J Cerebrovasc Endovasc Neurosurg > Volume 26(4); 2024 > Article
Taheri, Rahmatian, and Javadnia: Multiple AVM with separate nidi, a case report and review the literatures

Abstract

Multiple arteriovenous malformations (AVMs) are uncommon, accounting for only 0.3-3.2% of all AVM cases. These AVMs are often found in syndromic pediatrics of HHT and WMS. Consideration of the patient’s condition, the angioarchitecture of each AVM, and the hemodynamic connection of AVMs is crucial in determining the optimal therapeutic approach. However, the optimal therapeutic decision-making for these complex vascular lesions can be challenging due to the scarcity of their reports and their long-term follow-up. In this report, we present the case of a young man who presented with a headache, and DSA shows three left parietal AVMs, each with a separate nidus, feeder artery, and draining vein.

INTRODUCTION

Arteriovenous malformations (AVMs) arise from the maldevelopment of arteriovenous network connections, which are characterized by high-flow and low-resistance shunting. These malformations comprise dilated feeding arteries, thickwalled draining veins, and a nidus that lacks neural tissue. The nidus of AVMs is the most frequent bleeding site [2,12,15]. The clinical manifestations of AVMs are diverse, ranging from intracerebral hemorrhage [29], seizure, focal neurological deficits, and a simple headache. AVMs are mostly solitary, and multiple AVMs (MAVMs) are rare, accounting for only 0.3-3.2% of these malformations. MAVMs are mainly reported in children accompanied by syndromes such as hereditary hemorrhagic telangiectasia (HHT) or Wyburn Mason syndrome (WMS) [14,19,23]. There are also rare reports of asymptomatic non-syndromic multiple AVMs.
In some studies, the risk of bleeding in multiple AVMs is similar to a single AVM at 2.1% [10,29], but others report vise-versa; the risk of bleeding in multiple AVMs is nearly twice that of a single AVM [4,9], and in a meta-analysis, the risk of bleeding prior to diagnosis in multiple AVMs was 26.5% and 60% in syndromic and non-syndromic patients, respectively, comparing to 19.4% and 49.9% with single AVM in syndromic and non-syndromic patients [1,5].
The usual association of supratentorial AVM with infratentorial one can be assign of embryological origin of MAVM pathology [10,26,28]. The annual risk of hemorrhage for MAVM is 2-3 times more than solitary AVM about 6.7% [4,9].
The therapeutic approach to MAVM is not only determined by each AVM characteristic but also by angioarchitecture network connection of AVMs and the potential hemodynamic interactions are also essential to be considered.
The proportion of nidal instability following staged therapy in non-syndromic patients was 17.5% that half of them were intracranial hemorrhage accounting for 10% in one year following staged therapy [2]. That is higher than solitary AVM that underwent staged therapy (1.3-1.5%) [27].
Due to the rarity of such cases, there is still no consensus about the optimal therapeutic approach. Here we present a young patient with incidentally MAVM that reject treatment, we are also doing a literature review in this regard.

CASE DESCRIPTION

A 23-year-old man was referred to us with a diagnosis of a brain vascular lesion. On admission, the patient was conscious and had a Glasgow Coma Scale (GCS) score of 15. No defects were observed in the neurological examination. Medical history and general clinical examination of the patient revealed no signs or symptoms related to HHT, WMS, or other significant diseases. MRI revealed multiple signal voids and serpentine vessels in the left hemisphere in favor of a vascular lesion, mainly brain AVM or dural Arteriovenous Fistula (dAVF), prompting further evaluation by brain digital subtraction angiography (DSA).
DSA showed three left parietooccipital AVMs with separate nidi supplied by distal branches of the middle cerebral artery (MCA). There were two distinct nidi in the parietal region were supplied with their feeders from the MCA. The initial AVM was situated in the inferior parietal lobe, with a condensed nidus smaller than 3 cm, draining via two veins into the superior sagittal sinus (SSS) (classified as Spetzler-Martin Grade (SMG 2)). Another AVM with a compact nidus smaller than 3 cm was located in the inferior parietal lobe adjacent to the parieto-occipital sulcus, draining into the SSS and transverse sinus through two separate veins (also classified as SMG 2). The third AVM, situated in the temporal region, received a feeder supply from the distal branches of the left middle cerebral artery (MCA) and drained into the transverse sinus through a stenotic vein. This AVM’s nidus was also compact and less than 3 cm (SMG 2). Each AVM was found without an accompanying aneurysm (Fig. 1).
The heightened risk of hemorrhage in 3rd AVM due to the stenosis in the inferior draining vein, we opted for treatment. Given its critical location, we decided to employ an endovascular approach for the third AVM and close follow-up observation of the remaining AVMs due to their critical locations. Following a comprehensive discussion of the treatment’s benefits and drawbacks, the patient opted not to proceed with the recommended therapy. Consequently, we proposed regular follow-up visits and annual angiography. Despite our detailed explanations and cautions, the patient only attended the first follow-up visit after one year and declined to undergo angiography—however, the patient presented with a normal GCS and no neurological deficits.

DISCUSSION

Therapeutic approaches

The decision to treat multiple AVMs is complex. Some authors argue that managing multiple AVMs should be approached independently of their multiplicity. Conversely, others contend that the potential interactions between multiple lesions must be considered in the course of treatment [26].
The therapeutic approach to managing multiple AVMs is based on the principles of treating a single AVM. The available therapeutic approaches for multiple AVMs include microsurgery, endovascular embolization, stereotactic radiosurgery, or a combination of these approaches [17].
The selection of a particular approach is determined by the patient’s condition and the unique features of the multiple AVMs, such as their location and the Spletzer Martin grading of each AVM [15].

Management strategies

Symptomatic multiple AVMs

The treatment of cerebral AVMs should include all hemorrhagic AVMs and unruptured AVMs with high-risk angiographic features such as associated aneurysms, deep location, only deep venous drainage, and single venous drainage [22].
Microsurgical resection of the entire nidus of the AVM by omitting the primary source of bleeding is the mainstay treatment. Endovascular treatment is a reasonable therapeutic choice when the lesion is deep and inaccessible; it can also be used as an adjuvant therapy to microsurgery or radiosurgery [11]. Radiosurgery is a favorable alternative for managing small AVMs with a nidus lesser than 2-3cm and for patients who are medically unsuitable for surgery [8,25].
Two hypotheses exist regarding the impact of the resection or omission of one AVM on the remaining ones. According to one hypothesis, by omitting one AVM, the blood flow may undergo alteration or even increase toward the remaining AVMs, contributing to an increased chance of bleeding. As a result, these authors recommend prompt elimination of the remaining AVMs [6,18,20]. Several others argue that after removing one AVM, the blood flow to other AVMs may decrease, potentially resulting in thrombosis and even the disappearance of other AVMs [26,31]. So, it is reasonable that all related AVMs to the hemorrhagic one also be treated following the hemorrhagic one [13,20,26].

Asymptomatic multiple AVMs

According to ABURA (a randomized trial of unruptured brain arteriovenous malformations) guidelines, conservative management with follow-up imaging is proved to be the safest intervention for unruptured AVMs [16]. However, selected cases of unruptured AVMs, with low-grade Spetzler-Martin grading and situated in non-eloquent areas, may be considered for intervention after meticulous evaluation [3]. In patients with HHT and multiple AVMs, AVMs are primarily present in younger patients, located in non-eloquent, cortical regions and with smaller than 3 cm size [3,30]; conservative management is often recommended due to their reduced risk of bleeding [21,24].
There are rare reports of patients with multiple AVMs that present with irrelevant symptoms, and their AVMs are found incidentally.
A seven-year-old girl experienced recurrent episodes of fever without any apparent signs or symptoms indicative of generalized vascular disorders. An angiography evaluation revealed the presence of six distinct AVMs, of which one was located superficially in the temporal lobe and was relatively larger than the others. Surgical intervention was performed on it, while the remaining five underwent stereotaxic irradiation. However, the authors did not provide details regarding the outcomes or follow-up procedures performed [7].
A 48-year-old male patient presenting with mild occipitalgia was referred to the neurosurgical department for further evaluation. A brain CT scan revealed two small enhanced lesions in the right occipital and left parietal regions. Angiography subsequently confirmed the presence of two AVMs, one supplied by temporo-occipital and calcarine arteries and the other by parenchymal arteries; both were draining to the superior sagittal sinus. Despite the diagnosis, the patient refused treatment, and after two years of diligent follow-up, he remained free of hemorrhage and bleeding [29].
In a case series by Robert et al., they report three patients with multiple cerebral AVMs that present with irrelevant symptoms to their AVMs and are managed conservatively [22]. One patient was a 37-year-old man present with vertigo whose angiography revealed two cortical AVMs, one in the frontal and the other one in the occipital region, that was concomitant with intranidal aneurysm (SMG 3). The intranidal aneurysm coiled but two AVMs due to no history of bleeding and low risk of bleeding according to angiography approached conservatively during 26 months follow up was asymptomatic. The other patient was a 20-year-old man with HHT who had a headache on one side of his head. After an angiography, doctors found two AVMs in his brain. One was in the superior area, and the other was in the mesencephalic area. The supra-AVM was treated with endovascular treatment, while the mesencephalic AVM received conservative treatment due to the high risk of treatment and asymptomatic nature. After 35 months of follow-up, the patient was still asymptomatic. The last patient was a 63-year-old man referred with vertigo and a history of HIV. That angiography revealed two separate AVMs, one in the central region and one in the cerebellum (SMG 1). Both were asymptomatic, at low risk of bleeding and underwent conservative management. During one-year follow-up, they remain asymptomatic.
In our case, we had scheduled endovascular therapy for the third AVM due to stenosis in its draining vein and close follow-up observation of the remaining AVMs due to their sensitive locations, asymptomatic presentation, and the absence of high-risk imaging features. However, the patient declined treatment and angiography; after one year, the patient did not exhibit any neurological signs or symptoms. Our findings also support the concept of ABURA, suggesting that conservative management is reasonable for asymptomatic multiple AVMs located in eloquent regions where treatment carries a risk of complications. It is important to note that, in our case, only one of the three AVMs exhibited the high-risk imaging trait for hemorrhage. In instances where multiple AVMs present with a high-risk feature of hemorrhage, the decision-making process, as previously explained, would be different.

CONCLUSIONS

Conservative management with close monitoring may be considered for patients with asymptomatic multiple AVMs located within eloquent brain regions, where surgical intervention poses significant risks.

ACKNOWLEDGEMENTS

All authors declare no conflict of interests.

NOTES

Disclosure

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Fig. 1.
Cerebral digital subtraction angiogram (DSA) shows three separated nidi of arteriovenous malformation (AVM) supplied by different branches of left middle cerebral artery (MCA) (A to D: lateral view of the left carotid angiogram in different phases).
jcen-2024-e2024-05-002f1.jpg

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