Michael Kerin Morgan, Nirav J. Patel, Mary Simons, Elizabeth Anne Ritson and Gillian Z. Heller
Case reports suggest that young age is a critical factor in determining recurrence of brain arteriovenous malformations (AVMs) after surgery. However, other factors that may contribute to the increased risk of recurrence have not been considered. In this study, the authors' goal was to ascertain the risk and risk factors of recurrence after resection of AVMs of the brain.
A consecutive case series (prospectively collected data) of 600 cases of resection of brain AVMs was retrospectively analyzed. Radiological evidence of recurrence or nonrecurrence, as well as clinical evidence of recurrence, could be established in 427 of these cases that underwent follow-up for more than 350 days after initial surgery. These cases were analyzed using Kaplan-Meier curves and Cox regression with respect to age and the presence of deep venous drainage.
Nine recurrent AVMs were found in 8 patients. By analysis of the Kaplan-Meier curves, the 10-year recurrence rate was 14% for those with deep venous drainage, compared with 4% for those without deep venous drainage. Stratifying by age, in the 0- to 20-year age group, the 10-year recurrence rates were 63% and 13% for those with and without deep venous drainage, respectively. In the 20- to 39-year age group, the rates were 5% and 0% respectively, and in the 40-year and older age group they were 0% and 3%, respectively. The hazard ratio for deep venous drainage, adjusted for age, was 5.97 (95% CI 1.20–29.69, p = 0.029).
The risk of recurrence after AVM resection is significant for young patients with deep venous drainage.
Michael K. Morgan, Markus K. Hermann Wiedmann, Marcus A. Stoodley and Gillian Z. Heller
The purpose of this study was to adapt and apply the extended definition of favorable outcome established for Gamma Knife radiosurgery (GKRS) to surgery for brain arteriovenous malformations (bAVMs). The aim was to derive both an error around the point estimate and a model incorporating angioarchitectural features in order to facilitate comparison among different treatments.
A prospective microsurgical cohort was analyzed. This cohort included patients undergoing embolization who did not proceed to microsurgery and patients denied surgery because of perceived risk of treatment. Data on bAVM residual and recurrence during long-term follow-up as well as complications of surgery and preoperative embolization were analyzed. Patients with Spetzler-Ponce Class C bAVMs were excluded because of extreme selection bias. First, patients with a favorable outcome were identified for both Class A and Class B lesions. Patients were considered to have a favorable outcome if they were free of bAVM recurrence or residual at last follow-up, with no complication of surgery or preoperative embolization, and a modified Rankin Scale score of more than 1 at 12 months after treatment. Patients who were denied surgery because of perceived risk, but would otherwise have been candidates for surgery, were included as not having a favorable outcome. Second, the authors analyzed favorable outcome from microsurgery by means of regression analysis, using as predictors characteristics previously identified to be associated with complications. Third, they created a prediction model of favorable outcome for microsurgery dependent upon angioarchitectural variables derived from the regression analysis.
From a cohort of 675 patients who were either treated or denied surgery because of perceived risk of surgery, 562 had Spetzler-Ponce Class A or B bAVMs and were included in the analysis. Logistic regression for favorable outcome found decreasing maximum diameter (continuous, OR 0.62, 95% CI 0.51–0.76), the absence of eloquent location (OR 0.23, 95% CI 0.12–0.43), and the absence of deep venous drainage (OR 0.19, 95% CI 0.10–0.36) to be significant predictors of favorable outcome. These variables are in agreement with previous analyses of microsurgery leading to complications, and the findings support the use of favorable outcome for microsurgery. The model developed for angioarchitectural features predicts a range of favorable outcome at 8 years following microsurgery for Class A bAVMs to be 88%–99%. The same model for Class B bAVMs predicts a range of favorable outcome of 62%–90%.
Favorable outcome, derived from GKRS, can be successfully used for microsurgical cohort series to assist in treatment recommendations. A favorable outcome can be achieved by microsurgery in at least 90% of cases at 8 years following microsurgery for patients with bAVMs smaller than 2.5 cm in maximum diameter and, in the absence of either deep venous drainage or eloquent location, patients with Spetzler-Ponce Class A bAVMs of all diameters. For patients with Class B bAVMs, this rate of favorable outcome can only be approached for lesions with a maximum diameter just above 6 cm or smaller and without deep venous drainage or eloquent location.
David Bervini, Michael Kerin Morgan, Elizabeth Anne Ritson and Gillian Heller
The aim of this study was to identify patients who are likely to benefit from surgery for unruptured brain arteriovenous malformations (ubAVMs).
The authors' database was interrogated for the risk and outcome of hemorrhage after referral and the outcome from surgery. Furthermore, the outcome from surgery incorporated those cases excluded from surgery because of perceived greater risk (sensitivity analysis). Finally, a comparison was made for the authors' patients between the natural history and surgery. Data were collected for 427 consecutively enrolled patients with ubAVMs in a database that included patients who were conservatively managed. Kaplan-Meier analysis was performed on patients observed for more than 1 day to determine the risk of hemorrhage. Variables that may influence the risk of first hemorrhage were assessed using Cox proportional hazard regression models and Kaplan-Meier life table analyses from referral until the first occurrence of the following: hemorrhage, treatment, or last review. The outcome from surgery (leading to a new permanent neurological deficit with last review modified Rankin Scale [mRS] score > 1) was determined. Further sensitivity analysis was made to predict risk from surgery for the total ubAVM cohort by incorporating outcomes of surgical cases as well as cases excluded from surgery because of perceived risk, and assuming an adverse outcome for these excluded cases.
A total of 377 patients with a ubAVM were included in the analysis of the risk of hemorrhage. The 5-year risk of hemorrhage for ubAVM was 11.5%. Hemorrhage resulted in an mRS score > 1 in 14 cases (88% [95% CI 63%–98%]). Patients with Spetzler-Ponce Class A ubAVMs treated by surgery (n = 190) had a risk from surgery of 1.6% (95% CI 0.3%–4.8%) for a permanent neurological deficit leading to an mRS score > 1 and 0.5% (95% CI < 0.1%–3.2%) for a permanent neurological deficit leading to an mRS score > 2. Patients with Spetzler-Ponce Class B ubAVMs treated by surgery (n = 107) had a risk from surgery of 14.0% (95% CI 8.6%–22.0%) for a permanent neurological deficit leading to an mRS score > 1. Sensitivity analysis of Spetzler-Ponce Class B ubAVMs, including those in patients excluded from surgery, showed that the true risk for surgically eligible patients may have been as high as 15.6% (95% CI 9.9%–23.7%) for mRS score > 1, had all patients who were perceived to have a greater risk experienced an adverse outcome. Patients with Spetzler-Ponce Class C ubAVMs treated by surgery (n = 44) had a risk from surgery of 38.6% (95% CI 25.7%–53.4%) for a permanent neurological deficit leading to an mRS score > 1. Sensitivity analysis of Class C ubAVMs, including those harbored by patients excluded from surgery, showed that the true risk for surgically eligible patients may have been as high as 60.9% (95% CI 49.2%–71.5%) for mRS score > 1, had all patients who were perceived to have a greater risk experienced an adverse outcome.
Surgical outcomes for Spetzler-Ponce Class A ubAVMs are better than those for conservative management.
David Bervini, Michael Kerin Morgan, Marcus Andrew Stoodley and Gillian Ziona Heller
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.
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.
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.
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.
Michael Kerin Morgan, Markus Karl Hermann Wiedmann, Nazih N. A. Assaad, Michael J. A. Parr and Gillian Z. Heller
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+).
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.
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.
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.