REMODELING AND COMPARTMENTALIZATION OF THE NIDUS AS A SOLUTION FOR SAFE RESECTION OF RUPTURED UNEMBOLISED LARGE AND GIANT ARTERIOVENOUS MALFORMATIONS
Authors: Giovani Andrei , Sandu Aura , Gheorghiu Ana , Radu Roxana , Petrescu G. , Gorgan R.M. 
Published: November 2024

Introduction
Arteriovenous malformations (AVMs) consist of fistulous connections of arteries and veins without intervening capillaries, organized as a mass with definable sides. AVMs are composed of enlarged feeding arteries, a nidus of dysmorphic vessels in relationship with the brain parenchyma, through which arteriovenous shunting occurs and draining veins. In a series of corticalised and deep avm’s the senior author conceptualised the nidus as composed of two or more compartments that can be separated completely after partial disconnection from corresponding feeding arteries and unessential drainage veins. This surgical strategy allowed a wider surgical corridor to the deeper AVM compartments, a faster resection and reduced blood loss.

Material and Methods
In this study we review 4 large and one giant AVM cases removed surgically using the technique of nidus compartmentalization. Clinical and imaging data included complete surgical videos, gender, age, clinical presentation, Spetzler-Martin and Lawton-Young grade, nidus size, modified Rankin Score (mRS) were collected.

Surgical Nuances
The surgical strategy was adapted to the location of the main feeders. when the main feeders were deep we preferred opening a narrow deep surgical corridor to interrupt them first and then enlarging it circumferentially from depth to surface.

In this scenario, the main drainage vein has a trajectory that is not perpendicular to the nidus, folding many times in close contact with one or more faces of the nidus or even inside the nidus. In this case, the classical dissecting strategy by opening surgical corridors circumferentially around the AVM, can be hazardous as the main drainage vein can be injured, resulting in heavy haemorrhage from the remaining nidus which is attached to the vein. When the main feeders came from MCA branches a superficial to deep dissection of the nidus was followed.

In order to facilitate the resection, after a partial dissection of the nidus was performed, this part of it, completely freed from feeders and drainage veins was separated from the rest of the AVM with a large clip. After coagulation and resection of the nidus compartment above the clip, the circumferential interruption of deep feeders continued beyond the clip, securing another compartment of the AVM. In only one case this manoeuvrer was repeated more than 3 times. In 3 cases the division of the nidus in two compartments was enough. In three of the cases, we encountered bleeding from the nidus, especially the part of the nidus disconnected from feeders. Applying a clip to compartmentalize the nidus in this situation controlled the bleeding and opened new corridors to advance the dissection.

When bleeding was encountered from multiple sources, both in the compartment disconnected from feeders and in the not yet dissected compartment, clip disconnection of the compartments diminished the bleeding considerably and allowed us to focus on the bleeding from the perforators.

In other two cases we applied this strategy of nidus separation by clips even if there was no bleeding as we gained more space to access the rest of the nidus once one compartment was completely disconnected. For the giant AVM, complete resection presumed resection in multiple steps as six nidus compartments were separated from the residual nidus and resected.

Results
Compartmentalization and staged disconnection of the nidus with large clips was performed in five cases. Three patients presented in the emergency care unit with ruptured AVMs and subsequent hematomas and two had only minor intraoperative bleeding. There were three and 2 females in the study. The mean (± SD) age of the patients was 40 years (± 14.6 years). On admission, three patients presented with altered mental status and hemiplegia and two patients with refractory epileptic seizures. Four patients underwent digital subtraction angiography (DSA) prior to surgery, while in one case only a computed tomography angiography (CTA) was performed, since the patient was in a critical state and needed urgent surgery. Three AVMs were located in the left dominant hemisphere, (two in the temporal lobe and one at the parieto-occipital junction), one AVM was cited in the, fronto-parietal right hemisphere and one giant left hemispheric avm. The median (range) size of the nidus was 4 cm (3-6 cm). Two AVMs were classified as Spetzler-Martin and Lawton-Young Supplemented grade VIII, one grade X and two as grade V.

Total resection of AVM was achieved in all cases as confirmed by postoperative CT cerebral angiography (Fig 3). Immediate postoperative CTA or DSA and magnetic resonance angiography (MRA) were performed in selected cases, also confirming total removal of the AVM.

For ruptured AVMs, resection and hematoma evacuation was performed in less than 12 hours after the onset of symptoms. There were no signs of cerebral infarction attributable to the staged temporary clipping of AVM’s compartments shown on postoperative CT scans and due to the lack of symptoms indicating ischemia, there was no need for diffusion-weighted imaging (DWI) or perfusion-weighted imaging (PWI) MRI sequences. There was no mortality in this case series. A modified Rankin’s scale was used to assess the outcome at six months, with a score ranging from 0 to 2 points, all patients were free of seizures and neurological deficits, fully socially reintegrated and returned to their previous jobs one year after surgery.

Discussion
Once a high-flow AVM has ruptured and subsequent hematoma progresses, brain’s protection mechanisms, such as local vasoconstriction and increased blood pressure are failing as the volume of the hematoma increases and cerebral oedema takes over. Therefore, is expressed the need for a faster removal of the AVM, regardless of the bleeding’s mechanism: the rupture of the AVM with massive hematoma or intraoperative bleeding, especially from the perforating arteries which are more difficult to control. We propose in this paper a surgical reorganization of AVM’s with separated compartments that are disconnected step by step from the lesion, in a decrescendo or crescendo way. Depending on the location of the main feeders, superficial or deep, this approach involves working circumferentially and spiralling deep from the surface or in the second scenario attacking deep feeders first, after creating a corridor in one of the AVM’s walls, then coming toward the surface. For this staged disconnection and resection of each one of the “feeding compartments” is used a clip-by-clip technique, occluding the arterial input and even secondary drainage veins. After the flow arrest, vessels are more susceptible to be coagulated and cut (Fig 5).

In many cases, a unique apparency of the nidus, with numerous loops all over its surface, possibly in close contact with the brain parenchyma can compromise the dissection, hence we recommend less coagulation on the surface of the nidus, to maintain the intranidal draining system. Once bleeding from the nidus occurs, it is important to avoid enlarging the surgical corridor and opening of new bleeding fronts, until active feeders are identified and controlled.

Concrete identification and anatomical description of each AVM compartment, followed by stepwise disconnection as a whole entity, decreases the intranidal pressure with a better bleeding-control and easier mobilization of the remnant lesion and ensures a faster resection in case of emergency.

Our study is limited by the small sample size, the emergency circumstances and the lack of intraoperative imaging techniques, such as intraoperative angiography in order to identify missing feeding arteries.

Further understanding of the pathophysiology of brain AVM is a milestone for adapting microsurgical resection that suits better each one of these malformations, conceptualized as a box with multiple compartments.

Conclusions
Developing strategies in refining microsurgical resection is a continuous target in AVMs approach. In emergency cases, with rupture and consequent hematoma, quick resection is mandatory. In order to achieve that, remodelling of the nidus and segmentation, with gradual clip application and separate disconnection is a safe solution with a good outcome.