Risk for Brain Arteriovenous Malformation Rupture During Pregnancy and Puerperium

Neurosurgery 93:918–923, 2023

The hemorrhage risk of unruptured and untreated cerebral arteriovenous malformations (AVMs) has been shown to be higher for female patients than male patients in their child bearing ages. Although it has been neurosurgical practice to advise female patients in their childbearing ages to postpone pregnancy until proven AVM obliteration, there is no literature consensus regarding this potential hemorrhage risk increase.

OBJECTIVE: To accurately quantify the risk increase for AVM hemorrhage during pregnancy.

METHODS: This study is based on data from previous publications, consisting of known age at the first AVM hemorrhage in 3425 patients. The risk increase during pregnancy could be calculated from the difference in age distribution for the first AVM hemorrhage between male patients and female patients, taking the average pregnancy time per female into account. A comparison was also made with data for all hospital discharges (13751) in Germany 2008 to 2018 with the diagnosis brain AVM.

RESULTS: The average pregnancy and puerperium time was 1.54 years per female in the patient population, which was used to determine the annual AVM hemorrhage risk during pregnancy to be around 9%. The increased risk during pregnancy was further evidenced by analysis of a subgroup of 105 female patients, for which pregnancy status at the time of hemorrhage was known.

CONCLUSION: The quantified annual risk for AVM hemorrhage during pregnancy is about 3 times higher than that of male patients at corresponding age. This provides an important basis for advising female patients with patent AVMs about the increased risk for hemorrhage that a pregnancy would entail.

Embolized cerebral arteriovenous malformations: a multivariate analysis of 101 excised specimens

J Neurosurg 132:1140–1146, 2020

Endovascular approaches have evolved from a technique practiced at very few centers to a widely available option in the management of arteriovenous malformations (AVMs) of the central nervous system. Embolization can be employed as definitive therapy or as an adjunct to surgical excision. A wide variety of embolic agents have been successfully developed and used in the clinical setting. In addition to facilitating vascular occlusion, embolic agents induce a number of reactive and destructive changes in vessel walls and the surrounding tissue. However, studies examining the pathological changes induced by different embolic agents and varying times of exposure are scarce. The goal of the present study was to compare embolic agents and time of exposure on the pathology in excised specimens.

METHODS The records of the Department of Pathology at the London Health Sciences Centre were searched for embolized AVMs for the 35-year period 1980–2015. All cases were reevaluated for clinical and technical variables and standardized histopathological findings. Cases were grouped by embolic agent, volume of agent used, and time to excision.

RESULTS A total of 101 specimens were identified. Embolic agents were invariably associated with a range of pathological findings, some of which may affect the integrity of vessel walls or the reestablishment of flow, thrombosis, acute and chronic inflammatory changes, angionecrosis, extravasation, and recanalization. The type of embolic agent did not predict differences in the incidence or severity of histopathological changes. Larger volumes of embolic agent were associated with a greater proportion of vessels containing embolic material. AVMs excised early (< 1 week postembolization) contained more acute vasculitis, while those excised later (≥ 1 week postembolization) were more likely to exhibit recanalization and foreign body giant cell infiltrates.

CONCLUSIONS Embolic agents induce a predictable range and temporal progression of pathological changes in cerebral AVMs. The embolic agents studied are indistinguishable in terms of the range and frequency of pathological reactions induced. Greater volumes of embolic agent are associated with more abundant agent within the lesion, but the proportion of vessels and vascular cross-sectional areas containing agent is small. Several changes are significantly associated with time postembolization. Acute vasculitis is a more common finding in the 1st week, while recanalization and foreign body–type granulomatous inflammation are more common at 1 week and beyond.

 

Risk of First Hemorrhage of Brain Arteriovenous Malformations During Pregnancy

Neurosurgery 85:E806–E814, 2019

Recommendations on the management of brain arteriovenous malformations (bAVM) with respect to pregnancy are based upon conflicting literature.

OBJECTIVE: To systematically review the reported risk and annualized rate of first intracranial hemorrhage (ICH) from bAVM during pregnancy and puerperium.

METHODS: MEDLINE, EMBASE, and Scopus databases were searched for relevant articles in English published before April 2018. Studies providing a quantitative risk of ICH in bAVM during pregnancy were eligible.

RESULTS: From 7 initially eligible studies, 3 studies met the criteria for providing quanti- tative risk of first ICH bAVM during pregnancy. Data from 47 bAVM ICH during pregnancy across 4 cohorts were extracted for analysis. Due to differences in methodology and defini- tions of exposure period, it was not appropriate to combine the cases. The annualized risk of first ICH during pregnancy for these 4 cohorts was 3.0% (95% confidence interval [CI]: 1.7- 5.2%); 3.5% (95% CI: 2.4-4.5%); 8.6% (95% CI: 1.8-25%); and 30% (95% CI: 18-49%). Only the last result from the last cohort could be considered significantly increased in comparison with the nonpregnant period (relative rate 6.8, 95% CI: 3.6-13). The limited number of eligible studies and variability in results highlighted the need for enhanced rigor of future research.

CONCLUSION: There is no conclusive evidence of an increased risk of first hemorrhage during pregnancy from bAVM. Because advice to women with bAVM may influence the management of pregnancy or bAVM with significant consequences, we believe that a retrospective multicenter, case crossover study is urgently required.

Transdural arterial recruitment to brain arteriovenous malformation

J Neurosurg 127:51–58, 2017

The occurrence of transdural arterial recruitment (TDAR) in association with brain arteriovenous malformation (bAVM) is uncommon, and the reason for TDAR is not understood. The aim of this cohort study was to examine patient and bAVM characteristics associated with TDAR and the implications of TDAR on management.

METHODS A prospective surgical database of bAVMs was examined. Cases previously treated elsewhere or incompletely examined by digital subtraction angiography (DSA) assessment were excluded. Three studies of this cohort were performed, as follows: characteristics associated with TDAR, the relationship between TDAR and neurological deficits unassociated with hemorrhage (NDUH), and the impact of TDAR on outcome from surgery. Regression models were performed.

RESULTS Of 769 patients with complete DSA who had no previous treatment, 51 (6.6%) were found to have TDAR. The presence of TDAR was associated with increasing age (p < 0.01; OR 1.05; 95% CI 1.02–1.07); presentation with NDUH (p < 0.01; OR 2.71; 95% CI 1.29–5.71); increasing size of the bAVM (p < 0.01; OR 1.57; 95% CI 1.29–1.91); and combined supply from both anterior and posterior circulations (p = 0.02; OR 2.37; 95% CI 1.17–4.78). Further analysis of TDAR cases comparing those with and without NDUH found an association of larger size (6.6 cm [2.9 SD] compared with 4.7 cm [1.8 SD]; p < 0.01) and combined supply from both anterior and posterior circulations (relative risk 2.5; 95% CI 1.0–6.2; p = 0.04) to be associated with an NDUH presentation. For the 632 patients undergoing surgery there was an increased risk of complications (where this produced a new permanent neurological deficit at 12 months represented by a modified Rankin Scale score of > 1) with the following variables: size; location in eloquent brain; deep venous drainage; increasing age; and no presentation with hemorrhage. The presence of TDAR was not associated with an increased risk of complications from surgery.

CONCLUSIONS The authors found that TDAR occurs in older patients with larger bAVMs, and that TDAR is also more likely to be associated with bAVMs presenting with NDUH. The likely explanation for the presence of TDAR is a secondary recruitment arising as a consequence of shear stress, rather than a primary vascular supply present from the earliest development of the bAVM.

Microsurgery for cerebral arteriovenous malformations: subgroup outcomes in a consecutive series of 288 cases

J Neurosurg 126:1056–1063, 2017

The objective of this study was to review the outcomes after microsurgical resection of cerebral arteriovenous malformations (AVMs) from a consecutive single-surgeon series. Clinical and imaging data were analyzed to address the following questions concerning AVM treatment in the post-ARUBA (A Randomized Trial of Unruptured Brain Arteriovenous Malformations) era. 1) Are the patients who present with unruptured or ruptured AVMs doing better at long-term follow-up? 2) Is the differentiation between Ponce Class A (Spetzler-Martin Grade I and II) patients versus Ponce Class B and C patients (Spetzler-Martin Grade III and IV) meaningful and applicable to surgical practice? 3) How did the ARUBA-eligible patients of this surgical series compare with the results reported in ARUBA?

METHODS Two hundred eighty-eight patients with cerebral AVMs underwent microsurgical resection between 1983 and 2012 performed by the same surgeon (J.S.). This is a prospective case collection study that represents a consecutive series. The results are based on prospectively collected, early-outcome data that were supplemented by retrospectively collected, follow-up data for 94% of those cases. The analyzed data included the initial presentation, Spetzler-Martin grade, obliteration rates, surgical and neurological complications, and frequency of pretreatment with embolization or radiosurgery. The total cohort was compared using “small-AVM,” Spetzler-Martin Grade I and II, and ARUBA-eligible AVM subgroups.

RESULTS The initial presentation was hemorrhage in 50.0% and seizures in 43.1% of patients. The series included 53 Spetzler-Martin Grade I (18.4%), 114 Spetzler-Martin Grade II (39.6%), 90 Spetzler-Martin Grade III (31.3%), 28 Spetzler- Martin Grade IV (9.7%), and 3 Spetzler-Martin Grade V (1.0%) AVMs. There were 144 unruptured and 104 ARUBAeligible cases. Preembolization was used in 39 cases (13.5%). The occlusion rates for the total series and small AVM subgroup were 99% and 98.7%, respectively. The mean follow-up duration was 64 months. Early neurological deterioration was seen in 39.2% of patients, of which 12.2% had permanent and 5.6% had permanent significant deficits, and the mortality rate was 1.7% (n = 5). Outcome was better for patients with AVMs smaller than 3 cm (permanent deficit in 7.8% and permanent significant deficit in 3.2% of patients) and Ponce Class A status (permanent deficit in 7.8% and significant deficit in 3.2% of patients). Unruptured AVMs showed slightly higher new deficit rates (but 0 instances of mortality) among all cases, and in the small AVM and Ponce Class A subgroups. Unruptured Spetzler-Martin Grade I and II lesions had the best outcome (1.8% permanent significant deficit), and ARUBA-eligible Spetzler-Martin Grade I and II lesions had a slightly higher rate of permanent significant deficits (3.2%).

CONCLUSIONS Microsurgery has a very high cure rate. Focusing microsurgical AVM resection on unruptured lesions smaller than 3 cm or on Spetzler-Martin Grade I and II lesions is a good strategy for minimizing long-term morbidity. Well-selected microsurgical cases lead to better outcomes than with multimodal interventions, as in the ARUBA treatment arm, or conservative treatment alone. Long-term prospective data collection is valuable.

Microsurgery for cerebral arteriovenous malformations: subgroup outcomes in a consecutive series of 288 cases

J Neurosurg 126:1056–1063, 2017

The objective of this study was to review the outcomes after microsurgical resection of cerebral arteriovenous malformations (AVMs) from a consecutive single-surgeon series. Clinical and imaging data were analyzed to address the following questions concerning AVM treatment in the post-ARUBA (A Randomized Trial of Unruptured Brain Arteriovenous Malformations) era. 1) Are the patients who present with unruptured or ruptured AVMs doing better at long-term follow-up? 2) Is the differentiation between Ponce Class A (Spetzler-Martin Grade I and II) patients versus Ponce Class B and C patients (Spetzler-Martin Grade III and IV) meaningful and applicable to surgical practice? 3) How did the ARUBA-eligible patients of this surgical series compare with the results reported in ARUBA?

METHODS Two hundred eighty-eight patients with cerebral AVMs underwent microsurgical resection between 1983 and 2012 performed by the same surgeon (J.S.). This is a prospective case collection study that represents a consecutive series. The results are based on prospectively collected, early-outcome data that were supplemented by retrospectively collected, follow-up data for 94% of those cases. The analyzed data included the initial presentation, Spetzler-Mar-tin grade, obliteration rates, surgical and neurological complications, and frequency of pretreatment with embolization or radiosurgery. The total cohort was compared using “small-AVM,” Spetzler-Martin Grade I and II, and ARUBA-eligible AVM subgroups.

RESULTS The initial presentation was hemorrhage in 50.0% and seizures in 43.1% of patients. The series included 53 Spetzler-Martin Grade I (18.4%), 114 Spetzler-Martin Grade II (39.6%), 90 Spetzler-Martin Grade III (31.3%), 28 Spetzler-Martin Grade IV (9.7%), and 3 Spetzler-Martin Grade V (1.0%) AVMs. There were 144 unruptured and 104 ARUBA-eligible cases. Preembolization was used in 39 cases (13.5%). The occlusion rates for the total series and small AVM subgroup were 99% and 98.7%, respectively. The mean follow-up duration was 64 months. Early neurological deterioration was seen in 39.2% of patients, of which 12.2% had permanent and 5.6% had permanent significant deficits, and the mortality rate was 1.7% (n = 5). Outcome was better for patients with AVMs smaller than 3 cm (permanent deficit in 7.8% and permanent significant deficit in 3.2% of patients) and Ponce Class A status (permanent deficit in 7.8% and significant deficit in 3.2% of patients). Unruptured AVMs showed slightly higher new deficit rates (but 0 instances of mortality) among all cases, and in the small AVM and Ponce Class A subgroups. Unruptured Spetzler-Martin Grade I and II lesions had the best outcome (1.8% permanent significant deficit), and ARUBA-eligible Spetzler-Martin Grade I and II lesions had a slightly higher rate of permanent significant deficits (3.2%).

CONCLUSIONS Microsurgery has a very high cure rate. Focusing microsurgical AVM resection on unruptured lesions smaller than 3 cm or on Spetzler-Martin Grade I and II lesions is a good strategy for minimizing long-term morbidity. Well-selected microsurgical cases lead to better outcomes than with multimodal interventions, as in the ARUBA treatment arm, or conservative treatment alone. Long-term prospective data collection is valuable.

Factors Associated With Proximal Intracranial Aneurysms to Brain Arteriovenous Malformations

Factors Associated With Proximal Intracranial Aneurysms to Brain Arteriovenous Malformations

Neurosurgery 78:787–792, 2016

The risk of hemorrhage from a brain arteriovenous malformation (bAVM) is increased when an associated proximal intracranial aneurysm (APIA) is present. Identifying factors that are associated with APIA may influence the prediction of hemorrhage in patients with bAVM.

OBJECTIVE: To identify patient- and bAVM-specific factors associated with APIA.

METHODS: We analyzed a prospective database of bAVMs for factors associated with the presence of APIA. Factors analyzed included age, sex, bAVM size, aneurysm size, circulation contributing to the bAVM, location of the aneurysm, deep venous drainage, and Spetzler-Ponce categories. Multiple logistic regression was performed to identify an association with APIA.

RESULTS: Of 753 cases of bAVM with complete angiographic surveillance, 67 (9%) were found to have APIA. Older age (continuous variable; odds ratio, 1.04; 95% confidence interval, 1.02-1.05) and posterior circulation supply to the bAVM (odds ratio, 2.29; 95% confidence interval, 1.32-3.99) were factors associated with increased detection of APIA. The association of posterior circulation–supplied bAVM was not due to infratentorial bAVM location because 72% of posterior circulation APIAs were supplying supratentorial bAVM.

CONCLUSION: APIAs appear to develop with time, as evident from the increased age for those with APIAs. Furthermore, they were more likely present in bAVMs supplied by the posterior circulation. This may be due to a difference in hemodynamic stress.

Clinical experience with navigated 3D ultrasound angiography (power Doppler) in microsurgical treatment of brain arteriovenous malformations

Clinical experience with navigated 3D ultrasound angiography (power Doppler) in microsurgical treatment of brain arteriovenous malformations

Acta Neurochir (2016) 158:875–883

We have previously described a method that has the potential to improve surgery of arteriovenous malformations (AVMs). In the present paper, we present our clinical results.

Materials and methods Of 78 patients referred for AVMs to our University Hospital from our geographical catchment region from 2005 through 2013, 31 patients were operated on with microsurgical technique. 3D MR angiography (MRA) with neuronavigation was used for planning. Navigated 3D ultrasound angiography (USA) was used to identify and clip feeders in the initial phase of the operation. None of our patients was embolized preoperatively as part of the surgical procedure. The niduses were extirpated based on the 3D USA. After extirpation, controls were done with 3D USA to verify that the AVMs were completely removed. The Spetzler three-tier classification of the patients was: A: 21, B: 6, C: 4.

Results Sixty-eight feeders were identified on preoperative MRA and DSA and 67 feeders were identified and clipped by guidance of intraoperative 3D USA. Six feeders identified preoperatively were missed by 3D USA, while five preoperatively unknown feeders were found and clipped. The overall average bleeding was 440 ml. There was a significant reduction in average bleeding in the last 15 operations compared to the first 16 (340 vs. 559 ml, p = 0.019). We had no serious morbidity (GOS 3 or less). New deficits due to surgery were two patients with quadrantanopia (one class B and one class C), the latter (C) also acquired epilepsy. One patient (class A) acquired a hardly noticeable paresis in two fingers. One hundred percent angiographic cure was achieved in all patients, as evaluated by postoperative DSA.

Conclusions Navigated intraoperative 3D USA is a useful tool to identify and clip AVM feeders. Microsurgical extirpation assisted by navigated 3D USA is an effective and safe method for removing AVMs.

Transdural indocyanine green video-angiography of vascular malformations

Transdural indocyanine green video-angiography of vascular malformations

Acta Neurochir (2014) 156:1761–1767

The role of indocyanine green videoangiography (ICG-VA) in the surgical resection of vascular malformations has been largely described; conversely, the utility of ICG-VA before dural opening (transdural ICG-VA) in this situation remains unclear. The aim of this study is to present the application of transdural ICG-VA in a consecutive series of patients in order to explore the potential provided by a transdural visualisation of vascular malformations.

Method We retrospectively analysed the application of intraoperative ICG-VA before dural opening in 15 consecutive patients who underwent surgical resection of vascular malformations. The cases included 12 cerebral arterio-venous malformations (AVMs), 2 cerebral dural arterio-venous fistulas (dAVFs) and 1 spinal arterio-venous fistula (AVF).

Results ICG-VA before dural opening allowed the visualisation of the site and extension of the malformation in 13 out of 15 cases, whilst arterial feeders and venous drainages were identified in 9 out of 15 cases. In two patients with dAVF, the point of fistula could be transdurally identified through ICGVA. In 14% of cases, the size of bone flap designed on neuronavigation data was then modified according to transdural ICG-VA findings.

Conclusions Transdural ICG-VA proved an efficient tool that allows optimising the exposure of the malformation, performing a safe dural opening and identifying dural vascular connections of the lesion.

Temporal Lobe Arteriovenous Malformations: Surgical Outcomes With a Focus on Visual Field Defects and Epilepsy

Temporal lobe AVM

Neurosurgery 73:854–862, 2013

Temporal lobe arteriovenous malformations (AVMs) represent a subgroup of intracranial AVMs with particular characteristics and management issues.

OBJECTIVE: To characterize the surgical outcomes of temporal lobe AVMs with emphasis on visual field deficits (VFDs) and seizures.

METHODS: Between 1992 and 2008, 29 patients were operated on for temporal lobe AVMs. Patient data were retrospectively collected and analyzed.

RESULTS: Twelve of 29 patients (41.4%) presented with seizures and 4 (13.7%) presented with VFDs. Postoperatively, 6 patients (24%) showed new VFDs and 2 improved, with a rate of preservation of full visual fields of 84%. Larger AVMs (.3 cm) were significantly associated with postoperative VFD (P = .008). Epilepsy outcomes assessed by the Engel scale were as follows: 9 patients (75%) were in class I (seizure free), 1 patient (8.3%) was in class III, and 2 patients (16.6%) were in class IV (no change or worsening). Postoperative modified Rankin Scale outcomes were excellent (grade 0-1) in 18 patients, good (grade 2) in 7, and poor (grade 3-4) in 4. Older age at diagnosis correlated with a worse functional outcome (Spearman r = 0.369; P = .049). AVMs were totally removed in 27 of 29 patients (93.1%). Complete surgical excision was confirmed with angiography. Two patients needed reoperation for AVM remnant. Three patients had persistent hemiparesis (10.3% permanent morbidity). There was no mortality.

CONCLUSION: Seizure control is usually underappreciated in the surgical management of AVMs. However, in temporal lobe AVMs, good outcomes with low morbidity and good visual field preservation can be accomplished.