Risk of First Hemorrhage of Brain Arteriovenous Malformations During Pregnancy: A Systematic Review of the Literature.

BACKGROUND: 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 quantitative 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 definitions 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.

Laminar Wall Shear Stress in Brain Arteriovenous Malformations: Systematic Review of Literature.

BACKGROUND: Laminar wall sheer stress (LWSS) modulates inflammatory activity of the endothelium and may be a contributing factor in many cerebrovascular pathologies. There is a lack of consensus whether significant differences in LWSS exist between feeding vessels in brain arteriovenous malformation (bAVM) and healthy vessels. A systematic review of LWSS research in bAVM was undertaken, including the methods used and the assumptions made in determining LWSS. METHODS: Ovid MEDLINE, EMBASE, and Scopus electronic databases were systematically searched from inception for articles calculating LWSS in bAVM cases. LWSS values were extracted for comparison between ipsilateral bAVM feeding arteries and healthy contralateral vessels or healthy normative data. RESULTS: Three retrospective cohort studies were identified, reporting on 42 adult and pediatric bAVM cases. Mean LWSS (mLWSS) in healthy vessels (contralateral vessels or normative controls) typically ranged from 1.2-2.7 Pa, while mLWSS values in untreated bAVM feeding arteries typically ranged from 1.6-3.6 Pa. All studies had mixed cohorts of ruptured and unruptured cases, obscuring the relationship between LWSS and bAVM history. CONCLUSIONS: mLWSS values in healthy arteries and bAVM feeding vessels tend to be low and overlapping. Further research of high scientific and methodologic quality is necessary to improve understanding of how LWSS hemodynamics relate to bAVM formation, rupture, and treatment.

Kinked Perforator Due to Clipping of Parent Vessel Aneurysm: Technical Note and Lessons Learned.

BACKGROUND: Adverse outcomes after aneurysm clipping can be potentially reversible, when managed appropriately. METHODS: This is a case report describing kinking of a perforator due to clipping of parent vessel aneurysm. RESULTS: Complete recovery of a high-grade motor deficit was achieved after instant reintervention with application of smaller clips in combination with gelfoam soaked in papaverine. CONCLUSION: Use of evoked potentials and intraoperative digital subtraction angiography are recommended and may help in preclinical diagnosis. Knowledge of delayed perforator kinking as a complication may lead to a more rapid diagnosis and management.

Results of Surgery for Low-Grade Brain Arteriovenous Malformation Resection by Early Career Neurosurgeons: An Observational Study.

BACKGROUND: For sustainability of arteriovenous malformation (AVM) surgery, results from early career cerebrovascular neurosurgeons (ECCNs) must be acceptably safe. OBJECTIVE: To determine whether ECCNs performance of Spetzler-Ponce Class A AVM (SPC A) resection can be acceptably safe. METHODS: ECCNs completing a cerebrovascular fellowship (2004-2015) with the last author were included. Inclusion of the ECCN cases occurred if they: had a prospective database of all AVM cases since commencing independent practice; were the primary surgeon on SPC A; and had made the significant management decisions. All SPC A surgical cases from the beginning of the ECCN's independent surgical practice to a maximum of 8 yr were included. An adverse outcome was considered a complication of surgery leading to a new permanent neurological deficit with a last modified Rankin Scale score >1. A cumulative summation (Cusum) plot examined the performance of each surgery. The highest acceptable level of adverse outcomes for the Cusum was 3.3%, derived from the upper 95% confidence interval of the last author's reported series. RESULTS: Six ECCNs contributed 110 cases for analysis. The median number of SPC A cases operated by each ECCN was 16.5 (range 4-40). Preoperative embolization was performed in 5 (4.5%). The incidence of adverse outcomes was 1.8% (95% confidence interval: <0.01%-6.8%). At no point during the accumulated series did the combined cohort become unacceptable by the Cusum plot. CONCLUSION: ECCNs with appropriate training appointed to large-volume cerebrovascular centers can achieve results for surgery for SPC A that are not appreciably worse than those published from high-volume neurosurgeons.

De novo brain arteriovenous malformation after tumor resection: case report and literature review.

The congenital origin of brain arteriovenous malformations (bAVMs) has been increasingly challenged by reports of de novo bAVMs in patients previously confirmed to have no vascular malformation. We describe the oldest patient reported in the English language literature harboring a de novo bAVM. An uneventful frontal convexity meningioma resection was performed for a 60-year-old woman, and at 67 years of age, a bAVM was detected by MRI and confirmed by digital subtraction angiography at the site of the previous meningioma resection. This case adds to the growing literature that the etiology of bAVMs is most likely multifactorial.

Critical review of brain AVM surgery, surgical results and natural history in 2017.

BACKGROUND: An understanding of the present standing of surgery, surgical results and the role in altering the future morbidity and mortality of untreated brain arteriovenous malformations (bAVMs) is appropriate considering the myriad alternative management pathways (including radiosurgery, embolization or some combination of treatments), varying risks and selection biases that have contributed to confusion regarding management. The purpose of this review is to clarify the link between the incidence of adverse outcomes that are reported from a management pathway of either surgery or no intervention with the projected risks of surgery or no intervention. METHODS: A critical review of the literature was performed on the outcomes of surgery and non-intervention for bAVM. An analysis of the biases and how these may have influenced the outcomes was included to attempt to identify reasonable estimates of risks. RESULTS: In the absence of treatment, the cumulative risk of future hemorrhage is approximately 16% and 29% at 10 and 20 years after diagnosis of bAVM without hemorrhage and 35% and 45% at 10 and 20 years when presenting with hemorrhage (annualized, this risk would be approximately 1.8% for unruptured bAVMs and 4.7% for 8 years for bAVMs presenting with hemorrhage followed by the unruptured bAVM rate). The cumulative outcome of these hemorrhages depends upon whether the patient remains untreated and is allowed to have a further hemorrhage or is treated at this time. Overall, approximately 42% will develop a new permanent neurological deficit or death from a hemorrhagic event. The presence of an associated proximal intracranial aneurysm (APIA) and restriction of venous outflow may increase the risk for subsequent hemorrhage. Other risks for increased risk of hemorrhage (age, pregnancy, female) were examined, and their purported association with hemorrhage is difficult to support. Both the Spetzler-Martin grading system (and its compaction into the Spetzler-Ponce tiers) and Lawton-Young supplementary grading system are excellent in predicting the risk of surgery. The 8-year risk of unfavorable outcome from surgery (complication leading to a permanent new neurological deficit with a modified Rankin Scale score of greater than one, residual bAVM or recurrence) is dependent on bAVM size, the presence of deep venous drainage (DVD) and location in critical brain (eloquent location). For patients with bAVMs who have neither a DVD nor eloquent location, the 8-year risk for an unfavorable outcome increases with size (increasing from 1 cm to 6 cm) from 1% to 9%. For patients with bAVM who have either a DVD or eloquent location (but not both), the 8-year risk for an unfavorable outcome increases with the size (increasing from 1 cm to 6 cm) from 4% to 35%. For patients with bAVM who have both a DVD and eloquent location, the 8-year risk for unfavorable outcome increases with size (increasing from 1 cm to 3 cm) from 12% to 38%. CONCLUSION: Patients with a Spetzler-Ponce A bAVM expecting a good quality of life for the next 8 years are likely to do better with surgery in expert centers than remaining untreated. Ongoing research is urgently required on the outcome of management pathways for bAVM.

Deliberate employment of postoperative hypotension for brain arteriovenous malformation surgery and the incidence of delayed postoperative hemorrhage: a prospective cohort study.

OBJECTIVE The aim of this study was to examine the impact of deliberate employment of postoperative hypotension on delayed postoperative hemorrhage (DPH) for all Spetzler-Ponce Class (SPC) C brain arteriovenous malformations (bAVMs) and SPC B bAVMs ≥ 3.5 cm in diameter (SPC B 3.5+). METHODS A protocol of deliberate employment of postoperative hypotension was introduced in June 1997 for all SPC C and SPC B 3.5+ bAVMs. The aim was to achieve a maximum mean arterial blood pressure (BP) ≤ 70 mm Hg (with cerebral perfusion pressure > 50 mm Hg) for a minimum of 7 days after resection of bAVMs (BP protocol). The authors compared patients who experienced DPH (defined as brain hemorrhage into the resection bed that resulted in a new neurological deficit or that resulted in reoperation during the hospitalization for microsurgical bAVM resection) between 2 periods (prior to adopting the BP protocol and after introduction of the BP protocol) and 4 bAVM categories (SPC A, SPC B 3.5- [that is, SPC B < 3.5 cm maximum diameter], SPC B 3.5+, and SPC C). Patients excluded from treatment by the BP protocol were managed in the intensive care unit to avoid moderate hypertensive episodes. The pooled cases of all bAVM treated by surgery were analyzed to identify characteristics associated with the risk of DPH. These identified characteristics were then examined by multiple logistic regression analysis in both SPC B 3.5+ and SPC C cases. RESULTS From a cohort of 641 bAVMs treated by microsurgery, 32 patients with DPH were identified. Of those, 66% (95% CI 48-80) had a permanent new neurological deficit with a modified Rankin Scale score of 2-6. This included a mortality rate of 13% (95% CI 4.4-29). The BP protocol was used to treat 162 patients with either SPC B 3.5+ or SPC C. For SPC B 3.5+, there was no significant reduction in DPH with the introduction of the BP protocol (p = 0.77). For SPC C, there was a significant (p = 0.035) reduction of DPH from 29% (95% CI 13%-53%) to 8.2% (95% CI 3.2%-18%) associated with the introduction of the BP protocol. Multiple logistic regression analysis found that the absence of the BP protocol (p = 0.011, odds ratio 7.5, 95% CI 1.6-36) remained significant for the development of DPH in patients with SPC C bAVMs. CONCLUSIONS Treating patients with SPC C bAVMs with a protocol that lowers BP immediately after resection seems to reduce the risk of DPH. For SPC A and SPC B 3.5- bAVMs, there is unlikely to be a need to do more than avoid postoperative hypertension. For SPC B 3.5+ bAVMs, a larger number of patients would be required to test the absence of benefit of the BP protocol.

Complication-Effectiveness Analysis for Unruptured Intracranial Aneurysm Surgery: A Prospective Cohort Study.

BACKGROUND: The aim of intervention for unruptured intracranial aneurysms (UIAs) is safe, effective treatment. OBJECTIVE: To analyze a prospective database for variables influencing the risk of surgery to produce a risk model adjusting this risk for effectively treated aneurysms. METHODS: First, we identified variables to create a model from multiple logistic regression for complications of surgery leading to a 12-month modified Rankin Scale score >1. Second, we established the long-term cumulative incidence of freedom from retreatment or rupture (treated aneurysm) from Kaplan-Meier analysis. Third, we combined these analyses to establish a model of risk of surgery per effective treatment. RESULTS: One thousand twelve patients with 1440 UIA underwent 1080 craniotomies. We found that 10.1% (95% confidence interval [CI], 8.4-12.0) of craniotomies resulted in a complication leading to a modified Rankin Scale score >1 at 12 months. Logistic regression found age (odds ratio, 1.04; 95% CI, 1.02-1.06), size (odds ratio, 1.12; 95% CI, 1.09-1.15), and posterior circulation location (odds ratio, 2.95; 95% CI, 1.82-4.78) to be significant. Cumulative 10-year risk of retreatment or rupture was 3.0% (95% CI, 1.3-7.0). The complication-effectiveness model was derived by dividing the complication risk by the 10-year cumulative freedom from retreatment or rupture proportion. Risk per effective treatment ranged from 1% for a 5-mm anterior circulation UIA in a 20-year-old patient to 70% for a giant posterior circulation UIA in a 70-year-old patient. CONCLUSION: Complication-effectiveness analyses increase the information available with regard to outcome for the management of UIAs.

Factors Associated With Proximal Intracranial Aneurysms to Brain Arteriovenous Malformations: A Prospective Cohort Study.

BACKGROUND: 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. ABBREVIATIONS: APIA, associated proximal intracranial aneurysmbAVM, brain arteriovenous malformationDSA, digital subtraction angiographySMG, Spetzler-Martin gradeSPC, Spetzler-Ponce category.

Complication-Effectiveness Analysis for Brain Arteriovenous Malformation Surgery: A Prospective Cohort Study.

BACKGROUND: Intervention for brain arteriovenous malformations (bAVMs) should aim at treatment that is safe and effective. OBJECTIVE: To analyze a prospective database to derive the probability of neurological deficit and adjust this risk for effectively treated bAVMs (complication-effectiveness analysis [CEA]). METHODS: First, we calculated the percentage of surgical complications leading to a modified Rankin Scale >1 at 12 months after surgery for each Spetzler-Ponce class (SPC). Second, we performed a sensitivity analysis of these results by including bAVMs not undergoing surgery, to correct for bias. Third, we established the long-term cumulative incidence of freedom from recurrence from Kaplan-Meier analysis. Finally, we combined the results to calculate the risk of surgery per effective treatment in a complication-effectiveness analysis. RESULTS: Seven hundred seventy-nine patients underwent 641 microsurgical resections. Complications of surgery leading to a modified Rankin Scale >1 at 12 months occurred in 1.4% (95% confidence interval [CI]: 0.5-3.3), 20% (95% CI: 15-26), and 41% (95% CI: 30-52) of SPC A, SPC B, and SPC C, respectively. The cumulative 9-year freedom from recurrence was 97% for SPC A and 92% for other bAVMs. The 9-year CEA risk was 1.4% (credible range: 0.5%-3.4%) for SPC A, 22% to 24% (credible range: 16%-31%) for SPC B, and 45% to 63% (credible range: 33%-73%) for SPC C bAVM. CONCLUSION: CEA presents the treatment outcome in the context of efficacy and provides a basis for comparing outcomes from techniques with different times to elimination of the bAVM. ABBREVIATIONS: bAVM, brain arteriovenous malformationCEA, complication-effectiveness analysisCI, confidence intervalCTA, computerized tomographic angiographyDSA, digital subtraction angiographyMRA, magnetic resonance angiographymRS, modified Rankin ScaleSMG, Spetzler-Martin gradeSPC, Spetzler-Ponce class.

How does the participation of a resident surgeon in procedures for small intracranial aneurysms impact patient outcome?

OBJECT: In this paper the authors' goal was to evaluate whether resident neurosurgeons participating in entry-level aneurysm surgery have a negative impact on patient outcomes. METHODS: The authors searched the database for entry-level aneurysm surgeries (that is, those < or =10 mm and located in the internal carotid artery [beyond the paraclinoid segment] and middle cerebral artery) performed in 1991 through 2005. The presence or absence of an advanced resident (in his/her last 3 years of residency) was noted. The analysis was examined in 3-year quintiles. A total of 355 cases (196 with resident participation and 159 without) were evaluated. Permanent adverse outcomes were seen in 11 patients (3.1% of the total study population), all due to branch artery occlusion. The incidence of permanent adverse outcomes in the first 3 years was 10.7% and 2.4% thereafter. This difference was statistically significant (p = 0.015). There was no difference in the incidence of adverse outcomes when comparing surgery performed with and without participation of an advanced resident. CONCLUSIONS: In this study the authors have demonstrated a learning curve in this series of patients. This study also suggests that involving residents in the repair of small unruptured aneurysms will not compromise patient care. In addition, patients can be informed that the team approach to their surgery is at least as good as having the experienced surgeon performing all aspects of the surgery.