Angioarchitectural Characteristics Associated with Complications of Embolization in Supratentorial Brain Arteriovenous Malformation

Discussion

Endovascular embolization is an important part of the multimodality treatment for brain AVMs.^11⇓–13 Improvements in microcatheter technology and embolic agents, especially n-BCA and EVOH, have led to an increased curative rate of brain AVMs.^5,6,11 Furthermore, embolization can reduce the size and flow of AVMs, improving the safety and efficacy of microsurgery and radiosurgical treatment for brain AVMs.^{14⇓⇓⇓–18} In this series of 130 sbAVMs that underwent embolization for the first time, there was complete embolization in 28 patients (21.54%) and subtotal embolization in 26 patients (20%). In addition to the cases of complete obliteration of brain AVMs, patients in Spetzler-Martin grade I increased significantly after embolization (preprocedural, 16.31% versus postprocedural, 33.33%; P < .05) and the average Spetzler-Martin grade in the series declined (preprocedural, 2.94 versus postprocedural, 1.86; P < .05).

Either curative or adjuvant embolization can result in postprocedural hemorrhage and ischemia. Recent studies reported morbidity ranging from 3–11%, and mortality from 0–4%,^{2,4,5,7,8,11,19⇓⇓⇓⇓⇓⇓–26} with associations to angioarchitecture, embolic agents, microcatheters, and the manipulator's skills. Studies on different embolization materials, such as silk,²⁴ polyvinyl alcohol (PVA) and coil,²⁵ Onyx,¹¹ and n-BCA,²³ showed 1.4%, 13%, 19.5%, and 50% rates for morbidity and 0%, 0%, 2.9%, and 1.9% for rates of mortality, respectively. Frizzel and Fisher²⁷ reviewed 32 series of brain AVM embolization studies and revealed that permanent neurologic deficit and mortality were 9% and 2% before 1990, decreasing to 8% and 1% after 1990. Because some embolic agents such as PVA and isobutyl cyanoacrylate are no longer in use and new materials such as Onyx have been widely adopted, the complications of embolization should be reassessed. Moreover, the statistical bias caused by different embolic materials, different locations of AVMs, and technical-related complications need to be evaluated. We reviewed 11 series of embolization by use of n-BCA and Onyx (Table 7)^{2,4,5,7,8,11,19⇓⇓–22} and retrospectively studied sbAVMs treated by flow-directed microcatheters and liquid embolic agents in 5 recent years. We found a complication rate of 6.4–21%, permanent neurologic deficit of 1.6–12.2%, and mortality rate of 0–2.9%.

Complications of embolization can be categorized into technical-related and non–technical-related. Technical-related complications included vascular perforation, normal branch occlusion, and bleeding caused by catheter removal. Recent improvement in flow-directed microcatheter and nonadhesive embolic agents has reduced the risk of microcatheter delivery and removal. In our series with sbAVM embolization, contrast extravasation was noted in 3 cases during the procedure. None of these 3 patients ended with persistent neurologic deficit because of timely occlusion of microperforation sites. The technical-related complication rate in the present study was 2.31%, less than the results of Ledezma et al⁷ and less than our non–technical-related complications (21/130, 16.15%).

Non–technical-related complications are mainly associated with angioarchitectural characteristics of brain AVMs. Periprocedural hemorrhage rate was 3–15%,^28⇓–30 probably related to hemodynamic changes and alteration in nidus pressure.^30,31 Picard et al²⁸ demonstrated that venous outflow obstruction was correlated with hemorrhagic presentation after embolization. Furthermore, by progressively blocking draining veins in an AVM model, Hademenos and Massoud³² revealed that venous stenosis or occlusion would result in redistribution of blood flow in the nidus and cause intranidal hypertension. Nonetheless, not all venous occlusion resulted in hemorrhage; the extent and severity of outflow obstruction matter as well. In the present study, venous occlusion occurred in 29.23% of all 130 cases and did not correlate with embolization complications in the univariate model. In the 38 patients with venous occlusion, no postprocedural hemorrhagic presentation occurred when the AVM was completely or nearly completely embolized, whereas a significantly higher hemorrhage rate was seen in the subtotal and partial embolization group (0% versus 23.81%, P < .05). This result suggested that imbalance between inflow and outflow could be a predictive factor of postprocedural hemorrhage and that to avoid rupture of the residual AVM, sbAVMs should be completely or nearly completely embolized as soon as possible when venous outflow obstruction is identified.

Normal perfusion pressure breakthrough related to disruption of cerebral vascular autoregulation³³ and delayed venous thrombosis have been postulated as the etiologies of periprocedural hemorrhage. There was no normal perfusion pressure breakthrough in our series because blood pressure was tightly controlled in all patients immediately after embolization. One patient with subtotal embolization (and reserved draining veins) had severe brain edema, which could be attributed to delayed venous thrombosis and stagnation. Purdy et al³⁰ suggested that delayed venous outflow obstruction might occur because of sluggish blood flow rather than direct venous occlusion by embolic agents.

Although hemorrhage results in poorer outcome, ischemic events were the most common complications of AVM embolization.^{2,4,5,7,8,11,19⇓⇓–22} Sixteen patients (12.31%) in our series had cerebral infarction after embolization, with persistent neurologic deficits in 7 patients. Because of rapid shunting and complex angioarchitecture, perinidal or intranidal normal arteries were very difficult to identify, and neurologic deficits could result from occlusion of these arteries. The present study revealed that sbAVMs located in eloquent cortices had a significantly higher rate of postprocedural persistent ischemic neurologic dysfunction.

In addition to AVM location, other angioarchitectural characteristics that contribute to nonmanipulated complications of embolization remain controversial.^{2,7,8,19,20,34⇓⇓–37} Haw et al⁸ reviewed 306 consecutive patients and 513 embolization sessions from 1984–2002 at the University of Toronto and suggested that the factors associated with complications included the presence of a high-flow fistula or fistulous component to the nidus, eloquent cortex involvement, or venous glue embolization. The long interval of data collection (1984–2002) could have undermined the validity of these conclusions because significant advancement in the embolization technique occurred during this time period. Among all angiographic parameters investigated in 168 consecutive patients and 295 embolization sessions, Ledezma et al⁷ found that Spetzler-Martin grades III–V were significantly associated with unfavorable outcomes and embolization complications. Gobin et al³⁸ revealed that embolization complications were 0% (grade II), 5% (grade III), 15% (grade IV), and 22% (grade V) in their 125 patients studied on Spetzler-Martin classification. On the other hand, studies of Hartmann et al³⁶ and Kim et al¹⁰ failed to demonstrate the correlation between Spetzler-Martin grade and embolization complication and found that embolization sessions were the primary factor for postprocedural complications.

To eliminate the statistical bias caused by embolization sessions, we studied the complications of first-time embolization of 130 sbAVMs and demonstrated that postprocedural complications were associated with eloquent cortical location (OR, 2.57; 95% CI, 1.08–3.42) and exclusive deep venous drainage (OR, 4.56; 95% CI, 1.28–9.67) but not with Spetzler-Martin classification in univariate and multivariate models. The result suggested that the required multiple sessions in large AVMs but not the AVM size itself might be associated with procedural complications.^10,36 The higher complication rate in sbAVMs with exclusive deep venous drainage could be related to the relative lack of a collateral drainage pathway, making them prone to venous outflow obstruction by embolic agents. This observation may also be confounded by the deep location of these AVMs. Thus, sbAVMs with functional cortex and exclusive deep venous drainage would be more difficult to treat and would be at greater risk for embolization complications than the other types of sbAVMs.