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Prognostic variables and outcome in relation to different bleeding patterns in arteriovenous malformations

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Subarachnoid hemorrhage as bleeding pattern occurs rarely in ruptured arteriovenous malformations (AVM). The aim of the present study is to evaluate different bleeding patterns in hemorrhages due to an AVM and their impact on outcome in terms of risk and treatment stratification. We evaluated 158 patients with ruptured AVMs who were admitted to our neurosurgical department from 2002 to 2017. We compared different bleeding patterns, such as intracerebral hemorrhage (ICH), subarachnoid hemorrhage (SAH), or both (ICH + SAH) and evaluated predictive variables for outcome in the last follow-up. ICH was found in 48.7% of patients, isolated SAH in 20.9% of patients, and both in 30.4% of patients. The mean parenchymal blood volume was 34.5cm³. 38.6% of the patients had AVM-associated aneurysms, mostly located pre-nidal (77%). AVMs with ruptured aneurysms often resulted in ICH with SAH component (p < 0.001) and SAH pattern occurred more often infratentorial (p = 0.003). In a multivariate logistic regression model, poor clinical state on admission (WFNS IV-V) (p < 0.01), eloquence, infratentorial location (p = 0.05), and presence of ICH with SAH component (p = 0.02) were the most relevant predictors of a poor outcome after AVM rupture. Bleeding pattern in AVM hemorrhage depends on angioarchitectural and hemodynamic features and SAH component predicts outcome negatively. AVM-associated pre-nidal aneurysms may harbor a higher risk for rupture and SAH pattern when located infratentorial. Treatment decisions and risk stratifications should be considered in view of these findings.
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ORIGINAL ARTICLE
Prognostic variables and outcome in relation to different bleeding
patterns in arteriovenous malformations
Nazife Dinc
1
&Sae-Yeon Won
1
&Johanna Quick-Weller
1
&Joachim Berkefeld
2
&Volker Seifert
1
&Gerhard Marquardt
1
Received: 15 January 2019 /Revised: 12 February 2019 /Accepted: 25 February 2019 / Published online: 5 March 2019
#Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
Subarachnoid hemorrhage as bleeding pattern occurs rarely in ruptured arteriovenous malformations (AVM). The aim of the
present study is to evaluate different bleeding patterns in hemorrhages due to an AVM and their impact on outcome in terms of
risk and treatment stratification. We evaluated 158 patients with ruptured AVMs who were admitted to our neurosurgical
department from 2002 to 2017. We compared different bleeding patterns, such as intracerebral hemorrhage (ICH), subarachnoid
hemorrhage (SAH), or both (ICH + SAH) and evaluated predictive variables for outcome in the last follow-up. ICH was found in
48.7% of patients, isolated SAH in 20.9% of patients, and both in 30.4% of patients. The mean parenchymal blood volume was
34.5cm
3
. 38.6% of the patients had AVM-associated aneurysms,mostly located pre-nidal (77%). AVMs with ruptured aneurysms
often resulted in ICH with SAH component (p< 0.001) and SAH pattern occurred more often infratentorial (p= 0.003). In a
multivariate logistic regression model, poor clinical state on admission (WFNS IV-V) (p< 0.01), eloquence, infratentorial
location (p= 0.05), and presence of ICH with SAH component (p= 0.02) were the most relevant predictors of a poor outcome
after AVM rupture. Bleeding pattern in AVM hemorrhage depends on angioarchitectural and hemodynamic features and SAH
component predicts outcome negatively. AVM-associated pre-nidal aneurysms may harbor a higher risk for rupture and SAH
pattern when located infratentorial. Treatment decisions and risk stratifications should be considered in view of these findings.
Keywords Arteriovenous malformation .Subarachnoid hemorrhage .Hemorrhage pattern
Introduction
Outcome in hemorrhage due to an arteriovenous malforma-
tion (AVM) is infrequently devastating and depends on bleed-
ing pattern. While recent studies suggest that AVM hemor-
rhage is not as devastating as previously presumed compared
to aneurysmal subarachnoid hemorrhage (SAH), which is
more often lethal, AVM rupture tends to result in more neu-
rological deficits [1]. In addition to several negative prognos-
tic factors such as older age [2], poor initial admission state
[3], hematoma volume [4], and infratentorial location [5,6], a
subarachnoid component seems to impact outcome signifi-
cantly. Intraparenchymal hematoma is the most common
pattern in AVM-associated hemorrhage [7]. SAH due to an
AVM is described to amount 9% and literature therefore is
rare. The objective of our single-center study is to assess
how far subarachnoid component in AVM-associated hemor-
rhage impacts the final outcome negatively.
Materials and methods
Study design
The study was performed in accordance with our institutional
ethical review board. A retrospective review of patients with
ruptured brain arteriovenous malformation (AVM) who were
registered and evaluated at our neurosurgical department from
2002 to 2017 and entered into our prospectively maintained
database was carried out. The onset of hemorrhage was con-
sidered as the day at which the patient was admitted to our
emergency service. The diagnosis AVM was confirmed with
magnetic resonance imaging (MRI) or digital subtraction an-
giography (DSA). Different bleeding patterns such as
*Nazife Dinc
nazife.dinc@kgu.de
1
Department of Neurosurgery, Goethe University Hospital Frankfurt,
Schleusenweg 2-16, 60528 Frankfurt, Germany
2
Department of Neuroradiology, Goethe University Hospital,
Frankfurt, Germany
Neurosurgical Review (2019) 42:731736
https://doi.org/10.1007/s10143-019-01091-7
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... It can also be used for measuring depression severity [19]. It consists of 9 items, and the total score can be classified as minimal (0-4), mild (5-9), moderate (10)(11)(12)(13)(14), or severe (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27) depressive symptoms [19]. ...
... It is remarkable that the self-proclaimed items "health" and "life satisfaction" of the QOLS were scored higher in patients with ICH, despite their shortcomings in the mRS. Treatment modality, bleeding volume and bleeding pattern neither had a significant impact on the QOLS even though in the literature, patients with subarachnoid components have higher outcome impairment [14,30,31,45]. These findings contradict the current literature concerning the impact of ICH on the QoL which could be due to several potential biases: It is possible that the unruptured AVMs are likely to be more symptomatic and tend to seek medical help and get the diagnosis compared to non-symptomatic patients who get the diagnosis after haemorrhage. ...
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Objective Intracranial haemorrhage (ICH) is associated with permanent neurological disability resulting in deterioration of the quality of life (QoL). Our study assesses QoL in patients with ruptured arteriovenous malformation (AVM) in long-term follow-up at least five years after ICH and compares their QoL with the QoL of patient with non-ruptured AVM.Methods Using the Quality of Life Scale (QOLS), the Patient Health Questionnaire (PHQ-9) for depressive symptoms, and the socioeconomic status (SES), a prospective assessment was performed. The modified Rankin Scale (mRS) was assessed for outcome.ResultsOf 73 patients, 42 (57.5%) had ruptured (group 1) and 31 (42.5%) a non-ruptured AVM (group 2). Mean follow-up time was 8.6 ± 3.9 years (8.5 ± 4.2 years in group 1 and 8.9 ± 3.7 years in group 2). Favourable outcome (mRS 0–1) was assessed in 60 (83.3%) and unfavourable in 12 (16.7%) patients. Thirty-one of 42 patients (73.8%) in group 1 and 29 of 30 patients in group 2 (96.7%) had favourable outcomes. Mean QOLS was 85.6 ± 14.1 (group 1 86.1 ± 15.9, group 2 84.9 ± 11.4). Patients in group 1 did not show a significant difference in QoL compared to patients in group 2 (p = 0.23). Additional analyses in group 2 (rho = − 0.73; p < 0.01) and in untreated AVM patients (rho = − 0.81; p < 0.01) showed a strong correlation between QOLS and PHQ-9.Conclusion Long-term follow-up showed no difference in the QoL between patients with and without ICH caused by brain AVM. Outcome- and QoL-scores were high in both groups. Further studies are necessary to evaluate depression and anxiety symptoms in patients with AVM.
... On physical examination, auscultation typically demonstrates a bruit, which is due to abnormally high blood flow. Pulsation is a feature of AVMs as well (72). In this patient, an ultrasound revealed a vascular malformation in the musculature of the right neck/shoulder, with a clear communication with the right common carotid artery. ...
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The understanding of the physiology of cerebral arteriovenous malformations (AVMs) continues to expand. Knowledge of the hemodynamics of blood flow associated with AVMs is also progressing as imaging and treatment modalities advance. The authors present a comprehensive literature review that reveals the physical hemodynamics of AVMs, and the effect that various treatment modalities have on AVM hemodynamics and the surrounding cortex and vasculature. The authors discuss feeding arteries, flow through the nidus, venous outflow, and the relative effects of radiosurgical monotherapy, endovascular embolization alone, and combined microsurgical treatments. The hemodynamics associated with intracranial AVMs is complex and likely changes over time with changes in the physical morphology and angioarchitecture of the lesions. Hemodynamic change may be even more of a factor as it pertains to the vast array of single and multimodal treatment options available. An understanding of AVM hemodynamics associated with differing treatment modalities can affect treatment strategies and should be considered for optimal clinical outcomes.
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A man in his late forties had lived as a recluse for more than ten years. He was found dead in his room. At autopsy, subarachnoid hemorrhage (SAH) was detected at the base of the brain, which weighed 1333 g. The cerebellar tonsil was swollen. The cerebral ventricle was enlarged and filled with blood. A hematoma was observed in the upper part of the left side of the cerebellar hemisphere. The location and size of SAH in this case indicated that the rupture of a cerebral aneurysm (CA) had occurred; however, CA was not detected. A mass of blood vessels buried in the hematoma was observed at the left cerebellopontine angle (CPA). The vascular lesion showed round-shaped blood vessels as well as flat-shaped vessels with the appearance of veins, but with elastic fibers indicative of arteries. The lesion was considered to be the nidus and was 5-8 mm in size. Feeding arteries appeared to be from the anterior inferior cerebellar artery (AICA). However, the draining vein and anastomotic parts of the artery and vein were not confirmed. Based on these histopathological features, this vascular lesion was diagnosed as arteriovenous malformation (AVM). A differential diagnosis between AVM at CPA and CA is needed in order to identify the source of non-traumatic SAH.
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✓ An important factor in making a recommendation for treatment of a patient with arteriovenous malformation (AVM) is to estimate the risk of surgery for that patient. A simple, broadly applicable grading system that is designed to predict the risk of morbidity and mortality attending the operative treatment of specific AVM's is proposed. The lesion is graded on the basis of size, pattern of venous drainage, and neurological eloquence of adjacent brain. All AVM's fall into one of six grades. Grade I malformations are small, superficial, and located in non-eloquent cortex; Grade V lesions are large, deep, and situated in neurologically critical areas; and Grade VI lesions are essentially inoperable AVM's. Retrospective application of this grading scheme to a series of surgically excised AVM's has demonstrated its correlation with the incidence of postoperative neurological complications. The application of a standardized grading scheme will enable a comparison of results between various clinical series and ...
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Background Posterior fossa arteriovenous malformations (AVMs) are considered to have a higher risk of poor outcome, as are AVMs with associated aneurysms. We postulated that posterior fossa malformations may be more prone to associated feeder vessel aneurysms, and to aneurysmal source of hemorrhage. Objective To examine the prevalence and hemorrhagic risk of posterior fossa AVM-associated feeder vessel aneurysms. Methods A retrospective review of AVMs was performed with attention paid to location and presence of aneurysms. The hemorrhage status and origin of the hemorrhage was also reviewed. Results 571 AVMs were analyzed. Of 90 posterior fossa AVMs, 34 (37.8%) had aneurysms (85% feeder vessel, 9% intranidal, 15% with both). Of the 481 supratentorial AVMs, 126 (26.2%) harbored aneurysms (65% feeder vessel, 29% intranidal, 6% both). The overall incidence of feeder aneurysms was higher in posterior fossa AVMs, which were evident in 34.4% of infratentorial AVMs compared to 18.5% of supratentorial malformations (p<0.01). The presence of intranidal aneurysms was similar in both groups (9.2% vs 8.8%). Feeder artery aneurysms were much more likely to be the source of hemorrhage in posterior fossa AVMs than in supratentorial AVMs (30% vs 7.6%, p<0.01). Conclusions Posterior fossa AVMs are more prone to developing associated aneurysms, specifically feeder vessel aneurysms. Feeder vessel aneurysms are more likely to be the source of hemorrhage in the posterior fossa. As such, they may be the most appropriate targets for initial and prompt control by embolization or surgery due to their elevated threat.