INTRODUCTION
Intracranial arteriovenous malformations (AVMs) are lesions involving a network of anomalous vessels lacking capillaries [1,2,16]. AVMs have an estimated prevalence of approximately 10-18 cases per 100,000 people [1,2,16]. They affect both men and women and can occur at any age, although a peak incidence is observed between 20 and 40 years of age [3].
According to their location, intracranial AVMs can be classified as supratentorial or infratentorial, with the latter further classified into brainstem and cerebellar AVMs [4,5].
AVMs represent 7-15% of all intracranial AVMs. Cerebellar AVMs are the most common within this classification, representing 75-81.2% of these malformations in the posterior fossa [6]. AVMs in the brain stem make up the remaining percentage [4,5]. The estimated age of presentation for posterior fossa AVMs is, on average, 42 years. The age of presentation for brainstem AVMs tends to be lower, with an average age of 32 years. There is no gender predominance. Unlike supratentorial AVMs that often present with seizures, posterior fossa AVMs more commonly present with hemorrhage [4-6].
The treatment of intracranial AVMs, including cerebellar AVMs, focuses on reducing the risk of intracranial hemorrhage, which is approximately 1-4% per year collectively for all intracranial AVMs regardless of their location [7,9].
Endovascular treatment through preoperative embolization is used to reduce the size of the shunt and facilitate microsurgical resection [1], as well as to embolize intranidal aneurysms that could increase the risk of bleeding if necessary [10,11]. Transarterial embolization has become an important component in the treatment of AVMs, either as an independent curative method or, more commonly, as an adjunctive procedure prior to microsurgery or radiosurgery [1,10-12].
The aim of this study was to evaluate the reduction of blood loss and the duration of surgical resection by using preoperative embolization of cerebellar arteriovenous malformations with endovascular embolizing agents.
MATERIALS AND METHODS
Study design and sample
A descriptive, retrospective, preliminary study was conducted to determine the effectiveness of preoperative embolization in reducing intraoperative blood loss and intraoperative times during the surgical resection of cerebellar arteriovenous malformations in patients at Hospital Juárez de México. The study covered cases from January 1, 2011, to December 31, 2022, following the STROBE [21] recommendations.
The Hospital Juarez de México is a tertiary-level government hospital located in Mexico City, with a patient influx from a large area of the country. For practical purposes, AVMs were categorized as small when the maximum nidus diameter was <3 cm, and as large when the diameter was ≥3 cm, based on the Spetzler-Martin grading system [20].
Selection criteria
Patients of both sexes aged 10 to 90 years, who presented with either incidental intracranial arteriovenous malformation or intracranial hemorrhage secondary to arteriovenous malformation rupture, were included. Additionally, patients admitted to the hospital who underwent embolization of intracranial arteriovenous malformations were included. Subjects diagnosed with dural fistula, cavernous angioma, or malformations/anomalies of venous drainage were excluded. Patients with intracranial arteriovenous malformations who had undergone radiosurgery, as well as those with supratentorial vascular malformations, brainstem AVMs, or multiple arteriovenous malformations, were also excluded. Patients lacking complete imaging studies (including magnetic resonance imaging and cerebral angiography) were eliminated from the study.
Ethics
The research adhered to the principles outlined in the Declaration of Helsinki and followed the ethics protocols of the hospital unit where the research was conducted. The protocol was registered and approved under the institutional registration number of the project HJM 005/23-R.
Data collection
Sociodemographic data, such as sex, age, location, and predominant symptoms and/or clinical debut, were obtained. Data collection was performed manually and conducted daily by reviewing the electronic records. In case of missing data, the notebooks of each of the hemodynamic rooms were reviewed. Once the data of patients with a diagnosis of intracranial arteriovenous malformation were collected, the physical clinical record and the institutional image display system were reviewed to determine the type of intracranial arteriovenous malformation, data associated with post-intervention evolution, type of embolizer used, and associated complications or death, among others. Finally, the data obtained were electronically extracted into a spreadsheet using the Microsoft Office 2016™ package.
After the initial evaluation and data collection, the modified Rankin Scale (mRS) [11] was calculated preoperatively, postoperatively, and at the six-month follow-up.
Patients were divided into two groups:
(1) Hybrid group - those who underwent preoperative endovascular embolization followed by microsurgical resection within the same hospitalization.
(2) Surgery-only group - patients treated by direct microsurgical resection without prior embolization.
Surgical complexity was graded using the Ibáñez scale [8], which classifies microsurgical difficulty from I (low complexity) to IV (highest complexity) based on depth, vascular involvement, and anatomical accessibility.
Data analysis
Statistical analysis was performed using SPSS v25. Quantitative variables were presented as mean±standard deviation and range, or median (range) when not normally distributed. Categorical variables were reported as frequencies and percentages.
Intergroup comparisons were performed using the Mann-Whitney U test for continuous variables and Fisher’s exact test for categorical data.
Changes in mRS [17] across timepoints (preoperative, postoperative, 6-month follow-up) were assessed using the Wilcoxon signed-rank test.
Effect sizes were calculated using r = Z / √N for Mann-Whitney U tests; p-value thresholds were standardized to p<0.05.
RESULTS
Thirteen patients with cerebellar AVMs were analyzed. Three patients were excluded from the final analysis because postoperative angiographic studies were not available, preventing confirmation of resection completeness and outcome assessment.
The mean age for the sample was 31.3±16.37 years (range 4-63 years). A predominance was observed in women (62%), with a female-to-male ratio of 1.6:1 (Table 1).
The initial clinical presentation corresponded to thirteen patients. Nine patients presented with rupture. Among the six patients who initially reported headache, four had headaches as part of their hemorrhagic presentation and were therefore reclassified into the rupture group. After correction, the final distribution was rupture signs and symptoms in nine patients, isolated headache (non-hemorrhagic) in two patients, and cerebellar symptoms in two patients.
Rupture was confirmed in 62% of cases through imaging studies such as computed tomography and magnetic resonance imaging. The presentation of intracranial hemorrhage occurred in 50% of cases, with a breakdown as follows: 50% presented as an intraparenchymal hematoma, 12% as a subarachnoid hemorrhage, and 38% as a mixed component. The remaining data is shown in Table 2.
Characteristics and angioarchitecture
Angiographic analysis revealed that 55% of the cases involved large AVMs. The location of the AVMs was also examined, with 72% found in the cortical region and the rest in deep locations. Furthermore, they were classified based on their proximity to critical brain functions, with 23% located in eloquent areas and 77% in non-eloquent areas.
Analysis of the AVMs’ angioarchitecture showed that 61.5% were supplied by a single feeding artery, while the remaining 38.5% were fed by two nutrient arteries. Notably, only one case was associated with a ruptured fusiform aneurysm of the posteroinferior cerebellar artery. The remaining data is presented in Table 2.
Treatment and embolization details
For treatment, 11 cases (84.6%) underwent embolization prior to surgical resection, while the remaining two (15.4%) were treated with surgical resection alone, without prior embolization. However, only 10 of the embolized patients were included in the final statistical analysis (Fig. 1).
The endovascular embolization procedures were completed in a single session. The non-adhesive liquid embolization agents used were an ethylene vinyl alcohol copolymer (EVOH), specifically Onyx 18® (Medtronic, Minnesota, USA) and Squid 6%® (Balt, Montmorency, France). The single case involving a ruptured fusiform aneurysm was treated with coil placement.
Surgical approaches and outcomes
The majority of cerebellar AVM resections were performed using a suboccipital approach (92%), with only one case requiring a far lateral approach (8%).
Preoperative embolization was associated with significantly improved intraoperative metrics compared to the surgery-only group. Patients in the hybrid group 325±42.72 minutes (n=8) experienced a statistically significant reduction in surgical time compared to the surgery-only group (530±99 minutes). Furthermore, the hybrid cohort (437.14±410.68 cc, n=7) showed a dramatic and highly significant decrease in intraoperative blood loss compared to the surgery-only group (3,400±848.53 cc; n=2). The mean difference was -2,962.9 mL, with a 95% bootstrap confidence interval of -3,726.6 to -2,195.4 mL. Although this difference did not reach statistical significance in Welch’s t-test (t=-4.82, p=0.113), the effect size was extremely large (Cohen’s d=-3.42; Hedges’ g=-2.81), indicating a robust and clinically meaningful advantage of preoperative embolization. The lack of statistical significance is likely explained by the very small size of the non-embolized group. These results strongly support the use of embolization to mitigate key operative risks by devascularizing the malformation before resection (Table 3 and Fig. 2).
The median preoperative mRS was 3 (range 1-4). A significant improvement was observed postoperatively (median 2; p<0.01, Wilcoxon) and remained stable at 6 months (median 2; p=0.12).
No significant differences were found between the hybrid and surgery-only groups in terms of mRS improvement (p=0.27, Mann-Whitney U test). These results are illustrated in Fig. 3.
Complications and reintervention
Several complications were reported, including an intraoperative rupture of the transverse sinus during the resection of a previously embolized AVM. Two cases experienced a cerebrospinal fluid fistula and meningitis. One patient suffered from ischemia due to the migration of the embolizing fluid, which resulted in sequelae affecting the ateral lower cranial nerves. Another case involved a cerebellar cerebrovascular event (stroke), and one patient developed non-communicating hydrocephalus. One patient in the hybrid group required reintervention due to angiographically confirmed residual nidus. Despite successful preoperative embolization with significant devascularization, a small remnant was detected on follow-up digital subtraction angiography and subsequently treated surgically. No reinterventions occurred in the surgery-only group.
DISCUSSION
The objective of this study was to assess the efficacy of endovascular therapy using embolizing agents as adjuvant therapy to reduce intraoperative blood loss and intraoperative time in patients with arteriovenous malformations in the cerebellum. The results confirm that preoperative embolization reduces intraoperative bleeding and facilitates safe microsurgical resection in cerebellar AVMs, which pose greater technical challenges due to limited working space and venous drainage patterns.
Previous studies on patients with intracranial AVMs have often included only a small proportion of cerebellar AVMs, and in many cases, brainstem AVMs were also included and studied collectively as posterior fossa AVMs [14-19]. However, it is important to emphasize that cerebellar AVMs represent 10-15% of all intracranial AVMs and up to 70% of posterior fossa AVMs [20]. For this reason, the isolated study of cerebellar AVMs is essential because they present different results in terms of both morbidity and mortality compared to their counterparts in the brainstem.
Cerebellar AVMs are classified according to their location as suboccipital, vermian, tonsillar, tentorial, and petrosal [20,21]. In relation to the Spetzler-Martin [13] classification system, eloquent cerebellar AVMs are defined as those involving the peduncles or deep cerebellar nuclei [22-24].
Cerebellar AVMs represent a distinct clinical entity due to their compact surgical corridors, higher baseline rupture risk, and dependence on critical venous drainage pathways. Recent studies have emphasized that cerebellar AVMs exhibit different morbidity patterns, surgical risks, and angioarchitectural behavior compared to supratentorial AVMs.
It is critical to contextualize our findings within the unique anatomical constraints of the posterior fossa. Cerebellar AVMs represent a distinct clinical entity compared to their supratentorial counterparts, primarily due to their compact surgical corridors, higher baseline rupture risk, and dependence on critical venous drainage pathways. Because cerebellar AVMs comprise a significant portion of posterior fossa AVMs (up to 70% in some series), their management necessitates a tailored and often more aggressive approach. Our observation that embolization successfully mitigated intraoperative risk confirms its utility as a necessary measure for enhancing surgical safety in this challenging anatomical region, aligning with contemporary literature that emphasizes the distinct morbidity patterns and surgical risks associated with posterior circulation lesions. Although our sample is small, it reflects real-world practice for this rare pathology and reinforces the value of embolization in enhancing surgical safety in cerebellar AVMs.
Cerebellar AVMs constitute a distinct subset of malformations that, unlike their counterparts in the brain, exhibit dissimilar behavior and clinical presentation [2,23]. They are often referred to as “silent” due to the absence of focal neurological symptoms at the cortical level, and in most cases, they present with intracranial hemorrhage at onset [17,19]. This, combined with the angioarchitectural characteristics of cerebellar AVMs, makes their classification and management distinct from their supratentorial counterparts, necessitating a more aggressive study and treatment strategy [20,21].
However, the treatment of cerebellar AVMs remains a significant challenge, often requiring the analysis and individualization of several factors, including location, size, angioarchitecture, involvement of eloquent areas, and the risk of hemorrhage (including associated aneurysms) to determine the most appropriate treatment approach. The two primary treatment modalities are surgical resection and endovascular embolization, which are sometimes used in combination. This combined approach is increasingly common [22].
Endovascular embolization is a procedure performed via catheterization in an angiography suite. It involves inserting a catheter into the blood vessels, typically through the groin, navigating it to the AVM site, and intraluminally depositing cohesive and non-cohesive embolic agents intended to impede blood flow through the abnormal vessels, thereby reducing the risk of rupture and bleeding.
Complete obliteration of AVMs significantly reduces the risk of intraoperative blood loss, and even subtotal obliteration can decrease the risk of bleeding compared to untreated AVMs [7,8,22].
The most frequently used embolizing materials are n-butyl cyanoacrylate (nBCA) and ethylene vinyl alcohol (EVOH), such as Onyx® and Squid®. EVOH is a non-adhesive cohesive agent that offers better penetration into the short circuit, making it the preferred treatment option for preoperative embolization of intracranial AVMs [1,9,22].
The primary goal of preoperative embolization, particularly with EVOH agents like Onyx® and Squid®, is to achieve significant devascularization to render microsurgical resection safer and more effective10. Studies suggest that achieving 95% to 100% obliteration provides maximal intraoperative benefits, including reduced blood loss and decreased post-surgical complications [1,2,11,13,16]. However, the case requiring reintervention in our Hybrid group underscores that even successful preoperative devascularization does not guarantee complete obliteration [12,13]. This reinforces the standard that angiographic cure must be verified by post-operative digital subtraction angiography (DSA). Ultimately, the treatment decision requires a multidisciplinary evaluation, balancing the reduction of operative risk via embolization with the need for definitive microsurgical cure in appropriately selected cases.
The high prevalence of associated cerebral aneurysms may contribute to the propensity for initial hemorrhage in cerebellar AVMs [23]. Therefore, the targeted embolization of cerebral aneurysms associated with cerebellar AVMs should be given priority [24,25]. Preoperative embolization of intracranial AVMs has been demonstrated to reduce operative time and intraoperative blood loss, with no significant difference in surgical complications or long-term neurological outcomes [1,7,23].
In some cases, a combined approach may be employed. This entails preoperative embolization to diminish the size or blood flow of the AVM, rendering surgical resection safer and potentially more effective due to a bulk resection of the previously embolized AVM, thereby significantly reducing the risk of intraoperative rupture and blood loss [22].
While our data strongly indicate the protective benefit of embolization in reducing blood loss (p=0.018) and surgical time (p=0.018), a critical interpretation requires addressing the selection bias observed in our small cohort. The Hybrid Group presented with a significantly higher preoperative mRS median (3 vs. 1.5) 5, suggesting these were the higher-risk lesions deemed unsuitable for surgery alone. This disparity implies that the embolization technique was correctly applied to the most challenging cases, successfully transforming lesions associated with moderate disability into those capable of achieving excellent functional recovery (median mRS 1 at 6 months). Conversely, the sustained poor functional outcome in the Surgery-only group (median mRS 4 at 6 months), despite a better baseline mRS, may be a subtle indicator that, even for ostensibly lower-risk AVMs, the added security provided by embolization may be beneficial.
The decision between surgical resection, endovascular embolization, or a combination of both depends on several factors, including the size of the AVM, its location, angioarchitecture (feeding branches and draining veins), the patient’s overall condition, and the expertise available at the medical center. It is crucial for the medical team to thoroughly evaluate each case individually and tailor the treatment plan accordingly to achieve the best possible outcome while minimizing risks to the patient [1,9,22].
Research in this field continues to advance with the aim of enhancing treatment outcomes and reducing potential complications associated with both surgical and endovascular approaches.
Although embolization and microsurgery remain fundamental components of AVM management, radiosurgery represents a well-established curative option, particularly for deep or high-grade lesions. Long-term follow-up studies have demonstrated obliteration rates between 60% and 85%, depending on nidus size and angioarchitecture. Radiosurgery should therefore be acknowledged as a complementary or alternative treatment modality in selected cerebellar AVMs.
The clinical implications and limitations of the study are crucial aspects to consider when interpreting the results and applying them to clinical practice. The findings of our study offer valuable insights into the current treatment strategies employed in patients with cerebellar AVMs. Given the rarity of this entity in neurosurgery and neurological endovascular therapy, these results may aid in making more informed decisions regarding therapeutic approaches for these patients.
In our series, complications associated with the treatment of cerebellar AVMs were more frequently observed with surgical treatment, regardless of whether they were previously embolized or not. These complications must be recognized and managed effectively on an individual basis. The results of our study provide clinicians with a deeper understanding of the disease and the numerous factors that must be considered in the approach, analysis, and selection of treatment, as well as the types of complications that may arise with the chosen treatment, potentially influencing management and prevention strategies. Our descriptive study will assist healthcare professionals in recognizing that cerebellar AVMs (despite their lower frequency) require distinct considerations compared to supratentorial AVMs.
Our study is limited by its relatively small sample size, highlighting the need for further research in this field. We propose conducting prospective studies with larger samples to provide updated and statistically analyzable information to determine the optimal therapeutic approach for cerebellar AVMs.
Several limitations are inherent in our study. The small sample size restricts the generalizability of the results and precludes objective comparisons between our analyzed groups (only-surgery group versus hybrid group). The results obtained in this study show preliminary evidence of efficacy; however, it cannot be generalized to the broader population without larger prospective studies. A larger sample would offer a more representative depiction of the target population and enhance the reliability of the findings.
Furthermore, our study employed a retrospective design, relying on previously collected data, which may impact the quality and availability of the information. Additionally, the lack of direct control over data collection could introduce bias or errors in the medical records.
CONCLUSIONS
Microsurgical resection remains the most reliable immediate curative option for appropriately selected cerebellar AVMs. However, cure can also be achieved with embolization in select cases, and radiosurgery offers a viable long-term curative strategy for lesions not amenable to surgery. The optimal approach should be individualized based on angioarchitecture, location, rupture status, and available expertise.
At our institution, treatment strategies are determined through a multidisciplinary evaluation. This includes surgeons who specialize in both endovascular and microsurgical treatments for cerebellar AVMs. As surgical and endovascular techniques advance, the debate over the best way to manage these AVMs will likely continue. Ultimately, the decision on the most suitable approach will depend on each patient’s unique anatomy, angioarchitecture, and individual characteristics.
Microsurgical resection remains the most definitive curative option in appropriately selected cases, though embolization and radiosurgery may achieve cure in selected patients or serve as complementary modalities.
For a treatment to be considered successful, follow-up digital subtraction angiography must show a complete absence of the abnormal blood vessels that were supplying or draining the AVM’s core (nidus), as well as a normal associated circulation time.
The study provides strong preliminary evidence of efficacy and intraoperative safety in complex AVMs, but the postoperative morbidity results require validation in prospective studies with larger samples.
We present this study as a descriptive case series that supports the safety and utility of preoperative embolization in complex posterior fossa lesions, while explicitly acknowledging that the small “Surgery-only” cohort precludes a definitive comparative analysis.
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