Brain arteriovenous malformation treatment with transvenous endovascular technique after transarterial technique failure

1 Graduate student, Faculdade de Medicina, Universidade Federal do Amazonas (UFAM), Amazonas, AM, Brazil. 2 Medical doctor, Faculdade de Medicina, Universidade Federal do Amazonas (UFAM), Amazonas, AM, Brazil. 3 Professor of Neurology, Faculdade de Medicina, Universidade Federal do Amazonas (UFAM), Amazonas, AM, Brazil. 4 Neurosurgeon, Hemodinâmica, Hospital Santa Júlia (HSJ), Amazonas, AM, Brazil. 5 Professor of Neurosurgery, Faculdade de Medicina, Universidade Federal do Amazonas (UFAM), Amazonas, AM, Brazil.


Introduction
Arteriovenous malformations (AVMs) are unnatural connections in the vascular system. Epidemiological studies showed that the incidence of AVMs ranges from 1.12 to 1.42 cases per 100.000 individuals per year, with 38-68% of new cases presenting as firstever hemorrhage. Annual rates of hemorrhage in untreated AVMs have been estimated at 2.10-4.12% [1][2]. The brain AVMs can be associated with a broad spectrum of clinical manifestations -ranging from headaches and seizures to mass effect symptoms [3][4]. The main issue related to brain vascular malformations and patient's morbimortality is the presence of aneurysms and their rupture. Preventing intracranial bleeding is the primary purpose of AVMs treatment [5][6].
The treatment strategies are dictated by the angioarchitecture, location and presentation of AVMs. Currently employed treatment options include microsurgery, stereotactic radiosurgery, and endovascular embolization as standalone or combination therapies [7]. Surgical approach is usually performed from transarterial access, with arterial feeders disconnection followed by the draining vein ligation [8][9]. Nevertheless, the transvenous AVM embolization emerged as a feasible option, particularly in the following situations: small and compact AVM nidus, ruptured AVMs, AVMs without safe transarterial access, inaccessible residual nidus, incomplete microsurgery, and unsuccessful stereotactic radiosurgery [7].
On the downside, the transvenous access risks and benefits are still to be properly established due to a small number of reported cases, according to Chen and colleagues [7] The purpose of this study was to present a case report of a patient submitted to a transvenous AVM embolization after a previous transarterial embolization failure.

Case report
A 35-year-old female patient was diagnosed with a brain AVM, located at the corpus callosum's splenium. As a therapeutic approach, the patient was submitted to transarterial embolization. However, the procedure was performed too proximally in the arteries, which resulted in the total AVM persistency. Since then, the patient presented five episodes of intracranial bleeding.
After the last bleeding episode, the patient was admitted to an intensive care unit (ICU). Magnetic resonance imaging revealed intracranial hemorrhage (Figure 1), and a cerebral angiography was performed to evaluate the AVM. The exam showed dilated and tortuous entangled blood vessels with early venous opacification, characterizing the malformation ( Figure  1).
The present AVM was located in the region between the right lateral ventricle posterior horn projection and the corpus callosum's splenium. The nidus measured 2cm in its larger axis, with its opacification deriving from multiple tiny arterial supplies from the posterior cerebral artery. There was single vein drainage to the deep venous system, together with a stenosis in the level of its junction with Galen's vein.
Inside the surgical act, an occlusion in the junction between the posterior cerebral artery and the lateral occipital artery (P2P3 junction) was noticed through the arterial roadmapping, confirming that the previous embolization was made too proximally. Immediately, a Trevo 4x20 stent retriever was allocated, and the arterial reopening was confirmed. After that, an occlusion balloon was placed into the right P2 artery.
Subsequently, a Fargomini catheter was advanced into the straight sinus through jugular access. A Headway Duo microcatheter 1.3F was then advanced into the nidus through the draining vein, with microguidewire assistance.
Alongside intermittent arterial occlusion, a total of 2 Squid 18 flasks were injected. The patient was submitted to angiographic control until complete AVM occlusion.
A final series of angiographic images demonstrated AVM radioanatomic cure, without any further complications (Figure 1).

Discussion
There is an understanding that the bleeding risk in patients with AVMs grows at length. After classifying patients according to the Spetzler-Ponce grading system and evaluating each group association with hemorrhage, a review by Morgan et al. [10] concluded that even in the lowest classification (A), the patients benefited from surgical treatment [10].
Overall, approximately 42% of all intracranial hemorrhages cause permanent neurological deficit or death [10]. The patient's first surgery was through a failed transarterial approach and was followed by recurrent bleeding episodes.
One of the principal explanations for the AVM persistency has its basis on the endothelial cell theory. An incomplete nidus eradication induces the reminiscent endothelial cells to produce chemotactic and angiogenic substances due to the tissue's low oxygen level after the procedure. Consequently, cellular infiltration from the adjacent tissue and new vessel formation occurs. While the first leads to thrombus removal from the occluded vessel -thus reestablishing the blood flow, the latter provides irrigation to the thrombosed area. These factors ensure nidus blood supply and, therefore, its persistency [11].
After the previous failure, a retrograde vein pathway was used. This procedure is commonly attempted as salvage therapy, with restricted and specific indications. Some of them were present in the current patient, such as tiny perforating arteries and a single outflow vein [7,10] [13] demonstrated that the irrigation artery occlusion reduces the pressure inside the nidus and in the draining vein, leading to an appropriate nidu's embolization hemodynamic control [12][13]. In the present study, an artery occlusion balloon was used to secure optimal blood flow and pressure handling. Moreover, the selected embolic substance was Squid 18, an ethylene-vinyl alcohol copolymer (EVOH) based agent, which was demonstrated to be safe and effective in brain AVMs [14].

Conclusion
A transvenous embolization approach to treat brain AVMs with specific characteristics might work as an excellent therapeutic intervention, representing a possible alternative treatment to the usual transarterial access, with good relative results. Further clinical trials and long-term studies should be conducted to establish the technique's safety and efficacy throughout time.