CHAPTER 381 Multimodality Management of Complex Cerebrovascular Lesions
For vascular pathologies of the central nervous system, effective interventions include surgery, endovascular techniques, and stereotactic radiosurgery. Some patients have complex vascular lesions that require the use of more than one treatment modality. The term multimodality treatment has been used increasingly over the past 2 decades and refers to a variety of clinical scenarios and treatment algorithms of different complexity (Table 381-1).1–9 This chapter outlines the different concepts of treatment plans involving more than one treatment modality for complex vascular lesions, including difficult cerebral aneurysms, large arteriovenous malformations (AVMs), the coexistence of AVMs and aneurysms, and complex dural arteriovenous fistulas (DAVFs).
TABLE 381-1 Different Concepts of the Term Multimodality Treatments with Examples Mentioned in the Text
Patients With Cerebral Aneurysms
Aneurysmal subarachnoid hemorrhage accounts for more than 30,000 hospitalizations annually in the United States, with an in-hospital mortality rate of 25.3%.10 Over the past 
decades, management of ruptured and unruptured cerebral aneurysms has changed dramatically. Since 1995, detachable microcoils for endovascular obliteration of cerebral aneurysms have been approved and are used more frequently each year. In an international prospective randomized trial comparing coil versus clip obliteration in patients who were thought to be equally suitable for both endovascular treatment and open surgery, coil obliteration was favored over clip occlusion with regard to clinical outcome at 1 year.11 More recently, follow-up evaluation of these same patients seems to support clip ligation in patients younger than 40 years because of the lower long-term rehemorrhage rate with this procedure.12 However, neurovascular surgeons and endovascular interventionalists increasingly believe that both treatment modalities are complementary rather than competitive13 and that individualized treatment plans need to be established, especially if the clinical situation is complex. These treatment plans can include open surgery, endovascular treatment of the lesion, or a combination of these modalities in a one-step or staged fashion. In discussing the multimodality treatment of aneurysms, we focus on four distinct complex situations in which the complementary nature of clipping and coiling could best improve the clinical outcome of the patient. These situations include multiple aneurysms, surgery after failed embolization, embolization after failed surgery, and intentional combination therapy for complex and giant aneurysms.
Multiple Modalities for Multiple Aneurysms
Intracranial aneurysms are multiple in up to 15% to 20% of patients with subarachnoid hemorrhage14 and in up to 37% of patients with cerebral aneurysms. Risk factors for multiple aneurysms include female gender and cigarette smoking15; bilateral symmetrical aneurysms (mirror aneurysms) are common. In the setting of an aneurysmal subarachnoid hemorrhage, the risk for subsequent rupture of additional incidental aneurysms is significantly higher.16
In patients with nontraumatic subarachnoid hemorrhage, it is of importance to determine which aneurysm ruptured. The location of the intracranial hemorrhage, aneurysm size, and aneurysm morphology are all important factors in deciding which aneurysm bled. If such a determination has been made, the symptomatic aneurysm should be addressed first by whatever technique is appropriate. For the remaining incidental aneurysms, treatment options include observation, simultaneous endovascular treatment if the symptomatic lesion is being coiled, simultaneous surgical obliteration if the symptomatic lesion is being clipped, delayed elective endovascular treatment, delayed elective surgical treatment, or a combination thereof (Fig. 381-1). Even subsequent endovascular and surgical treatment during the same anesthesia for two different lesions has been described. A 31-year-old patient with subarachnoid hemorrhage underwent coiling of a basilar artery aneurysm followed immediately by clipping of a right middle cerebral artery bifurcation aneurysm.17
Simultaneous treatment of all lesions in the acute or subacute phase of hemorrhage eliminates the risk of mistaking the wrong aneurysm as the site of rupture and decreases the risk for rupture of incidental aneurysms during treatment of vasospasm. Simultaneous clipping should be taken into consideration if all lesions can be approached safely through a single craniotomy and if endovascular treatment is less likely to be successful. Simultaneous endovascular treatment can be taken into consideration if the aneurysm shapes and sizes are conducive to achieving total aneurysm occlusion. This approach has been reported in particular for lesions of the posterior fossa18 and can be accomplished safely even in the acute phase of subarachnoid hemorrhage.19
One report reviewed a surgical series of 124 patients with multiple aneurysms (N = 323) and acute subarachnoid hemorrhage. In 57 patients, the index aneurysm and additional incidental aneurysms were clipped during the first operation. In 9 patients, only the index aneurysm and some of the coexisting aneurysms were treated surgically. In 55 patients, just the ruptured aneurysm was treated initially. One of the patients waiting for the additional procedure to secure an incidental aneurysm suffered a second hemorrhage. Of all patients, 78% had a Glasgow Outcome Scale score of 4 or 5.8 Another report focusing on the role of endovascular management of multiple aneurysmal lesions reviewed 38 consecutive patients with a total of 101 aneurysms. Twenty-five patients (66%) underwent embolization of more than 1 aneurysm in a single session. Of 21 patients with acute subarachnoid hemorrhage, 15 underwent embolization of all aneurysms in a single session. Excellent or good outcomes were achieved in 35 of 38 patients (92%).19
In patients who harbor multiple asymptomatic aneurysms or have recovered from an acute hemorrhagic event, the treatment plan can be elective and staged. This approach has to balance the risks and benefits of observation against the different treatment options available for all the patient’s aneurysms. The advantages of a staged procedure versus the additional strain caused by prolongation of a procedure have to be considered carefully.8 A case was reported of a 39-year-old woman with bilateral carotid occlusion and five aneurysms of the vertebrobasilar circulation who underwent clipping of a right anterior inferior cerebellar artery, a right superior cerebellar artery, and a basilar tip aneurysm and delayed coiling of a second, more posterior basilar tip aneurysm.20
Surgery after Failed Embolization of Aneurysms
Rates of failed coil embolization were found to be as high as 14.5% of attempted procedures because of an inability to place coils into the aneurysmal sac, with an intraprocedural mortality rate of 2%.21 Retreatment and rehemorrhage rates of the target aneurysm after coil embolization within the first year were 7.7% and 3.0%, respectively22; late retreatment after a mean of 20.7 months was necessary in 9.0% of patients undergoing coil embolization, with an overall retreatment rate of 17.4%.23
Because greater than 80% of aneurysms rupture at the dome, partial embolization and thrombosis of the dome may decrease the rupture rate until definitive treatment can be undertaken. In many cases, coil compaction over time facilitates additional coil placement, and complete obliteration of the aneurysm may be feasible. If complete obliteration by means of repeated coil embolization does not seem possible or is threatening blood flow in the parent vessel, consideration of surgery is warranted (Fig. 381-1). If coil embolization was being considered as the first option for the treatment of ruptured intracerebral aneurysms, up to 11.6% of aneurysms undergoing coil embolization were subsequently clipped24,25; multicenter trials have reported that 9.3% of coiled aneurysms will eventually require surgical clip occlusion.23 Further classification of these complex surgical cases of inadequately embolized aneurysms was attempted. Group A (65% of cases) allowed direct surgical clipping; group B (23% of cases) showed parent vessel narrowing after clip application, which required extraction of coils from the fundus and reconstruction of the neck by clip or suture; and group C (12% of cases) consisted of emergency coil removal after embolization procedures.26
A number of technical sequelae can be encountered with clip occlusion of previously coil-embolized aneurysms, in addition to the aforementioned narrowing of the parent vessel after clip placement. After a few weeks, coils can become embedded within the wall of the aneurysm and thus make coil removal difficult. This situation increases the risk of tearing the neck of the aneurysm or the parent vessel. Coils can even extrude through the aneurysm sac into the subarachnoid space27; in this case, a number of authors recommend that the coils not be extracted.28,29 Dense subarachnoid scarring around the aneurysm sac potentially endangers the preservation of exiting vessels.27 It is important to recognize that partially coiled aneurysms are frequently less mobile, which makes three-dimensional visualization more difficult at surgery.30 In contrast, some authors point out that partial coil occlusion stabilizes the dome of the aneurysm and decreases the risk for intraoperative rupture.29
Although the majority of these patients will achieve an excellent or good outcome with high occlusion rates, perioperative mortality rates as high as 7.9% have been reported.31
Unique difficulties were observed in a patient who initially underwent stent-assisted coiling of a 6-mm left posterior communicating artery aneurysm. In an attempt to surgically occlude a neck remnant, the aneurysm ripped off its base and created a hole in the internal carotid artery. The authors believe that the stent prevented the clip from gathering enough vessel tissue to close the aneurysm and hence created a tissue stress situation.29 Because stent-assisted coiling for broad-based aneurysms is becoming increasingly popular, these unique difficulties will probably be encountered more often.
Embolization after Failed Surgery for Aneurysms
Failure to completely occlude an aneurysm by surgical clipping is reported in up to 5.9% of procedures, as determined by postoperative angiography.32 Retreatment and rehemorrhage rates of the target aneurysm within the first year after clipping were found to be 1.7% and 1.3%, respectively22; late retreatment after a mean of 5.7 months was performed in 0.9% of patients undergoing clip occlusion, with an overall retreatment rate of 3.8%.23 Reoperation after incomplete clip occlusion is associated with high morbidity and mortality rates.33
In cases of incomplete clip occlusion, subsequent aneurysm regrowth, or clip slippage, coil embolization can be a useful adjunct to promote progressive thrombosis of the aneurysm (Fig. 381-2). Partial clip occlusion may also result in a smaller neck, thereby improving the likelihood of complete occlusion with subsequent coil embolization.34 A large case series (N = 21) of endovascular coil embolization after incomplete clipping reported total occlusion in 81% of patients and nearly total occlusion in the remaining patients without associated morbidity or mortality. The mean size of the aneurysm remnant before coiling was 6.4 mm. Over a mean follow-up of 22 months, no cases of subarachnoid hemorrhage or symptomatic aneurysm regrowth were noted.5 Equally promising results have been reported by other authors.35 In a review of 25 residual and recurrent previously clipped aneurysms with a mean remnant size of 11 mm, retreatment consisted of coiling (44%), reclipping (32%), parent vessel occlusion (8%), and extracranial-intracranial bypass surgery with occlusion or trapping (16%). The authors concluded that reoperation is advisable for anterior circulation aneurysm remnants less than 10 mm in size because of the superior cure rates noted on radiography.36
Intentional Multimodality Approach for the Treatment of Complex Aneurysms
Intentional staged multimodality approaches have been described for patients with acute subarachnoid hemorrhage in whom vasospasm was believed to be a relative contraindication to open surgery. After partial coil occlusion of the dome of a broad-necked middle cerebral artery aneurysm to prevent rebleeding and angioplasty of the stenotic vessel, definitive clipping was performed in delayed fashion.37
The complementary nature of endovascular and surgical approaches to the treatment of cerebral aneurysms can best be appreciated in case reports and series on intentional single-stage multimodality treatment of more complex aneurysmal lesions. A number of authors rely on intraoperative endovascular coil or balloon occlusion of proximal vessels in surgical attempts to permanently trap aneurysms,38 as well as in conjunction with complex revascularization procedures (Fig. 381-3).4,39,40 Balloon occlusion of proximal vessels has been shown to successfully facilitate surgical suction decompression of large paraclinoid aneurysms.41 In a very similar approach to these challenging lesions, suction decompression was applied endovascularly by gentle aspiration with a catheter before clip placement in 24 consecutive patients. Complete occlusion of the aneurysm was achieved in 83% of patients.1 In 4 patients with paraclinoid aneurysms, endovascular nondetachable balloons were used to temporarily stent the internal carotid artery at the neck of the aneurysm not only to gain proximal control but also to improve the accuracy of clip placement and reduce the risk for distal embolization of intraluminal thrombus.42 To perfect the clipping process of a complex anterior communicating artery aneurysm and to avoid a second staged procedure, intraoperative transaneurysmal coil placement has been reported.2
Patients With Large Arteriovenous Malformations
The incidence of AVMs of the brain is estimated to be 12.4 cases per 1 million people per year. Of these, large, Spetzler-Martin grade IV and V AVMs account for 15%.43,44 These high-grade AVMs carry an annual risk for hemorrhage of 1.5%.45 Lesions harboring all three independent risk factors for AVM hemorrhage—previous hemorrhagic manifestation, deep brain location, and exclusive deep venous drainage—have an annual hemorrhage rate of 34.4%.46 Treatment-related permanent major neurological morbidity rates are 21.9% for grade IV lesions and 16.7% for grade V lesions.47
Modalities for the treatment of AVMs include microsurgery, embolization, and radiosurgery. Multimodality treatment algorithms combining (1) embolization with surgery and possible subsequent radiosurgery, (2) embolization with radiosurgery, and (3) surgery with subsequent radiosurgery have been described. Their application, however, shows great variability among institutions.48 The fact that patients treated after 1990 with treatment plans involving microembolization procedures and radiosurgery had a lower long-term complication rate than did patients treated before 1990 led to the concept that a multimodality approach improves outcomes in selected patients with large and complex AVMs.49 A careful, individualized assessment of the risks and benefits associated with different treatment modalities along with consideration of conservative management is essential in counseling patients with high-grade AVMs.47,50
Microsurgery for Arteriovenous Malformations with Preoperative Embolization, with or without Radiosurgery
The goal of preoperative embolization of large AVMs is reduction of blood flow, reduction of the nidus,51 and elimination of deep or surgically inaccessible feeding vessels. With new liquid embolic systems (Onyx, MicroTherapeutics, Irvine, CA), a mean reduction in the nidus of 84% can be achieved.52 Preoperative embolization results in reduced operating time and less blood loss and often allows clearer delineation of the AVM margins.53,54 With presurgical embolization, five of eight high-grade AVMs were downgraded by at least 1 point on the Spetzler-Martin scale.55 The postoperative complication rate is believed to be lower because of reduced perilesional hyperemia.
A number of large case series support the use of preoperative embolization. In a report on 101 malformations, including 60 high-grade AVMs (grade IV and V), preoperative embolization achieved a 50% to 75% reduction in size in 50 patients and a 75% to 90% reduction in size in 31 patients.56
