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Balloon test occlusion and endosurgical parent artery sacrifice for the evaluation and management of complex intracranial aneurysmal disease
  1. W S Lesley,
  2. R Rangaswamy
  1. Texas A&M University Health Science Center College of Medicine, Scott and White Clinic, Temple, Texas, USA
  1. Correspondence to Dr W S Lesley, Scott and White Clinic, Departments of Radiology, Surgery and Neurosurgery, Division of Neuroradiology, Section of Neurointerventional Surgery, Texas A&M University Health Science Center College of Medicine, 2401 South 31st Street, Temple, TX 76508, USA; wlesley{at}swmail.sw.org

Abstract

The lifetime risk of developing a cerebral aneurysm is about 5%. For some patients, aneurysms can be reasonably managed by conservative measures, including periodic clinical and imaging surveillance. However, the definitive treatment of cerebral aneurysm disease requires securing the aneurysm by surgically excluding it from the cerebrovascular circulation. Most commonly, this can be achieved by either open surgical clipping or embosurgery. Unfortunately, for a minority of patients, these interventions are inadequate because of many aneurysmal factors, such as complex anatomy, giant and wide neck aneurysmal morphology, peripheral small branch origin and skull base location. In situations like these, sacrifice of the parent artery may be preferable, especially when clinical tolerance or image based vascular reserve can be preoperatively demonstrated during temporary occlusion of the vessel. This preoperative procedure, which is known as the Balloon Test Occlusion (BTO), has several variations and technical nuances that can assist the surgeon in predicting which patients may best benefit from parent artery sacrifice (PAS). Together, BTO and PAS are invaluable tools in the management of complicated and atypical cerebral aneurysms. With regard to cerebrovascular aneurysm disease, this review will summarize the development of these procedures, condense the predictability of the numerous BTO variations and provide an overview of the currently available PAS techniques.

  • Aneurysm

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Historical background of the carotid test occlusion and cerebrovascular parent artery sacrifice

Cerebrovascular arterial occlusion for the treatment of downstream aneurysms was first described in 1805 by Sir Astley Cooper who ligated the carotid artery in a patient with a carotid artery aneurysm. Unfortunately, the patient developed hemiplegia and died shortly thereafter.1 2 Undaunted, Cooper successfully repeated the procedure 3 years later in another patient with the same disease, who subsequently lived another 13 years.3 In 1829, Chiari also ligated a carotid artery in Hunterian fashion by tying off the vessel proximal to the suspected distal aneurysm and over the next 20 years other carotid ligation reports followed, but à la Chiari, these interventions failed because the aneurysms were actually located on the vertebral artery!4 5 Not until 1849 did surgeon Warren Stone select the correct vessel for sacrifice in first curing a traumatic vertebral artery aneurysm.6 American surgeon Rudolph Matas also achieved success in 1888 in obliterating a traumatic vertebral artery aneurysm by parent artery sacrifice (PAS) but his fame and recognition as the master of carotid PAS arrived later with his PAS successes in more than 80 patients with carotid aneurysms.7 8

Matas also recognized the need for a ‘preliminary test occlusion’ in evaluating treatment options for carotid aneurysms.9 He understood that while manual compression of the carotid artery on clinical examination might effectively evaluate a patient for carotid sacrifice, this bedside test can result in simultaneous compression of the proximal vertebral artery and unfortunately give rise to the diagnostic errors encountered by Chiari and others.5 Furthermore, the Matas test can give a falsely positive result owing to stimulation of the carotid sinus. So, while history has eponymously designated this compression maneuver the Matas Test, Matas himself and his colleague Carroll Allen discounted its usefulness. Instead, they advocated a more reliable occlusive test procedure be carried out by placing a temporary soft metal band on the carotid artery for 36–48 h before PAS.2 7 9 10

Excluding later refinements in the clamps that were used for testing cerebrovascular reserve and insufficiency prior to PAS, the carotid occlusion test remained essentially unchanged until the 1960s.11 12 A new era in carotid test and permanent occlusion evolved throughout this decade and into the early 1970s as innovative endovascular catheters and balloons were evaluated, and either embraced or abandoned as was the fate with the ingeniously designed magnetic field navigation catheters and detachable magnetic tip devices.13 14 15 16 In 1963, Fogarty used his balloon catheter to temporarily occlude the carotid artery to protect against emboli arising during cardiothoracic surgery but this fell out of favor because of complications related to its use, including iatrogenic caroticocavernous sinus fistula (CCF).17 Luessenhop and Velasquez demonstrated in 1964 that a balloon catheter could be navigated to a supraclinoid aneurysm while achieving temporary aneurysm occlusion.18 That same year, Russian neurosurgeon Fedor Serbinenko temporarily occluded the internal carotid artery (ICA) by inserting an endovascular balloon tipped catheter via a direct common carotid artery (CCA) needle puncture.19 Serbinenko used his balloon catheters to temporarily occlude 304 arteries of the extracranial and intracranial vasculature as far distal as the A3 while incurring an astoundingly low 0.7% complication rate.20 Serbinenko's seminal work firmly established the utility of the basic carotid Balloon Test Occlusion (BTO). Furthermore, he showed that superselective cerebral artery BTO can both map brain function and identify candidate vessels for sacrifice beyond the circle of Willis.

In regards to the early years of endovascular PAS, Robert Dawbarn detailed how in 1904 he injected a paraffin based slurry into an exposed external carotid artery for palliative treatment of head and neck cancer.21 In 1931, Barney Brooks reported the first successful internal carotid endovascular PAS by using a piece of muscle to embolize a patient's CCF.22 23 In October 1969, Prolo and Hanbery advanced a No 3 Fogarty balloon catheter into the cavernous ICA to bridge a traumatic CCF. On balloon inflation, the CCF was eliminated and the catheter was permanently secured to the cervical carotid with ligation of the vessel.13 In 1968, Kessler and Wholey performed the first successful use of a balloon catheter in achieving PAS for an intracranial aneurysm (M H Wholey, personal communication, 2009).24 In this landmark procedure which was publicly reported in November 1969, the balloon catheter was directly inserted into the cervical carotid artery and left inflated within the proximal ICA for 2 days.25 Angiography confirmed vessel occlusion after deflating the balloon and again after withdrawing it from her neck. Shortly after this in December 1969, the PAS technique, sometimes termed permanent balloon occlusion (PBO), was first performed to treat a cerebral aneurysm.26 27 Serbinenko achieved this feat by floating a balloon catheter downstream into position near the subclinoid aneurysm, then inflating the balloon catheter with a liquid silicone polymer. Solidification of the polymer quickly ensued and the balloon was permanently left in place by shearing off the catheter with the carotid artery introducer needle.20 Between 1969 and 1973, a total of 162 patients, including 10 with aneurysms, were operated on by Serbinenko using this PBO technique. While one (10%) of the aneurysm patients died, only two deaths occurred in the entire cohort (1.2%) and the overwhelming majority (98.8%) had no complications whatsoever.20 26

In the 1970s, several inventor–clinicians independently developed prototypical detachable balloons for transfemoral approaches to cranial vasculopathies, including Debrun et al who were first to effectively use the detachable PBO technique in a patient with a subclinoid aneurysm.28 29 30 31 Design improvements to the permanently occlusive balloons have included the addition of a balloon valve detachment mechanism and a radiopaque marker. At the present time, detachable balloons are not currently available in the USA but at least one detachable balloon device is currently under FDA review (T Schnell, personal communication, 2009; J C Chaloupka, personal communication, 2009).

Ongoing investigations by many other endovascular pioneers during the latter third part of the 20th century yielded devices of varying materials designed for extirpative filling of the aneurysm sac itself while preserving the parent artery.32 33 34 35 These constructive strategies—vital though they are to the maturation of neuroendosurgery—are beyond the scope of this article and have been previously reviewed.12 Fortunately, fascinating eyewitness accounts related to these and other facets of the formative years of minimally invasive neurovascular surgery have been preserved by several neurointerventional visionaries.36 37 38

Endovascular balloon test occlusion

Before the availability of antibiotics and the practice of aseptic surgical technique, the short term mortality rate from either carotid resection or ligation in patients with diseases such as head and neck cancer, CCF and carotid aneurysms was frequently above 50% and as high as 55%.11 39 In the post-listerian era, the mortality rate greatly improved, ranging from 0% to 29% in series published between 1960 and 1981 in patients with intracranial aneurysms managed by carotid artery ligation.40 However, the morbidity from ischemic stroke continued to afflict 17–30% of patients subjected to empiric carotid ligation.41 As originally demonstrated by Serbinenko, successful tolerance to BTO can correlate greatly with the likelihood of uncomplicated PAS. Still, many investigators have since shown that despite an uneventful BTO, 4.7–25% of patients will nevertheless suffer immediate or delayed cerebral ischemia following PAS.42 43 44 45 46 47

BTO technique

All patients who fail the standard clinical BTO examination have 100% certitude of developing ischemic compromise following PAS unless extracranial to intracranial bypass is performed beforehand.44 As a result, it is imperative that BTO be performed properly. After obtaining a standard catheter cerebral angiogram to evaluate the circle of Willis, the BTO can be set up using a 5 or 6 French guide catheter positioned in the mid or distal CCA or, for posterior circulation BTO, in the proximal vertebral artery. The guide catheter is maintained to a slow drip, heparinized saline flush in addition to administering systemic heparin anticoagulation so as to minimize clot formation in the stagnated column of blood. In the adult population, a heparin intravenous bolus of 5000 units is usually sufficient to elevate the activating clotting time to about 250 s. The Hyperform and Hyperglide balloons (eV3; Neurovascular, Irvine, California, USA) are well suited for ICA and vertebral BTO because of their size and compliance. An alternative set-up can be done to minimize stagnant intravascular blood during BTO by using a continuous saline flush, double lumen balloon catheter (eg, Merci balloon guide catheter; Concentric Medical, Mountain View, California, USA) placed in the proximal ICA.48 For either BTO scenario and prior to balloon inflation, it is recommended that blood pressure be pharmacologically decreased in order to maximize the sensitivity of the BTO.49 This is the essence of the provocative hypotensive challenge BTO. Blood pressure is measured with an arterial line, and intravenous nitroprusside is administered at 2 μg/kg/min titrated up to 7.5 μg/kg/min in order to drop mean arterial pressure by a third.50 This drug has a rapid onset and its effect quickly stops when discontinued. Next, the balloon is positioned in the cervical ICA or distal vertebral artery and then carefully inflated with diluted contrast while checking for vessel occlusion using contrast injected in the guide catheter. Over-inflation should be avoided to prevent vessel dissection. Connecting a stopcock to the balloon syringe is helpful in maintaining a hands free BTO during clinical neurological testing. Intravenous sedation should be avoided as it may interfere with proper neurological assessment. For the anterior circulation, a 20 min BTO is sufficient while 30 min is recommended for the posterior circulation. It is advisable to inject the guide catheter with contrast to observe for sustained balloon occlusion every 5–10 min. Digital subtraction angiography (DSA) is strongly recommended during cervical ICA BTO to observe for filling of the ophthalmic artery–ICA anastomosis.

Neurological testing is non-standardized and cumbersome due to patient draping constraints but should consist of: extremity and facial muscle testing (“squeeze my hand; show me your teeth; wiggle your toes”); sensation testing (touch) of the extremities; extraocular muscle examination (“follow my finger with your eyes”); visual examination and visual comprehension plus speech assessment by having the patient read large print and name common objects shown to the patient; memory and orientation assessment (“who is the President; what state do you live in”); basic calculation (what is 10 plus 5; count backwards from 20); judgment (interpretation of common proverbs by asking the patient “what does ‘look before you leap’ mean to you?”); and for the posterior circulation assessment, an evaluation for dysmetria is added (finger to nose testing). Unlike the patient who passes the BTO, a positive or ‘failed’ BTO is documented for any baseline deviation regardless of subtly. Frequently, patients who fail BTO do so within the first minute or two; often, the patient will appear to have fallen asleep but may not respond to verbal command. At this point, a quick guide catheter angiogram (DSA) is done to detect any clot along the inferior aspect of the balloon before deflating the balloon. If thrombus is present, the guide catheter can be carefully advanced to the clot, followed by vigorous guide catheter aspiration. An alternative is to mindfully withdraw the inflated balloon to the CCA bifurcation where the clot will then be safely whisked into the external carotid artery territory.

The cervical ICA BTO is most appropriate for patients who await planned cervical carotid artery sacrifice, since as a general rule the BTO should be performed at the targeted site of the proposed PAS. However, since extracranial BTO is technically easier and theoretically safer than an intracranial procedure when evaluating patients with planned intracranial artery sacrifice, a cervical BTO may be initially acceptable to identify gross vascular insufficiency. But, for patients in whom supraclinoid PAS is planned and in which retrograde ophthalmic artery filling of the intracranial ICA is observed on DSA during cervical BTO, a selective paraophthalmic ICA BTO is required. This modified BTO procedure is performed with the ICA balloon placed at or beyond the level of the ophthalmic artery. BTO performed at this location will identify an additional 14% subgroup intolerant to supraclinoid PAS.51

The provocative BTO can increase the sensitivity of detecting inadequate cerebrovascular reserve. In one study, 9% of patients failed the clinical BTO but this number increased to 28% with a hypotensive BTO challenge.50 A variety of other adjuvant assessments have been employed with the BTO in an attempt to further stratify collateral cerebral blood flow (CBF) or measure other physiologic indices of cerebral function. These adjunctive BTO physiologic tests include angiographic evaluation of the circle of Willis, EEG monitoring, transcranial Doppler velocity and pulsatility measurements of the ipsilateral middle cerebral artery (MCA), measurement of somatosensory evoked potentials, ICA stump pressure measurement, calculation of cerebral oximetry (near infrared spectroscopy), measurement of CBF by xenon enhanced CT, single photon emission computed tomography (SPECT), positron emission tomography and acetazolamide (Diamox) challenge with or without MRI perfusion.49 52 53 54 55 56 57 58 59 60 61 Unfortunately, meaningful comparison of the outcomes of adjuvant BTO series in predicting ischemic stroke following PAS is hampered by the small number of studied patients, the relatively low incidence of reported neurologic complications and by variations regarding occlusion techniques, post-occlusion care and patient selection.41 53 62 63 Surdell et al interrogate the CBF of each patient using a battery of BTO tests comprised of clinical assessment, EEG, SPECT and hypotensive challenge in order to stratify each individual's risk from carotid occlusion.64 Based on their protocol, the need for carotid bypass and the specific type of bypass (eg, low flow, high flow) is determined.

More recently, several investigators have reported a simple, quick, single angiographic criterion BTO technique known as the venous phase BTO which has been shown to improve the positive predictive value of the BTO to 98–100%.65 66 67 Originally described by Vazquez-Añon et al in 1992 and advocated by Anton Valavanis in 1995 at the Zurich Course on Interventional Neuroradiology, the venous phase BTO stratifies the risk of PAS based on the angiographically measured time lag between the hemispheric cortical draining veins during BTO.68 69 Because of potential dilution of contrast by collaterals, van Rooij et al point out that the important indicator is the synchronicity, not the symmetry of the bilateral cortical vein opacification.65 While the venous phase BTO requires additional catheter placement in the contralateral ICA, this test appears to adequately address the cerebrovascular reserve without a requisitely protracted clinical neurologic examination. Furthermore, this BTO has been proven safe when performed under general anesthesia—a beneficial option that permits intraoperative assessment for either planned PAS or as a bail-out strategy during complicated or deteriorating reconstructive aneurysm endosurgery (figures 1–4). Based on the available data, PAS can be safely done with cortical venous delays of less than 3 s while delays of 4 s or greater indicate poor collateral reserve.65 66 70 A hypotensive challenge is not generally required during surgery, as general anesthesia typically lowers mean blood pressure by 26%.66 Future research is needed to determine if the venous phase BTO in conscious patients requires provocative hypotensive testing and, whether the neurologic examination can be completely eliminated for these patients since a brief but well designed neuropsychologic assessment test might yet elicit subtle cognitive deficits during the procedure.

Figure 1

Baseline three-dimensional (A) and conventional (B) left internal carotid artery (ICA) angiograms in a middle-aged female demonstrate tandem, unruptured ICA aneurysms. No preoperative Balloon Test Occlusion (BTO) was done.

Figure 2

Intraoperative left internal carotid artery (ICA) angiogram. A stent could not be implanted prior to coiling (A). An incompletely detached coil withdrew into the left ICA during microcatheter manipulation; an alligator snare could not negotiate the posterior genu of the cavernous ICA to retrieve this coil (B). Clot began to form in the ICA (B) and the aberrant coil began to migrate distally (C).

Figure 3

Venous phase left internal carotid artery (ICA) Balloon Test Occlusion (BTO) was done. Right venous drainage is seen (arrows) on the 3 s frame while left-sided venous drainage is observed 1 s later on the 4 s frame (arrows). Retrograde filling from the left ophthalmic artery to the ICA was noted during left common carotid artery BTO. Parent artery sacrifice was performed at the paraclinoid left ICA. The postoperative course included right shoulder weakness and mild slurred speech. These symptoms completely resolved after 3 days of induced hypertensive therapy with intravenous heparin drip and 3 weeks of physiotherapy.

Figure 4

Postoperative day 2 head CT. Small infarcts were noted (arrows) in deep white matter, likely due to coil related thromboembolic sequela and not parent artery sacrifice per se. The patient was discharged on aspirin and clopidogrel for 2 months to minimize sump effect delayed thromboembolism. Three month follow-up MRA revealed complete occlusion of the ICA with patency of the left anterior cerebral artery and middle cerebral artery. The patient had no neurological deficits on clinical examination but reported occasional word finding difficulty.

Despite the superiority of the venous phase BTO in predicting subsequent stroke due to cerebrovascular collateral failure after PAS, no BTO can augur delayed thromboembolism originating from the PAS stump.71 72 Organized thrombus within the occluded PAS vessel may dislodge at any time due to sump effect or clot propagation. The latter may result from a slow but progressive contraction of the occluded vessel that over time ejects some of the organized clot into the distal cerebrovasculature, like toothpaste squeezed from its tube. Berenstein et al have advocated minimizing the occluded vessel's dead space and thus the column of stagnant blood and potential clot volume in reducing this unanticipated complication.48

Overall, serious complications arising from the BTO itself are infrequent. In the largest ICA BTO series published (500 cases), Mathis et al reported a procedural BTO complication rate of 1.6%, including a 0.4% incidence of permanent neurological deficit.44 In another large series which evaluated clinical and xenon CT perfusion BTO in 300 patients, Tarr et al described a 1.7% neurologic complication rate, including a 0.33% occurrence of permanent neurological deficit.73 Reported complications owing to extracranial BTO are, in general, no different than those reported with cerebrovascular catheter angiography and include vessel dissection and thromboembolic stroke.

Ischemia of the 2nd–6th cranial nerves has been observed in patients during cervical BTO despite demonstrating normal hemispheric CBF. While these patients possess a functional circle of Willis or sufficient leptomeningeal collaterals for maintaining cerebral function, stagnant blood flow below the ophthalmic artery during BTO may nevertheless manifest as upper cranial nerve ischemia due to poor perfusion of the meningohypophyseal trunk and inferior cavernous sinus artery. Reported symptoms of this transient cavernous sinus syndrome include mild discomfort or paresthesia of the face.74 Cervical BTO using a double lumen catheter with unchecked rapid infusion of saline flush (10 ml/min) may produce ocular ischemic syndrome, which in this situation is manifested by ipsilateral orbital pain and progressive but transient monocular blindness.75 It is worth noting that these cranial nerve deficits would not be detected during an intraoperative venous phase BTO.

Parent artery sacrifice

Ideally, aneurysmal repair involves a reconstructive approach that preserves the parent artery while excluding the aneurysm from the circulation thru either open surgical clipping or by endosurgical means. On the other hand, PAS represents a deconstructive way towards affecting aneurysmal thrombosis following open parent artery ligation or transvascular embosurgery. In one meta-analysis, endosurgical PAS completely thrombosed 97.5% of the cavernous segment ICA aneurysms reviewed.76 In addition, PAS can be an effective option for managing persistent or recurrent aneurysm disease due to failed reconstructive surgery and, PAS can also pose the best initial surgical choice in certain clinical presentations.77

Excluding intolerance to a BTO, any complex saccular aneurysm may optimally be initially treated by PAS whether the aneurysm is wide neck, multilobulated, giant, containing thrombus, exhibiting symptomatic mass effect, peripherally located, arising from a small parent artery, arising from a meningeal vessel, associated with a vascular malformation or tumoral pedicle.63 78 79 80 81 82 83 84 85 Wide neck, multilobulated, giant or fusiform aneurysms have relatively poor long term obliteration rates following endovascular parent vessel preservation surgery. In one series of 29 giant aneurysms embolized with platinum coils, only 24% were permanently occluded while a residual aneurysm neck remained in 69%.63 86 87 PAS may minimize distal embolic complications arising from endosaccular coiling of clot containing aneurysms since the latter are prone to ejecting thrombus during coil implantation.88 Small peripherally located aneurysms as well as aneurysms arising from proximal but small caliber arteries are difficult to eliminate while preserving the parent artery, whether or not the approach is by coiling or by clipping with and without bypass. Furthermore, PAS of small vessel aneurysms is typically well tolerated and, any resulting deficit is usually mild or transient.89 90 Typical aneurysm locations amenable to peripheral or small vessel PAS include the posterior inferior cerebellar artery distal to the anterior medullary segment, M2–3 segments of the MCA, the superior cerebellar artery, P2–P3 segments of the posterior cerebral artery (PCA), A2 segment of the anterior cerebral artery, the anterior inferior cerebellar artery and the posterolateral choroidal artery.63 81 87 90 91 92 Virtually every named artery touting an aneurysm has been successfully subjugated by PAS management, including the basilar, trigeminal, ophthalmic, the A1 segment of the anterior cerebral artery, the M1 segment of the MCA, the P1 segment of the PCA and both vertebral arteries.70 77 93 94 Other vasculopathic related aneurysms have been successfully addressed by PAS and include fusiform or serpentine, bacterial and fungal mycotic, vasculitic and dissecting aneurysms.80 95 96 97 98

Numerous effective devices and techniques are available for endovascular PAS. While detachable balloons are effective and relatively inexpensive, balloons may migrate, rupture or deflate over time.99 Nevertheless, complex skull base ICA aneurysms are classic candidates for balloon PAS. When used, three balloons are ideally implanted—the first is placed as far distal as feasible without inciting ischemia, and the second and third ones are nestled just distal and proximal to the aneurysm neck. This trapping technique eliminates any filling of the aneurysm by either retrograde parent artery flow or by delayed recanalization from small nearby perforator vessels. The distal-most balloon caps off the stagnant column of blood, thereby reducing the possibility of delayed thromboembolism.

Packing the parent vessel with platinum or fibered coils is likewise effective; a stent may be used to minimize the total number of coils (and total expense) needed for PAS by keeping the coils from herniating into aneurysm.99 100 The aneurysm should be trapped on both sides with the coils to prevent recanalization; and, in the case of giant aneurysms, leaving the mid-portion of the parent vessel free of coils can maximize resorption of the devascularized mass and result in rapid improvement in any mass effect related clinical symptoms.101

Between 39% and 75% of patients with giant aneurysms present with mass effect.63 Symptoms generally improve over time following PAS. In one study of 31 patients with cranial nerve dysfunction due to cavernous segment ICA aneurysm for which an average follow-up of 31 months was done after PAS, 61.3% had complete symptom resolution, 29.0% were improved and 9.7% were unchanged.102 While giant aneurysms can be treated by over coiling of the aneurysm so that the parent artery is occluded, the combination of the coil bulk and any subsequent thrombosis related edema may create new symptoms of, or exacerbate pre-existing signs of, mass effect. But for aneurysms managed by PAS, and without additional intra-aneurysmal coiling, significant postoperative worsening of the mass effect symptoms is both infrequently observed and well controlled with steroids.103 As shown by MRI, an increase in aneurysmal mass effect corresponds to the time of thrombus completion, which takes place as late as 6 weeks after PAS.103 104

During initial coil or balloon positioning for PAS, flow related migration of these devices can be problematic. In such situations, a fixed anchoring implant called the Amplatzer vascular plug can facilitate occlusion, especially in vascular segments of the vertebral and carotid arteries not encased by a bony canal.105 This detachable nitinol implant has been successfully used for aneurysm PAS either as a standalone construct, with coils, or with Onyx glue plus coils.106 107 Extremely variable vessel thrombosis can occur with this device owing to its porous design, so delayed angiography is advised to demonstrate durable occlusion.108

Peripheral aneurysms are best eliminated with liquid embolics, especially the cyanoacrylates such as nBCA glue, because the coil incompatible smaller microcatheters and microwires offer a less traumatic approach in negotiating the smaller delicate branches of the brain.78 81 109 After placing the microcatheter just proximal to the aneurysm, glue is carefully injected so that the parent artery is filled on both sides of the aneurysm. While coils have been used effectively in these locations, vessel perforation and incomplete vessel occlusion are anecdotally more frequent, dissuading routine use. Coils are best utilized for proximally located, small caliber vessel PAS where precise embolization is paramount and where any amount of glue reflux cannot be permitted.

Direct thrombin injection is a potent technique for inciting aneurysm thrombosis for which only two reports exist concerning its parent vessel sparing success in dealing with this disease in the cerebrovasculature.110 111 Thrombin can be effectively administered to cause PAS as well. In an unpublished account, thrombin induced PAS was chosen to treat a left-sided 22 mm broad neck, lobulated, cavernous sinus ICA aneurysm in a 62-year-old white female who presented with diplopia in 1999 (A M Borowski, personal communication, 2009). Endovascular exploration of the aneurysm could neither define the aneurysm neck nor could the microwire pass into the supraclinoid segment. She underwent uneventful carotid BTO using clinical, EEG and SPECT assessment. Next, using a double lumen balloon for flow arrest in the proximal left ICA, PAS was performed with a concoction of 2000 units of bovine thrombin plus contrast that was instilled into the petrous and high cervical left ICA. A few coils were placed in the ICA beyond the balloon as a surgical fiducial. The balloon was left in place for 24 h during which time she had a left sided headache but no neurologic deficits. Intravenous heparin was maintained to ward off potential thromboemboli arising from the balloon catheter which crossed the bovine configured brachiocephalic artery. After balloon removal the next day, her headache slowly improved. She was lost to surveillance care for 7 years until she presented herself to the senior author (WSL) in 2006 for follow-up. Her diplopia had long since resolved as had her left-sided headaches. A catheter angiogram was performed which showed an obliterated aneurysm due to occlusion of the left ICA from its origin to the ophthalmic artery as well as a new asymptomatic 3–4 mm aneurysm of the right MCA bifurcation.

Miscellaneous caveats of PAS

The treatment of an acutely ruptured, complex ICA aneurysm presents a diametric management conundrum. Specifically stated, the need to eliminate the risk of rebleeding by PAS handicaps the cerebrovascular capacity for bearing any additional stress incurred from delayed vasospasm. Nevertheless, where the risk for vasospasm is low (Fisher grades 1 or 2) in patients exhibiting favorable clinical signs, PAS should not be postponed. But for those in poor clinical condition and in patients with Fisher grades 3 or 4, partial coiling is recommended until PAS can be done after the threat of vasospasm has passed. For ruptured large complex aneurysms at other locations, PAS should not be delayed.112

Following major vessel PAS, the hemodynamic forces are altered to varying degrees in the remaining vessels burdened by delivery of a relatively increased CBF. Whether or not such physiologic changes in the cerebrovascular flow dynamics adversely affect the growth or rupture of any additional pre-existing aneurysms or contribute to the formation of de novo aneurysms remains unproven and controversial. In observing 60 patients for a total of 468 patient years, Tomsick et al found two patients who suffered subarachnoid hemorrhage (SAH) due to de novo anterior communicating artery aneurysms following PAS. The resulting calculated incidence of delayed SAH from this cohort is 0.4 per 100 patient years which was stated to be 40 times greater than the risk of SAH in the general population and five times greater than expected for patients with previous SAH.113 114 While anecdotal cases have surfaced over the years describing de novo aneurysms after PAS (including the thrombin PAS vignette, above), other investigators have not found delayed SAH, de novo aneurysm formation or enlargement of pre-existing aneurysms following PAS in their cohorts.112 115 Prospective outcome predictions employing computational fluid dynamic simulation prior to PAS will likely provide the easiest opportunity to settle this debate, given the small numbers of patients subjected to PAS.116

Finally, the neurointerventional surgeon will be called upon, at some point, to decide the fate of a vital parent artery, perhaps a PCA, stricken with a giant, ruptured dissecting aneurysm that threatens to finish off its host, if left unsecured. Precious little comfort comes with the knowledge that a life will be saved at the price of causing possible or even anticipated disability such as hemianopsia. The decision to proceed may or may not be straightforward, given the patient's overall clinical condition, but after the course of action has been carried out and results of surgery are known, living with the consequences of one's decision can be punctuated with moments of second guessing and self-doubt. Until perfect outcomes are enjoyed by every patient, further investigative work remains to be done.

Conclusions

BTO remains an invaluable prognosticating tool in predicting cerebrovascular tolerance to planned PAS. In the elective setting, a clinical BTO performed with provocative hypotensive challenge and a venous phase evaluation appears superior to other adjuvant imaging measurements of cerebral blood flow. Reducing the incidence of a false negative BTO is optimized when the BTO balloon is positioned at the same site as the planned PAS. In the intraoperative setting of complicated endosurgical aneurysm repair, the venous phase BTO offers a relatively expeditious and reasonable assessment when considering emergent bail-out PAS. Future investigations are warranted with regard to understanding of the relationship between the occasional false negative BTO and PAS related ischemia. The proven efficacy of the endovascular PAS assures its continued future role in the angio-operating arena.

Acknowledgments

Presented in part at the 7th Annual Practicum Meeting of the Society of NeuroInterventional Surgery, Vancouver, British Columbia, Canada, 2009.

References

Footnotes

  • Competing interests None.

  • Provenance and peer review Commissioned; not externally peer reviewed.