Accepted Manuscript Near-complete resolution of clinical and radiographic findings after endovascular embolization of a giant serpentine A1 aneurysm Paul R. Krafft, M.D., Howard Yonas, M.D., Andrew P. Carlson, M.D. PII: S1878-8750(15)01224-3 DOI: 10.1016/j.wneu.2015.09.057 Reference: WNEU 3243 To appear in: World Neurosurgery Received Date: 24 July 2015 Revised Date: 17 September 2015 Accepted Date: 19 September 2015 Please cite this article as: Krafft PR, Yonas H, Carlson AP, Near-complete resolution of clinical and radiographic findings after endovascular embolization of a giant serpentine A1 aneurysm, World Neurosurgery (2015), doi: 10.1016/j.wneu.2015.09.057. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. ACCEPTED MANUSCRIPT Krafft et al. Near-complete resolution of clinical and radiographic findings after RI PT endovascular embolization of a giant serpentine A1 aneurysm SC Paul R. Krafft, M.D.; Howard Yonas, M.D.; Andrew P. Carlson, M.D. Department of Neurosurgery, University of New Mexico, School of Medicine, M AN U Albuquerque, New Mexico, USA Corresponding author: Andrew P. Carlson, M.D.; Department of Neurosurgery, University of New Mexico, School of Medicine, Albuquerque, NM 87131-0001, USA. EP TE D Phone: (505) 272-3401, Fax: (505) 272-3401, Email: AndrewCarlson@salud.unm.edu AC C Key words: Anterior cerebral artery, giant serpentine aneurysm, endovascular Running title: Embolization of a giant serpentine A1 aneurysm Word count: 2,764 Figures: 5 1 ACCEPTED MANUSCRIPT Krafft et al. ABSTRACT Giant serpentine aneurysms are complex intracranial lesions, associated with a poor prognosis if left untreated. Treatment usually involves surgical trapping of the aneurysm RI PT with arterio-arterial anastomosis; however, recent endovascular management has been implemented for the management of such aneurysms. We report the unique case of a 71-year-old woman who presented with visual deficits due to mass effect of a giant SC serpentine aneurysm arising from the A1 segment of the anterior cerebral artery. Because of its location proximal to a widely patent anterior communicating artery, M AN U angiographic cure was achieved with sacrifice of the A1 segment. Clinical and radiographic follow-up demonstrated resolution of the presenting symptoms and nearcomplete obliteration of the aneurysm. Thrombosed giant serpentine aneurysms can TE D show dramatic resolution of mass effect with endovascular treatment. EP HIGHLIGHTS AC C - Currently, intracranial giant serpentine aneurysms (GSA) are not well studied. - Here, we describe our experience with the management of a patient with an A1 GSA. - Endovascular treatment resulted in a good long-term outcome of our patient. 2 ACCEPTED MANUSCRIPT Krafft et al. INTRODUCTION Giant serpentine aneurysms are greater than or equal to 2.5 cm in diameter, RI PT partially thrombosed, and contain tortuous vascular channels with a separate inflow and outflow tract.1 These nonendothelialized, intrathrombotic channels enable blood flow to distal branches of the artery from which the aneurysm originates, thus supplying vital brain parenchyma.1,6 For this reason, and in contrast to saccular variants, giant SC serpentine aneurysms cannot be occluded without ensuring adequate blood supply to M AN U the distal territories, either through spontaneous collateral circulation or surgical arterioarterial anastomosis. Here, we describe the clinical course of a patient with a symptomatic giant serpentine aneurysm of the right anterior cerebral artery (ACA), arising from the A1 segment, which was successfully treated by endovascular embolization. To our best knowledge, this is the first report describing a giant serpentine EP CASE REPORT TE D A1 aneurysm treated by endovascular embolization. AC C A 71-year-old woman with no significant medical history, presented with an acute onset of left-sided blurred vision. At that time, she was able to discern the shape of objects but could not recognize facial expressions, nor was she able to read. Because of persistence of her symptom, the patient went to an outside hospital and a computed tomography (CT) scan of her head was obtained, which demonstrated a suprasellar mass measuring approximately 3.0 x 2.3 cm in its greatest transaxial dimension with high peripheral attenuation (Figure 1). The patient was referred to our hospital for 3 ACCEPTED MANUSCRIPT Krafft et al. further evaluation and management. On arrival, her neurologic exam was intact with the exception of decreased visual acuity in the left visual field. This was also confirmed with formal Humphrey visual field testing, which showed decreased average detection RI PT sensitivity mostly in the temporal visual field of the left eye as well as in the nasal visual field of the right eye. Furthermore, an arcuate scotoma was appreciated in the right superior quadrant of the left eye (Figure 3 A). Magnetic resonance imaging (MRI) of the SC patient’s brain was performed, which confirmed the finding of a suprasellar mass lesion (Figure 2). T1-weigthed imaging demonstrated a peripheral hyperintensity of the mass M AN U (Figure 2 A) with partial contrast enhancement (Figure 2 B). Fluid-attenuated inversion recovery (FLAIR) imaging demonstrated a T2-weighted hyperintense mass with foci of hypoattenuation, possibly indicating a flow void (Figure 2 C). Diffusion-weighted imaging showed restricted diffusion within the mass (Figure 2 D), which was confirmed with an TE D apparent diffusion coefficient (ADC) map (not shown). Based on these findings, the possibility of cystic neoplasm versus dermoid/epidermoid tumor versus abscess versus aneurysm was discussed and a diagnostic cerebral angiogram was suggested to rule EP out an aneurysm prior to further treatment. AC C The angiogram of the right internal carotid artery (ICA) revealed displacement of the A1 segment and an irregular rim of serpentine filling was appreciated within the distal A1, terminating within the right A2 segment. This was thought to represent serpentine filling of a mostly thrombosed giant A1 aneurysm (Figure 4 A-D). A cross compression test was performed, which demonstrated patency of the anterior communicating artery (Acom). The decision was made to proceed with endovascular sacrifice of the involved segment of the A1. A guiding catheter was placed into the right 4 ACCEPTED MANUSCRIPT Krafft et al. ICA and a microcatheter was advanced over a 0.014” wire through the aneurysm to the A1-Acom junction. Detachable coils were then deployed from the distal A1 through the aneurysm to the normal proximal A1 segment while preserving the ipsilateral A2-Acom RI PT junction. Follow-up angiography showed occlusion of the right A1 with no filling of the aneurysm. An angiogram was then performed of the left ICA, which showed robust filling of bilateral ACA territories with no retrograde filling into the aneurysm. (Figure 4 E, SC F). M AN U The first day following endovascular embolization of the giant serpentine A1 aneurysm, the patient was complaining of worsening of her vision. Confrontation visual field testing demonstrated a left homonymous hemianopsia. At that time, the patient received dexamethasone and surgical decompression was considered; however, the patient denied any further intervention. Besides her impaired vision, the patient was in a TE D stable condition and was therefore discharged home after four hospital days. The patient had regular follow-up visits in our clinic. At 10 days post-coiling she EP underwent visual field testing, which demonstrated a worsened left homonymous hemianopsia as well as right superior quadrantanopsia of the right eye (Figure 3 B). AC C This study was repeated at 10 weeks, showing an interval improvement of the visual field deficits (Figure 3 C). She received follow-up brain MRI at 16 weeks, which showed the thrombosed giant serpentine aneurysm measuring 1.96 cm diagonally (Figure 5 A, B). Neither perilesional nor remote areas of brain ischemia were appreciated on postcoiling MR studies. Visual field testing at 14 months after aneurysm embolization demonstrated resolution of the initial visual field deficits. Brain MRI at the same time showed near-complete resolution of the giant serpentine aneurysm. The only visible 5 ACCEPTED MANUSCRIPT Krafft et al. residual abnormality was a small amount of suprasellar susceptibly artifact from the coils (Figure 5 C, D). RI PT DISCUSSION Giant serpentine aneurysms were first introduced by McLaurin and Segal in 1977 as a separate entity of intracranial aneurysms,12 distinguishable from the saccular subtype by formation of tortuous, intrathrombotic vascular channels with separate inflow SC and outflow tracts.1 It has been suggested that these lesions evolve from fusiform M AN U aneurysms, which expand due to repeated intramural bleeds.8 The oftentimes eccentrically located vascular channels form as a result of the Coandă effect, which describes an increased jet flow of fluid (e.g., blood) adjacent to a surface (e.g., aneurysmal wall); thus facilitating blood flow peripherally, while forming a thrombus centrally due to an overall decreased jet flow within the aneurysm.7 Another anatomical TE D feature of giant serpentine aneurysms is the 1 to 4 mm thick fibrous wall, containing small vessels similar to the vasa vasorum of large blood vessels.12,14 The primarily acellular fibrous tissue provides enhanced stability as compared to the wall of EP intracranial saccular or fusiform aneurysms, which usually contains a thin tunica media AC C as well as a fragmented internal elastica lamina.11 Thus, giant serpentine aneurysms are less likely to rupture, and usually present initially with signs of increased intracranial pressure or mass effect. Indeed, based on 29 of 33 giant serpentine aneurysm cases, for which clinical data was available, the predominant symptoms at presentation were headaches 72% (21 of 29), hemiparesis or hemiplegia 55% (16 of 29), decreased visual acuity or visual field deficits 48% (14 of 29), cranial nerve palsy 31% (9 of 29), and 6 ACCEPTED MANUSCRIPT Krafft et al. seizures 21% (6 of 29).1 However, subarachnoid hemorrhage was reported in 4 to 23.5% of cases.2,6 RI PT Giant serpentine aneurysms account for less than 0.1% of all intracranial aneurysms, and for 17.6% of giant aneurysms.3,15 These vascular lesions commonly involve the middle cerebral artery (50%), posterior cerebral artery (18%), vertebral artery or vertebrobasilar junction (15%), ICA (13%), and less commonly, the distal ACA SC (3%).6 Radiographically, giant serpentine aneurysms present characteristics of M AN U neoplasms and are oftentimes misdiagnosed as such.2 Pre-contrast CT imaging demonstrates well-circumscribed, heterogeneous lesions, with associated edema and mass effect.6,9 Post-contrast CT imaging reveals homogenous enhancement of the serpiginous vascular channel, with a nonenhancing central thrombus, known as the “target sign”. T1-weigthed magnetic resonance imaging findings include heterogeneous TE D hyperintensities, reflecting primarily extracellular methemoglobin as well as other blood products of varying age. Post-contrast T1-weigthed imaging shows heterogeneous enhancement; however, the vascular lumen may not enhance with gadolinium contrast.9 EP Surrounding edema and hypointense flow voids within the aneurysmal channels are AC C commonly demonstrated with T2-weigthed imaging. The natural history of giant serpentine aneurysms is variable. Suzuki et al. reported that 12 of 39 patients (30%), diagnosed with a giant serpentine aneurysm, demonstrated radiographic evidence of aneurysmal enlargement over a time period between 26 days and 5 years.13 Spontaneous and complete thrombosis, with or without revascularization, has also been reported in patients suffering from a giant serpentine aneurysm.6 Conservative management of these lesions is associated with a poor 7 ACCEPTED MANUSCRIPT Krafft et al. prognosis.13 The goal of treatment is, therefore, to arrest growth, to obliterate mass effect, and to prevent rupturing while preserving blood supply distally. RI PT Our patient presented with mass effect from the giant serpentine A1 aneurysm. Because of the fortuitous location proximal to a widely patent Acom, curative treatment could be achieved with simple occlusion of the vascular lumen and reliance on the contralateral filling of the A2. This is in contradistinction to most reported cases of giant SC serpentine aneurysms, where the distal vessel needed to be re-vascularized prior to M AN U trapping of the aneurysm, in order to avoid cerebral ischemia. The other surprising element of this case was the resolution of radiographic and clinical presentation of this aneurysm. Patients undergoing treatment of cavernous carotid aneurysms, either with parent vessel sacrifice or more recently with flow diversion, are known to have transient worsening of cranial neuropathies likely related to swelling and inflammatory TE D reactions.4,10 Therefore, it was thought to be reasonable to follow the patient conservatively despite the transient worsening of visual field deficits. In the case of flow diversion, improvement of preexisting cranial neuropathies has been reported as 75%; EP however, 25% of patients experienced a transient worsening of their symptoms.10 AC C Although flow diverter devices are now frequently deployed in patients with complex intracranial aneurysms, including giant aneurysm, for which complete occlusion was found to be 76% at 6 months post-embolization,5 we decided to sacrifice the vascular channel of the giant serpentine A1 aneurysm, due to patency of the Acom and sufficient blood supply to the ipsilateral A2 segment from the contralateral side. Furthermore, we preferred not to place our patient on antiplatelet therapy, which is obligatory when utilizing a flow diverter device. Navigating the device through the tortuous vascular 8 ACCEPTED MANUSCRIPT Krafft et al. channel of the aneurysm would likely have been challenging. Lastly, the procedurerelated morbidity and mortality rates of 4% and 5% respectively, associated with RI PT placement of a flow diverter device, are not negligible [5]. CONCLUSIONS SC We present the first reported case of a giant serpentine aneurysm of the A1 segment, treated endovascularly. Because of its location proximal to a widely patent M AN U Acom, angiographic cure was achieved with sacrifice of the A1 segment. Clinical and radiographic follow-up demonstrated resolution of the presenting visual complaints and near-complete obliteration of the aneurysm itself. The principle of treatment of giant serpentine aneurysms involves trapping and distal revascularization either with surgical TE D anastomosis or with internal collaterals. Thrombosed aneurysms can show dramatic resolution of mass effect with adequate treatment, despite initial worsening of EP symptoms. AC C DISCLOSURE: The authors have no disclosures to report. 9 ACCEPTED MANUSCRIPT Krafft et al. REFERENCES 7. 8. 9. 10. 11. 12. 13. 14. 15. RI PT 6. SC 5. M AN U 4. TE D 3. EP 2. Aletich VA, Debrun GM, Monsein LH, Nauta HJ, Spetzler RF: Giant serpentine aneurysms: a review and presentation of five cases. AJNR Am J Neuroradiol 16:1061-1072, 1995 Anshun W, Feng L, Daming W: Giant serpentine aneurysms: multidisciplinary management. Report of four cases and review of the literature. Interv Neuroradiol 6:41-52, 2000 Anson JA, Lawton MT, Spetzler RF: Characteristics and surgical treatment of dolichoectatic and fusiform aneurysms. J Neurosurg 84:185-193, 1996 Berge J, Tourdias T, Moreau JF, Barreau X, Dousset V: Perianeurysmal brain inflammation after flow-diversion treatment. AJNR Am J Neuroradiol 32:1930-1934, 2011 Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF: Endovascular treatment of intracranial aneurysms with flow diverters: a meta-analysis. Stroke 44:442-447, 2013 Christiano LD, Gupta G, Prestigiacomo CJ, Gandhi CD: Giant serpentine aneurysms. Neurosurg Focus 26:E5, 2009 Fodstad H, Liliequist B, Wirell S, Nilsson PE, Boquist L, Abdul-Rahman A: Giant serpentine intracranial aneurysm after carotid ligation. Case report. J Neurosurg 49:903-909, 1978 Lukin RR, Chambers AA, McLaurin R, Tew J, Jr.: Thrombosed giant middle cerebral aneurysms. Neuroradiology 10:125-129, 1975 Mawad ME, Klucznik RP: Giant serpentine aneurysms: radiographic features and endovascular treatment. AJNR Am J Neuroradiol 16:1053-1060, 1995 Moon K, Albuquerque FC, Ducruet AF, Crowley RW, McDougall CG: Resolution of cranial neuropathies following treatment of intracranial aneurysms with the Pipeline Embolization Device. J Neurosurg 121:1085-1092, 2014 Schievink WI: Intracranial aneurysms. N Engl J Med 336:28-40, 1997 Segal HD, McLaurin RL: Giant serpentine aneurysm. Report of two cases. J Neurosurg 46:115120, 1977 Suzuki S, Takahashi T, Ohkuma H, Shimizu T, Fujita S: Management of giant serpentine aneurysms of the middle cerebral artery--review of literature and report of a case successfully treated by STA-MCA anastomosis only. Acta Neurochir (Wien) 117:23-29, 1992 Terao H, Muraoka I: Giant aneurysm of the middle cerebral artery containing an important blood channel. Case report. J Neurosurg 37:352-356, 1972 Vlahovitch B, Fuentes JM, Reynaud C, Benbouzid T, Mazariegos R: [Series of 17 cases of giant intracranial aneurysms. Long-term surgical follow-up and hemodynamic effects of arterial occlusions]. Neurochirurgie 31:255-263, 1985 AC C 1. 10 ACCEPTED MANUSCRIPT Krafft et al. FIGURE LEGENDS Figure 1: CT Head without contrast. Multidetector helical computed axial tomogram of RI PT the head demonstrates a suprasellar mass measuring approximately 3.0 x 2.3 cm in its greatest transaxial dimension with high peripheral attenuation. Arrows depict margins of the suprasellar mass. SC Figure 2: MRI brain with and without contrast. A) T1-weighted sagittal sequence without contrast demonstrates a suprasellar mass lesion, measuring 2.66 cm diagonally M AN U (red line), with a peripheral hyperintense pattern B) T1-weighted sagittal sequence after intravenous administration of Gadolinium DTPA contrast shows partial contrast enhancement of the lesion margin (arrows). C) Axial fluid-attenuated inversion recovery (FLAIR) imaging demonstrates a T2-weighted hyperintense mass with foci of TE D hypoattenuation, possibly indicating a flow void (arrow head). The suprasellar mass is located in the anterior midline extending paramedially to the right causing partial effacement of the third ventricle. D) Axial diffusion-weighted imaging obtained at b1000 EP shows a well-demarcated area of restricted diffusion (dotted arrow). Figure 3: Humphrey visual field perimetry. A) Pre-embolization: The gray scale AC C shows regions of decreased average detection sensitivity mostly in the temporal visual field of the left eye as well as in the nasal visual field of the right eye, consistent with left homonymous hemianopsia. An arcuate scotoma is appreciated in the right superior quadrant of the left eye. B) 10 days post coiling: The gray scale demonstrates an interval worsening of the left homonymous hemianopsia as well as right superior quadrantanopsia of the right eye. C) 10 weeks post coiling: The gray scale shows 11 ACCEPTED MANUSCRIPT Krafft et al. interval improvement of the left homonymous hemianopsia. D) 14 months post coiling: The gray scale demonstrates complete resolution of the initial visual field defects. RI PT Figure 4: Diagnostic cerebral angiography and embolization of an A1 aneurysm: A) Right ICA injection, anteroposterior projection: Arterial phase cerebral angiogram demonstrates M1 (dotted arrow) and S1 segments (encircled), inflow of the giant serpentine aneurysm (white arrow), as well as delayed filling of its vascular channel SC (asterisk). B) Right ICA injection, transorbital oblique projection: Arterial phase cerebral M AN U angiogram shows M1 (dotted arrow), S1 (encircled), and S2 (arrow head) segments, as well as inflow (white arrow) and vascular channel (asterisk) of the giant serpentine aneurysm. C) Right ICA angiogram, 3D reconstruction: Visualization of the aneurysm from a left lateral perspective. Inflow (white arrow), outflow (arrow head), and vascular channel are depicted. D) Right ICA angiogram, 3D reconstruction: Visualization of the TE D aneurysm from a right lateral perspective. Inflow (white arrow), outflow (arrow head), and vascular channel are depicted. E) Right ICA injection, anteroposterior projection, post-coiling: Arterial phase cerebral angiogram demonstrates M1 (dotted arrow) and S1 EP segments (encircled), as well as complete occlusion of the aneurysms (white box). F) AC C Left ICA injection, anteroposterior projection, post-coiling: Arterial phase demonstrates contralateral M1 (dotted arrow), S1 (black arrow), S2 (black arrow head) segments, as well as complete occlusion of the aneurysm (white box). Filling of the ipsilateral A2 segment (white arrowhead) is enabled through the Acom (white arrow). Figure 5: MRI brain with and without contrast, post-coiling. A) T1-weighted sagittal sequence without contrast at 4 month post-coiling demonstrates the thrombosed giant serpentine aneurysm measuring 1.96 cm diagonally (red line). B) T1-weighted coronal 12 ACCEPTED MANUSCRIPT Krafft et al. sequence without contrast at 4 months post-coiling shows the thrombosed suprasellar aneurysm. The pituitary gland is depicted (white arrow). C) T1-weighted sagittal sequence without contrast at 14 months post-coiling demonstrates near-complete RI PT resolution of the giant serpentine aneurysm. Small hypointense mass (dotted arrow) situated superiorly to the optic chiasm (arrow head) and pituitary gland (white arrow) likely represents the coil within the aneurysm. D) T1-weigthed coronal sequence without SC contrast at 14 months post-coiling shows the optic chiasm (arrow head) and the pituitary AC C EP TE D superiorly to the optic chiasm. M AN U gland (white arrow). A remnant of the aneurysm may be appreciated right laterally and 13 AC C EP TE D M AN U SC RI PT ACCEPTED MANUSCRIPT AC C EP TE D M AN U SC RI PT ACCEPTED MANUSCRIPT AC C EP TE D M AN U SC RI PT ACCEPTED MANUSCRIPT AC C EP TE D M AN U SC RI PT ACCEPTED MANUSCRIPT AC C EP TE D M AN U SC RI PT ACCEPTED MANUSCRIPT ACCEPTED MANUSCRIPT RI PT HIGHLIGHTS - Currently, intracranial giant serpentine aneurysms (GSA) are not well studied. - Here, we describe our experience with the management of a patient with an A1 SC GSA. AC C EP TE D M AN U - Blood flow diversion resulted in a good long-term outcome of our patient. ACCEPTED MANUSCRIPT Krafft et al. Abbreviations: ACA: anterior cerebral artery, Acom: anterior communicating artery, ADC: apparent diffusion coefficient, CT: computed tomography, FLAIR: Fluidattenuated inversion recovery, ICA: internal carotid artery, MRI: Magnetic resonance AC C EP TE D M AN U SC RI PT imaging 1