branches feeding the AVM nidus. There is an infundibulum at the origin of the anterior temporal artery seen. The caliber of the left anterior choroidal artery (arrows), despite arising from this dilated left MCA, did not show significant increase in size. (A-C) DSA from the patient’s initial presentation with IVH shows the small left anterior choroidal artery aneurysm (*) that is best seen on the 3D-DSA (B) and lateral projection (C). On the lateral projection, the aneurysm is seen as a double density. (D-F) Stage I embolization after the patient re-presented with acute headache and IVH. Note the left anterior choroidal artery aneurysm (*) is much better visualized both on traditional DSA (D), 3D-DSA (E), and lateral projections (F).
similar to the type III Perata et al. classification or type IIb based on the Redekop et al. classification, but both systems incompletely categorize this aneurysm. The lack of consistently used classification system for aneurysm-associated AVMs is noted in the sometimes conflicting results from papers looking at hemorrhage in this population. Meisel et al. classified aneurysms as simply intranidal (IN) or proximal (PROX)—defined only as arising off a feeding artery—and failed to find an increased risk of hemorrhage in patients with AVM alone versus those with
INs or PROXs (11). They did find that INs had a higher risk of rebleeding. Looking at only feeding vessel aneurysms, excluding intranidal and noneflowrelated aneurysms, Kim et al. found increased rates of hemorrhage in the aneurysm group compared with the AVMonly group (8). In subgroup analysis, both studies were consistent in their findings that there was a greater association with hemorrhage and distal flowerelated aneurysms, though not statistically significant (8, 11). In the studies using the more detailed classification systems, consistent results favor that flow-related
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and/or intranidal aneurysms are associated with an increased risk of hemorrhage (5, 14, 19, 22). These studies conclude that distal flowerelated aneurysms, in particular, present a significant risk factor for hemorrhage. Interestingly, it would appear that the source of hemorrhage is equally divided between the aneurysm and AVM itself (5, 19). Treatment Practices There remains controversy with regards to whether all AVM-associated aneurysms should be treated and, if so, the exact timing of aneurysm treatment relative to
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Figure 3. Anterior-posterior view digital subtraction angiography (DSA) (A) and oblique view 3D-DSA (B) from the patient’s follow-up angiography 3 days after stage I embolization. Note that there is no further persistence of the previously seen distal left anterior choroidal artery (*). This result persisted when the patient returned for her stage II embolization 2 months later (not shown). We hypothesize that even with partial AVM nidus, this caused enough hemodynamic change in the proximal MCA that was transmitted to the left anterior choroidal artery, leading to complete aneurysm regression.
AVM treatment (5, 15, 23, 25). Current trends would favor treatment of ruptured aneurysms given their higher likelihood of rerupture (5, 15, 22, 25). Endovascular treatment with coil embolization of larger feeding pedicle aneurysms or liquid embolic treatment of more distal aneurysms have been well reported in the literature with good efficacy and safety
Table 1. Arteriovenous Malformation (AVM)-Associated Aneurysm Classification Systems. Lasjaunias et al. (10)
Perata Redekop et al. et al. (14) (19)
Unrelated to AVM
Type III
Type I
Type I
Proximal vessel, flow related
Type II
Type II
Type IIa
Distal vessel, flow related
Type I
Type III
Type IIb
Intranidal
Type I
Type IV
Type III
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profile (6, 11, 15, 25). Given the complex high-flow hemodynamics of AVMs and the relative anatomic relationships of the aneurysm to nidus, it is generally difficult to concurrently treat both pathologies in the same setting, even endovascularly (25). For unruptured aneurysms, there is a paucity of definitive guidelines for prophylactic aneurysm treatment (5, 19, 25). Regression of aneurysms associated with AVM nidal treatment has been previously described (5, 18, 19, 23). Of the distal aneurysms that resolved, embolization was undertaken on feeder pedicles associated or in close proximity to the aneurysm, but none of the proximal flowrelated aneurysms regressed with treatment (5, 14, 19). It is postulated that obliterative treatment of the AVM eventually decreased overall blood flow through feeder vessels, thereby decreasing intravascular pressure and reducing the vessel wall stress, allowing for vessel remodeling and leading to aneurysm resolution (8, 14, 18, 19). In one study, at least 50% nidal reduction was necessary for distal flowe related aneurysm regression (19). None of
these studies indicated whether the aneurysm or AVM was the source for hemorrhage. Our case of a deep perforator, flowrelated aneurysm completely regressing after only partial embolization of an AVM feeder unrelated to the aneurysm vessel has not been described. We hypothesize that this spontaneous resolution was likely secondary to changes in flow dynamics after AVM embolization arising from the left MCA. The patient had a significantly enlarged left MCA secondary to the AVM with increased blood flow even through the proximal M1 segment as seen on DSA (Figure 2). This likely also increased the blood flow through the left anterior choroidal artery, and as the vessel naturally tapers more distally, this distal segment could not compensate for the increased blood flow or intravascular pressure, thus leading to formation of the aneurysm. During the first embolization, an estimated 40% of the nidal volume was obliterated, which should reduce the blood flow through the proximal left MCA and by proxy through the left anterior choroidal artery (4). Flow-Related Aneurysm Formation in Moyamoya A similar phenomenon of deep perforator artery aneurysm formation and resolution in the setting of hemodynamic changes after circulatory bypass has been reported in the moyamoya disease (MMD) literature (2, 9, 12, 13). The incidence of aneurysm formation in MMD has been reported as being between 3% and 14% (3, 12, 24). It is believed that aneurysm formation in MMD is related to both hemodynamic stress and pathologic vessel architecture. Deep perforator collateral branch aneurysms account for 44% of MMD-associated aneurysms (2). It is hypothesized that high flows in these collateral vessels occur secondary to lack of flow through the internal carotid arteries, and this increased flow combined with a lack of robust muscular layer in these smaller vessels makes them prone to aneurysmal formation. Amin-Hanjani et al. summarized the available case reports for deep perforator aneurysm resolution after superficial temporal artery (STA)-MCA bypass, with or without encephaloduroarteriosynangiosis
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(EDAS), in MMD patients. The postulated mechanism was secondary to reduction in hemodynamic stress of the deep perforator vessels with revascularization through the bypass and/or EDAS procedure. Imaging confirmed resolution occurred as early as 1 month post procedure (9), though the average was after 6 months. It is not clear if aneurysm resolution could have occurred at a time point earlier than 1 month because there was no set criteria for when repeat DSA was undertaken in the reported cases. The exact etiology of distal flowerelated aneurysms is not well understood. However, resolution of this type of aneurysm in our patient and others with AVM nidal treatment along with the MMD data lends credit to the theory that global hemodynamic disturbances are causative. Alleviation of increased intravascular pressure, in the form of AVM nidal treatment or bypass in the setting of MMD, relieves significant stress on these more distal vessels and can lead to aneurysm resolution. This mechanism may differ from the formation of other proximal or noneflow-related aneurysms and explain why AVM treatment seems to have little effect on their regression (5, 14, 19). Our case of aneurysm regression highlights the dynamic nature of AVMs and global hemodynamic changes that can occur with nidal treatment. We highlight that in cases of ruptured AVM-associated aneurysms arising off small distal arterial feeders, treatment of unrelated main pedicle feeders can bring about changes in vessel stresses that can cause aneurysm regression. This may be particularly important in cases of acute hemorrhage where endovascular treatment is considered high risk due to small vessel caliber or tortuosity. Our lone case is not enough to make definitive conclusions about cause and effect of nidal treatment and regression of this aneurysm. It is possible that this aneurysm would regress spontaneously and that the timing of embolization was merely coincidental. In situations where direct treatment of the ruptured aneurysm associated with an AVM is too high risk, it is reasonable to attempt AVM nidal treatment first, followed by short-term DSA (within 1e2 weeks) to assess for changes in the aneurysm. If there is continued aneurysm filling, then risk/benefit regarding
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treatment of the aneurysm can be considered versus continued observation or AVM nidal treatment. CONCLUSION Aneurysm formation in the context of AVM disease still lacks a clear etiology and may be caused by multiple mechanisms given the differences in how these aneurysms respond to nidal treatment. We present a case of distal flowerelated artery aneurysm formation, a source of recurrent IVH, which spontaneously resolved after partial embolization of the AVM nidus via distant pedicle feeders. Our lone patient cannot be used to draw cause and effect relationships, and the conclusion that these aneurysms can regress with nidal treatment alone is anecdotal. We postulate that there are gross hemodynamic changes associated with AVMs that place particular stress on the distal areas of arterial feeders and predispose to aneurysm formation and/or rupture. Although primary treatment of ruptured distal flowerelated aneurysms is recommended, our case demonstrates that even when this cannot safely be done, primary treatment of the AVM may offer concurrent treatment of the at-risk aneurysm. REFERENCES 1. Akabane A, Jokura H, Ogasawara K, Takahashi K, Sugai K, Ogawa A, Yoshimoto T: Rapid development of an intranidal aneurysm with perifocal brain edema in an unruptured cerebral arteriovenous malformation. J Neurosurg 97 (6):1436-1440, 2002. 2. Amin-Hanjani S, Goodin S, Charbel FT, Alaraj A: Resolution of bilateral moyamoya associated collateral vessel aneurysms: Rationale for endovascular versus surgical intervention. Surg Neurol Int 5 (Suppl 4):S155-S160, 2014. 3. Borota L, Marinkovic S, Bajic R, Kovacevic M: Intracranial aneurysms associated with moyamoya disease. Neurol Med Chir (Tokyo) 36 (12):860-864, 1996. 4. Chuang YM, Guo W, Lin CP: Appraising the plasticity of the circle of Willis: a model of hemodynamic modulation in cerebral arteriovenous malformations. Eur Neurol 63:295-301, 2010. 5. Flores BC, Klinger DR, Rickert KL, Barnett SL, Welch BG, White JA, Batjer HH, Samson DS: Management of intracranial aneurysms associated with arteriovenous malformations. Neurosurg Focus 37:E11, 2014. 6. Garcia-Monaco R, Rodesch G, Alvarez H, Iizuka Y, Hui F, Lasjaunias P: Pseudoaneurysms within ruptured intracranial arteriovenous malformations:
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19. Redekop G, TerBrugge K, Montanera W, Willinsky R: Arterial aneurysms associated with cerebral arteriovenous malformations: classification, incidence, and risk of hemorrhage. J Neurosurg 89:539-546, 1998. 20. Sakata Y, Aoki H, Higashi K, Tsue M: Simultaneous occurrence of intracranial aneurysm and arteriovenous malformation. Nihon Geka Hokan Arch Für Jpn Chir 37:242-247, 1968.
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malformations: a clinical analysis of 14 hemorrhagic cases. Interv Neuroradiol 17:78-86, 2011.
Conflict of interest statement: All authors affirm that they have no conflicts of interest. Received 24 February 2015; accepted 28 May 2015 Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.05.065 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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