The incidence rate of cavernous malformations (CMs) ranges from 0.4 to 0.9% of the general population. These incidences constitute 8 to 15% of all cerebrovascular malformations [1–5] and occur in the supratentorial compartment in 63 to 90% of cases [6, 7]. Posterior fossa CMs represent 7.8 to 35.8% of all cases, and the brainstem is the most commonly involved site in this compartment (9-35% of all cases) [4, 7]. Based on a large sample size, cerebellar CMs (CCMs) constitute 1.2 to 11.8% of all intracranial cases and 9.3 to 52.9% of all infratentorial cases [7, 8]. The current data in the literature regarding CMs localized in the cerebellum are limited to case reports [7, 9–12].

The coexistence of a CM and an associated developmental venous anomaly (DVA) is the most common mixed vascular malformation [13]. Patients with CMs associated with DVAs are more likely to have lesions in the posterior fossa [11]. The difference in the clinical profiles and surgical outcome between patients with CMs with and without associated DVAs in the cerebellum is unclear, which makes it difficult to determine the long-term prognosis of these patients.

There is controversy regarding the management of CMs associated with DVAs. Recent findings support the hypothesis that DVAs can be considered the initial pathophysiological factor that leads to the formation of CMs [14–18]. Additionally, some authors have proposed the coagulation and division of the transcerebral vein of the DVA during the removal of the CM as a means to prevent the recurrence of CMs [18]. However, due to the compromise of venous drainage of normal cerebellum, this strategy might increase the risk of serious postoperative cerebellar edema and might even cause cerebellar tonsillar herniation. The identification of a balance between the recurrence of the associated CM and herniation, which is a devastating consequence, currently remains unknown.

We retrospectively reviewed 41 patients suffering from cerebellar CMs with or without associated DVAs in our hospital to analyze the clinical and radiological characteristics of CCMs and to assess the various therapeutic strategies.

Intracranial vascular malformations were originally classified by McCormick [22] into five types: telangiectasias, varix, cavernous malformation, arteriovenous malformation, and venous malformation. The definition of each of these types of malformations depends on distinct pathological criteria. However, mixed or transitional vascular malformations with the pathological features of more than one type of malformation within the same lesion have been recently described. The detection of a wide spectrum of intermediate forms of McCormick’s original categories suggests that these lesions might be a continuum of progression from a single pathological process [12]. The coexistence of a CM and a DVA is the most common presentation of a mixed vascular malformation. Much discrepancy exists in the literature concerning the prevalence of coexisting CMs and DVAs [13]. Based on findings from MR imaging studies, Abdulrauf [11] found that 13 (24%) of 55 patients with supratentorial and infratentorial CMs also had associated DVAs. A similar percentage was reported by Wurm [18], who found this type of association in 15 (25.9%) of 58 patients with cerebral, cerebellar, and brain stem CMs based on MR imaging and intraoperative findings. In 86 surgically treated patients with brainstem CMs, Porter [4] found a DVA that was intimately associated with each resected CM. Oliveira [7] reported cerebellar CMs in 10 cases, but none of these were associated with a DVA. In our study, 11 cerebellar CMs (26.8%) with associated DVAs were identified in 41 consecutive cerebellar CM patients.

Abdulrauf [11] compared the clinical profile of patients harboring CMs with and without associated DVAs. Compared with patients with CMs alone, patients with CMs associated with DVAs are more likely to be female, have associated symptomatic hemorrhage, have lesions in the posterior fossa (statistically significant), and suffer from repeated symptomatic hemorrhage and are less likely to present with seizures or to have familial histories. The authors of several reports have suggested that the CMs associated with a DVA have a more aggressive clinical course than CMs alone [11, 14, 15, 23]. In our study, the CCMs associated with DVAs did not present a more aggressive nature. There were no statistically significant differences between the patients with CCMs with and without DVAs regarding age, sex, location and size of the lesions, and initial clinical presentation. Five of the 30 patients (16.7%) in the CM group and none of the 11 patients (0%) in the CM + DVA group had multiple CMs (P = 0.30, not statistically significant). Familial cerebral CMs caused by loss-of-function mutations are often characterized by multiple lesions [24]. If substantiated in a larger case series, this difference of multiplicity may suggest different pathogenesis mechanisms (i.e., genetic factors, structural venous outflow factors, and hemodynamic variables) of the host’s predisposition to CCMs with and without associated DVAs.

The association of CMs and DVAs within the same lesion has generated hypotheses about the causation–evolution relationship among different types of malformations. It has been postulated that the abnormal hemodynamics of DVAs might induce the formation of CMs [12]. It has also been suggested that chronically increased intraluminal pressure and the resulting reduced tissue perfusion leading to tissue hypoxia may stimulate a local increase in angiogenic factors, which would induce the formation of vascular malformations [17]. If there are mixed vascular malformations in a region, DVAs can be considered the primary congenital lesion, and venous hypertension can be regarded as the initial pathophysiological factor leading to the formation of CMs [14, 17, 18, 25].

At the same time, DVAs are also responsible for the venous drainage of otherwise normal brain tissue. The removal of the whole DVA to prevent the reoccurrence of the associated CM could result in venous engorgement and cerebral edema, which might have devastating consequences. As a result, the following treatment protocol is recommended for patients with CMs associated with DVAs to avoid the risk of venous infarction: microsurgical resection of the CM alone and an “untouching” strategy for the DVA [4, 10, 16].

These two vascular malformations are usually connected by small medullary veins. The concurrent CM is located in the territory of the DVA, and the DVA’s distal radicles are part of the CM. The untouching of the DVA is difficult and even unrealistic unless residual CM is left in the region, which might result in CM reoccurrence and rehemorrhage.

The authors of some surgical reports have challenged this prevalent thinking and have described a significantly improved operative treatment of DVAs [12]. In a recent provocative report, Wurm [18] proposed the coagulation and division of the transcerebral vein of the DVAs to prevent CM recurrence. In their series of 15 patients with DVAs and CMs, these researchers removed the CM and divided the transcerebral vein of the DVA in nine of the patients: in six during the first operation and in the remaining three patients after recurrence of the associated CM with symptomatic hemorrhage. These authors observed no brain swelling intraoperatively, and the postoperative course was uneventful in all of these nine patients. Their experience supports the theory that the abnormal draining vein might be the actual pathological lesion that causes blood flow disturbances with recurrent and newly developing malformations. Coagulation of the large transcerebral draining vein did not lead to any ischemic or hemorrhagic infarction or any other complication.

The four patterns of relationship between CCMs and associated DVAs found in our study were summarized. The distal branches of the DVAs always covered the anterior top aspects of the CM, and the trunk of the DVA is more likely to extend upward and forward. In no cases did the distal radicles of the DVA cover the bottom aspect of the CM, and the trunk of the DVA never extended downward. In most surgical cases, the cerebellum is exposed from the back and lower head; thus, the relationship patterns of the CCMs and associated DVAs provide the surgeon great convenience to reach the CM and to coagulate and dissect the connected radicles without the barrier of the trunk. This surgical strategy might markedly aid the safe and radical removal of CMs and prevent the reoccurrence of CMs, and these patients may also have good long-term prognosis. It has to be emphasized that the surgeon must be alert when completing the resection of the CM because the trunk of the DVA is usually hidden behind the CM. In two of the patients analyzed in our study, the trunks of the DVAs might have been injured during the dissection of the anterior aspect and top aspect of the CMs, which would cause serious and dangerous cerebellar edema.

It is not rare that associated DVAs are found in CCM cases. There were no statistically significant differences between the patients with pure CCMs and the patients with CCMs with associated DVAs with respect to age, sex, location and size of lesions, multiplicity, initial clinical presentation, frequency of symptomatic hemorrhage, preoperative mRS, and surgical prognosis. The total removal of the CCM combined with the coagulation and dissection of the distal radicles at the length of the associated CM and the preservation of the trunk of the developmental venous anomalies can result in good long-term prognosis in patients.

Written informed consent was obtained from the patient for the publication of this report and any accompanying images.