Decision Making in Surgery for Nonsaccular Posterior Inferior Cerebellar Artery Aneurysms With Special Reference to Intraoperative Assessment of Collateral Blood Flow and Neurophysiological Function

Decision Making in Surgery for Nonsaccular Posterior Inferior Cerebellar Artery Aneurysms With... Abstract BACKGROUND Posterior inferior cerebellar artery (PICA) aneurysms represent a challenging pathology. PICA sacrifice is often necessary, due to the high proportion of nonsaccular aneurysms that can be found in this location. Several treatments are available, but the infrequency of these aneurysms and the increasing number of endovascular techniques have limited the development of a standardized algorithm for cases in which open surgery is indicated. OBJECTIVE We present our series of nonsaccular PICA aneurysms, in the attempt to define an algorithm for their surgical management. METHODS We retrospectively reviewed the operation database, identifying patients harboring nonsaccular PICA aneurysms who were surgically treated at our institution from 2007 to 2016. RESULTS During a 9-yr period, 17 patients harboring 18 nonsaccular PICA aneurysms were surgically treated at our institution. Fourteen (7.7%) aneurysms were located within the proximal PICA (including those located at the vertebral artery–PICA junction), and 4 were located distally. We performed PICA revascularization in 8 (57.1%) cases of proximal aneurysms (n = 4, PICA–PICA bypass; n = 4, occipital artery–PICA bypass). We based our decision whether to perform bypass on intraoperative test occlusion with indocyanine green (ICG) videoangiography and neurophysiological monitoring. In no cases, bypass was necessary for distal aneurysms. CONCLUSION For nonsaccular PICA aneurysms, in which vessel occlusion is often necessary, it is possible to adopt a selective use of revascularization techniques. Intraoperative occlusion test with ICG videoangiography and neurophysiological monitoring provides reliable indications, allowing real-time assessment of collateral circulation. Aneurysm, Bypass, Indocyanine green angiography, Posterior inferior cerebellar artery, Vascular disorders ABBREVIATIONS ABBREVIATIONS BTO balloon test occlusion CT computed tomography CTA computed tomography angiography DSA digital subtraction angiography H-H Hunt-Hess ICG indocyanine green MEP motor evoked potential OA occipital artery PICA posterior inferior cerebellar artery SSEP somatosensory evoked potential VA vertebral artery The posterior inferior cerebellar artery (PICA) is the most complex, tortuous, and variable of the cerebellar arteries.1,2 Aneurysms arising from PICA are uncommon, with a reported incidence between 0.5% and 3% of all intracranial aneurysms,3,4 and their treatment is particularly challenging and mandatory, because they tend to have a fragile wall and consequently a higher tendency to rupture even if small in size.5,6 Although endovascular coiling or direct clip ligation represents obvious strategies in most cases of saccular aneurysms, the high proportion of nonsaccular aneurysms that can be found in this location poses complex treatment challenges.7 When parent vessel sacrifice is deemed necessary, endovascular procedures carry nonnegligible risks8 and unpredictable consequences, since performing a reliable test occlusion is technically difficult in most cases.9 Open surgery provides a wide range of possibilities, including revascularization procedures, lowering the risk of ischemia. Literature is scarce regarding a standardized surgical decision-making process, due to the small number of series published, so that the strategy depends in most cases on the surgeon's personal expertise. The aim of this paper is to present our experience in microsurgical treatment of nonsaccular PICA aneurysms in an attempt to define a treatment algorithm with special emphasis on intraoperative assessment of collateral vascularization. METHODS The study was approved by our local ethics committee (EA4/143/16). The paper is reported following the STROBE statement. All patients signed an informed consent form prior to the surgical procedure. A specific consent form was not required for this study. We retrospectively reviewed the operation database of our institution, identifying patients who underwent microsurgical treatment for nonsaccular PICA aneurysms during a period between January 2007 and the present. Medical records, including pre- and postoperative imaging, operative reports, and hospital course, were reviewed. We identified aneurysms basing on preoperative digital subtraction angiography (DSA), computed tomography angiography (CTA), or magnetic resonance angiography (MRA). Patients presenting with symptoms or signs of subarachnoid hemorrhage were assessed both clinically, basing on Hunt-Hess scale (H-H) and radiologically through conventional computed tomography (CT). A decision regarding the best treatment for aneurysms without obvious surgical indication (ie, posterior fossa hematoma) was made after discussion between endovascular and neurosurgical teams. Nomenclature and Anatomic Location Aneurysms can be divided into vertebral artery (VA)–PICA junction and proper PICA ones. Lister and coworkers1 divided PICA, and consequently aneurysms arising from this artery, into 5 segments: anterior medullary (I), lateral medullary (II), tonsillomedullary (III), telovelotonsillar (IV), and cortical (V; Figure 1).1 These segments can also be named using numeric nomenclature as p1 (anterior medullary), p2 (lateral medullary), p3 (tonsillomedullary including caudal loop), p4 (telovelotonsillar including cranial loop), and p5 (cortical).10 FIGURE 1. View largeDownload slide PICA segment classification. Proximal PICA (blue) corresponds to anterior medullary (I), lateral medullary (II), and proximal part of tonsillomedullary (III) segments. Distal PICA (pink) corresponds to distal part of tonsillomedullary (III), telovelotonsillar (IV), and cortical (V) segments. In most cases, brainstem perforators take origin from proximal PICA. FIGURE 1. View largeDownload slide PICA segment classification. Proximal PICA (blue) corresponds to anterior medullary (I), lateral medullary (II), and proximal part of tonsillomedullary (III) segments. Distal PICA (pink) corresponds to distal part of tonsillomedullary (III), telovelotonsillar (IV), and cortical (V) segments. In most cases, brainstem perforators take origin from proximal PICA. In this study, we defined aneurysms as proximal if located in the portion of vessel going from VA–PICA junction to the proximal tonsillomedullary segment (III), and as distal if located beyond this segment (Figure 1).11 This classification is, in our opinion, the most useful for surgical planning, since it divides segments with different surgical problematic, particularly in terms of perforator anatomy. Operative Strategies A midline suboccipital approach was performed for distal PICA aneurysms and a midline suboccipital craniotomy with far lateral extension for those located within proximal segments. Parent vessel occlusion was performed when clip reconstruction was not feasible, due to complex anatomy, intraluminal thrombus, giant size, parent vessel stenosis, and/or hemodynamic impairment after clip positioning. In all cases, we performed an intraoperative test occlusion, placing a temporary clip proximal to the aneurysm neck with a subsequent indocyanine green (ICG) videoangiography, in order to assess the distal cerebellar filling of the PICA vascular territory. We compared capillary filling and transit times for the fluorescence between the affected and healthy cerebellar hemisphere. If in the ipsilateral hemisphere the venous phase showed a delay of more than 1 s compared to the contralateral cerebellar hemisphere, we empirically defined collateralization of the PICA territory as insufficient. Neurophysiological monitoring was used for the entire length of surgery, especially for evaluation of motor evoked potentials (MEPs) and somatosensory evoked potentials (SSEPs) variation during test occlusion. For safety reasons, we used very strict criteria to assess the need of revascularization; in fact, electrophysiological signs of insufficient collateralization were defined as any SEEP or MEP variation from baseline. PICA sacrifice without revascularization was considered only in case both tests (ICG videoangiography and neurophysiological monitoring) were suggestive of good collateralization. Patients with very poor H-H grade on admission (V) and patients with signs of raised intracranial pressure were not considered for revascularization during acute phase. PICA–PICA bypass (intracranial–intracranial) and occipital artery (OA) to PICA bypass (extracranial–intracranial) represent the revascularization techniques used in our series. In all cases the tonsillomedullary caudal loop of the artery was used as anastomosis site. As first step of surgery, we mapped the course of the OA using Doppler or neuronavigation. We then proceeded with craniotomy and exploration of intradural anatomy (firstly the state of the aneurysm and collateralization, and secondly the feasibility of PICA–PICA bypass). If preoperative imaging clearly showed that PICA–PICA bypass was not feasible, we started with dissection of OA before craniotomy. ICG videoangiography was repeated as final stage of procedure to assess aneurysm exclusion, parent vessel and perforator patency (in case of clip reconstruction), graft patency and flow (in case of bypass), and to confirm collateral circulation within PICA in case of vessel sacrifice without bypass. Conventional CT scan and DSA (or CTA) were used as a routinely postoperative radiological assessment. RESULTS Patient and Aneurysm Characteristics During the 9-yr period from January 2007 to July 2016, 18 nonsaccular PICA aneurysms in 17 patients were surgically treated in our Institution. The average patient age was 52.2 yr (range 16-78) with a slight male predominance (n = 9, 53%; Table). TABLE. Patient Data and Characteristics Case no.  Age, sex  Aneurysm location  Aneurysm size (mm)  Ruptured (R) or Unruptured (U)  Approach  Surgical strategy  Preoperative clinical condition  Latest clinical follow-up  Latest angiographic follow-up  1  71, M  Proximal (AMS)  6  R  Midline + far lateral paracondylar extension  Trapping + OA-PICA bypass  HH II  No new neurological deficit  Complete occlusion, bypass occluded  2  78, M  Proximal (LMS)  26  U  Midline + far lateral paracondylar extension  Proximal occlusion + OA-PICA bypass  Brain stem symptoms  No neurological deficit  Complete occlusion  3  73, F  Distal (CS-2 aneurysms)  5-4  R  Midline suboccipital  Proximal occlusion  HH V  No new neurological deficit  Complete occlusion  4  44, M  Proximal (VA–PICA)  9  U  Midline + far lateral paracondylar extension  Proximal occlusion  No manifest focal neurological deficit, intermittent aphasia  No neurological deficit  Complete occlusion  5  49, M  Proximal (AMS)  6  R  Midline + far lateral transcondylar extension  Trapping + OA-PICA bypass  HH IV  No new neurological deficit  Complete occlusion  6  36, M  Distal (TVTS)  8  U  Midline suboccipital  Wrapping  No focal neurological deficit, headache and dizziness  Nistagmus and dysmetria  Complete occlusion  7  45, F  Proximal (AMS)  4  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  No focal neurological deficit  No neurological deficit  Complete occlusion  8  30, F  Proximal (AMS)  5  R  Midline + far lateral paracondylar extension  Clip reconstruction  HH IV  No neurological deficit  Complete occlusion  9  57, M  Proximal (VA–PICA)  15  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  HH II  No neurological deficit  Complete occlusion  10  48, M  Proximal (VA–PICA)  7  U  Midline + far lateral paracondylar extension  Clip reconstruction  No focal neurological deficit, dizziness and intermittend headaches  No neurological deficit  Complete occlusion  11  48, F  Proximal (VA–PICA)  10  R  Midline + far lateral paracondylar extension  Clip reconstruction  Left-sided facial paresis  Stable left facial paresis,  Partial occlusion of previously coiled aneurysm (4 mm neck remnant stable on angiographic follow-up)  12  16, F  Proximal (VA–PICA)  18  U  Midline + far lateral paracondylar extension  Proximal occlusion + OA PICA bypass  No focal neurological deficit, headache, dizziness and nausea  No neurological deficit  Complete occlusion  13  73, F  Distal (TMS)  13  U  Midline suboccipital  Trapping  Slight dysmetria  Stable slight dysmetria  Complete occlusion  14  58, F  Proximal (LMS)  6  U  Midline + far lateral paracondylar extension  Trapping  No focal neurological deficit  No neurological deficit  Complete occlusion  15  43, F  Proximal (VA–PICA)  5  R  Midline + far lateral transcondylar extension  Proximal occlusion + PICA-PICA bypass  HH I  No neurological deficit  Complete occlusion  16  68, M  Proximal (AMS)  4  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  HH II (slight confusion)  No new neurological deficit  Complete occlusion  17  52, M  Proximal (AMS)  6  U  Midline + far lateral paracondylar extension  Clip reconstruction  No neurological deficit  No neurological deficit  Complete occlusion  Case no.  Age, sex  Aneurysm location  Aneurysm size (mm)  Ruptured (R) or Unruptured (U)  Approach  Surgical strategy  Preoperative clinical condition  Latest clinical follow-up  Latest angiographic follow-up  1  71, M  Proximal (AMS)  6  R  Midline + far lateral paracondylar extension  Trapping + OA-PICA bypass  HH II  No new neurological deficit  Complete occlusion, bypass occluded  2  78, M  Proximal (LMS)  26  U  Midline + far lateral paracondylar extension  Proximal occlusion + OA-PICA bypass  Brain stem symptoms  No neurological deficit  Complete occlusion  3  73, F  Distal (CS-2 aneurysms)  5-4  R  Midline suboccipital  Proximal occlusion  HH V  No new neurological deficit  Complete occlusion  4  44, M  Proximal (VA–PICA)  9  U  Midline + far lateral paracondylar extension  Proximal occlusion  No manifest focal neurological deficit, intermittent aphasia  No neurological deficit  Complete occlusion  5  49, M  Proximal (AMS)  6  R  Midline + far lateral transcondylar extension  Trapping + OA-PICA bypass  HH IV  No new neurological deficit  Complete occlusion  6  36, M  Distal (TVTS)  8  U  Midline suboccipital  Wrapping  No focal neurological deficit, headache and dizziness  Nistagmus and dysmetria  Complete occlusion  7  45, F  Proximal (AMS)  4  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  No focal neurological deficit  No neurological deficit  Complete occlusion  8  30, F  Proximal (AMS)  5  R  Midline + far lateral paracondylar extension  Clip reconstruction  HH IV  No neurological deficit  Complete occlusion  9  57, M  Proximal (VA–PICA)  15  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  HH II  No neurological deficit  Complete occlusion  10  48, M  Proximal (VA–PICA)  7  U  Midline + far lateral paracondylar extension  Clip reconstruction  No focal neurological deficit, dizziness and intermittend headaches  No neurological deficit  Complete occlusion  11  48, F  Proximal (VA–PICA)  10  R  Midline + far lateral paracondylar extension  Clip reconstruction  Left-sided facial paresis  Stable left facial paresis,  Partial occlusion of previously coiled aneurysm (4 mm neck remnant stable on angiographic follow-up)  12  16, F  Proximal (VA–PICA)  18  U  Midline + far lateral paracondylar extension  Proximal occlusion + OA PICA bypass  No focal neurological deficit, headache, dizziness and nausea  No neurological deficit  Complete occlusion  13  73, F  Distal (TMS)  13  U  Midline suboccipital  Trapping  Slight dysmetria  Stable slight dysmetria  Complete occlusion  14  58, F  Proximal (LMS)  6  U  Midline + far lateral paracondylar extension  Trapping  No focal neurological deficit  No neurological deficit  Complete occlusion  15  43, F  Proximal (VA–PICA)  5  R  Midline + far lateral transcondylar extension  Proximal occlusion + PICA-PICA bypass  HH I  No neurological deficit  Complete occlusion  16  68, M  Proximal (AMS)  4  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  HH II (slight confusion)  No new neurological deficit  Complete occlusion  17  52, M  Proximal (AMS)  6  U  Midline + far lateral paracondylar extension  Clip reconstruction  No neurological deficit  No neurological deficit  Complete occlusion  VA: vertebral artery; PICA: posterior inferior cerebellar artery; AMS: anterior medullary segment; LMS: lateral medullary segment; TMS: tonsillomedullary segment; TVTS: telovelotonsillar segment; CS: cortical segment; OA: occipital artery; H-H: Hunt-Hess grade. View Large Nine (53%) patients presented with subarachnoid hemorrhage. The average H-H grade on admission was 3.5. In ruptured cases, surgery was performed within 4 d after hemorrhage in all but 1 case, treated after 77 d, due to angiographic evidence of aneurysm recurrence after coiling. VA–PICA junction (n = 6/18, 33%) and anterior medullary (p1) segment of PICA (n = 6/18, 33%) were the most common location. Two (11%) aneurysms were located in the lateral medullary (p2) segment, 1 in the tonsillomedullary (p3), 1 in the telovelotonsillar (p4), and 2 (11%) in the cortical (p5) segment. We can observe that 14 (78%) aneurysms were located within the proximal PICA (including those located at VA–PICA junction). In this group of patients, in 10 (71%) cases vessel sacrifice was required, only in 2 cases without the need of PICA revascularization. Four proximal aneurysms were treated via clip reconstruction. The mean size of aneurysms was 8.4 mm, ranging from 4 to 26 mm; 4 (22%) aneurysms had intraluminal thrombus and 2 (11%) had been previously coiled with aneurysm refilling evidence on follow-up control. In 3 (18%) patients, we found at least 1 associated aneurysm of anterior circulation (5 aneurysms: 4 internal carotid artery and 1 middle cerebral artery), and in 1 case we found an associated ipsilateral VA blister aneurysm. The median clinical follow-up was 7 mo (range: 1 wk-65 mo) and the median angiographic follow-up was 3.4 mo (range: 1 wk-65 mo). Results of latest clinical and angiographic follow-up are presented in Table. Surgical Treatment Four aneurysms (22%), located in the most proximal segments (VA–PICA, n = 2; anterior medullary segment, n = 2), were feasible for clip reconstruction. PICA occlusion was necessary in 12 patients (70%), in 10 cases harboring a proximal aneurysm, in 2 cases distal. In 4 patients (proximal, n = 2; distal, n = 2; 23%) vessel sacrifice without revascularization was performed after good collateral circulation was established, without postoperative sequelae (Figure 2). In 1 case, we performed wrapping of a telovelotonsillar segment aneurysm, because of unusual presence of perforators along the entire segment and aneurysm wall. Bypass was technically not feasible due to deep location of caudal loops. FIGURE 2. View largeDownload slide Case 14. Trapping and excision of proximal left PICA aneurysm. A, A 3-dimensional reconstruction showing a proximal fusiform left PICA aneurysm in a 58-yr-old woman who presented to our institution with the diagnosis of right ICA and left proximal PICA aneurysms, after investigations for vertigo. B, Intraoperative inspection of vessel and cranial nerve anatomy; the aneurysm was located just anterior to the lower cranial nerve plane. C, Proximal PICA clipping for intraoperative test occlusion. D, Intraoperative ICG videoangiography showing retrograde flow within an occluded PICA provided by a second PICA branch, with retrograde filling of the main PICA and perforators distal to the aneurysm. E and F, Trapping and excision of aneurysm. FIGURE 2. View largeDownload slide Case 14. Trapping and excision of proximal left PICA aneurysm. A, A 3-dimensional reconstruction showing a proximal fusiform left PICA aneurysm in a 58-yr-old woman who presented to our institution with the diagnosis of right ICA and left proximal PICA aneurysms, after investigations for vertigo. B, Intraoperative inspection of vessel and cranial nerve anatomy; the aneurysm was located just anterior to the lower cranial nerve plane. C, Proximal PICA clipping for intraoperative test occlusion. D, Intraoperative ICG videoangiography showing retrograde flow within an occluded PICA provided by a second PICA branch, with retrograde filling of the main PICA and perforators distal to the aneurysm. E and F, Trapping and excision of aneurysm. Eight (47%) patients harboring proximal aneurysms underwent revascularization procedures via PICA–PICA bypass (n = 4, 23%; Figure 3) or, alternatively, OA to PICA bypass (n = 4, 23%). FIGURE 3. View largeDownload slide Case 16. In Situ PICA–PICA bypass. A, Conventional CT scan showing subarachnoid hemorrhage in a 68-yr-old man who presented to the Emergency Room of our institution with sudden onset of severe headache, vomiting, and diplopia. B and C, DSA and 3-dimensional reconstruction showing right small fusiform proximal PICA aneurysm. D, Intraoperative view of caudal loop position close to midline and good caliber of both loops. We proceeded with PICA–PICA bypass and proximal occlusion of aneurysm after exposure of aneurysm, inspection of anatomy, and test occlusion that showed poor collateral flow within PICA territory. E, Postoperative DSA showing good PICA–PICA bypass function. F, Postoperative sagittal CTA showing clip position. FIGURE 3. View largeDownload slide Case 16. In Situ PICA–PICA bypass. A, Conventional CT scan showing subarachnoid hemorrhage in a 68-yr-old man who presented to the Emergency Room of our institution with sudden onset of severe headache, vomiting, and diplopia. B and C, DSA and 3-dimensional reconstruction showing right small fusiform proximal PICA aneurysm. D, Intraoperative view of caudal loop position close to midline and good caliber of both loops. We proceeded with PICA–PICA bypass and proximal occlusion of aneurysm after exposure of aneurysm, inspection of anatomy, and test occlusion that showed poor collateral flow within PICA territory. E, Postoperative DSA showing good PICA–PICA bypass function. F, Postoperative sagittal CTA showing clip position. A midline suboccipital craniotomy with far-lateral extension was performed in 14 (82%) patients. Partial condylar removal was necessary in 2 (12%) cases. None of them experienced postoperative cranio-cervical junction instability, since we drilled only the dorsomedial part of the occipital condyle. In no cases did we observe postoperative cranial nerve neuropathies nor cerebellar and/or brainstem ischemia. In 3 (18%) patients, a postoperative cerebrospinal fluid leak occurred, promptly resolved after lumbar drain placement. One patient died few weeks after surgical procedure, due to his poor clinical grade on admission (H-H V). DISCUSSION For PICA aneurysms, endovascular procedures provide the advantage of avoiding cranial nerve manipulation, which represents the main risk of surgery. Despite this, for nonsaccular aneurysms, when vessel sacrifice is required for treatment, at present, no modalities are available to reliably assess the risk of brainstem and cerebellar ischemia, which occurs in a nonnegligible number of cases, even in the largest and most recent endovascular series.8,12,13 Park et al14 reported on the use of balloon test occlusion (BTO) for assessment of tolerance for PICA occlusion. Performing BTO in the PICA, however, is technically difficult because of small caliber of the artery, and unreliable in identifying true ischemia. Moreover, PICA aneurysm location represents an independent risk factor for recurrence after endovascular treatment.15 Open surgery includes several options, allowing the surgeon to perform clip reconstruction when possible or, alternatively, occlusion and revascularization of PICA, lowering significantly the risk of ischemia. An accurate patient selection can therefore reasonably reduce the overall morbidity. Role of Intraoperative Test Occlusion We did not use bypass as universal approach for all cases of PICA sacrifice. Our choice whether to proceed with revascularization was based on careful anatomic evaluation of vessels and perforators, and on intraoperative test occlusion with ICG videoangiography and neurophysiological monitoring. In 4 cases, this strategy allowed us to avoid unnecessary bypass. At present, there is no consensus regarding the most reliable intraoperative technique for collateral flow assessment. Completion of intraoperative DSA takes time, requiring prolonged temporary clipping, and therefore placing the brain tissue at risk of ischemia. Conversely, microdoppler probes can represent a useful tool to assess quantitative flow, but their feasibility shows limits with the decrease of vessel caliber (ie, PICA-perforating arteries), providing signals difficult to interpret.16 The importance of ICG during test occlusion has already been reported in literature, both for artery and vein sacrifice.17,18 ICG provides a unique aid for “live” assessment of vascular collateralization, through evaluation of the presence of retrograde flow within the occluded vessel and small perforators,19 superior to DSA, which is often not able to detect small arteries.18 However, although ICG provides a qualitative assessment of collateral circulation, scarce information about quantitative flow is available, making it difficult to establish whether collateralization is sufficient to supply PICA territory.18 For this reason, we did not use ICG videoangiography as a stand-alone technique, and we additionally utilized neurophysiological monitoring as an adjuvant tool to estimate risks of ischemia following vessel sacrifice.20,21 In our opinion, the combined use of these techniques has the advantage of being able to provide a dual point of view on collateral circulation with good reliability, even if the risk of ischemia cannot be reduced to zero. Algorithm for Surgical Strategy In times when many different revascularization strategies have been proposed by cerebrovascular surgeons, some confusion could be generated by the versatility of techniques. Thus, it is our strong belief to keep things safe and simple and provide the younger generation of bypass surgeons with an intuitive road map to the therapy of these lesions, preferring just a few and logical solutions over too individualized strategies. Based on our experience, which represents one of the largest reported surgical series of nonsaccular PICA aneurysms,3,6,7,22-25 we propose an algorithm for decision-making process during microsurgery (Figure 4). FIGURE 4. View largeDownload slide Algorithm for surgical strategy. FIGURE 4. View largeDownload slide Algorithm for surgical strategy. Proximal PICA aneurysm complexity is mainly due to their location more proximal to midline, anterior to the lower cranial nerve plane, usually requiring wider craniotomy, and the presence of brainstem and cerebellar perforators. Although nonsaccular aneurysms can rarely be clipped without vessel sacrifice and need of revascularization, clip reconstruction should be considered in all cases as the first option, as preoperative imaging sometimes cannot precisely clarify the existent intraoperative anatomy. When PICA sacrifice is deemed necessary, the second step is to evaluate the existence of collateral flow. In our experience, only if insufficient collateral circulation was detected did we consider revascularization, via PICA–PICA or OA–PICA bypass. Distal p3 is the portion of PICA utilized in all our cases as recipient vessel site. This segment is characterized by some degree of variation, with a possible location superior or inferior to the caudal pole of the tonsil, even without forming a loop.2 The presence of 2 good loops allows performing PICA–PICA in Situ bypass (Figure 5). In case of absence of good donor PICA, OA–PICA bypass represents a more than acceptable and low-risk alternative option. FIGURE 5. View largeDownload slide Caudal loop variations. Caudal loop anatomy is fundamental for bypass strategy. Loops close to midline, within the cisterna magna, allow us to perform revascularization through PICA–PICA bypass (arrows show anastomosis site). Caudal loop absence or location superior or inferior to the caudal pole of tonsil forces the surgeon to choose an alternative strategy. FIGURE 5. View largeDownload slide Caudal loop variations. Caudal loop anatomy is fundamental for bypass strategy. Loops close to midline, within the cisterna magna, allow us to perform revascularization through PICA–PICA bypass (arrows show anastomosis site). Caudal loop absence or location superior or inferior to the caudal pole of tonsil forces the surgeon to choose an alternative strategy. PICA–PICA bypass is the most popular and straightforward technique for PICA revascularization. When feasible, it usually represents the first option to consider for flow replacement on this site,22 because of different reasons. First, it is less vulnerable to occlusion. Secondly, it requires minimal anatomic distortion, being caudal loops easy to reach and the procedure entirely intracranial; moreover, surgical time is shorter compared to other techniques, since it is possible to spare the time needed for extracranial artery harvesting or graft preparation. Thirdly, diameters of donor and recipient artery are usually well matched. OA–PICA represents the best alternative technique to PICA–PICA anastomosis, being a low-risk procedure in experienced hands. As for PICA–PICA bypass, p3 caudal loop is utilized as recipient artery, without the need to cross the lower cranial nerve plane to make the anastomosis, a step usually required for other techniques (ie, PICA reimplantation). This is a crucial advantage of this procedure, since it represents one of the major causes of morbidity related to surgical treatment. The only disadvantage of OA–PICA bypass is the intricate OA dissection (ie, compared to superficial temporal artery), usually time consuming. The use of neuronavigation helps in shortening the time required for OA harvesting, since this artery is characterized by tortuosity and variable course, deeply located in the occipital muscles (Figure 6). A linear skin incision over the course of artery can be performed, with subsequent tunneling to reach the recipient PICA caudal loop. Cranial and skin closure assumes a great importance, in order to avoid donor vessel stenosis, kinking, and consequent bypass failure due to bone and pericranial tissue compression. FIGURE 6. View largeDownload slide OA isolation technique. A, Skin mark on OA course with the aid of navigation. B, OA dissection. C, Final steps of isolation. FIGURE 6. View largeDownload slide OA isolation technique. A, Skin mark on OA course with the aid of navigation. B, OA dissection. C, Final steps of isolation. Other bypass techniques have been described for proximal aneurysms, but we find them rarely feasible and associated with higher complication rate, as PICA reimplantation to VA and radial graft interposition. PICA reimplantation represents the most difficult bypass procedure, subject to the greatest risk of occlusion, and associated with a high rate of postoperative lower cranial neuropathies, as the surgical corridor crosses the cranial nerve plane through vagoaccessory triangle.26 Moreover, it requires aggressive condylectomy, adding a potential considerable morbidity. Radial graft interposition between proximal VA and PICA is another alternative, but it should be reserved for cases in which the other techniques are not feasible or high flow is requested, because it is more time consuming and demanding, due to the necessity to perform preparation of the radial artery as well as 2 anastomoses. Distal aneurysms are less challenging, as commonly perforating arteries are not present within this segment. These aneurysms can be clipped, trapped, or proximally occluded with or without revascularization. In our series, we did not perform any revascularization during distal aneurysm procedures, as PICA could be safely occluded in all cases. When revascularization is needed, the most appealing technique for distal aneurysms is excision and PICA reanastomosis. The main limitation of this procedure is related to the restricted number of cases in which it can be performed; it is only feasible in cases of a small- or medium-size aneurysm with single afferent and efferent arteries. The possible presence of perforators, due to anatomic variability, represents another potential limitation. Limitations Limitations of this study include its retrospective nature, the surgical bias, and the absence of long-term follow-up. CONCLUSION For surgical treatment of nonsaccular PICA aneurysms, when vessel sacrifice is required, it is possible to use a selective approach to revascularization, after careful evaluation of the existent anatomy and the presence of collateral supply. For this purpose, an intraoperative occlusion test with the combined use of ICG videoangiography and neurophysiological monitoring provides reliable information. For proximal aneurysms, when bypass is required, PICA–PICA and OA–PICA provide good results with low complication rates; thus, they should be preferred to other available techniques. Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Lister JR, Rhoton AL Jr, Matsushima T, Peace DA. Microsurgical anatomy of the posterior inferior cerebellar artery. Neurosurgery . 1982; 10( 2): 170- 199. Google Scholar PubMed  2. Rhoton AL Jr. The cerebellar arteries. Neurosurgery . 2000; 47( 3 suppl): S29- S68. Google Scholar CrossRef Search ADS PubMed  3. Lewis SB, Chang DJ, Peace DA, Lafrentz PJ, Day AL. Distal posterior inferior cerebellar artery aneurysms: clinical features and management. J Neurosurg . 2002; 97( 4): 756- 766. Google Scholar CrossRef Search ADS PubMed  4. Petr O, Sejkorova A, Bradac O, Brinjikji W, Lanzino G. Safety and efficacy of treatment strategies for posterior inferior cerebellar artery aneurysms: a systematic review and meta-analysis. Acta Neurochir . 2016; 158( 12): 2415- 2428. Google Scholar CrossRef Search ADS PubMed  5. Tokimura H, Yamahata H, Kamezawa T et al.   Clinical presentation and treatment of distal posterior inferior cerebellar artery aneurysms. Neurosurg Rev . 2011; 34( 1): 57- 67. Google Scholar CrossRef Search ADS PubMed  6. Horiuchi T, Tanaka Y, Hongo K, Nitta J, Kusano Y, Kobayashi S. Characteristics of distal posteroinferior cerebellar artery aneurysms. Neurosurgery . 2003; 53( 3): 589- 595; discussion 595-586. Google Scholar CrossRef Search ADS PubMed  7. Lehto H, Harati A, Niemela M et al.   Distal posterior inferior cerebellar artery aneurysms: clinical features and outcome of 80 patients. World Neurosurg . 2014; 82( 5): 702- 713. Google Scholar CrossRef Search ADS PubMed  8. Chalouhi N, Jabbour P, Starke RM et al.   Endovascular treatment of proximal and distal posterior inferior cerebellar artery aneurysms. J Neurosurg . 2013; 118( 5): 991- 999. Google Scholar CrossRef Search ADS PubMed  9. Huang L, Zee CS, Zhang XL. Temporary occlusion test using a microcatheter. World Neurosurg . 2012; 77( 2): 398.E397- 310. Google Scholar CrossRef Search ADS   10. Rodriguez-Hernandez A, Rhoton AL Jr, Lawton MT. Segmental anatomy of cerebellar arteries: a proposed nomenclature. Laboratory investigation. J Neurosurg . 2011; 115( 2): 387- 397. Google Scholar CrossRef Search ADS PubMed  11. Bacigaluppi S, Bergui M, Crobeddu E, Garbossa D, Ducati A, Fontanella M. Aneurysms of the medullary segments of the posterior-inferior cerebellar artery: considerations on treatment strategy and clinical outcome. Neurol Sci . 2013; 34( 4): 529- 536. Google Scholar CrossRef Search ADS PubMed  12. Peluso JP, van Rooij WJ, Sluzewski M, Beute GN, Majoie CB. Posterior inferior cerebellar artery aneurysms: incidence, clinical presentation, and outcome of endovascular treatment. AJNR Am J Neuroradiol . 2008; 29( 1): 86- 90. Google Scholar CrossRef Search ADS PubMed  13. Crowley RW, Albuquerque FC, Ducruet AF, Williamson RW, McDougall CG. Technical considerations in the endovascular management of aneurysms of the posterior inferior cerebellar artery. Neurosurgery . 2012; 71( 2 Suppl Operative): ons204- ons217; discussion ons217-ons208. Google Scholar PubMed  14. Park W, Ahn JS, Park JC, Kwun BD, Kim CJ. Occipital artery-posterior inferior cerebellar artery bypass for the treatment of aneurysms arising from the vertebral artery and its branches. World Neurosurg . 2014; 82( 5): 714- 721. Google Scholar CrossRef Search ADS PubMed  15. Kim BM, Shin YS, Kim SH et al.   Incidence and risk factors of recurrence after endovascular treatment of intracranial vertebrobasilar dissecting aneurysms. Stroke . 2011; 42( 9): 2425- 2430. Google Scholar CrossRef Search ADS PubMed  16. de Oliveira JG, Beck J, Seifert V, Teixeira MJ, Raabe A. Assessment of flow in perforating arteries during intracranial aneurysm surgery using intraoperative near-infrared indocyanine green videoangiography. Neurosurgery . 2008; 62( 6 suppl 3): 1300- 1310. Google Scholar PubMed  17. Ferroli P, Nakaji P, Acerbi F, Albanese E, Broggi G. Indocyanine green (ICG) temporary clipping test to assess collateral circulation before venous sacrifice. World Neurosurg . 2011; 75( 1): 122- 125. Google Scholar CrossRef Search ADS PubMed  18. Kim DL, Cohen-Gadol AA. Indocyanine-green videoangiogram to assess collateral circulation before arterial sacrifice for management of complex vascular and neoplastic lesions: technical note. World Neurosurg . 2013; 79( 2): 404.e401- 406. Google Scholar CrossRef Search ADS   19. Li J, Lan Z, He M, You C. Assessment of microscope-integrated indocyanine green angiography during intracranial aneurysm surgery: a retrospective study of 120 patients. Neurol India . 2009; 57( 4): 453- 459. Google Scholar CrossRef Search ADS PubMed  20. Pancucci G, Potts MB, Rodriguez-Hernandez A, Andrade H, Guo L, Lawton MT. Rescue bypass for revascularization after ischemic complications in the treatment of giant or complex intracranial aneurysms. World Neurosurg . 2015; 83( 6): 912- 920. Google Scholar CrossRef Search ADS PubMed  21. Chen L, Spetzler RF, McDougall CG, Albuquerque FC, Xu B. Detection of ischemia in endovascular therapy of cerebral aneurysms: a perspective in the era of neurophysiological monitoring. Neurosurg Rev . 2011; 34( 1): 69- 75. Google Scholar CrossRef Search ADS PubMed  22. Abla AA, McDougall CM, Breshears JD, Lawton MT. Intracranial-to-intracranial bypass for posterior inferior cerebellar artery aneurysms: options, technical challenges, and results in 35 patients. J Neurosurg . 2016; 124( 5): 1275- 1286. Google Scholar CrossRef Search ADS PubMed  23. Nussbaum ES, Mendez A, Camarata P, Sebring L. Surgical management of fusiform aneurysms of the peripheral posteroinferior cerebellar artery. Neurosurgery . 2003; 53( 4): 831- 834; discussion 834-835. Google Scholar CrossRef Search ADS PubMed  24. Liew D, Ng PY, Ng I. Surgical management of ruptured and unruptured symptomatic posterior inferior cerebellar artery aneurysms. Br J Neurosurg . 2004; 18( 6): 608- 612. Google Scholar CrossRef Search ADS PubMed  25. Williamson RW, Wilson DA, Abla AA et al.   Clinical characteristics and long-term outcomes in patients with ruptured posterior inferior cerebellar artery aneurysms: a comparative analysis. J Neurosurg . 2015; 123( 2): 441- 445. Google Scholar CrossRef Search ADS PubMed  26. Rodriguez-Hernandez A, Lawton MT. Anatomical triangles defining surgical routes to posterior inferior cerebellar artery aneurysms. J Neurosurg . 2011; 114( 4): 1088- 1094. Google Scholar CrossRef Search ADS PubMed  COMMENTS The authors describe an informative case series of a very challenging cerebrovascular problem: fuciform (non-saccular) PICA aneurysm. They manage to illustrate the process of clinical decision making in the OR - whether revascularization is required or not, and what logical steps to undertake in cases which do. Despite advances in endovascular techniques, especially ruptured non-saccular aneurysm pose a real challenge, as potent antithrombotic and anticoagulant medications often required during and after stenting and flow-diverting procedures do not mix particularly well with a clinical setting of an acute posterior fossa hemorrhage. Obviously, open revascularization surgery in that same setting is no trivial feat, either. Wisely, the authors admit that patients with highest grade SAHs are not suitable for this methodology. Aki Laakso Helsinki, Finland The authors report on their retrospective series of 18 non-saccular PICA aneurysms treated microsurgically and provide an algorithm the neurosurgeon can use to determine whether or not revascularization is needed if PICA preservation is not feasible. The need for revascularization is determined by assessing collateral flow in the affected PICA territory after temporary occlusion using ICG video angiography in combination with neurophysiological monitoring with SSEP and MEP. Fifty-three percent of the patients presented with subarachnoid hemorrhage. More than three-fourths were located within proximal PICA (14); of those, 10 had vessel sacrifice of which 8 needed revascularization with PICA-PICA (4) and OA-PICA bypass (4). Of the 4 distal PICA aneurysms, none had revascularization. As mentioned by the authors, these are rare and aggressive lesions that should be treated promptly. The technique and algorithm presented herein are interesting, easy to perform, and can be very useful to the neurosurgeon. Both ICG video angiography and neuromonitoring are widely used modalities in cerebrovascular neurosurgery and aneurysm treatment. In this article, the authors nicely combine their use to help decide whether revascularization is necessary during surgical treatment of this disease entity; they use stringent selection criteria for revascularization. At our institution, we routinely use Flow Assisted Surgical Technique (FAST) which utilizes the Charbel microflow probe for intraoperative flow measurement. This tool gives real time measurement of intravascular flow in cc/min as well as direction of blood flow, among other features. When selecting the patient for PICA revascularization intraoperatively in such situations, it would be very useful if the surgeon could quantify retrograde collateral filling after temporary clipping of PICA, and determine if this would be sufficient without the need for revascularization. The flow probe cannot be used to obtain such data at this time, however we use it routinely to confirm adequate flow through the completed bypass. It can also be used for planning purposes when determining how much flow replacement is needed prior to performing vessel sacrifice and selecting an adequate donor. We congratulate the authors for their efforts, and are confident that further technological advances should provide more accurate means to quantify collateral flow in such situations and tolerance to PICA sacrifice. Ziad A. Hage Charlotte, North Carolina The authors report a sophisticated and effective strategy for surgical management of non-saccular PICA aneurysms. They report a series of 17 patients with 18 non-saccular PICA aneurysms treated surgically over a 9-year period. Of the 17 patients, 9 presented with a subarachnoid hemorrhage. Intraoperatively, test occlusion with temporary clipping proximal to the aneurysm neck was performed in all cases, and it was followed by ICG videoangiography. In addition, MEPs and SSEPs were evaluated during test occlusion. They compared capillary filling and transit times between the involved and contralateral cerebellar hemispheres, and if there was a delay of more than 1 second they proceeded with a bypass. Of the 17 patients, 8 required either a PICA-PICA or OA-PICA bypass. The authors advocate using a PICA-PICA anastomosis whenever possible, and resorting to an OA-PICA anastomosis only as a second choice. They report outstanding results in this series with only 3 CSF leaks and 1 death due to poor neurological condition on admission. Remarkably, the authors report no postoperative cranial nerve neuropathies or cerebellar and/or brainstem ischemia. Rafael J. Tamargo Baltimore, Maryland Copyright © 2017 by the Congress of Neurological Surgeons http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Operative Neurosurgery Oxford University Press

Decision Making in Surgery for Nonsaccular Posterior Inferior Cerebellar Artery Aneurysms With Special Reference to Intraoperative Assessment of Collateral Blood Flow and Neurophysiological Function

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Congress of Neurological Surgeons
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Copyright © 2017 by the Congress of Neurological Surgeons
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2332-4252
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2332-4260
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10.1093/ons/opx141
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Abstract

Abstract BACKGROUND Posterior inferior cerebellar artery (PICA) aneurysms represent a challenging pathology. PICA sacrifice is often necessary, due to the high proportion of nonsaccular aneurysms that can be found in this location. Several treatments are available, but the infrequency of these aneurysms and the increasing number of endovascular techniques have limited the development of a standardized algorithm for cases in which open surgery is indicated. OBJECTIVE We present our series of nonsaccular PICA aneurysms, in the attempt to define an algorithm for their surgical management. METHODS We retrospectively reviewed the operation database, identifying patients harboring nonsaccular PICA aneurysms who were surgically treated at our institution from 2007 to 2016. RESULTS During a 9-yr period, 17 patients harboring 18 nonsaccular PICA aneurysms were surgically treated at our institution. Fourteen (7.7%) aneurysms were located within the proximal PICA (including those located at the vertebral artery–PICA junction), and 4 were located distally. We performed PICA revascularization in 8 (57.1%) cases of proximal aneurysms (n = 4, PICA–PICA bypass; n = 4, occipital artery–PICA bypass). We based our decision whether to perform bypass on intraoperative test occlusion with indocyanine green (ICG) videoangiography and neurophysiological monitoring. In no cases, bypass was necessary for distal aneurysms. CONCLUSION For nonsaccular PICA aneurysms, in which vessel occlusion is often necessary, it is possible to adopt a selective use of revascularization techniques. Intraoperative occlusion test with ICG videoangiography and neurophysiological monitoring provides reliable indications, allowing real-time assessment of collateral circulation. Aneurysm, Bypass, Indocyanine green angiography, Posterior inferior cerebellar artery, Vascular disorders ABBREVIATIONS ABBREVIATIONS BTO balloon test occlusion CT computed tomography CTA computed tomography angiography DSA digital subtraction angiography H-H Hunt-Hess ICG indocyanine green MEP motor evoked potential OA occipital artery PICA posterior inferior cerebellar artery SSEP somatosensory evoked potential VA vertebral artery The posterior inferior cerebellar artery (PICA) is the most complex, tortuous, and variable of the cerebellar arteries.1,2 Aneurysms arising from PICA are uncommon, with a reported incidence between 0.5% and 3% of all intracranial aneurysms,3,4 and their treatment is particularly challenging and mandatory, because they tend to have a fragile wall and consequently a higher tendency to rupture even if small in size.5,6 Although endovascular coiling or direct clip ligation represents obvious strategies in most cases of saccular aneurysms, the high proportion of nonsaccular aneurysms that can be found in this location poses complex treatment challenges.7 When parent vessel sacrifice is deemed necessary, endovascular procedures carry nonnegligible risks8 and unpredictable consequences, since performing a reliable test occlusion is technically difficult in most cases.9 Open surgery provides a wide range of possibilities, including revascularization procedures, lowering the risk of ischemia. Literature is scarce regarding a standardized surgical decision-making process, due to the small number of series published, so that the strategy depends in most cases on the surgeon's personal expertise. The aim of this paper is to present our experience in microsurgical treatment of nonsaccular PICA aneurysms in an attempt to define a treatment algorithm with special emphasis on intraoperative assessment of collateral vascularization. METHODS The study was approved by our local ethics committee (EA4/143/16). The paper is reported following the STROBE statement. All patients signed an informed consent form prior to the surgical procedure. A specific consent form was not required for this study. We retrospectively reviewed the operation database of our institution, identifying patients who underwent microsurgical treatment for nonsaccular PICA aneurysms during a period between January 2007 and the present. Medical records, including pre- and postoperative imaging, operative reports, and hospital course, were reviewed. We identified aneurysms basing on preoperative digital subtraction angiography (DSA), computed tomography angiography (CTA), or magnetic resonance angiography (MRA). Patients presenting with symptoms or signs of subarachnoid hemorrhage were assessed both clinically, basing on Hunt-Hess scale (H-H) and radiologically through conventional computed tomography (CT). A decision regarding the best treatment for aneurysms without obvious surgical indication (ie, posterior fossa hematoma) was made after discussion between endovascular and neurosurgical teams. Nomenclature and Anatomic Location Aneurysms can be divided into vertebral artery (VA)–PICA junction and proper PICA ones. Lister and coworkers1 divided PICA, and consequently aneurysms arising from this artery, into 5 segments: anterior medullary (I), lateral medullary (II), tonsillomedullary (III), telovelotonsillar (IV), and cortical (V; Figure 1).1 These segments can also be named using numeric nomenclature as p1 (anterior medullary), p2 (lateral medullary), p3 (tonsillomedullary including caudal loop), p4 (telovelotonsillar including cranial loop), and p5 (cortical).10 FIGURE 1. View largeDownload slide PICA segment classification. Proximal PICA (blue) corresponds to anterior medullary (I), lateral medullary (II), and proximal part of tonsillomedullary (III) segments. Distal PICA (pink) corresponds to distal part of tonsillomedullary (III), telovelotonsillar (IV), and cortical (V) segments. In most cases, brainstem perforators take origin from proximal PICA. FIGURE 1. View largeDownload slide PICA segment classification. Proximal PICA (blue) corresponds to anterior medullary (I), lateral medullary (II), and proximal part of tonsillomedullary (III) segments. Distal PICA (pink) corresponds to distal part of tonsillomedullary (III), telovelotonsillar (IV), and cortical (V) segments. In most cases, brainstem perforators take origin from proximal PICA. In this study, we defined aneurysms as proximal if located in the portion of vessel going from VA–PICA junction to the proximal tonsillomedullary segment (III), and as distal if located beyond this segment (Figure 1).11 This classification is, in our opinion, the most useful for surgical planning, since it divides segments with different surgical problematic, particularly in terms of perforator anatomy. Operative Strategies A midline suboccipital approach was performed for distal PICA aneurysms and a midline suboccipital craniotomy with far lateral extension for those located within proximal segments. Parent vessel occlusion was performed when clip reconstruction was not feasible, due to complex anatomy, intraluminal thrombus, giant size, parent vessel stenosis, and/or hemodynamic impairment after clip positioning. In all cases, we performed an intraoperative test occlusion, placing a temporary clip proximal to the aneurysm neck with a subsequent indocyanine green (ICG) videoangiography, in order to assess the distal cerebellar filling of the PICA vascular territory. We compared capillary filling and transit times for the fluorescence between the affected and healthy cerebellar hemisphere. If in the ipsilateral hemisphere the venous phase showed a delay of more than 1 s compared to the contralateral cerebellar hemisphere, we empirically defined collateralization of the PICA territory as insufficient. Neurophysiological monitoring was used for the entire length of surgery, especially for evaluation of motor evoked potentials (MEPs) and somatosensory evoked potentials (SSEPs) variation during test occlusion. For safety reasons, we used very strict criteria to assess the need of revascularization; in fact, electrophysiological signs of insufficient collateralization were defined as any SEEP or MEP variation from baseline. PICA sacrifice without revascularization was considered only in case both tests (ICG videoangiography and neurophysiological monitoring) were suggestive of good collateralization. Patients with very poor H-H grade on admission (V) and patients with signs of raised intracranial pressure were not considered for revascularization during acute phase. PICA–PICA bypass (intracranial–intracranial) and occipital artery (OA) to PICA bypass (extracranial–intracranial) represent the revascularization techniques used in our series. In all cases the tonsillomedullary caudal loop of the artery was used as anastomosis site. As first step of surgery, we mapped the course of the OA using Doppler or neuronavigation. We then proceeded with craniotomy and exploration of intradural anatomy (firstly the state of the aneurysm and collateralization, and secondly the feasibility of PICA–PICA bypass). If preoperative imaging clearly showed that PICA–PICA bypass was not feasible, we started with dissection of OA before craniotomy. ICG videoangiography was repeated as final stage of procedure to assess aneurysm exclusion, parent vessel and perforator patency (in case of clip reconstruction), graft patency and flow (in case of bypass), and to confirm collateral circulation within PICA in case of vessel sacrifice without bypass. Conventional CT scan and DSA (or CTA) were used as a routinely postoperative radiological assessment. RESULTS Patient and Aneurysm Characteristics During the 9-yr period from January 2007 to July 2016, 18 nonsaccular PICA aneurysms in 17 patients were surgically treated in our Institution. The average patient age was 52.2 yr (range 16-78) with a slight male predominance (n = 9, 53%; Table). TABLE. Patient Data and Characteristics Case no.  Age, sex  Aneurysm location  Aneurysm size (mm)  Ruptured (R) or Unruptured (U)  Approach  Surgical strategy  Preoperative clinical condition  Latest clinical follow-up  Latest angiographic follow-up  1  71, M  Proximal (AMS)  6  R  Midline + far lateral paracondylar extension  Trapping + OA-PICA bypass  HH II  No new neurological deficit  Complete occlusion, bypass occluded  2  78, M  Proximal (LMS)  26  U  Midline + far lateral paracondylar extension  Proximal occlusion + OA-PICA bypass  Brain stem symptoms  No neurological deficit  Complete occlusion  3  73, F  Distal (CS-2 aneurysms)  5-4  R  Midline suboccipital  Proximal occlusion  HH V  No new neurological deficit  Complete occlusion  4  44, M  Proximal (VA–PICA)  9  U  Midline + far lateral paracondylar extension  Proximal occlusion  No manifest focal neurological deficit, intermittent aphasia  No neurological deficit  Complete occlusion  5  49, M  Proximal (AMS)  6  R  Midline + far lateral transcondylar extension  Trapping + OA-PICA bypass  HH IV  No new neurological deficit  Complete occlusion  6  36, M  Distal (TVTS)  8  U  Midline suboccipital  Wrapping  No focal neurological deficit, headache and dizziness  Nistagmus and dysmetria  Complete occlusion  7  45, F  Proximal (AMS)  4  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  No focal neurological deficit  No neurological deficit  Complete occlusion  8  30, F  Proximal (AMS)  5  R  Midline + far lateral paracondylar extension  Clip reconstruction  HH IV  No neurological deficit  Complete occlusion  9  57, M  Proximal (VA–PICA)  15  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  HH II  No neurological deficit  Complete occlusion  10  48, M  Proximal (VA–PICA)  7  U  Midline + far lateral paracondylar extension  Clip reconstruction  No focal neurological deficit, dizziness and intermittend headaches  No neurological deficit  Complete occlusion  11  48, F  Proximal (VA–PICA)  10  R  Midline + far lateral paracondylar extension  Clip reconstruction  Left-sided facial paresis  Stable left facial paresis,  Partial occlusion of previously coiled aneurysm (4 mm neck remnant stable on angiographic follow-up)  12  16, F  Proximal (VA–PICA)  18  U  Midline + far lateral paracondylar extension  Proximal occlusion + OA PICA bypass  No focal neurological deficit, headache, dizziness and nausea  No neurological deficit  Complete occlusion  13  73, F  Distal (TMS)  13  U  Midline suboccipital  Trapping  Slight dysmetria  Stable slight dysmetria  Complete occlusion  14  58, F  Proximal (LMS)  6  U  Midline + far lateral paracondylar extension  Trapping  No focal neurological deficit  No neurological deficit  Complete occlusion  15  43, F  Proximal (VA–PICA)  5  R  Midline + far lateral transcondylar extension  Proximal occlusion + PICA-PICA bypass  HH I  No neurological deficit  Complete occlusion  16  68, M  Proximal (AMS)  4  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  HH II (slight confusion)  No new neurological deficit  Complete occlusion  17  52, M  Proximal (AMS)  6  U  Midline + far lateral paracondylar extension  Clip reconstruction  No neurological deficit  No neurological deficit  Complete occlusion  Case no.  Age, sex  Aneurysm location  Aneurysm size (mm)  Ruptured (R) or Unruptured (U)  Approach  Surgical strategy  Preoperative clinical condition  Latest clinical follow-up  Latest angiographic follow-up  1  71, M  Proximal (AMS)  6  R  Midline + far lateral paracondylar extension  Trapping + OA-PICA bypass  HH II  No new neurological deficit  Complete occlusion, bypass occluded  2  78, M  Proximal (LMS)  26  U  Midline + far lateral paracondylar extension  Proximal occlusion + OA-PICA bypass  Brain stem symptoms  No neurological deficit  Complete occlusion  3  73, F  Distal (CS-2 aneurysms)  5-4  R  Midline suboccipital  Proximal occlusion  HH V  No new neurological deficit  Complete occlusion  4  44, M  Proximal (VA–PICA)  9  U  Midline + far lateral paracondylar extension  Proximal occlusion  No manifest focal neurological deficit, intermittent aphasia  No neurological deficit  Complete occlusion  5  49, M  Proximal (AMS)  6  R  Midline + far lateral transcondylar extension  Trapping + OA-PICA bypass  HH IV  No new neurological deficit  Complete occlusion  6  36, M  Distal (TVTS)  8  U  Midline suboccipital  Wrapping  No focal neurological deficit, headache and dizziness  Nistagmus and dysmetria  Complete occlusion  7  45, F  Proximal (AMS)  4  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  No focal neurological deficit  No neurological deficit  Complete occlusion  8  30, F  Proximal (AMS)  5  R  Midline + far lateral paracondylar extension  Clip reconstruction  HH IV  No neurological deficit  Complete occlusion  9  57, M  Proximal (VA–PICA)  15  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  HH II  No neurological deficit  Complete occlusion  10  48, M  Proximal (VA–PICA)  7  U  Midline + far lateral paracondylar extension  Clip reconstruction  No focal neurological deficit, dizziness and intermittend headaches  No neurological deficit  Complete occlusion  11  48, F  Proximal (VA–PICA)  10  R  Midline + far lateral paracondylar extension  Clip reconstruction  Left-sided facial paresis  Stable left facial paresis,  Partial occlusion of previously coiled aneurysm (4 mm neck remnant stable on angiographic follow-up)  12  16, F  Proximal (VA–PICA)  18  U  Midline + far lateral paracondylar extension  Proximal occlusion + OA PICA bypass  No focal neurological deficit, headache, dizziness and nausea  No neurological deficit  Complete occlusion  13  73, F  Distal (TMS)  13  U  Midline suboccipital  Trapping  Slight dysmetria  Stable slight dysmetria  Complete occlusion  14  58, F  Proximal (LMS)  6  U  Midline + far lateral paracondylar extension  Trapping  No focal neurological deficit  No neurological deficit  Complete occlusion  15  43, F  Proximal (VA–PICA)  5  R  Midline + far lateral transcondylar extension  Proximal occlusion + PICA-PICA bypass  HH I  No neurological deficit  Complete occlusion  16  68, M  Proximal (AMS)  4  R  Midline + far lateral paracondylar extension  Proximal occlusion + PICA-PICA bypass  HH II (slight confusion)  No new neurological deficit  Complete occlusion  17  52, M  Proximal (AMS)  6  U  Midline + far lateral paracondylar extension  Clip reconstruction  No neurological deficit  No neurological deficit  Complete occlusion  VA: vertebral artery; PICA: posterior inferior cerebellar artery; AMS: anterior medullary segment; LMS: lateral medullary segment; TMS: tonsillomedullary segment; TVTS: telovelotonsillar segment; CS: cortical segment; OA: occipital artery; H-H: Hunt-Hess grade. View Large Nine (53%) patients presented with subarachnoid hemorrhage. The average H-H grade on admission was 3.5. In ruptured cases, surgery was performed within 4 d after hemorrhage in all but 1 case, treated after 77 d, due to angiographic evidence of aneurysm recurrence after coiling. VA–PICA junction (n = 6/18, 33%) and anterior medullary (p1) segment of PICA (n = 6/18, 33%) were the most common location. Two (11%) aneurysms were located in the lateral medullary (p2) segment, 1 in the tonsillomedullary (p3), 1 in the telovelotonsillar (p4), and 2 (11%) in the cortical (p5) segment. We can observe that 14 (78%) aneurysms were located within the proximal PICA (including those located at VA–PICA junction). In this group of patients, in 10 (71%) cases vessel sacrifice was required, only in 2 cases without the need of PICA revascularization. Four proximal aneurysms were treated via clip reconstruction. The mean size of aneurysms was 8.4 mm, ranging from 4 to 26 mm; 4 (22%) aneurysms had intraluminal thrombus and 2 (11%) had been previously coiled with aneurysm refilling evidence on follow-up control. In 3 (18%) patients, we found at least 1 associated aneurysm of anterior circulation (5 aneurysms: 4 internal carotid artery and 1 middle cerebral artery), and in 1 case we found an associated ipsilateral VA blister aneurysm. The median clinical follow-up was 7 mo (range: 1 wk-65 mo) and the median angiographic follow-up was 3.4 mo (range: 1 wk-65 mo). Results of latest clinical and angiographic follow-up are presented in Table. Surgical Treatment Four aneurysms (22%), located in the most proximal segments (VA–PICA, n = 2; anterior medullary segment, n = 2), were feasible for clip reconstruction. PICA occlusion was necessary in 12 patients (70%), in 10 cases harboring a proximal aneurysm, in 2 cases distal. In 4 patients (proximal, n = 2; distal, n = 2; 23%) vessel sacrifice without revascularization was performed after good collateral circulation was established, without postoperative sequelae (Figure 2). In 1 case, we performed wrapping of a telovelotonsillar segment aneurysm, because of unusual presence of perforators along the entire segment and aneurysm wall. Bypass was technically not feasible due to deep location of caudal loops. FIGURE 2. View largeDownload slide Case 14. Trapping and excision of proximal left PICA aneurysm. A, A 3-dimensional reconstruction showing a proximal fusiform left PICA aneurysm in a 58-yr-old woman who presented to our institution with the diagnosis of right ICA and left proximal PICA aneurysms, after investigations for vertigo. B, Intraoperative inspection of vessel and cranial nerve anatomy; the aneurysm was located just anterior to the lower cranial nerve plane. C, Proximal PICA clipping for intraoperative test occlusion. D, Intraoperative ICG videoangiography showing retrograde flow within an occluded PICA provided by a second PICA branch, with retrograde filling of the main PICA and perforators distal to the aneurysm. E and F, Trapping and excision of aneurysm. FIGURE 2. View largeDownload slide Case 14. Trapping and excision of proximal left PICA aneurysm. A, A 3-dimensional reconstruction showing a proximal fusiform left PICA aneurysm in a 58-yr-old woman who presented to our institution with the diagnosis of right ICA and left proximal PICA aneurysms, after investigations for vertigo. B, Intraoperative inspection of vessel and cranial nerve anatomy; the aneurysm was located just anterior to the lower cranial nerve plane. C, Proximal PICA clipping for intraoperative test occlusion. D, Intraoperative ICG videoangiography showing retrograde flow within an occluded PICA provided by a second PICA branch, with retrograde filling of the main PICA and perforators distal to the aneurysm. E and F, Trapping and excision of aneurysm. Eight (47%) patients harboring proximal aneurysms underwent revascularization procedures via PICA–PICA bypass (n = 4, 23%; Figure 3) or, alternatively, OA to PICA bypass (n = 4, 23%). FIGURE 3. View largeDownload slide Case 16. In Situ PICA–PICA bypass. A, Conventional CT scan showing subarachnoid hemorrhage in a 68-yr-old man who presented to the Emergency Room of our institution with sudden onset of severe headache, vomiting, and diplopia. B and C, DSA and 3-dimensional reconstruction showing right small fusiform proximal PICA aneurysm. D, Intraoperative view of caudal loop position close to midline and good caliber of both loops. We proceeded with PICA–PICA bypass and proximal occlusion of aneurysm after exposure of aneurysm, inspection of anatomy, and test occlusion that showed poor collateral flow within PICA territory. E, Postoperative DSA showing good PICA–PICA bypass function. F, Postoperative sagittal CTA showing clip position. FIGURE 3. View largeDownload slide Case 16. In Situ PICA–PICA bypass. A, Conventional CT scan showing subarachnoid hemorrhage in a 68-yr-old man who presented to the Emergency Room of our institution with sudden onset of severe headache, vomiting, and diplopia. B and C, DSA and 3-dimensional reconstruction showing right small fusiform proximal PICA aneurysm. D, Intraoperative view of caudal loop position close to midline and good caliber of both loops. We proceeded with PICA–PICA bypass and proximal occlusion of aneurysm after exposure of aneurysm, inspection of anatomy, and test occlusion that showed poor collateral flow within PICA territory. E, Postoperative DSA showing good PICA–PICA bypass function. F, Postoperative sagittal CTA showing clip position. A midline suboccipital craniotomy with far-lateral extension was performed in 14 (82%) patients. Partial condylar removal was necessary in 2 (12%) cases. None of them experienced postoperative cranio-cervical junction instability, since we drilled only the dorsomedial part of the occipital condyle. In no cases did we observe postoperative cranial nerve neuropathies nor cerebellar and/or brainstem ischemia. In 3 (18%) patients, a postoperative cerebrospinal fluid leak occurred, promptly resolved after lumbar drain placement. One patient died few weeks after surgical procedure, due to his poor clinical grade on admission (H-H V). DISCUSSION For PICA aneurysms, endovascular procedures provide the advantage of avoiding cranial nerve manipulation, which represents the main risk of surgery. Despite this, for nonsaccular aneurysms, when vessel sacrifice is required for treatment, at present, no modalities are available to reliably assess the risk of brainstem and cerebellar ischemia, which occurs in a nonnegligible number of cases, even in the largest and most recent endovascular series.8,12,13 Park et al14 reported on the use of balloon test occlusion (BTO) for assessment of tolerance for PICA occlusion. Performing BTO in the PICA, however, is technically difficult because of small caliber of the artery, and unreliable in identifying true ischemia. Moreover, PICA aneurysm location represents an independent risk factor for recurrence after endovascular treatment.15 Open surgery includes several options, allowing the surgeon to perform clip reconstruction when possible or, alternatively, occlusion and revascularization of PICA, lowering significantly the risk of ischemia. An accurate patient selection can therefore reasonably reduce the overall morbidity. Role of Intraoperative Test Occlusion We did not use bypass as universal approach for all cases of PICA sacrifice. Our choice whether to proceed with revascularization was based on careful anatomic evaluation of vessels and perforators, and on intraoperative test occlusion with ICG videoangiography and neurophysiological monitoring. In 4 cases, this strategy allowed us to avoid unnecessary bypass. At present, there is no consensus regarding the most reliable intraoperative technique for collateral flow assessment. Completion of intraoperative DSA takes time, requiring prolonged temporary clipping, and therefore placing the brain tissue at risk of ischemia. Conversely, microdoppler probes can represent a useful tool to assess quantitative flow, but their feasibility shows limits with the decrease of vessel caliber (ie, PICA-perforating arteries), providing signals difficult to interpret.16 The importance of ICG during test occlusion has already been reported in literature, both for artery and vein sacrifice.17,18 ICG provides a unique aid for “live” assessment of vascular collateralization, through evaluation of the presence of retrograde flow within the occluded vessel and small perforators,19 superior to DSA, which is often not able to detect small arteries.18 However, although ICG provides a qualitative assessment of collateral circulation, scarce information about quantitative flow is available, making it difficult to establish whether collateralization is sufficient to supply PICA territory.18 For this reason, we did not use ICG videoangiography as a stand-alone technique, and we additionally utilized neurophysiological monitoring as an adjuvant tool to estimate risks of ischemia following vessel sacrifice.20,21 In our opinion, the combined use of these techniques has the advantage of being able to provide a dual point of view on collateral circulation with good reliability, even if the risk of ischemia cannot be reduced to zero. Algorithm for Surgical Strategy In times when many different revascularization strategies have been proposed by cerebrovascular surgeons, some confusion could be generated by the versatility of techniques. Thus, it is our strong belief to keep things safe and simple and provide the younger generation of bypass surgeons with an intuitive road map to the therapy of these lesions, preferring just a few and logical solutions over too individualized strategies. Based on our experience, which represents one of the largest reported surgical series of nonsaccular PICA aneurysms,3,6,7,22-25 we propose an algorithm for decision-making process during microsurgery (Figure 4). FIGURE 4. View largeDownload slide Algorithm for surgical strategy. FIGURE 4. View largeDownload slide Algorithm for surgical strategy. Proximal PICA aneurysm complexity is mainly due to their location more proximal to midline, anterior to the lower cranial nerve plane, usually requiring wider craniotomy, and the presence of brainstem and cerebellar perforators. Although nonsaccular aneurysms can rarely be clipped without vessel sacrifice and need of revascularization, clip reconstruction should be considered in all cases as the first option, as preoperative imaging sometimes cannot precisely clarify the existent intraoperative anatomy. When PICA sacrifice is deemed necessary, the second step is to evaluate the existence of collateral flow. In our experience, only if insufficient collateral circulation was detected did we consider revascularization, via PICA–PICA or OA–PICA bypass. Distal p3 is the portion of PICA utilized in all our cases as recipient vessel site. This segment is characterized by some degree of variation, with a possible location superior or inferior to the caudal pole of the tonsil, even without forming a loop.2 The presence of 2 good loops allows performing PICA–PICA in Situ bypass (Figure 5). In case of absence of good donor PICA, OA–PICA bypass represents a more than acceptable and low-risk alternative option. FIGURE 5. View largeDownload slide Caudal loop variations. Caudal loop anatomy is fundamental for bypass strategy. Loops close to midline, within the cisterna magna, allow us to perform revascularization through PICA–PICA bypass (arrows show anastomosis site). Caudal loop absence or location superior or inferior to the caudal pole of tonsil forces the surgeon to choose an alternative strategy. FIGURE 5. View largeDownload slide Caudal loop variations. Caudal loop anatomy is fundamental for bypass strategy. Loops close to midline, within the cisterna magna, allow us to perform revascularization through PICA–PICA bypass (arrows show anastomosis site). Caudal loop absence or location superior or inferior to the caudal pole of tonsil forces the surgeon to choose an alternative strategy. PICA–PICA bypass is the most popular and straightforward technique for PICA revascularization. When feasible, it usually represents the first option to consider for flow replacement on this site,22 because of different reasons. First, it is less vulnerable to occlusion. Secondly, it requires minimal anatomic distortion, being caudal loops easy to reach and the procedure entirely intracranial; moreover, surgical time is shorter compared to other techniques, since it is possible to spare the time needed for extracranial artery harvesting or graft preparation. Thirdly, diameters of donor and recipient artery are usually well matched. OA–PICA represents the best alternative technique to PICA–PICA anastomosis, being a low-risk procedure in experienced hands. As for PICA–PICA bypass, p3 caudal loop is utilized as recipient artery, without the need to cross the lower cranial nerve plane to make the anastomosis, a step usually required for other techniques (ie, PICA reimplantation). This is a crucial advantage of this procedure, since it represents one of the major causes of morbidity related to surgical treatment. The only disadvantage of OA–PICA bypass is the intricate OA dissection (ie, compared to superficial temporal artery), usually time consuming. The use of neuronavigation helps in shortening the time required for OA harvesting, since this artery is characterized by tortuosity and variable course, deeply located in the occipital muscles (Figure 6). A linear skin incision over the course of artery can be performed, with subsequent tunneling to reach the recipient PICA caudal loop. Cranial and skin closure assumes a great importance, in order to avoid donor vessel stenosis, kinking, and consequent bypass failure due to bone and pericranial tissue compression. FIGURE 6. View largeDownload slide OA isolation technique. A, Skin mark on OA course with the aid of navigation. B, OA dissection. C, Final steps of isolation. FIGURE 6. View largeDownload slide OA isolation technique. A, Skin mark on OA course with the aid of navigation. B, OA dissection. C, Final steps of isolation. Other bypass techniques have been described for proximal aneurysms, but we find them rarely feasible and associated with higher complication rate, as PICA reimplantation to VA and radial graft interposition. PICA reimplantation represents the most difficult bypass procedure, subject to the greatest risk of occlusion, and associated with a high rate of postoperative lower cranial neuropathies, as the surgical corridor crosses the cranial nerve plane through vagoaccessory triangle.26 Moreover, it requires aggressive condylectomy, adding a potential considerable morbidity. Radial graft interposition between proximal VA and PICA is another alternative, but it should be reserved for cases in which the other techniques are not feasible or high flow is requested, because it is more time consuming and demanding, due to the necessity to perform preparation of the radial artery as well as 2 anastomoses. Distal aneurysms are less challenging, as commonly perforating arteries are not present within this segment. These aneurysms can be clipped, trapped, or proximally occluded with or without revascularization. In our series, we did not perform any revascularization during distal aneurysm procedures, as PICA could be safely occluded in all cases. When revascularization is needed, the most appealing technique for distal aneurysms is excision and PICA reanastomosis. The main limitation of this procedure is related to the restricted number of cases in which it can be performed; it is only feasible in cases of a small- or medium-size aneurysm with single afferent and efferent arteries. The possible presence of perforators, due to anatomic variability, represents another potential limitation. Limitations Limitations of this study include its retrospective nature, the surgical bias, and the absence of long-term follow-up. CONCLUSION For surgical treatment of nonsaccular PICA aneurysms, when vessel sacrifice is required, it is possible to use a selective approach to revascularization, after careful evaluation of the existent anatomy and the presence of collateral supply. For this purpose, an intraoperative occlusion test with the combined use of ICG videoangiography and neurophysiological monitoring provides reliable information. For proximal aneurysms, when bypass is required, PICA–PICA and OA–PICA provide good results with low complication rates; thus, they should be preferred to other available techniques. Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Lister JR, Rhoton AL Jr, Matsushima T, Peace DA. Microsurgical anatomy of the posterior inferior cerebellar artery. Neurosurgery . 1982; 10( 2): 170- 199. Google Scholar PubMed  2. Rhoton AL Jr. The cerebellar arteries. Neurosurgery . 2000; 47( 3 suppl): S29- S68. Google Scholar CrossRef Search ADS PubMed  3. Lewis SB, Chang DJ, Peace DA, Lafrentz PJ, Day AL. Distal posterior inferior cerebellar artery aneurysms: clinical features and management. J Neurosurg . 2002; 97( 4): 756- 766. Google Scholar CrossRef Search ADS PubMed  4. Petr O, Sejkorova A, Bradac O, Brinjikji W, Lanzino G. Safety and efficacy of treatment strategies for posterior inferior cerebellar artery aneurysms: a systematic review and meta-analysis. Acta Neurochir . 2016; 158( 12): 2415- 2428. Google Scholar CrossRef Search ADS PubMed  5. Tokimura H, Yamahata H, Kamezawa T et al.   Clinical presentation and treatment of distal posterior inferior cerebellar artery aneurysms. Neurosurg Rev . 2011; 34( 1): 57- 67. Google Scholar CrossRef Search ADS PubMed  6. Horiuchi T, Tanaka Y, Hongo K, Nitta J, Kusano Y, Kobayashi S. Characteristics of distal posteroinferior cerebellar artery aneurysms. Neurosurgery . 2003; 53( 3): 589- 595; discussion 595-586. Google Scholar CrossRef Search ADS PubMed  7. Lehto H, Harati A, Niemela M et al.   Distal posterior inferior cerebellar artery aneurysms: clinical features and outcome of 80 patients. World Neurosurg . 2014; 82( 5): 702- 713. Google Scholar CrossRef Search ADS PubMed  8. Chalouhi N, Jabbour P, Starke RM et al.   Endovascular treatment of proximal and distal posterior inferior cerebellar artery aneurysms. J Neurosurg . 2013; 118( 5): 991- 999. Google Scholar CrossRef Search ADS PubMed  9. Huang L, Zee CS, Zhang XL. Temporary occlusion test using a microcatheter. World Neurosurg . 2012; 77( 2): 398.E397- 310. Google Scholar CrossRef Search ADS   10. Rodriguez-Hernandez A, Rhoton AL Jr, Lawton MT. Segmental anatomy of cerebellar arteries: a proposed nomenclature. Laboratory investigation. J Neurosurg . 2011; 115( 2): 387- 397. Google Scholar CrossRef Search ADS PubMed  11. Bacigaluppi S, Bergui M, Crobeddu E, Garbossa D, Ducati A, Fontanella M. Aneurysms of the medullary segments of the posterior-inferior cerebellar artery: considerations on treatment strategy and clinical outcome. Neurol Sci . 2013; 34( 4): 529- 536. Google Scholar CrossRef Search ADS PubMed  12. Peluso JP, van Rooij WJ, Sluzewski M, Beute GN, Majoie CB. Posterior inferior cerebellar artery aneurysms: incidence, clinical presentation, and outcome of endovascular treatment. AJNR Am J Neuroradiol . 2008; 29( 1): 86- 90. Google Scholar CrossRef Search ADS PubMed  13. Crowley RW, Albuquerque FC, Ducruet AF, Williamson RW, McDougall CG. Technical considerations in the endovascular management of aneurysms of the posterior inferior cerebellar artery. Neurosurgery . 2012; 71( 2 Suppl Operative): ons204- ons217; discussion ons217-ons208. Google Scholar PubMed  14. Park W, Ahn JS, Park JC, Kwun BD, Kim CJ. Occipital artery-posterior inferior cerebellar artery bypass for the treatment of aneurysms arising from the vertebral artery and its branches. World Neurosurg . 2014; 82( 5): 714- 721. Google Scholar CrossRef Search ADS PubMed  15. Kim BM, Shin YS, Kim SH et al.   Incidence and risk factors of recurrence after endovascular treatment of intracranial vertebrobasilar dissecting aneurysms. Stroke . 2011; 42( 9): 2425- 2430. Google Scholar CrossRef Search ADS PubMed  16. de Oliveira JG, Beck J, Seifert V, Teixeira MJ, Raabe A. Assessment of flow in perforating arteries during intracranial aneurysm surgery using intraoperative near-infrared indocyanine green videoangiography. Neurosurgery . 2008; 62( 6 suppl 3): 1300- 1310. Google Scholar PubMed  17. Ferroli P, Nakaji P, Acerbi F, Albanese E, Broggi G. Indocyanine green (ICG) temporary clipping test to assess collateral circulation before venous sacrifice. World Neurosurg . 2011; 75( 1): 122- 125. Google Scholar CrossRef Search ADS PubMed  18. Kim DL, Cohen-Gadol AA. Indocyanine-green videoangiogram to assess collateral circulation before arterial sacrifice for management of complex vascular and neoplastic lesions: technical note. World Neurosurg . 2013; 79( 2): 404.e401- 406. Google Scholar CrossRef Search ADS   19. Li J, Lan Z, He M, You C. Assessment of microscope-integrated indocyanine green angiography during intracranial aneurysm surgery: a retrospective study of 120 patients. Neurol India . 2009; 57( 4): 453- 459. Google Scholar CrossRef Search ADS PubMed  20. Pancucci G, Potts MB, Rodriguez-Hernandez A, Andrade H, Guo L, Lawton MT. Rescue bypass for revascularization after ischemic complications in the treatment of giant or complex intracranial aneurysms. World Neurosurg . 2015; 83( 6): 912- 920. Google Scholar CrossRef Search ADS PubMed  21. Chen L, Spetzler RF, McDougall CG, Albuquerque FC, Xu B. Detection of ischemia in endovascular therapy of cerebral aneurysms: a perspective in the era of neurophysiological monitoring. Neurosurg Rev . 2011; 34( 1): 69- 75. Google Scholar CrossRef Search ADS PubMed  22. Abla AA, McDougall CM, Breshears JD, Lawton MT. Intracranial-to-intracranial bypass for posterior inferior cerebellar artery aneurysms: options, technical challenges, and results in 35 patients. J Neurosurg . 2016; 124( 5): 1275- 1286. Google Scholar CrossRef Search ADS PubMed  23. Nussbaum ES, Mendez A, Camarata P, Sebring L. Surgical management of fusiform aneurysms of the peripheral posteroinferior cerebellar artery. Neurosurgery . 2003; 53( 4): 831- 834; discussion 834-835. Google Scholar CrossRef Search ADS PubMed  24. Liew D, Ng PY, Ng I. Surgical management of ruptured and unruptured symptomatic posterior inferior cerebellar artery aneurysms. Br J Neurosurg . 2004; 18( 6): 608- 612. Google Scholar CrossRef Search ADS PubMed  25. Williamson RW, Wilson DA, Abla AA et al.   Clinical characteristics and long-term outcomes in patients with ruptured posterior inferior cerebellar artery aneurysms: a comparative analysis. J Neurosurg . 2015; 123( 2): 441- 445. Google Scholar CrossRef Search ADS PubMed  26. Rodriguez-Hernandez A, Lawton MT. Anatomical triangles defining surgical routes to posterior inferior cerebellar artery aneurysms. J Neurosurg . 2011; 114( 4): 1088- 1094. Google Scholar CrossRef Search ADS PubMed  COMMENTS The authors describe an informative case series of a very challenging cerebrovascular problem: fuciform (non-saccular) PICA aneurysm. They manage to illustrate the process of clinical decision making in the OR - whether revascularization is required or not, and what logical steps to undertake in cases which do. Despite advances in endovascular techniques, especially ruptured non-saccular aneurysm pose a real challenge, as potent antithrombotic and anticoagulant medications often required during and after stenting and flow-diverting procedures do not mix particularly well with a clinical setting of an acute posterior fossa hemorrhage. Obviously, open revascularization surgery in that same setting is no trivial feat, either. Wisely, the authors admit that patients with highest grade SAHs are not suitable for this methodology. Aki Laakso Helsinki, Finland The authors report on their retrospective series of 18 non-saccular PICA aneurysms treated microsurgically and provide an algorithm the neurosurgeon can use to determine whether or not revascularization is needed if PICA preservation is not feasible. The need for revascularization is determined by assessing collateral flow in the affected PICA territory after temporary occlusion using ICG video angiography in combination with neurophysiological monitoring with SSEP and MEP. Fifty-three percent of the patients presented with subarachnoid hemorrhage. More than three-fourths were located within proximal PICA (14); of those, 10 had vessel sacrifice of which 8 needed revascularization with PICA-PICA (4) and OA-PICA bypass (4). Of the 4 distal PICA aneurysms, none had revascularization. As mentioned by the authors, these are rare and aggressive lesions that should be treated promptly. The technique and algorithm presented herein are interesting, easy to perform, and can be very useful to the neurosurgeon. Both ICG video angiography and neuromonitoring are widely used modalities in cerebrovascular neurosurgery and aneurysm treatment. In this article, the authors nicely combine their use to help decide whether revascularization is necessary during surgical treatment of this disease entity; they use stringent selection criteria for revascularization. At our institution, we routinely use Flow Assisted Surgical Technique (FAST) which utilizes the Charbel microflow probe for intraoperative flow measurement. This tool gives real time measurement of intravascular flow in cc/min as well as direction of blood flow, among other features. When selecting the patient for PICA revascularization intraoperatively in such situations, it would be very useful if the surgeon could quantify retrograde collateral filling after temporary clipping of PICA, and determine if this would be sufficient without the need for revascularization. The flow probe cannot be used to obtain such data at this time, however we use it routinely to confirm adequate flow through the completed bypass. It can also be used for planning purposes when determining how much flow replacement is needed prior to performing vessel sacrifice and selecting an adequate donor. We congratulate the authors for their efforts, and are confident that further technological advances should provide more accurate means to quantify collateral flow in such situations and tolerance to PICA sacrifice. Ziad A. Hage Charlotte, North Carolina The authors report a sophisticated and effective strategy for surgical management of non-saccular PICA aneurysms. They report a series of 17 patients with 18 non-saccular PICA aneurysms treated surgically over a 9-year period. Of the 17 patients, 9 presented with a subarachnoid hemorrhage. Intraoperatively, test occlusion with temporary clipping proximal to the aneurysm neck was performed in all cases, and it was followed by ICG videoangiography. In addition, MEPs and SSEPs were evaluated during test occlusion. They compared capillary filling and transit times between the involved and contralateral cerebellar hemispheres, and if there was a delay of more than 1 second they proceeded with a bypass. Of the 17 patients, 8 required either a PICA-PICA or OA-PICA bypass. The authors advocate using a PICA-PICA anastomosis whenever possible, and resorting to an OA-PICA anastomosis only as a second choice. They report outstanding results in this series with only 3 CSF leaks and 1 death due to poor neurological condition on admission. Remarkably, the authors report no postoperative cranial nerve neuropathies or cerebellar and/or brainstem ischemia. Rafael J. Tamargo Baltimore, Maryland Copyright © 2017 by the Congress of Neurological Surgeons

Journal

Operative NeurosurgeryOxford University Press

Published: Apr 1, 2018

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