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Parent vessel occlusion for treatment of cerebral aneurysms: Is there still an indication? A series of 17 patients
Journal of the Neurological Sciences 372 (2017) 250–255
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Parent vessel occlusion for treatment of cerebral aneurysms: Is there still an indication? A series of 17 patients Nishant Ganesh Kumar d,⁎, Travis R. Ladner d, Imad S. Kahn e, Scott L. Zuckerman d, Christopher B. Baker a,c, Marybess Skaletsky a, Deborah Cushing a, Matthew R. Sanborn a, J Mocco f, Robert D. Ecker a,b a
Maine Medical Center, Neuroscience Institute, Portland, Maine, USA Maine Medical Center, Department of Surgery, Portland, ME, USA c Maine Medical Center, Department of Radiology, Portland, ME, USA d Vanderbilt University Medical Center, Department of Neurosurgery, Nashville, Tenessee, USA e Dartmouth Hitchcock Medical Center, Department of Neurosurgery, Hanover, New Hampshire, USA f Mt. Sinai Medical Center, Department of Neurosurgery, New York, New York, USA b
a r t i c l e
i n f o
Article history: Received 11 June 2016 Received in revised form 27 October 2016 Accepted 22 November 2016 Available online 23 November 2016 Keywords: Aneurysm Balloon test occlusion Parent vessel occlusion Giant aneurysm
a b s t r a c t Introduction/purpose: Flow diversion has allowed cerebrovascular neurosurgeons and neurointerventionalists to treat complex, large aneurysms, previously treated with trapping, bypass, and/or parent vessel sacrifice. However, a minority of aneurysms remain that cannot be treated endovascularly, and microsurgical treatment is too dangerous. However, balloon test occlusion (macro and micro), micro WADA testing, ICG, intra-angiography and intra-operative monitoring are all available to clinically test the hypothesis that vessel sacrifice is safe. We describe a dual-institution series of aneurysms successfully treated with parent vessel occlusion (PVO). Materials/methods: Prospectively collected databases of all endovascular and open cerebrovascular cases performed at Maine Medical Center and Vanderbilt University Medical Center from 2011 to 2013 were screened for patients treated with primary vessel sacrifice. A total of 817 patients were screened and 17 patients were identified who underwent parent vessel sacrifice as primary treatment. Results: All 17 patients primarily treated with PVO are described below. Nine patients presented with SAH, and 3/ 17 involved anterior circulation. Complete occlusion was achieved in 15/17 patients. In the remaining 2 patients, significant reduction in the aneurysm occurred. Modified Rankin Score (mRS) of 0, signifying complete independence, was achieved for 16/17 patients. One patient died due to an extracranial process. Conclusions: Parent vessel sacrifice remains a viable and durable solution in select ruptured and unruptured intracranial aneurysms. Many adjuncts are available to aid in the decision making. In this small series, patients naturally divided into vertebral dissecting aneurysms, giant aneurysms and small distal aneurysms. Outcomes were favorable in this highly selected group. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Parent vessel occlusion (PVO) is a traditional method for treating aneurysms that are not amenable to direct coiling/clipping or particularly complex saccular or fusiform aneurysms. It has been successfully
Abbreviations: AICA, Anterior Inferior Cerebellar Artery; AVM, Arterial-venous Malformation; BTO, Balloon test occlusion; ICA, Internal Carotid Artery; ICG, Indocyanine green; MMC, Maine Medical Center; MCA, Middle Cerebral Artery; mRS, Modified Rankin Score; NBCA, n-butyl cyanoacrylate; PVO, Parent Vessel Occlusion; PICA, Posterior inferior cerebellar artery; SAH, Subarachnoid hemorrhage; SCA, Superior Cerebellar Artery and Vanderbilt University Medical Center (VUMC). ⁎ Corresponding author at: Vanderbilt University School of Medicine, Medical Center North T-4224, Nashville, TN 37212, USA. E-mail address: [email protected] (N. Ganesh Kumar).
http://dx.doi.org/10.1016/j.jns.2016.11.057 0022-510X/© 2016 Elsevier B.V. All rights reserved.
implemented in the treatment of aneurysms involving the vertebrobasilar junction [1–4], posterior cerebral artery [5–7] and peripheral cerebral aneurysms [8,9] when adequate collateral flow is present. Flow diverters have introduced another class of treatment options for these complex aneurysms that historically would have undergone trapping, parent vessel sacrifice, or bypass. However, PVO still remains a viable option. There are many well-established diagnostic modalities to determine feasibility of PVO, including intra-operative monitoring, balloon test occlusion (BTO), and Wada testing. These can aid in patient selection to ensure that PVO, if indicated, is safe. Therefore, interventionalists and neurosurgeons should keep PVO in their armamentarium of treatment options. Here we review the experiences of two centers using PVO as a favorable solution in a select group of patients with intracranial aneurysms.
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2. Methods
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subocippital craniotomy was made, from the superior pinna running inferiorly to the midline underneath the inion to the spinous process of C2. Pericranium was harvested during exposure for the duraplasty. The avascular midline was followed down to the spinous process of C1 and C2. A craniotomy was performed from the transverse-sigmoid junction to the midline of the foramen magnum. The ipsilateral lamina of C1 was removed, with care taken to visualize the extradural vertebral artery. The dura was opened from the transverse-sigmoid junction to the arch of C1. After the operating microscope was brought into the field, the arachnoid was opened and CSF was drained from the cisterna magna. Based on location of the pathology along the vertebral artery or PICA, surgical corridors between the inferior cranial nerve IX, X and XI in the middle, and VII and VIII superiorly are utilized to safely sacrifice the involved vessel. Though most open cases involved the posterior circulation, for any anterior circulation procedures, a standard curvilinear pterional incision was made and a myocutaneous flap was reflected anteriorly. Exposure of the keyhole and the temporal bone was achieved, and a standard pterional craniotomy bone flap was turned. In the case of anterior circulation sacrifice, the sphenoid wing was aggressively drilled down and flattened. If periorbita was encountered, the area was immediately waxed. A curvilinear dural incision was then made after hemostasis was achieved, and the microscope was brought into the field. A subfrontal approach was taken. The olfactory tract was found and followed to the optic nerve, leading to the supraoptic cistern, which was then decompressed. The ICA was then located, and the sylvian fissure was carefully opened with sharp dissection. Depending on the pathology, the involved intracranial vessel was dissected out, able to obtain proximal and distal control when needed. For either approach, a combination of bayoneted and/or straight clips was used to ensure the aneurysm and parent vessel were occluded. Once the necessary vessel sacrifice was performed, attention was turned to hemostasis and closure. The dura was approximated, a pericranial graft was sewed in when necessary, the bone flap was replaced, and the scalp was closed in a usual fashion. A post-procedure angiogram was then performed to confirm occlusion of the parent vessel. A representative open case is presented in Fig. 1. For endovascular PVO, the patient was intubated and positioned supine in the angiogram suite. Whereas the patient was kept awake for any BTO or Wada test, all patients were placed under general anesthesia for endovascular PVO. The groin area was prepped and draped in a sterile fashion. Access into the right common femoral artery with a needle,
2.1. Study design and data collection A retrospective case series was obtained from two prospectively collected databases of all patients undergoing endovascular and open cerebrovascular treatment over a two-year period at Maine Medical Center (MMC) and Vanderbilt University Medical Center (VUMC). From February 2011 to April 2013, 817 patient records were screened between both databases, and 17 patients were identified who underwent PVO as the primary treatment for an aneurysm not amenable to direct embolization or clipping (Table 1). This is a highly selected group representing approximately 2–3 patients per year from each medical center where the total combined annual number of aneurysm presenting cases is greater than 250. The electronic medical records for these patients were reviewed, using clinic notes, operative notes, and angiographic images. Demographic variables were collected and defined as age and sex. Clinical variables were collected and defined as presence of subarachnoid hemorrhage (SAH), aneurysm location, aneurysm morphology, and treatment modality. Outcome variables were collected and defined as aneurysm occlusion on follow-up angiography, presence of postoperative complications, and functional outcome as measured by the modified Rankin score (mRS) at last follow-up. 2.2. Operative technique All patients were treated endovascularly or with open sacrifice, as depicted in Table 1. Preoperatively, a BTO was performed in line with technique previously published [10]. The patient was kept awake, and groin access was obtained through the right common femoral artery up to the involved parent vessel. A balloon was then inflated in the proximal segment of the involved vessel to complete occlusion. Neurologic exams were obtained in the 10–20 min after occlusion, and the balloon was immediately deflated with any deviation in exam. Given the extensive collateral circulation, BTO was not used in everyone, but rather select patients. For open PVO, the patient was intubated, a right groin sheath was placed and a pre-procedure angiogram performed. The patient was then positioned on the appropriate side of the aneurysm. Neuromonitoring with SSEP and EEG were utilized. For distal vertebral artery and PICA lesions, an S-shaped incision for a far-lateral
Table 1 Patient demographics and location of aneurysm along with treatment method and post-operative aneurysm occlusion status, procedural complications and mRS. SAH: Subarachnoid hemorrhage, PICA: Posterior inferior cerebellar artery, MCA: Middle Cerebral Artery, SCA: Superior Cerebellar Artery, ICA: Internal Carotid Artery, AICA: Anterior Inferior Cerebellar Artery, AVM: Arterial-venous Malformation, NBCA: n-butyl cyanoacrylate, mRS: Modified Rankin Score, I: Incomplete, C: Complete. Case SAH Aneurysm type and morphology
Treatment
Occlusion Complication
mRS
1 2 3 4 5 6 7
N N Y Y Y Y N
Dissecting vertebral Giant ICA Distal PICA Dissecting vertebral Dissecting vertebral Distal mycotic MCA Giant basilar
I C C C C C I
None None None None None SMA infarct MCA infarct
0 0 0 0 0 0 0
8 9 10 11 12 13
N Y Y N N N
C C C C C C
None None None Scattered SCA infarcts None None
0 0 0 0 0 0
14
Y
Giant PICA Dissecting vertebral Distal PICA Distal SCA Giant vertebral Residual distal SCA feeding aneurysm after AVM resection Ruptured AICA feeding aneurysm to AVM
Coil Coil NBCA Coil Coil Onyx Mid basilar clipping Distal clipping Coil Clip trapping Coil Coil + Amplatzer Coil Onyx
C
6
15 16 17
Y N Y
Dissecting vertebral Dissecting fusiform PCA Dissecting blister ICA
Coil Coil + onyx Clip trapping
C C C
Tonsillar infarct. Death from bleeding esophageal varices 2.5 weeks post-op None None None
0 0 0
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Fig. 1. Case 7. Patient in 60s with 1 month of progressive gait difficulty with decrement from unaided to walker assisted, swallowing difficulty and double vision. Imaging revealed a giant basilar tip aneurysm with brainstem compression. Preoperative axial T2 MRI revealed basilar aneurysm with severe brainstem compression (A). Sagittal CTA demonstrated the smaller filling and larger thromboses portion of the aneurysm (B), and 3-D right vertebral angiogram showed the filling portion of the giant basilar aneurysm (C). The patient was taken for an extended pterional craniotomy, utilizing a combined subtemporal and pterional corridors, where basilar artery was clipped. Post-operatively, left sided weakness was noted, and ischemic injury at the anterior temporal pole and inferior frontal lobe was seen on MRI. This was thought to be a venous infarction due to retraction injury, as the stroke did not fit a single artery distribution. Weakness improved over time and became clinically insignificant. At 3 months post-operatively, patient was independent at home with all pre-operative symptoms resolved. At 6 months post-operatively, a right ICA selective angiogram showed dramatic involution of the aneurysm (D), and a right selective vertebral artery injection demonstrated the clip position above the AICAs (E). At 1 year, axial T2 MRI showed significant improvement in the brainstem compression and aneurysm shrinkage (F).
wire, and sheath was achieved without complication. After a right femoral angiogram, a #6 French Envoy was advanced over an 0.035 Glidewire up the aortic arch to catheterize the involved common carotid
artery. Additional selective catheterization and angiograms were performed in order to visualize collateral circulation to the area of interest. Once enough collateral circulation was present and other options (i.e.
Fig. 2. Case 15. Patient in 30s presented with a subarachnoid hemorrhage (A), with evidence of a right dissecting fusiform vertebral artery aneurysm on CTA (B). On arrival to our hospital patient re-ruptured and clinical status worsened to Hunt and Hess grade 4, and ventriculostomy was performed. Patient underwent angiography which demonstrated the aneurysm and a distal AICA/PICA vessel at the junction of the right vertebral artery and basilar artery. Angiographic run through the left vertebral artery also demonstrated filling of the right AICA/PICA vessel. Consideration was made for flow diversion or other options; however, this did not appear to be safe or appropriate particularly as the patient had just re-ruptured. The anatomy was favorable for parent vessel occlusion, and therefore a total of 60 coils were deployed in the V3 segment of the right vertebral artery (D). Final angiographic run demonstrated complete shutdown of flow through the right vertebral artery with no residual aneurysm (E), with complete preservation of flow to the remainder of the posterior circuclation through the left vertebral artery (F). On postoperative day 3, the patient developed clinical vasospasm with elevated velocities in the bilateral MCA and left ACA territories on transcranial doppler but negative CTA. Neurological exam improved with hemodynamic support with no other interventions. Patient remained neurologically intact, the external ventricular drain was removed, and was discharged home on postoperative day 19 with a modified Rankin score of 0.
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flow diversion, stent coil, etc.) were deemed too risky, parent vessel sacrifice was chosen as the method of treatment. This was often done in the setting of a co-dominant vertebral artery or an aneurysm far enough in the peripheral vasculature that occlusion would not cause significant ischemia. The parent vessel was then coiled. Multiple angiograms were performed during and after coil embolization to determine the extent of occlusion and ensure no thromboembolic complications. Once this was done, the microcatheter was removed in a standard fashion, and the groin closed with a range of closure devices. A representative case of endovascular occlusion is presented in Fig. 2. Of note, the decision to choose PVO over other options such as stentcoil and flow diversion was made after careful consideration. For acute SAH, any option to avoid antiplatelet agents were preferred due to the recent hemorrhage and presence of an external ventricular drain (EVD). For example, the patient with a dissecting blister ICA aneurysm had a poor grade, an EVD, and adequate collateral circulation based on intraoperative angiography. PVO was deemed the safest and most effective treatment. Distal aneurysms where microcatheter insertion and/or stent/coil deployment were deemed unsafe were also considered good candidates for PVO. Overall, final treatment decisions were made based on presentation, collateral flow, vascular anatomy, and prior treatments. It is our practice to provide dual antiplatelet therapy after flow diversion with aspirin and Plavix for a minimum of 3 months when using a metal stent or Pipeline. For all cases, all patients received 5000 U of heparin at the start of the procedure and 1000 U every hour until completion. Potentially relevant vessels and perforators were avoided during PVO.
2.3. Data analysis Descriptive statistical analysis was performed in Microsoft Excel 2011 (Microsoft Corp, Redmond, WA). For patient age, mean, standard deviation, and range were determined. For categorical variables (all other variables), number and percentage were determined.
3. Results During the study period, 17 aneurysms were treated in 17 patients via PVO. The mean age of the patients was 53.5 ± 13.5 (range 37–84) years. There were 7 (41.2%) female patients. Nine (52.9%) patients presented with subarachnoid hemorrhage, with 4 of these 9 ruptured aneurysms being dissecting vertebral artery aneurysms. The majority of aneurysms (14, 82.4%) involved the posterior circulation: vertebral (n = 6), PICA (n = 3), AICA (n = 1), SCA (n = 2), basilar (n = 1), and PCA (n = 1). The remaining aneurysms in the anterior circulation were a dissecting ICA, a giant ICA, and a mycotic MCA aneurysm. Aneurysm morphologies were primarily vertebral dissecting aneurysms (n = 5), giant aneurysms (n = 7), and small distal aneurysms (n = 5). Four aneurysms were treated via open surgical clipping of the parent vessel. Ten were treated via coiling, with adjunctive use of the Amplatzer atrial septal occluder device (AGA Medical Corporation, Golden Valley, MN) in 1 patient and Onyx (Covidien, Irvine, CA) in 1 patient. Of the remaining patients, 2 vessels were embolized using Onyx alone and 1 was occluded via NBCA (n-butyl cyanoacrylate). Complete occlusion was achieved in 15 (88.2%) cases. In the remaining 2 patients (coiled dissecting vertebral and clipped giant basilar) significant reduction in the aneurysm occurred. Postoperatively, there were three patients with new cerebral infarcts: 1) SMA infarct in a distal MCA aneurysm, 2) MCA territory infarct in a giant basilar aneurysm, and 3) scattered SCA territory infarcts in a distal SCA aneurysm. One patient developed a tonsillar infarct after Onyx embolization of an AICA aneurysm; this patient died from ruptured esophageal varices 2.5 weeks after treatment. Modified Rankin Score (mRS) of 0, signifying complete independence, was achieved for the other 16 (94.1%) patients.
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4. Discussion With well-developed endovascular and open techniques, the use of PVO has fallen out of favor. However, in the case of complex, posterior circulation, giant, or dissecting aneurysms, there are still instances where PVO may play an important role in safe aneurysm occlusion [8, 9]. We reviewed the results of PVO for a subset of complex aneurysms treated in the era of flow diversion. In this highly selected group, PVO was still a viable option with favorable outcomes [5]. Complete occlusion was achieved in 15/17 patients. In the remaining 2 patients, significant reduction in the aneurysm occurred. Modified Rankin Score (mRS) of 0 was achieved for 16/17 patients. Three patients developed new cerebral infarcts. One patient died, though this was due to systemic hepatic disease. We review the relevant literature on PVO below. 4.1. Diagnostic testing Diagnostic modalities are essential if PVO is performed due to the higher risk of ischemic events. In PICA dissecting aneurysms, Trivelato et al. found an ischemic complication rate of 20.4% (11/54) in PVO vs. 14.3% (4/28) in coiling [11]. Similarly, van der Schaaf et al., found that late ischemic complications occurred in 3.4% of patients treated with permanent balloon occlusion compared to no complications in patients treated with coil embolization [12]. The Wada test and the balloon test occlusion (BTO) are two commonly used pre-PVO tests [7]. However, BTO has its limitations, including rare complications such as aneurysm rupture after deflation of the temporary balloon [13]. In addition, BTO has been associated with false positive and negative results [14–16]. Given this, other diagnostic methods are necessary including micro WADA testing, ICG (Indocyanine green), intraoperative angiography and intraoperative monitoring. All of these are available to clinically test the hypothesis in an individual patient that PVO is safe. 4.2. Embolization agents Some of the most commonly used embolization agents for PVO include GDCs, detachable balloons and fibered and non-fibered platinum coils [4,17–20]. Due to being more thrombogenic, fibered platinum coils are considered more useful in carrying out short segment thrombosis compared to non-fibered coils [21]. Kurata et al., successfully performed aneurysm occlusion in 18/18 patients using platinum coil embolization for dissecting vertebral aneurysms with complete occlusion at the site still present at 9 month follow up. While the clinical experience of flow diversion is growing, economic projections by Withers et al. suggest a higher cost for flow diversion (£24,341) compared to endovascular PVO (£16,893) and surgical PVO (£11,654) over a 10-year period [22]. While this may suggest a cost advantage to PVO, cost modeling proves challenging. The price of the devices required for the procedure is the major driver of total cost; however, complication rate and healthcare resource utilization also factor into costs associated with PVO, as stroke is a not uncommon complication, and greater experience is needed to accurately compare PVO with flow diversion [23]. 4.3. Outcomes with PVO 4.3.1. PCA Large or giant P2 segment aneurysms of the PCA are suitable for PVO [24]. The thalamoperforating vessels arise from the P1 segment and an aneurysm distal to these branches may be safely managed with sacrifice of the parent vessel. Hallacq and colleagues used PVO to manage 9 patients with P2 segment aneurysms [7]. They had successful aneurysm occlusion in all 9 patients and no neurological complications. Arat et al. reported similar results in their series of eight patients with large or giant P2 aneurysms treated with PVO with immediate post-operative infarcts 37.5% of patients (3/8) [6]. On long term 1 year follow up, the
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only complication was occipital infarct with homonymous hemianopsia. With dissecting P2 aneurysms, Lv et al. reported complete occlusion in 8/8 and no permanent complications after coil-mediated PVO [25]. Liu et al., had similar results in a series of 12 patients with PCA aneurysms treated with coil-mediated PVO, with excellent embolization but one case of transient hemianopsia [26].
4.3.2. Distal location Distally located aneurysms can be very challenging to treat while keeping the parent vessel patent due to the small vessel diameters involved. In these instances, PVO has been reported to be very useful. Eckard et al. reported using PVO in 9 patients with peripheral aneurysms [8]. Coil occlusion was performed proximal to the aneurysm in six cases, and the aneurysm was trapped in three cases. Complete obliteration was achieved in all patients and for the six patients with followup angiograms, continued complete occlusion was documented. Others have also reported the use of PVO in the distal circulation with limited or no collateral blood flow [20,27,28]. Cui and colleagues reported a series of 12 patients with peripheral intracranial aneurysms not amenable to selective embolization that underwent PVO with platinum coils [5]. On long-term follow-up, the authors reported no permanent neurological sequelae and enduring obliteration of the aneurysms in all patients. Non-mycotic fusiform peripheral aneurysms have also been managed with PVO. Andreou and colleagues described their experience with 18 patients who underwent PVO (15 coiled, 4 glued). Five patients developed transient neurologic deficits and 2 had permanent neurologic deficits (a visual field defect in both).
4.3.3. Mycotic Mycotic aneurysms are amenable to PVO because they are almost always found in the peripheral branches, making isolation of the aneurysm and vessel challenging. Khayata et al. reported successful obliteration in two patients with mycotic aneurysms treated with PVO (glue for PCA aneurysm, autologous blood clot for MCA aneurysm) [27]. Teitelbaum et al. also reported the successful treatment of a mycotic PICA aneurysm using PVO with microcoils [28]. 4.3.4. Posterior Circulation Aneurysms Peripheral posterior circulation aneurysms may also be managed with PVO. Lubicz and colleagues described the endovascular management of eight cerebellar aneurysms, out of which two large peripheral cerebellar artery aneurysms and one small aneurysm with a wide neck were treated by PVO [29]. PVO in these cases was achieved with GDCs. The authors reported complete obliteration in these aneurysms and excellent outcome in two patients while one patient developed CN VII nerve palsy. Overall, obliteration of the aneurysm should be the aim in cases where PVO is being employed, as the outcomes are notably better compared to cases with residual filling [30]. We were able to achieve complete obliteration of the aneurysm in 15 of the 17 cases. One of our patients with a dissecting VA aneurysm had a residual filling aneurysm after treatment but has remained asymptomatic since the procedure. Table 2 represents a summary of some of the cases series discussed above. While the landscape of cerebrovascular intervention continues to rapidly evolve, the long-term effects of PIPELINE embolization are unknown. Moreover, with favorable outcomes associated with using PVO
Table 2 Summary of case series and reviews involving Parent Vessel Occlusion (PVO). PICA: Posterior inferior cerebellar artery, MCA: Middle Cerebral Artery, SCA: Superior Cerebellar Artery, ICA: Internal Carotid Artery, AICA: Anterior Inferior Cerebellar Artery, AVM: Arterial-venous Malformation. BA: Basilar Artery, VA: Vertebral Artery, IC: Internal Carotid. Study
Aneurysm location (patients)
Surgical approach
Outcomes
Lv et al., 2009 [25]
P2 dissecting [8]
Endovascular PVO with detachable coils
No patient developed neurological deficits
Trivelato et al., 2014 [11]
PICA dissecting [14]
8 selective coiling 6 PVO
Liu et al., 2011 [26]
PCA non-saccular [12]
Detachable coils
Leibowitz et al., 2003 [30]
VA and BA [13]
I: PVO with complete aneurysm thrombosis [6]
Kallmes et al., 2004 [21] Hallacq et al., 2002 [7]
IC [2], VA [3] P2 [10]
Cui et al., 2009 [5]
PCA [7], AICA [2], PICA [1], MCA [2]
Eckard et al., 2000 [8]
PICA [2], SCA [2], AICA [1], PCA [3], MCA [1], ACA [1] Large/Fusiform distal PCA [8]
Arat et al., 2002 [6]
Andreou et al., 2007 [9]
PCA [9], SCA [5], AICA [1], PICA [5], MCA [5], ACA [2]
II: PVO without complete aneurysm thrombosis [7] PVO using HES coils Endovascular PVO [9]. 1 deferred due to vascular tortuosity. PAO with detachable coils
PVO using microcoils
Urgent treatment after SAH [3] Elective treatment [5]
Detachable coils [7]. Fusiform aneurysms with PAO coils [15], glue [4]. Spontaneous thrombosed aneurysm [1].
Conclusion
P2 dissecting aneurysms can be treated with PVO in cases in which selective embolization of the aneurysmal sac with detachable platinum coils or surgical clipping cannot be achieved. No statistical difference between both Both interventions are highly effective in preventing groups regarding complications. rebleeding. PVO is significantly associated with higher risk of ischemic events. Total complication rate is similar between both modalities. No neurological complications [11]. PVO via detachable coils appears to be well tolerated for Transient hemianopsia [1]. non-saccular aneurysms in P2 distal segment of PCA location All in group I showed improvement [6] In patients with an aneurysm including one vertebral In group II, 4 died during follow-up. 2 due artery (VA) where complete thrombosis can be achieved, to aneurysms. better clinical outcomes are attainable when compared to 2 others had worsening symptoms. 1 those with aneurysms of the basilar artery (BA) or both VA other remained stable. where complete thrombosis cannot be achieved. None reported No neurologic deficit after treatment.
No patient developed neurological deficits. Transient diplopia and vertigo [1]. Mild nondisabling neurologic deficits [3].
Permanent homonymous hemianopia [1]. Excellent recovery [6]. Lost to follow up [1]. 5/18 who underwent PAO developed neurological deficits. 2/18 had permanent neurological deficit (visual field defect)
HES could be a viable option for rapid short segment occlusion Acute parent artery occlusion appears to be safe in treatment of P2 segment aneurysms, whatever the location of occlusion. Distally located cerebral aneurysms can be treated with PAO when selective embolization of aneurysmal sac with detachable coils or surgical clipping cannot be achieved. PVO for aneurysms that are difficult surgically or for intra-aneurysmal coil placement. Endovascular PAO may be alternative to surgical PAO in distal PCA aneurysms not convenient for selective endovascular treatment or surgical clipping. Distally located aneurysms can be treated with endovascular PAO in the cases in which selective occlusion of aneurysmal sac with coil or clipping cannot be achieved.
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in carefully chosen patients, further exploration into the frequency of its use is warranted and how both methods can be used in tandem to provide the optimal treatment. Our case series is not without limitation. First, this is retrospective. Second, this cohort was highly selected at institutions where flow diversion is also regularly performed. Third, our series is limited to a small number of patients. Finally, clinical and angiographic follow-up is short and there is no comparison group. 5. Conclusion PVO remains a viable solution in select ruptured and unruptured intracranial aneurysms. In this highly-selected series of 17 patients, favorable outcomes were obtained using PVO. Many adjuncts are available to aid in the decision making enabling personalized and safe treatment in cases not amenable to direct clipping, coiling, or flow diversion. Preoperative testing and angiography are essential tools in patient selection, particularly in understanding collateral circulation to maintain preservation of flow to important structures after PVO. Though flow diversion is an effective option for many large and complex aneurysms, with appropriate patient selection guided by manifold preoperative diagnostic modalities, PVO still remains a safe option. Funding statement This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors. Competing interests statement There are no competing interests to report for the authors of this publication. Contributorship statement All authors have contributed substantially and have reviewed and approved the final version. Data sharing statement No unpublished data is referenced in this study. Study approval statement The study was approved by Institutional Review Board (#121403, #4726X). References [1] R.T. Higashida, V.V. Halbach, L.D. Cahan, G.B. Hieshima, Y. Konishi, Detachable balloon embolization therapy of posterior circulation intracranial aneurysms, J. Neurosurg. 71 (4) (1989) 512–519. [2] L. Picard, S. Bracard, S. Lehericy, R. Anxionnat, S. Miyachi, E. Prada, et al., Endovascular occlusion of intracranial aneurysms of the posterior circulation: comparison of balloons, free coils and detachable coils in 38 patients, Neuroradiology 38 (Suppl. 1) (1996) S133–S141. [3] A. Aymard, Y.P. Gobin, J.E. Hodes, S. Bien, D. Rufenacht, D. Reizine, et al., Endovascular occlusion of vertebral arteries in the treatment of unclippable vertebrobasilar aneurysms, J. Neurosurg. 74 (3) (1991) 393–398. [4] A.J. Fox, F. Vinuela, D.M. Pelz, S.J. Peerless, G.G. Ferguson, C.G. Drake, et al., Use of detachable balloons for proximal artery occlusion in the treatment of unclippable cerebral aneurysms, J. Neurosurg. 66 (1) (1987) 40–46.
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[5] L. Cui, Q. Peng, W. Ha, D. Zhou, Y. Xu, Parent artery occlusion for intracranial aneurysms, Interv. Neuroradiol. 15 (3) (2009) 309–315. [6] A. Arat, C. Islak, I. Saatci, N. Kocer, S. Cekirge, Endovascular parent artery occlusion in large-giant or fusiform distal posterior cerebral artery aneurysms, Neuroradiology 44 (8) (2002) 700–705. [7] P. Hallacq, M. Piotin, J. Moret, Endovascular occlusion of the posterior cerebral artery for the treatment of p2 segment aneurysms: retrospective review of a 10-year series, AJNR Am. J. Neuroradiol. 23 (7) (2002) 1128–1136. [8] D.A. Eckard, P.L. O'Boynick, C.M. McPherson, V.R. Eckard, P. Han, P. Arnold, et al., Coil occlusion of the parent artery for treatment of symptomatic peripheral intracranial aneurysms, AJNR Am. J. Neuroradiol. 21 (1) (2000) 137–142. [9] A. Andreou, I. Ioannidis, A. Mitsos, Endovascular treatment of peripheral intracranial aneurysms, AJNR Am. J. Neuroradiol. 28 (2) (2007) 355–361. [10] P.M. Meyers, G.A. Thakur, T.A. Tomsick, Temporary endovascular balloon occlusion of the internal carotid artery with a nondetachable silicone balloon catheter: analysis of technique and cost, AJNR Am. J. Neuroradiol. 20 (4) (1999) 559–564. [11] F.P. Trivelato, M.T. Salles Rezende, G.D. Castro, L.B. Manzato, J.F. Santoro Araujo, A.C. Ulhoa, Endovascular treatment of isolated posterior inferior cerebellar artery dissecting aneurysms: parent artery occlusion or selective coiling? Clin. Neuroradiol. 24 (3) (2014) 255–261. [12] I.C. van der Schaaf, E.H. Brilstra, E. Buskens, G.J. Rinkel, Endovascular treatment of aneurysms in the cavernous sinus: a systematic review on balloon occlusion of the parent vessel and embolization with coils, Stroke 33 (1) (2002) 313–318. [13] P.N. Jayakumar, S. Desai, S.G. Srikanth, S. Ravishankar, J.M. Kovoor, Relevance of occlusion test in endovascular coiling of posterior cerebral artery (p2 segment) aneurysms, Interv. Neuroradiol. 10 (3) (2004) 235–248. [14] W.J. van Rooij, M. Sluzewski, N.H. Metz, P.C. Nijssen, D. Wijnalda, G.J. Rinkel, et al., Carotid balloon occlusion for large and giant aneurysms: evaluation of a new test occlusion protocol, Neurosurgery 47 (1) (2000) 116–121 (discussion 22). [15] R. Kurokawa, Y. Kuroshima, K. Yoshida, T. Kawase, Spontaneous thrombosis of intracavernous internal carotid artery aneurysm and parent artery occlusion in patients with positive balloon test occlusion–two case reports, Neurol. Med. Chir. 41 (9) (2001) 436–441. [16] K. Yamashita, W. Taki, S. Nishi, A. Sadato, H. Kikuchi, H. Iwata, et al., Treatment of unclippable giant posterior cerebral artery aneurysms with detachable balloons–report of three cases, Neurol. Med. Chir. 32 (9) (1992) 679–683. [17] T. Tsukahara, H. Wada, K. Satake, H. Yaoita, A. Takahashi, Proximal balloon occlusion for dissecting vertebral aneurysms accompanied by subarachnoid hemorrhage, Neurosurgery 36 (5) (1995) 914–919 (discussion 9-20). [18] G. Debrun, A. Fox, C. Drake, S. Peerless, J. Girvin, G. Ferguson, Giant unclippable aneurysms: treatment with detachable balloons, AJNR Am. J. Neuroradiol. 2 (2) (1981) 167–173. [19] A. Kurata, T. Ohmomo, Y. Miyasaka, K. Fujii, S. Kan, T. Kitahara, Coil embolization for the treatment of ruptured dissecting vertebral aneurysms, AJNR Am. J. Neuroradiol. 22 (1) (2001) 11–18. [20] J.E. Hodes, A. Aymard, Y.P. Gobin, D. Rufenacht, S. Bien, D. Reizine, et al., Endovascular occlusion of intracranial vessels for curative treatment of unclippable aneurysms: report of 16 cases, J. Neurosurg. 75 (5) (1991) 694–701. [21] D.F. Kallmes, H.J. Cloft, The use of hydrocoil for parent artery occlusion, AJNR Am. J. Neuroradiol. 25 (8) (2004) 1409–1410. [22] K. Withers, G. Carolan-Rees, M. Dale, Pipeline embolization device for the treatment of complex intracranial aneurysms: a NICE medical technology guidance, Appl. Health Econ Health Policy 11 (1) (2013) 5–13. [23] Y. Duan, K. Blackham, J. Nelson, W. Selman, N. Bambakidis, Analysis of short-term total hospital costs and current primary cost drivers of coiling versus clipping for unruptured intracranial aneurysms, J. Neurointervent. Surg. 7 (8) (2015) 614–618. [24] E.F. Ciceri, R.P. Klucznik, R.G. Grossman, J.E. Rose, M.E. Mawad, Aneurysms of the posterior cerebral artery: classification and endovascular treatment, AJNR Am. J. Neuroradiol. 22 (1) (2001) 27–34. [25] X. Lv, Y. Li, C. Jiang, X. Yang, Z. Wu, Parent vessel occlusion for P2 dissecting aneurysms of the posterior cerebral artery, Surg. Neurol. 71 (3) (2009) 319–325 (discussion 25). [26] L. Liu, H. He, C. Jiang, X. Lv, Y. Li, Deliberate parent artery occlusion for non-saccular posterior cerebral artery aneurysms, Interv. Neuroradiol. 17 (2) (2011) 159–168. [27] M.H. Khayata, A. Aymard, A. Casasco, D. Herbreteau, F. Woimant, J.J. Merland, Selective endovascular techniques in the treatment of cerebral mycotic aneurysms. Report of three cases, J. Neurosurg. 78 (4) (1993) 661–665. [28] G.P. Teitelbaum, C.F. Dowd, D.W. Larsen, C.G. McDougall, V.V. Halbach, R.T. Higashida, et al., Endovascular management of biopsy-related posterior inferior cerebellar artery pseudoaneurysm, Surg. Neurol. 43 (4) (1995) 357–359. [29] B. Lubicz, X. Leclerc, J.Y. Gauvrit, J.P. Lejeune, J.P. Pruvo, Endovascular treatment of peripheral cerebellar artery aneurysms, AJNR Am. J. Neuroradiol. 24 (6) (2003) 1208–1213. [30] R. Leibowitz, H.M. Do, M.L. Marcellus, S.D. Chang, G.K. Steinberg, M.P. Marks, Parent vessel occlusion for vertebrobasilar fusiform and dissecting aneurysms, AJNR Am. J. Neuroradiol. 24 (5) (2003) 902–907.
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Parent vessel occlusion for treatment of cerebral aneurysms: Is there still an indication? A series of 17 patients Nishant Ganesh Kumar d,⁎, Travis R. Ladner d, Imad S. Kahn e, Scott L. Zuckerman d, Christopher B. Baker a,c, Marybess Skaletsky a, Deborah Cushing a, Matthew R. Sanborn a, J Mocco f, Robert D. Ecker a,b a
Maine Medical Center, Neuroscience Institute, Portland, Maine, USA Maine Medical Center, Department of Surgery, Portland, ME, USA c Maine Medical Center, Department of Radiology, Portland, ME, USA d Vanderbilt University Medical Center, Department of Neurosurgery, Nashville, Tenessee, USA e Dartmouth Hitchcock Medical Center, Department of Neurosurgery, Hanover, New Hampshire, USA f Mt. Sinai Medical Center, Department of Neurosurgery, New York, New York, USA b
a r t i c l e
i n f o
Article history: Received 11 June 2016 Received in revised form 27 October 2016 Accepted 22 November 2016 Available online 23 November 2016 Keywords: Aneurysm Balloon test occlusion Parent vessel occlusion Giant aneurysm
a b s t r a c t Introduction/purpose: Flow diversion has allowed cerebrovascular neurosurgeons and neurointerventionalists to treat complex, large aneurysms, previously treated with trapping, bypass, and/or parent vessel sacrifice. However, a minority of aneurysms remain that cannot be treated endovascularly, and microsurgical treatment is too dangerous. However, balloon test occlusion (macro and micro), micro WADA testing, ICG, intra-angiography and intra-operative monitoring are all available to clinically test the hypothesis that vessel sacrifice is safe. We describe a dual-institution series of aneurysms successfully treated with parent vessel occlusion (PVO). Materials/methods: Prospectively collected databases of all endovascular and open cerebrovascular cases performed at Maine Medical Center and Vanderbilt University Medical Center from 2011 to 2013 were screened for patients treated with primary vessel sacrifice. A total of 817 patients were screened and 17 patients were identified who underwent parent vessel sacrifice as primary treatment. Results: All 17 patients primarily treated with PVO are described below. Nine patients presented with SAH, and 3/ 17 involved anterior circulation. Complete occlusion was achieved in 15/17 patients. In the remaining 2 patients, significant reduction in the aneurysm occurred. Modified Rankin Score (mRS) of 0, signifying complete independence, was achieved for 16/17 patients. One patient died due to an extracranial process. Conclusions: Parent vessel sacrifice remains a viable and durable solution in select ruptured and unruptured intracranial aneurysms. Many adjuncts are available to aid in the decision making. In this small series, patients naturally divided into vertebral dissecting aneurysms, giant aneurysms and small distal aneurysms. Outcomes were favorable in this highly selected group. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Parent vessel occlusion (PVO) is a traditional method for treating aneurysms that are not amenable to direct coiling/clipping or particularly complex saccular or fusiform aneurysms. It has been successfully
Abbreviations: AICA, Anterior Inferior Cerebellar Artery; AVM, Arterial-venous Malformation; BTO, Balloon test occlusion; ICA, Internal Carotid Artery; ICG, Indocyanine green; MMC, Maine Medical Center; MCA, Middle Cerebral Artery; mRS, Modified Rankin Score; NBCA, n-butyl cyanoacrylate; PVO, Parent Vessel Occlusion; PICA, Posterior inferior cerebellar artery; SAH, Subarachnoid hemorrhage; SCA, Superior Cerebellar Artery and Vanderbilt University Medical Center (VUMC). ⁎ Corresponding author at: Vanderbilt University School of Medicine, Medical Center North T-4224, Nashville, TN 37212, USA. E-mail address: [email protected] (N. Ganesh Kumar).
http://dx.doi.org/10.1016/j.jns.2016.11.057 0022-510X/© 2016 Elsevier B.V. All rights reserved.
implemented in the treatment of aneurysms involving the vertebrobasilar junction [1–4], posterior cerebral artery [5–7] and peripheral cerebral aneurysms [8,9] when adequate collateral flow is present. Flow diverters have introduced another class of treatment options for these complex aneurysms that historically would have undergone trapping, parent vessel sacrifice, or bypass. However, PVO still remains a viable option. There are many well-established diagnostic modalities to determine feasibility of PVO, including intra-operative monitoring, balloon test occlusion (BTO), and Wada testing. These can aid in patient selection to ensure that PVO, if indicated, is safe. Therefore, interventionalists and neurosurgeons should keep PVO in their armamentarium of treatment options. Here we review the experiences of two centers using PVO as a favorable solution in a select group of patients with intracranial aneurysms.
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2. Methods
251
subocippital craniotomy was made, from the superior pinna running inferiorly to the midline underneath the inion to the spinous process of C2. Pericranium was harvested during exposure for the duraplasty. The avascular midline was followed down to the spinous process of C1 and C2. A craniotomy was performed from the transverse-sigmoid junction to the midline of the foramen magnum. The ipsilateral lamina of C1 was removed, with care taken to visualize the extradural vertebral artery. The dura was opened from the transverse-sigmoid junction to the arch of C1. After the operating microscope was brought into the field, the arachnoid was opened and CSF was drained from the cisterna magna. Based on location of the pathology along the vertebral artery or PICA, surgical corridors between the inferior cranial nerve IX, X and XI in the middle, and VII and VIII superiorly are utilized to safely sacrifice the involved vessel. Though most open cases involved the posterior circulation, for any anterior circulation procedures, a standard curvilinear pterional incision was made and a myocutaneous flap was reflected anteriorly. Exposure of the keyhole and the temporal bone was achieved, and a standard pterional craniotomy bone flap was turned. In the case of anterior circulation sacrifice, the sphenoid wing was aggressively drilled down and flattened. If periorbita was encountered, the area was immediately waxed. A curvilinear dural incision was then made after hemostasis was achieved, and the microscope was brought into the field. A subfrontal approach was taken. The olfactory tract was found and followed to the optic nerve, leading to the supraoptic cistern, which was then decompressed. The ICA was then located, and the sylvian fissure was carefully opened with sharp dissection. Depending on the pathology, the involved intracranial vessel was dissected out, able to obtain proximal and distal control when needed. For either approach, a combination of bayoneted and/or straight clips was used to ensure the aneurysm and parent vessel were occluded. Once the necessary vessel sacrifice was performed, attention was turned to hemostasis and closure. The dura was approximated, a pericranial graft was sewed in when necessary, the bone flap was replaced, and the scalp was closed in a usual fashion. A post-procedure angiogram was then performed to confirm occlusion of the parent vessel. A representative open case is presented in Fig. 1. For endovascular PVO, the patient was intubated and positioned supine in the angiogram suite. Whereas the patient was kept awake for any BTO or Wada test, all patients were placed under general anesthesia for endovascular PVO. The groin area was prepped and draped in a sterile fashion. Access into the right common femoral artery with a needle,
2.1. Study design and data collection A retrospective case series was obtained from two prospectively collected databases of all patients undergoing endovascular and open cerebrovascular treatment over a two-year period at Maine Medical Center (MMC) and Vanderbilt University Medical Center (VUMC). From February 2011 to April 2013, 817 patient records were screened between both databases, and 17 patients were identified who underwent PVO as the primary treatment for an aneurysm not amenable to direct embolization or clipping (Table 1). This is a highly selected group representing approximately 2–3 patients per year from each medical center where the total combined annual number of aneurysm presenting cases is greater than 250. The electronic medical records for these patients were reviewed, using clinic notes, operative notes, and angiographic images. Demographic variables were collected and defined as age and sex. Clinical variables were collected and defined as presence of subarachnoid hemorrhage (SAH), aneurysm location, aneurysm morphology, and treatment modality. Outcome variables were collected and defined as aneurysm occlusion on follow-up angiography, presence of postoperative complications, and functional outcome as measured by the modified Rankin score (mRS) at last follow-up. 2.2. Operative technique All patients were treated endovascularly or with open sacrifice, as depicted in Table 1. Preoperatively, a BTO was performed in line with technique previously published [10]. The patient was kept awake, and groin access was obtained through the right common femoral artery up to the involved parent vessel. A balloon was then inflated in the proximal segment of the involved vessel to complete occlusion. Neurologic exams were obtained in the 10–20 min after occlusion, and the balloon was immediately deflated with any deviation in exam. Given the extensive collateral circulation, BTO was not used in everyone, but rather select patients. For open PVO, the patient was intubated, a right groin sheath was placed and a pre-procedure angiogram performed. The patient was then positioned on the appropriate side of the aneurysm. Neuromonitoring with SSEP and EEG were utilized. For distal vertebral artery and PICA lesions, an S-shaped incision for a far-lateral
Table 1 Patient demographics and location of aneurysm along with treatment method and post-operative aneurysm occlusion status, procedural complications and mRS. SAH: Subarachnoid hemorrhage, PICA: Posterior inferior cerebellar artery, MCA: Middle Cerebral Artery, SCA: Superior Cerebellar Artery, ICA: Internal Carotid Artery, AICA: Anterior Inferior Cerebellar Artery, AVM: Arterial-venous Malformation, NBCA: n-butyl cyanoacrylate, mRS: Modified Rankin Score, I: Incomplete, C: Complete. Case SAH Aneurysm type and morphology
Treatment
Occlusion Complication
mRS
1 2 3 4 5 6 7
N N Y Y Y Y N
Dissecting vertebral Giant ICA Distal PICA Dissecting vertebral Dissecting vertebral Distal mycotic MCA Giant basilar
I C C C C C I
None None None None None SMA infarct MCA infarct
0 0 0 0 0 0 0
8 9 10 11 12 13
N Y Y N N N
C C C C C C
None None None Scattered SCA infarcts None None
0 0 0 0 0 0
14
Y
Giant PICA Dissecting vertebral Distal PICA Distal SCA Giant vertebral Residual distal SCA feeding aneurysm after AVM resection Ruptured AICA feeding aneurysm to AVM
Coil Coil NBCA Coil Coil Onyx Mid basilar clipping Distal clipping Coil Clip trapping Coil Coil + Amplatzer Coil Onyx
C
6
15 16 17
Y N Y
Dissecting vertebral Dissecting fusiform PCA Dissecting blister ICA
Coil Coil + onyx Clip trapping
C C C
Tonsillar infarct. Death from bleeding esophageal varices 2.5 weeks post-op None None None
0 0 0
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Fig. 1. Case 7. Patient in 60s with 1 month of progressive gait difficulty with decrement from unaided to walker assisted, swallowing difficulty and double vision. Imaging revealed a giant basilar tip aneurysm with brainstem compression. Preoperative axial T2 MRI revealed basilar aneurysm with severe brainstem compression (A). Sagittal CTA demonstrated the smaller filling and larger thromboses portion of the aneurysm (B), and 3-D right vertebral angiogram showed the filling portion of the giant basilar aneurysm (C). The patient was taken for an extended pterional craniotomy, utilizing a combined subtemporal and pterional corridors, where basilar artery was clipped. Post-operatively, left sided weakness was noted, and ischemic injury at the anterior temporal pole and inferior frontal lobe was seen on MRI. This was thought to be a venous infarction due to retraction injury, as the stroke did not fit a single artery distribution. Weakness improved over time and became clinically insignificant. At 3 months post-operatively, patient was independent at home with all pre-operative symptoms resolved. At 6 months post-operatively, a right ICA selective angiogram showed dramatic involution of the aneurysm (D), and a right selective vertebral artery injection demonstrated the clip position above the AICAs (E). At 1 year, axial T2 MRI showed significant improvement in the brainstem compression and aneurysm shrinkage (F).
wire, and sheath was achieved without complication. After a right femoral angiogram, a #6 French Envoy was advanced over an 0.035 Glidewire up the aortic arch to catheterize the involved common carotid
artery. Additional selective catheterization and angiograms were performed in order to visualize collateral circulation to the area of interest. Once enough collateral circulation was present and other options (i.e.
Fig. 2. Case 15. Patient in 30s presented with a subarachnoid hemorrhage (A), with evidence of a right dissecting fusiform vertebral artery aneurysm on CTA (B). On arrival to our hospital patient re-ruptured and clinical status worsened to Hunt and Hess grade 4, and ventriculostomy was performed. Patient underwent angiography which demonstrated the aneurysm and a distal AICA/PICA vessel at the junction of the right vertebral artery and basilar artery. Angiographic run through the left vertebral artery also demonstrated filling of the right AICA/PICA vessel. Consideration was made for flow diversion or other options; however, this did not appear to be safe or appropriate particularly as the patient had just re-ruptured. The anatomy was favorable for parent vessel occlusion, and therefore a total of 60 coils were deployed in the V3 segment of the right vertebral artery (D). Final angiographic run demonstrated complete shutdown of flow through the right vertebral artery with no residual aneurysm (E), with complete preservation of flow to the remainder of the posterior circuclation through the left vertebral artery (F). On postoperative day 3, the patient developed clinical vasospasm with elevated velocities in the bilateral MCA and left ACA territories on transcranial doppler but negative CTA. Neurological exam improved with hemodynamic support with no other interventions. Patient remained neurologically intact, the external ventricular drain was removed, and was discharged home on postoperative day 19 with a modified Rankin score of 0.
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flow diversion, stent coil, etc.) were deemed too risky, parent vessel sacrifice was chosen as the method of treatment. This was often done in the setting of a co-dominant vertebral artery or an aneurysm far enough in the peripheral vasculature that occlusion would not cause significant ischemia. The parent vessel was then coiled. Multiple angiograms were performed during and after coil embolization to determine the extent of occlusion and ensure no thromboembolic complications. Once this was done, the microcatheter was removed in a standard fashion, and the groin closed with a range of closure devices. A representative case of endovascular occlusion is presented in Fig. 2. Of note, the decision to choose PVO over other options such as stentcoil and flow diversion was made after careful consideration. For acute SAH, any option to avoid antiplatelet agents were preferred due to the recent hemorrhage and presence of an external ventricular drain (EVD). For example, the patient with a dissecting blister ICA aneurysm had a poor grade, an EVD, and adequate collateral circulation based on intraoperative angiography. PVO was deemed the safest and most effective treatment. Distal aneurysms where microcatheter insertion and/or stent/coil deployment were deemed unsafe were also considered good candidates for PVO. Overall, final treatment decisions were made based on presentation, collateral flow, vascular anatomy, and prior treatments. It is our practice to provide dual antiplatelet therapy after flow diversion with aspirin and Plavix for a minimum of 3 months when using a metal stent or Pipeline. For all cases, all patients received 5000 U of heparin at the start of the procedure and 1000 U every hour until completion. Potentially relevant vessels and perforators were avoided during PVO.
2.3. Data analysis Descriptive statistical analysis was performed in Microsoft Excel 2011 (Microsoft Corp, Redmond, WA). For patient age, mean, standard deviation, and range were determined. For categorical variables (all other variables), number and percentage were determined.
3. Results During the study period, 17 aneurysms were treated in 17 patients via PVO. The mean age of the patients was 53.5 ± 13.5 (range 37–84) years. There were 7 (41.2%) female patients. Nine (52.9%) patients presented with subarachnoid hemorrhage, with 4 of these 9 ruptured aneurysms being dissecting vertebral artery aneurysms. The majority of aneurysms (14, 82.4%) involved the posterior circulation: vertebral (n = 6), PICA (n = 3), AICA (n = 1), SCA (n = 2), basilar (n = 1), and PCA (n = 1). The remaining aneurysms in the anterior circulation were a dissecting ICA, a giant ICA, and a mycotic MCA aneurysm. Aneurysm morphologies were primarily vertebral dissecting aneurysms (n = 5), giant aneurysms (n = 7), and small distal aneurysms (n = 5). Four aneurysms were treated via open surgical clipping of the parent vessel. Ten were treated via coiling, with adjunctive use of the Amplatzer atrial septal occluder device (AGA Medical Corporation, Golden Valley, MN) in 1 patient and Onyx (Covidien, Irvine, CA) in 1 patient. Of the remaining patients, 2 vessels were embolized using Onyx alone and 1 was occluded via NBCA (n-butyl cyanoacrylate). Complete occlusion was achieved in 15 (88.2%) cases. In the remaining 2 patients (coiled dissecting vertebral and clipped giant basilar) significant reduction in the aneurysm occurred. Postoperatively, there were three patients with new cerebral infarcts: 1) SMA infarct in a distal MCA aneurysm, 2) MCA territory infarct in a giant basilar aneurysm, and 3) scattered SCA territory infarcts in a distal SCA aneurysm. One patient developed a tonsillar infarct after Onyx embolization of an AICA aneurysm; this patient died from ruptured esophageal varices 2.5 weeks after treatment. Modified Rankin Score (mRS) of 0, signifying complete independence, was achieved for the other 16 (94.1%) patients.
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4. Discussion With well-developed endovascular and open techniques, the use of PVO has fallen out of favor. However, in the case of complex, posterior circulation, giant, or dissecting aneurysms, there are still instances where PVO may play an important role in safe aneurysm occlusion [8, 9]. We reviewed the results of PVO for a subset of complex aneurysms treated in the era of flow diversion. In this highly selected group, PVO was still a viable option with favorable outcomes [5]. Complete occlusion was achieved in 15/17 patients. In the remaining 2 patients, significant reduction in the aneurysm occurred. Modified Rankin Score (mRS) of 0 was achieved for 16/17 patients. Three patients developed new cerebral infarcts. One patient died, though this was due to systemic hepatic disease. We review the relevant literature on PVO below. 4.1. Diagnostic testing Diagnostic modalities are essential if PVO is performed due to the higher risk of ischemic events. In PICA dissecting aneurysms, Trivelato et al. found an ischemic complication rate of 20.4% (11/54) in PVO vs. 14.3% (4/28) in coiling [11]. Similarly, van der Schaaf et al., found that late ischemic complications occurred in 3.4% of patients treated with permanent balloon occlusion compared to no complications in patients treated with coil embolization [12]. The Wada test and the balloon test occlusion (BTO) are two commonly used pre-PVO tests [7]. However, BTO has its limitations, including rare complications such as aneurysm rupture after deflation of the temporary balloon [13]. In addition, BTO has been associated with false positive and negative results [14–16]. Given this, other diagnostic methods are necessary including micro WADA testing, ICG (Indocyanine green), intraoperative angiography and intraoperative monitoring. All of these are available to clinically test the hypothesis in an individual patient that PVO is safe. 4.2. Embolization agents Some of the most commonly used embolization agents for PVO include GDCs, detachable balloons and fibered and non-fibered platinum coils [4,17–20]. Due to being more thrombogenic, fibered platinum coils are considered more useful in carrying out short segment thrombosis compared to non-fibered coils [21]. Kurata et al., successfully performed aneurysm occlusion in 18/18 patients using platinum coil embolization for dissecting vertebral aneurysms with complete occlusion at the site still present at 9 month follow up. While the clinical experience of flow diversion is growing, economic projections by Withers et al. suggest a higher cost for flow diversion (£24,341) compared to endovascular PVO (£16,893) and surgical PVO (£11,654) over a 10-year period [22]. While this may suggest a cost advantage to PVO, cost modeling proves challenging. The price of the devices required for the procedure is the major driver of total cost; however, complication rate and healthcare resource utilization also factor into costs associated with PVO, as stroke is a not uncommon complication, and greater experience is needed to accurately compare PVO with flow diversion [23]. 4.3. Outcomes with PVO 4.3.1. PCA Large or giant P2 segment aneurysms of the PCA are suitable for PVO [24]. The thalamoperforating vessels arise from the P1 segment and an aneurysm distal to these branches may be safely managed with sacrifice of the parent vessel. Hallacq and colleagues used PVO to manage 9 patients with P2 segment aneurysms [7]. They had successful aneurysm occlusion in all 9 patients and no neurological complications. Arat et al. reported similar results in their series of eight patients with large or giant P2 aneurysms treated with PVO with immediate post-operative infarcts 37.5% of patients (3/8) [6]. On long term 1 year follow up, the
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only complication was occipital infarct with homonymous hemianopsia. With dissecting P2 aneurysms, Lv et al. reported complete occlusion in 8/8 and no permanent complications after coil-mediated PVO [25]. Liu et al., had similar results in a series of 12 patients with PCA aneurysms treated with coil-mediated PVO, with excellent embolization but one case of transient hemianopsia [26].
4.3.2. Distal location Distally located aneurysms can be very challenging to treat while keeping the parent vessel patent due to the small vessel diameters involved. In these instances, PVO has been reported to be very useful. Eckard et al. reported using PVO in 9 patients with peripheral aneurysms [8]. Coil occlusion was performed proximal to the aneurysm in six cases, and the aneurysm was trapped in three cases. Complete obliteration was achieved in all patients and for the six patients with followup angiograms, continued complete occlusion was documented. Others have also reported the use of PVO in the distal circulation with limited or no collateral blood flow [20,27,28]. Cui and colleagues reported a series of 12 patients with peripheral intracranial aneurysms not amenable to selective embolization that underwent PVO with platinum coils [5]. On long-term follow-up, the authors reported no permanent neurological sequelae and enduring obliteration of the aneurysms in all patients. Non-mycotic fusiform peripheral aneurysms have also been managed with PVO. Andreou and colleagues described their experience with 18 patients who underwent PVO (15 coiled, 4 glued). Five patients developed transient neurologic deficits and 2 had permanent neurologic deficits (a visual field defect in both).
4.3.3. Mycotic Mycotic aneurysms are amenable to PVO because they are almost always found in the peripheral branches, making isolation of the aneurysm and vessel challenging. Khayata et al. reported successful obliteration in two patients with mycotic aneurysms treated with PVO (glue for PCA aneurysm, autologous blood clot for MCA aneurysm) [27]. Teitelbaum et al. also reported the successful treatment of a mycotic PICA aneurysm using PVO with microcoils [28]. 4.3.4. Posterior Circulation Aneurysms Peripheral posterior circulation aneurysms may also be managed with PVO. Lubicz and colleagues described the endovascular management of eight cerebellar aneurysms, out of which two large peripheral cerebellar artery aneurysms and one small aneurysm with a wide neck were treated by PVO [29]. PVO in these cases was achieved with GDCs. The authors reported complete obliteration in these aneurysms and excellent outcome in two patients while one patient developed CN VII nerve palsy. Overall, obliteration of the aneurysm should be the aim in cases where PVO is being employed, as the outcomes are notably better compared to cases with residual filling [30]. We were able to achieve complete obliteration of the aneurysm in 15 of the 17 cases. One of our patients with a dissecting VA aneurysm had a residual filling aneurysm after treatment but has remained asymptomatic since the procedure. Table 2 represents a summary of some of the cases series discussed above. While the landscape of cerebrovascular intervention continues to rapidly evolve, the long-term effects of PIPELINE embolization are unknown. Moreover, with favorable outcomes associated with using PVO
Table 2 Summary of case series and reviews involving Parent Vessel Occlusion (PVO). PICA: Posterior inferior cerebellar artery, MCA: Middle Cerebral Artery, SCA: Superior Cerebellar Artery, ICA: Internal Carotid Artery, AICA: Anterior Inferior Cerebellar Artery, AVM: Arterial-venous Malformation. BA: Basilar Artery, VA: Vertebral Artery, IC: Internal Carotid. Study
Aneurysm location (patients)
Surgical approach
Outcomes
Lv et al., 2009 [25]
P2 dissecting [8]
Endovascular PVO with detachable coils
No patient developed neurological deficits
Trivelato et al., 2014 [11]
PICA dissecting [14]
8 selective coiling 6 PVO
Liu et al., 2011 [26]
PCA non-saccular [12]
Detachable coils
Leibowitz et al., 2003 [30]
VA and BA [13]
I: PVO with complete aneurysm thrombosis [6]
Kallmes et al., 2004 [21] Hallacq et al., 2002 [7]
IC [2], VA [3] P2 [10]
Cui et al., 2009 [5]
PCA [7], AICA [2], PICA [1], MCA [2]
Eckard et al., 2000 [8]
PICA [2], SCA [2], AICA [1], PCA [3], MCA [1], ACA [1] Large/Fusiform distal PCA [8]
Arat et al., 2002 [6]
Andreou et al., 2007 [9]
PCA [9], SCA [5], AICA [1], PICA [5], MCA [5], ACA [2]
II: PVO without complete aneurysm thrombosis [7] PVO using HES coils Endovascular PVO [9]. 1 deferred due to vascular tortuosity. PAO with detachable coils
PVO using microcoils
Urgent treatment after SAH [3] Elective treatment [5]
Detachable coils [7]. Fusiform aneurysms with PAO coils [15], glue [4]. Spontaneous thrombosed aneurysm [1].
Conclusion
P2 dissecting aneurysms can be treated with PVO in cases in which selective embolization of the aneurysmal sac with detachable platinum coils or surgical clipping cannot be achieved. No statistical difference between both Both interventions are highly effective in preventing groups regarding complications. rebleeding. PVO is significantly associated with higher risk of ischemic events. Total complication rate is similar between both modalities. No neurological complications [11]. PVO via detachable coils appears to be well tolerated for Transient hemianopsia [1]. non-saccular aneurysms in P2 distal segment of PCA location All in group I showed improvement [6] In patients with an aneurysm including one vertebral In group II, 4 died during follow-up. 2 due artery (VA) where complete thrombosis can be achieved, to aneurysms. better clinical outcomes are attainable when compared to 2 others had worsening symptoms. 1 those with aneurysms of the basilar artery (BA) or both VA other remained stable. where complete thrombosis cannot be achieved. None reported No neurologic deficit after treatment.
No patient developed neurological deficits. Transient diplopia and vertigo [1]. Mild nondisabling neurologic deficits [3].
Permanent homonymous hemianopia [1]. Excellent recovery [6]. Lost to follow up [1]. 5/18 who underwent PAO developed neurological deficits. 2/18 had permanent neurological deficit (visual field defect)
HES could be a viable option for rapid short segment occlusion Acute parent artery occlusion appears to be safe in treatment of P2 segment aneurysms, whatever the location of occlusion. Distally located cerebral aneurysms can be treated with PAO when selective embolization of aneurysmal sac with detachable coils or surgical clipping cannot be achieved. PVO for aneurysms that are difficult surgically or for intra-aneurysmal coil placement. Endovascular PAO may be alternative to surgical PAO in distal PCA aneurysms not convenient for selective endovascular treatment or surgical clipping. Distally located aneurysms can be treated with endovascular PAO in the cases in which selective occlusion of aneurysmal sac with coil or clipping cannot be achieved.
N. Ganesh Kumar et al. / Journal of the Neurological Sciences 372 (2017) 250–255
in carefully chosen patients, further exploration into the frequency of its use is warranted and how both methods can be used in tandem to provide the optimal treatment. Our case series is not without limitation. First, this is retrospective. Second, this cohort was highly selected at institutions where flow diversion is also regularly performed. Third, our series is limited to a small number of patients. Finally, clinical and angiographic follow-up is short and there is no comparison group. 5. Conclusion PVO remains a viable solution in select ruptured and unruptured intracranial aneurysms. In this highly-selected series of 17 patients, favorable outcomes were obtained using PVO. Many adjuncts are available to aid in the decision making enabling personalized and safe treatment in cases not amenable to direct clipping, coiling, or flow diversion. Preoperative testing and angiography are essential tools in patient selection, particularly in understanding collateral circulation to maintain preservation of flow to important structures after PVO. Though flow diversion is an effective option for many large and complex aneurysms, with appropriate patient selection guided by manifold preoperative diagnostic modalities, PVO still remains a safe option. Funding statement This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors. Competing interests statement There are no competing interests to report for the authors of this publication. Contributorship statement All authors have contributed substantially and have reviewed and approved the final version. Data sharing statement No unpublished data is referenced in this study. Study approval statement The study was approved by Institutional Review Board (#121403, #4726X). References [1] R.T. Higashida, V.V. Halbach, L.D. Cahan, G.B. Hieshima, Y. Konishi, Detachable balloon embolization therapy of posterior circulation intracranial aneurysms, J. Neurosurg. 71 (4) (1989) 512–519. [2] L. Picard, S. Bracard, S. Lehericy, R. Anxionnat, S. Miyachi, E. Prada, et al., Endovascular occlusion of intracranial aneurysms of the posterior circulation: comparison of balloons, free coils and detachable coils in 38 patients, Neuroradiology 38 (Suppl. 1) (1996) S133–S141. [3] A. Aymard, Y.P. Gobin, J.E. Hodes, S. Bien, D. Rufenacht, D. Reizine, et al., Endovascular occlusion of vertebral arteries in the treatment of unclippable vertebrobasilar aneurysms, J. Neurosurg. 74 (3) (1991) 393–398. [4] A.J. Fox, F. Vinuela, D.M. Pelz, S.J. Peerless, G.G. Ferguson, C.G. Drake, et al., Use of detachable balloons for proximal artery occlusion in the treatment of unclippable cerebral aneurysms, J. Neurosurg. 66 (1) (1987) 40–46.
255
[5] L. Cui, Q. Peng, W. Ha, D. Zhou, Y. Xu, Parent artery occlusion for intracranial aneurysms, Interv. Neuroradiol. 15 (3) (2009) 309–315. [6] A. Arat, C. Islak, I. Saatci, N. Kocer, S. Cekirge, Endovascular parent artery occlusion in large-giant or fusiform distal posterior cerebral artery aneurysms, Neuroradiology 44 (8) (2002) 700–705. [7] P. Hallacq, M. Piotin, J. Moret, Endovascular occlusion of the posterior cerebral artery for the treatment of p2 segment aneurysms: retrospective review of a 10-year series, AJNR Am. J. Neuroradiol. 23 (7) (2002) 1128–1136. [8] D.A. Eckard, P.L. O'Boynick, C.M. McPherson, V.R. Eckard, P. Han, P. Arnold, et al., Coil occlusion of the parent artery for treatment of symptomatic peripheral intracranial aneurysms, AJNR Am. J. Neuroradiol. 21 (1) (2000) 137–142. [9] A. Andreou, I. Ioannidis, A. Mitsos, Endovascular treatment of peripheral intracranial aneurysms, AJNR Am. J. Neuroradiol. 28 (2) (2007) 355–361. [10] P.M. Meyers, G.A. Thakur, T.A. Tomsick, Temporary endovascular balloon occlusion of the internal carotid artery with a nondetachable silicone balloon catheter: analysis of technique and cost, AJNR Am. J. Neuroradiol. 20 (4) (1999) 559–564. [11] F.P. Trivelato, M.T. Salles Rezende, G.D. Castro, L.B. Manzato, J.F. Santoro Araujo, A.C. Ulhoa, Endovascular treatment of isolated posterior inferior cerebellar artery dissecting aneurysms: parent artery occlusion or selective coiling? Clin. Neuroradiol. 24 (3) (2014) 255–261. [12] I.C. van der Schaaf, E.H. Brilstra, E. Buskens, G.J. Rinkel, Endovascular treatment of aneurysms in the cavernous sinus: a systematic review on balloon occlusion of the parent vessel and embolization with coils, Stroke 33 (1) (2002) 313–318. [13] P.N. Jayakumar, S. Desai, S.G. Srikanth, S. Ravishankar, J.M. Kovoor, Relevance of occlusion test in endovascular coiling of posterior cerebral artery (p2 segment) aneurysms, Interv. Neuroradiol. 10 (3) (2004) 235–248. [14] W.J. van Rooij, M. Sluzewski, N.H. Metz, P.C. Nijssen, D. Wijnalda, G.J. Rinkel, et al., Carotid balloon occlusion for large and giant aneurysms: evaluation of a new test occlusion protocol, Neurosurgery 47 (1) (2000) 116–121 (discussion 22). [15] R. Kurokawa, Y. Kuroshima, K. Yoshida, T. Kawase, Spontaneous thrombosis of intracavernous internal carotid artery aneurysm and parent artery occlusion in patients with positive balloon test occlusion–two case reports, Neurol. Med. Chir. 41 (9) (2001) 436–441. [16] K. Yamashita, W. Taki, S. Nishi, A. Sadato, H. Kikuchi, H. Iwata, et al., Treatment of unclippable giant posterior cerebral artery aneurysms with detachable balloons–report of three cases, Neurol. Med. Chir. 32 (9) (1992) 679–683. [17] T. Tsukahara, H. Wada, K. Satake, H. Yaoita, A. Takahashi, Proximal balloon occlusion for dissecting vertebral aneurysms accompanied by subarachnoid hemorrhage, Neurosurgery 36 (5) (1995) 914–919 (discussion 9-20). [18] G. Debrun, A. Fox, C. Drake, S. Peerless, J. Girvin, G. Ferguson, Giant unclippable aneurysms: treatment with detachable balloons, AJNR Am. J. Neuroradiol. 2 (2) (1981) 167–173. [19] A. Kurata, T. Ohmomo, Y. Miyasaka, K. Fujii, S. Kan, T. Kitahara, Coil embolization for the treatment of ruptured dissecting vertebral aneurysms, AJNR Am. J. Neuroradiol. 22 (1) (2001) 11–18. [20] J.E. Hodes, A. Aymard, Y.P. Gobin, D. Rufenacht, S. Bien, D. Reizine, et al., Endovascular occlusion of intracranial vessels for curative treatment of unclippable aneurysms: report of 16 cases, J. Neurosurg. 75 (5) (1991) 694–701. [21] D.F. Kallmes, H.J. Cloft, The use of hydrocoil for parent artery occlusion, AJNR Am. J. Neuroradiol. 25 (8) (2004) 1409–1410. [22] K. Withers, G. Carolan-Rees, M. Dale, Pipeline embolization device for the treatment of complex intracranial aneurysms: a NICE medical technology guidance, Appl. Health Econ Health Policy 11 (1) (2013) 5–13. [23] Y. Duan, K. Blackham, J. Nelson, W. Selman, N. Bambakidis, Analysis of short-term total hospital costs and current primary cost drivers of coiling versus clipping for unruptured intracranial aneurysms, J. Neurointervent. Surg. 7 (8) (2015) 614–618. [24] E.F. Ciceri, R.P. Klucznik, R.G. Grossman, J.E. Rose, M.E. Mawad, Aneurysms of the posterior cerebral artery: classification and endovascular treatment, AJNR Am. J. Neuroradiol. 22 (1) (2001) 27–34. [25] X. Lv, Y. Li, C. Jiang, X. Yang, Z. Wu, Parent vessel occlusion for P2 dissecting aneurysms of the posterior cerebral artery, Surg. Neurol. 71 (3) (2009) 319–325 (discussion 25). [26] L. Liu, H. He, C. Jiang, X. Lv, Y. Li, Deliberate parent artery occlusion for non-saccular posterior cerebral artery aneurysms, Interv. Neuroradiol. 17 (2) (2011) 159–168. [27] M.H. Khayata, A. Aymard, A. Casasco, D. Herbreteau, F. Woimant, J.J. Merland, Selective endovascular techniques in the treatment of cerebral mycotic aneurysms. Report of three cases, J. Neurosurg. 78 (4) (1993) 661–665. [28] G.P. Teitelbaum, C.F. Dowd, D.W. Larsen, C.G. McDougall, V.V. Halbach, R.T. Higashida, et al., Endovascular management of biopsy-related posterior inferior cerebellar artery pseudoaneurysm, Surg. Neurol. 43 (4) (1995) 357–359. [29] B. Lubicz, X. Leclerc, J.Y. Gauvrit, J.P. Lejeune, J.P. Pruvo, Endovascular treatment of peripheral cerebellar artery aneurysms, AJNR Am. J. Neuroradiol. 24 (6) (2003) 1208–1213. [30] R. Leibowitz, H.M. Do, M.L. Marcellus, S.D. Chang, G.K. Steinberg, M.P. Marks, Parent vessel occlusion for vertebrobasilar fusiform and dissecting aneurysms, AJNR Am. J. Neuroradiol. 24 (5) (2003) 902–907.