Neurosurgery Blog


Daily bibliographic review of the Neurosurgery Department. La Fe University Hospital. Valencia, Spain

Clinical Experience and Results of Microsurgical Resection of Arteriovenous Malformation in the Presence of Space-Occupying Intracerebral Hematoma

Neurosurgery 81:75–86, 2017

Management of ruptured arteriovenous malformations (AVMs) with a mass-producing intracerebral hematoma (ICH) represents a surgical dilemma.

OBJECTIVE: To evaluate the clinical outcome and obliteration rates of microsurgical resection of AVM when performed concomitantly with evacuation of an associated spaceoccupying ICH.

METHODS: Data of patients with AVMwere collected prospectively. Cases were identified in which an AVM was resected and an associated space-occupying ICH was evacuated at the same time, and divided into “group 1,” in which the surgery was performed acutely within 48 h of presentation (secondary to elevated intracranial pressure); and “group 2,” in which selected patients were operated upon in the presence of a liquefying ICH in the “subacute”stage. Clinical outcomes were assessed using themodified Rankin Scale, with a score of 0 to 2 considered a good outcome. Obliteration rateswere assessed using postoperative angiography.

RESULTS: From 2001 to 2015, 131 patients underwent microsurgical resection of an AVM, of which 65 cases were included. In “group 1” (n = 21; Spetzler-Ponce class A = 13, class B = 5, and class C = 3), 11 of 21 (52%) had a good outcome and in 18 of 19 (95%) of those who had a postoperative angiogramthe AVMswere completely obliterated. In “group 2”(n=44; Spetzler-Ponce class A=33, class B=9, and class C=2), 31 of 44 (93%) had a good outcome and 42 of 44 (95%) were obliterated with a single procedure. For supratentorial AVMs, the ICH cavity was utilized to provide an operative trajectory to a deep AVM in 11 cases, and in 26 cases the ICH cavity was deep to the AVM and hence facilitated the deep dissection of the nidus.

CONCLUSION: In selected patients the presence of a liquefying ICH cavity may facilitate the resection of AVMs when performed in the subacute stage resulting in a good neurological outcome and high obliteration rate.

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.

Volume-Staged Stereotactic Radiosurgery for Intracranial Arteriovenous Malformations

Neurosurgery 80:543–550, 2017

Radiation-based treatment options of large intracranial arteriovenous malformations (AVM) must balance the likelihood of obliteration with the risk of adverse radiation effects (ARE).
OBJECTIVE: To analyze the efficacy and risks of volume-staged stereotactic radiosurgery (VS-SRS) for AVM.

METHODS: Retrospective study of 34 AVM patients having VS-SRS between 1997 and 2012. A median of 2 stages (range, 2-4) was used to treat a median AVM volume of 22.2 cm3 (range, 7.4-56.7). The median AVM margin dose was 16 Gy (range, 14-18); the median radiosurgery- based AVM score was 2.81 (range, 1.54-6.45). The median follow-up after VS-SRS was 8.2 years (range, 3-13.3).

RESULTS: Nidus obliteration was noted in 18 patients (53%) after VS-SRS. The rate of obliteration was 14% at 3 years, 54% at 5 years, and 75% at 7 years. Six patients (18%) had 11 bleeds after VS-SRS. Two patients (6%) remained neurologically stable, 2 (6%) patients had significant deficits, and 2 patients (6%) died. The actuarial risk of a first bleed after VS-SRS was 6% at 1 year, 12% at 3 years, and 19% at 7 years. Six patients (18%) underwent repeat SRS; all achieved nidus obliteration for an overall cure rate of 71%. Two patients (6%) had a permanent ARE after VS-SRS or repeat SRS.

CONCLUSION: VS-SRS permitted large volume intracranial AVM to be treated with a low rate of ARE. Further study is needed on dose escalation and decreasing the treatment volume per stage to determine if this will increase the rate of obliteration with this technique.

Staged-Volume Radiosurgery of Large Arteriovenous Malformations Improves Outcome by Reducing the Rate of Adverse Radiation Effects

Neurosurgery 80:180–192, 2017

The treatment of large arteriovenous malformations (AVMs) remains challenging. Recently, staged-volume radiosurgery (SVRS) has become an option.

OBJECTIVE: To compare the outcome of SVRS on large AVMs with our historical, single- stage radiosurgery (SSRS) series.

METHODS: We have been prospectively collecting data of patients treated by SVRS since 2007. There were 84 patients who had a median age of 37 years (range, 9-62 years) who were treated until July 2013. The outcomes of 76 of those who had follow-ups available were analyzed and compared with the outcomes of 122 patients treated with the best SSRS technique.

RESULTS: There were 21.5% of AVMs that were deep seated, and 44% presented with hemorrhage resulting in 45% fixed neurological deficit. There were 14% of patients who had undergone embolization before radiosurgery. The median nidus treatment volume was 19.7 cm 3 (6.65-68.7) and 17.5 Gy (13-22.5) prescription isodose was given. Of the 44 lesions having radiological follow-up at 4 years, 61.4% were completely obliterated. Previous embolization (50% with and 63% without) and higher Spetzler-Martin grades appeared to be the negative factors in successful obliteration, but treatment volume was not. Within 3 years after radiosurgery, the annual bleed rates of unruptured and previously ruptured AVMs were 3.2% and 5.6%, respectively. Three bleeds were fatal and 2 resulted in significant modified Rankin scale 3 morbidity. These rates differ little from SSRS. Temporary adverse radiation effects (AREs) did not change significantly, but permanent AREs dropped from 15% to 6.5% (P = .03) compared with SSRS.

CONCLUSION: Obliteration and hemorrhage rates of large AVMs treated by SVRS are similar to historical SSRS. However, SVRS offers a lower rate of AREs.


Long-term Outcomes of Patients With Giant Intracranial Arteriovenous Malformations

giant AVM

Neurosurgery 79:116–124, 2016

Giant intracranial arteriovenous malformations (AVMs) are rare cerebrovascular lesions that pose management challenges.

OBJECTIVE: To further clarify outcomes in patients with giant cerebral AVMs managed with conservative or interventional therapies.

METHODS: We performed a retrospective review of all patients diagnosed with AVMs evaluated at our institution from 1990 to 2013. Patients with a single intracranial AVM .6 cm were included. Patients were divided into 2 groups: conservative management or intervention (microsurgery, radiosurgery, or embolization). Functional outcome was assessed with the modified Rankin Scale (mRS) and compared between the 2 groups.

RESULTS: A total of 55 patients with giant AVMs were included, and 35 patients (63.6%) had clinical follow-up with a mean of 11.8 years. Spetzler-Martin grades were as follows: grade III, n = 2 (3.6%); grade IV, n = 15 (27.3%); and grade V, n = 38 (69.1%). Twenty-four patients (43.6%) were conservatively managed. The patients in the conservatively managed group had larger AVMs (P , .05) with more frequent involvement of the temporal lobe (P = .02). Five patients (26.3%) in the conservatively managed group and 5 (31.3%) in the intervention group experienced hemorrhage during follow-up, translating to an annualized risk of 2.7% and 4.1%, respectively. No significant difference in risk of first subsequent hemorrhage was observed (P = .78). Despite comparable mRS scores at presentation, we observed a trend toward better outcomes (mRS , 2) in patients undergoing conservative management (P = .06) compared with the intervention group at last follow-up.

CONCLUSION: This study suggests that interventions for giant AVMs should be considered cautiously because hemorrhagic risk is similar regardless of management strategy and functional outcome is likely to be same or better in the conservatively managed population.

Semi-quantitative assessment of flow dynamics during indocyanine green video-angiography in the treatment of intracranial dural arteriovenous fistulas

Semi-quantitative assessment of flow dynamics during indocyanine green video-angiography in the treatment of intracranial dural arteriovenous fistulas

Acta Neurochir (2016) 158:1387–1391

Indocyanine green video-angiography (IG-VA) is applied for intraoperative localisation and verification of surgical disconnection of intracranial dural arteriovenous fistulas (iDAVFs).

Method We describe the technique of semiquantitative flow analysis using Flow800 software that implements conventional IG-VA. Our method relies on simple comparison of the fluorescence curves of the exposed vessels, allowing precise localisation of the DAVF draining vein and verification of its surgical disconnection.

Conclusions Semi-quantitative flow analysis with Flow800 software during IG-VA is a reproducible technique that may overcome the limitations of conventional IG-VA in the surgical treatment of DAVFs.

Recurrence of Cerebral Arteriovenous Malformations Following Resection in Adults: Does Preoperative Embolization Increase the Risk?

Recurrence of Cerebral Arteriovenous Malformations Following Resection in Adults- Does Preoperative Embolization Increase the Risk?

Neurosurgery 78:562–571, 2016

Complete surgical resection of arteriovenous malformations (AVMs), documented by postoperative angiography, is generally felt to represent cure, obviating the need for long-term follow-up imaging. Although AVM recurrence has been reported in the pediatric population, this phenomenon has only rarely been documented in adults. Recurrence after treatment solely with embolization, however, has been reported more frequently. Thus, patients undergoing multimodal therapy with surgery following preoperative embolization may also be at higher risk for recurrence.

OBJECTIVE: To determine if preoperative embolization contributes to recurrences of AVMs after complete surgical resection.

METHODS: A retrospective study of patients undergoing AVM resection was performed. Those with complete surgical AVM resection, confirmed by negative early postoperative cerebral angiography and with available follow-up angiographic imaging .6 months postoperatively were included.

RESULTS: Two hundred three patients underwent AVM resection between 1995 and 2012. Seventy-two patients met eligibility criteria. There were 3 recurrences (4%). Deep venous drainage and diffuse type of AVM nidus were significantly associated with recurrence. Although preoperative embolization did not reach statistical significance as an independent risk factor, radiographic data supported its role in every case, with the site of recurrence correlating with deep regions of nidus previously obliterated by embolization.

CONCLUSION: AVM recurrences in the adult population may have a multifactorial origin. Although deep venous drainage and diffuse nidus are clearly risk factors, preoperative embolization may also be a contributing factor with the potential for recurrence of unresected but embolized portions of the AVM. Follow-up angiography at 1 to 3 years appears to be warranted.

Stereotactic Radiosurgery for Arteriovenous Malformations: The Effect of Treatment Period on Patient Outcomes


Neurosurgery 78:499–509, 2016

Stereotactic radiosurgery (SRS) has been performed on patients with cerebral arteriovenous malformations (AVMs) for over 40 years.

OBJECTIVE: To evaluate the impact of treatment period on obliteration, intracranial hemorrhage (ICH), and radiation-induced complications (RICs).

METHODS: Retrospective comparison of 381 AVM patients having SRS during a 20-year period (group 1, January 1990 through March 1997, n = 160; group 2, April 1997 through December 2009, n = 221). The median radiological and clinical follow-up after initial SRS was 77 months and 93 months, respectively.

RESULTS: Obliteration was 59.1% at 4 years and 85.1% at 8 years. Obliteration was more common in patients with hemispheric or cerebellar AVMs (P = .001), smaller prescription isodose volume (PIV) (P < .001), and group 1 patients (P < .001). The ICH rate was 7.7% at 4 years and 10.6% at 8 years. ICH was more common in older patients (P = .02), patients with deep AVM (P = .01), and larger PIV (P < .001). There was no difference in the ICH rate between the treatment groups (P = .18). The rate of permanent RICs was 4.4% at 4 years and 8.6% at 8 years. RICs were more common with larger PIVs (P < .001) and group 1 patients (P = .02). There was no difference in the number of patients having obliteration without new deficits between the 2 treatment periods (68.8% vs 73.3%, P = .33).

CONCLUSION: Advances in SRS procedures over the past 20 years have resulted in a lower risk of RIC, but fewer patients had AVM obliteration. Increasing the prescription dose for patients with medium- and large-volume AVMs by using current conformal dose-planning techniques may improve the obliteration rate while maintaining a low risk of RICs.

Endovascular Management of Deep Arteriovenous Malformations

Endovascular management AVM

Neurosurgery 78:34–41, 2016

The management of arteriovenous malformations (AVMs) in the basal ganglia, insula, and thalamus is demanding for all treatment modalities.

OBJECTIVE: To define safety and outcomes of embolization used as a stand-alone therapy for deep-seated AVMs.

METHODS: A cohort of 22 patients with AVMs located in the basal ganglia, thalamus, and insula who underwent embolization between January 2008 and December 2013.

RESULTS: Eighteen of 22 (82%) patients had anatomic exclusion. The mean size was 2.98 6 1.28 cm, and the mean number of sessions was 2.1 per patient. Most patients presented with hemorrhage (82%, n = 18), and 3 (14%) patients were in a deteriorated neurological status (modified Rankin Scale .2) at presentation. Sixty-eight percent of ruptured AVMs had size #3 cm. A single transarterial approach was performed in 9 (41%) cases, double catheterization was used in 4 (18%), and the transvenous approach was required in 8 (36%) cases. Procedure-related complications were registered in 3 (14%) cases. One death was associated with treatment, and complementary radiosurgery was required in 2 (9%) patients.

CONCLUSION: Embolization therapy appears to be safe and potentially curative for certain deep AVMs. Our results demonstrate a high percentage of anatomic obliteration with rates of complications that may approach radiosurgery profile. In particular, embolization as stand-alone therapy is most suitable to deep AVMs with small nidus size (#3 cm) and/or associated with single venous drainage in which microsurgery might not be indicated.

Safety and Efficacy of Surgical Resection of Unruptured Low-grade Arteriovenous Malformations From the Modern Decade


Neurosurgery 77:948–953, 2015

Recent studies have questioned the utility of surgical resection of unruptured brain arteriovenous malformations (bAVMs).

OBJECTIVE: We performed an assessment of outcomes and complications of surgical resection of low-grade bAVMs (Spetzler-Martin grade I or II) at a single high-volume neurosurgical center.

METHODS: We reviewed all unruptured low-grade bAVMs treated with surgery (with or without preoperative embolization) between January 2004 and January 2014. Stroke rate, mortality, and clinical and radiographic outcomes were examined.

RESULTS: Of 95 patients treated surgically, 85 (25 grade I, 60 grade II) met inclusion criteria, and all achieved radiographic cure postoperatively. Ten patients (11.8%) were lost to follow-up; the mean follow-up of the remaining 85 was 3.3 years. Three patients (3.5%) with grade II bAVMs experienced a stroke; no patients died. Although 20 patients (23.5%) had temporary postoperative neurological deficit, only 3 (3.5%) had new clinical impairment (modified Rankin Scale score $2) at last follow-up. Eight of the 13 patients (61.5%) with preexisting clinical impairment had improved modified Rankin Scale scores of 0 or 1; and 17 of 30 patients (56.7%) with preoperative seizures were seizure-free without antiepileptic medication postoperatively. No significant differences existed in stroke rate or clinical outcome between grades I and II patients at follow-up (Fisher exact test, P = .55 and P . .99, respectively).

CONCLUSION: Surgical resection of low-grade unruptured bAVMs is safe, with a high rate of improvement in functional status and seizure reduction. Although transient postoperative neurological deficit was observed in some patients, permanent treatment- related neurological morbidity was rare.

Posterior interhemispheric transfalcine transprecuneus approach for microsurgical resection of periatrial lesions

posterior interhemispheric transfalcine transprecuneus approach

J Neurosurg 123:1045–1054, 2015

Surgical exposure of the peritrigonal or periatrial region has been challenging due to the depth of the region and overlying important functional cortices and white matter tracts. The authors demonstrate the operative feasibility of a contralateral posterior interhemispheric transfalcine transprecuneus approach (PITTA) to this region and present a series of patients treated via this operative route. Methods Fourteen consecutive patients underwent the PITTA and were included in this study. Pre- and postoperative clinical and radiological data points were retrospectively collected. Complications and extent of resection were reviewed.

Results The mean age of patients at the time of surgery was 39 years (range 11–64 years). Six of the 14 patients were female. The mean duration of follow-up was 4.6 months (range 0.5–19.6 months). Pathology included 6 arteriovenous malformations, 4 gliomas, 2 meningiomas, 1 metastatic lesion, and 1 gray matter heterotopia. Based on the results shown on postoperative MRI, 1 lesion (7%) was intentionally subtotally resected, but ≥ 95% resection was achieved in all others (93%) and gross-total resection was accomplished in 7 (54%) of 13. One patient (7%) experienced a temporary approach-related complication. At last follow-up, 1 patient (7%) had died due to complications of his underlying malignancy unrelated to his cranial surgery, 2 (14%) demonstrated a Glasgow Outcome Scale (GOS) score of 4, and 11 (79%) manifested a GOS score of 5.

Conclusions Based on this patient series, the contralateral PITTA potentially offers numerous advantages, including a wider, safer operative corridor, minimal need for ipsilateral brain manipulation, and better intraoperative navigation and working angles.

Microsurgical resection of an intramedullary glomus arteriovenous malformation in the high cervical spinal cord

Microsurgical resection of an intramedullary glomus arteriovenous malformation in the high cervical spinal cord

Acta Neurochir (2015) 157:1659–1664

Spinal intramedullary arteriovenous malformations (AVMs) fed by an anterior spinal artery are surgically challenging vascular lesions.

Method We herein presented microsurgical resection techniques for an intramedullary glomus AVM located in the lateral part of the high cervical spinal cord with an operative video.

These techniques included (1) a lateral suboccipital approach via cervical hemilaminectomy in the lateral position; (2) retrograde dissection of the AVM located between the spinal tracts; (3) coagulation and division of multiple narrow sulcal branches of the anterior spinal artery.

Conclusion Patients who underwent these techniques achieved good outcomes with minimal bleeding and morbidity.

Integration of Indocyanine Green Videoangiography With Operative Microscope: Augmented Reality for Interactive Assessment of Vascular Structures and Blood Flow

Integration of Indocyanine Green Videoangiography With Operative Microscope

Operative Neurosurgery 11:252–258, 2015

Preservation of adequate blood flow and exclusion of flow from lesions are key concepts of vascular neurosurgery. Indocyanine green (ICG) fluorescence videoangiography is now widely used for the intraoperative assessment of vessel patency.

OBJECTIVE: Here, we present a proof-of-concept investigation of fluorescence angiography with augmented microscopy enhancement: real-time overlay of fluorescence videoangiography within the white light field of view of conventional operative microscopy.

METHODS: The femoral artery was exposed in 7 anesthetized rats. The dissection microscope was augmented to integrate real-time electronically processed near-infrared filtered images with conventional white light images seen through the standard oculars. This was accomplished by using an integrated organic light-emitting diode display to yield superimposition of white light and processed near-infrared images. ICG solution was injected into the jugular vein, and fluorescent femoral artery flow was observed.

RESULTS: Fluorescence angiography with augmented microscopy enhancement was able to detect ICG fluorescence in a small artery of interest. Fluorescence appeared as a bright-green signal in the ocular overlaid with the anatomic image and limited to the anatomic borders of the femoral artery and its branches. Surrounding anatomic structures were clearly visualized. Observation of ICG within the vessel lumens permitted visualization of the blood flow. Recorded video loops could be reviewed in an offline mode for more detailed assessment of the vasculature.

CONCLUSION: The overlay of fluorescence videoangiography within the field of view of the white light operative microscope allows real-time assessment of the blood flow within vessels during simultaneous surgical manipulation. This technique could improve intraoperative decision making during complex neurovascular procedures.

Treatment Outcomes of Unruptured Arteriovenous Malformations With a Subgroup Analysis of ARUBA Eligible Patients


Neurosurgery 76:563–570, 2015

The design and conclusions of A Randomized Trial of Unruptured Brain Arteriovenous Malformations (ARUBA) trial are controversial, and its structure limits analysis of patients who could potentially benefit from treatment.

OBJECTIVE: To analyze the results of a consecutive series of patients with unruptured brain arteriovenous malformations (BAVMs), including a subgroup analysis of ARUBAeligible patients.

METHODS: One hundred five patients with unruptured BAVMs were treated over an 8-year period. From this series, 90 adult patients and a subgroup of 61 patients determined to be ARUBA eligible were retrospectively reviewed. A subgroup analysis for Spetzler-Martin grades I/II, III, and IV/V was performed. The modified Rankin Scale was used to assess functional outcome.

RESULTS: Persistent deficits, modified Rankin Scale score deterioration, and impaired functional outcome occurred less frequently in ARUBA-eligible grade I/II patients compared with grade III to V patients combined (P = .04, P = .04, P = .03, respectively). Twenty-two of 39 patients (56%) unruptured grade I and II BAVMs were treated with surgery without and with preoperative embolization, and all had a modified Rankin Scale score of 0 to 1 at the last follow-up. All patients treated with surgery without and with preoperative embolization had radiographic cure at the last follow-up.

CONCLUSION: The results of ARUBA-eligible and unruptured grade I/II patients overall show that excellent outcomes can be obtained in this subgroup of patients, especially with surgical management. Functional outcomes for ARUBA-eligible patients were similar to those of patients who were randomized to medical management in ARUBA. On the basis of these data, in appropriately selected patients, we recommend treatment for low-grade BAVMs.

Silent Arteriovenous Malformation Hemorrhage and the Recognition of “Unruptured” Arteriovenous Malformation Patients Who Benefit From Surgical Intervention

Silent Arteriovenous Malformation Hemorrhage and the Recognition of “Unruptured” Arteriovenous Malformation Patients Who Benefit From Surgical Intervention

Neurosurgery 76:592–600, 201

Arteriovenous malformation (AVM) patients present in 4 ways relative to hemorrhage: (1) unruptured, without a history or radiographic evidence of old hemorrhage (EOOH); (2) silent hemorrhage, without a bleeding history but with EOOH; (3) ruptured, with acute bleeding but without EOOH; and (4) reruptured, with acute bleeding and EOOH. OBJECTIVE: We hypothesized that characteristics and outcomes in the unrecognized group of silent hemorrhage patients may differ from those of unruptured patients.

METHODS: Two hundred forty-two patients operated-on since 1997 were categorized by hemorrhage status and hemosiderin positivity in this cohort study: unruptured (group 1), silent hemorrhage (group 2), and ruptured/reruptured (group 3/4). Group 3/4 was combined because hemosiderin cannot distinguish acute hemorrhage from older silent hemorrhage.

RESULTS: Hemosiderin was found in 45% of specimens. Seventy-five patients (31.0%) had unruptured AVMs, 30 (12.4%) had silent hemorrhage, and 137 (56.6%) had ruptured/ reruptured AVMs. Deep drainage, posterior fossa location, preoperative modified Rankin Scale (mRS) score, outcome, and macrophage score were different across groups. Only the macrophage score was different between the groups without clinical hemorrhage. Outcomes were better in silent hemorrhage patients than in those with frank rupture (mean mRS scores of 1.2 and 1.7, respectively).

CONCLUSION: One-third of patients present with silent AVM hemorrhage. No clinical or anatomic features differentiate these patients from unruptured patients, except the presence of hemosiderin and macrophages. Silent hemorrhage can be diagnosed using magnetic resonance imaging with iron-sensitive imaging. Silent hemorrhage portends an aggressive natural history, and surgery halts progression to rerupture. Good final mRS outcomes and better outcomes than in those with frank rupture support surgery for silent hemorrhage patients, despite the findings of ARUBA.

Current surgical results with low-grade brain arteriovenous malformations

Low-grade brain arteriovenous malformations

J Neurosurg 122:912–920, 2015

Resection is an appealing therapy for brain arteriovenous malformations (AVMs) because of its high cure rate, low complication rate, and immediacy, and has become the first-line therapy for many AVMs. To clarify safety, efficacy, and outcomes associated with AVM resection in the aftermath of A Randomized Trial of Unruptured Brain AVMs (ARUBA), the authors reviewed their experience with low-grade AVMs—the most favorable AVMs for surgery and the ones most likely to have been selected for treatment outside of ARUBA’s randomization process.

Methods A prospective AVM registry was searched to identify patients with Spetzler-Martin Grade I and II AVMs treated using resection during a 16-year period.

Results Of the 232 surgical patients included, 120 (52%) presented with hemorrhage, 33% had Spetzler-Martin Grade I, and 67% had Grade II AVMs. Overall, 99 patients (43%) underwent preoperative embolization, with unruptured AVMs embolized more often than ruptured AVMs. AVM resection was accomplished in all patients and confirmed angiographically in 218 patients (94%). There were no deaths among patients with unruptured AVMs. Good outcomes (modified Rankin Scale [mRS] score 0–1) were found in 78% of patients, with 97% improved or unchanged from their preoperative mRS scores. Patients with unruptured AVMs had better functional outcomes (91% good outcome vs 65% in the ruptured group, p = 0.0008), while relative outcomes were equivalent (98% improved/unchanged in patients with ruptured AVMs vs 96% in patients with unruptured AVMs).

Conclusions Surgery should be regarded as the “gold standard” therapy for the majority of low-grade AVMs, utilizing conservative embolization as a preoperative adjunct. High surgical cure rates and excellent functional outcomes in patients with both ruptured and unruptured AVMs support a dominant surgical posture for low-grade AVMS, with radiosurgery reserved for risky AVMs in deep, inaccessible, and highly eloquent locations. Despite the technological advances in endovascular and radiosurgical therapy, surgery still offers the best cure rate, lowest risk profile, and greatest protection against hemorrhage for low-grade AVMs. ARUBA results are influenced by a low randomization rate, bias toward nonsurgical therapies, a shortage of surgical expertise, a lower rate of complete AVM obliteration, a higher rate of delayed hemorrhage, and short study duration. Another randomized trial is needed to reestablish the role of surgery in unruptured AVM management.

A treatment paradigm for high-grade brain arteriovenous malformations: volume-staged radiosurgical downgrading followed by microsurgical resection

A treatment paradigm for high-grade brain arteriovenous malformations- volume-staged radiosurgical downgrading followed by microsurgical resection

J Neurosurg 122:419–432, 2015

The surgical treatment of many large arteriovenous malformations (AVMs) is associated with substantial risks, and many are considered inoperable. Furthermore, AVMs larger than 3 cm in diameter are not usually treated with conventional single-session radiosurgery encompassing the entire AVM volume. Volume-staged stereotactic radiosurgery (VS-SRS) is an option for large AVMs, but it has mixed results. The authors report on a series of patients with highgrade AVMs who underwent multiple VS-SRS sessions with resultant downgrading of the AVMs, followed by resection.

Methods. A cohort of patients was retrieved from a single-institution AVM patient registry consisting of prospectively collected data. VS-SRS was performed as a planned intentional treatment. Surgery was considered as salvage therapy in select patients.

Results Sixteen AVMs underwent VS-SRS followed by surgery. Four AVMs presented with rupture. The mean patient age was 25.3 years (range 13–54 years). The average initial Spetzler-Martin grade before any treatment was 4, while the average supplemented Spetzler-Martin grade (Spetzler-Martin plus Lawton-Young) was 7.1. The average AVM size in maximum dimension was 5.9 cm (range 3.3–10 cm). All AVMs were supratentorial in location and all except one were in eloquent areas of the brain, with 7 involving primary motor cortex. The mean number of VS-SRS sessions was 2.7 (range 2–5 sessions). The mean interval between first VS-SRS session and resection was 5.7 years. There were 4 hemorrhages that occurred after VS-SRS. The average Spetzler-Martin grade was reduced to 2.5 (downgrade, -1.5) and the average supplemented Spetzler-Martin grade was reduced to 5.6 (downgrade, -1.5). The maximum AVM size was reduced to an average of 3.0 cm (downsize = -2.9 cm). The mean modified Rankin Scale (mRS) scores were 1.2, 2.3, and 2.2 before VS-SRS, before surgery, and at last follow-up, respectively (mean follow-up, 6.9 years). Fifteen AVMs were cured after surgery. Ten patients had good outcomes at last follow-up (7 with mRS Score 0 or 1, and 3 with mRS Score 2). There were 2 deaths (both mRS Score 1 before treatment) and 4 patients with mRS Score 3 outcome (from mRS Scores 0, 1, and 2 [n = 2]).

Conclusions Volume-staged SRS can downgrade AVMs, transforming high-grade AVMs (initially considered inoperable) into operable AVMs with acceptable surgical risks. This treatment paradigm offers an alternative to conservative observation for young patients with unruptured AVMs and long life expectancy, where the risk of hemorrhage is substantial. Difficult AVMs were cured in 15 patients. Surgical morbidity associated with downgraded AVMs is reduced to that of postradiosurgical/preoperative supplemented Spetzler-Martin grades, not their initial AVM grades.

Validation of the Supplemented Spetzler-Martin Grading System for Brain Arteriovenous Malformations in a Multicenter Cohort of 1009 Surgical Patients


Neurosurgery 76:25–33, 2015

The supplementary grading system for brain arteriovenous malformations (AVMs) was introduced in 2010 as a tool for improving preoperative risk prediction and selecting surgical patients.

OBJECTIVE: To demonstrate in this multicenter validation study that supplemented Spetzler-Martin (SM-Supp) grades have greater predictive accuracy than Spetzler-Martin (SM) grades alone.

METHODS: Data collected from 1009 AVM patients who underwent AVM resection were used to compare the predictive powers of SM and SM-Supp grades. Patients included the original 300 University of California, San Francisco patients plus those treated thereafter (n = 117) and an additional 592 patients from 3 other centers.

RESULTS: In the combined cohort, the SM-Supp system performed better than SM system alone: area under the receiver-operating characteristics curve (AUROC) = 0.75 (95% confidence interval, 0.71-0.78) for SM-Supp and AUROC = 0.69 (95% confidence interval, 0.65-0.73) for SM (P , .001). Stratified analysis fitting models within 3 different follow-up groupings (,6 months, 6 months-2 years, and .2 years) demonstrated that the SM-Supp system performed better than SM system for both medium (AUROC = 0.71 vs 0.62; P = .003) and long (AUROC = 0.69 vs 0.58; P = .001) follow-up. Patients with SMSupp grades #6 had acceptably low surgical risks (0%-24%), with a significant increase in risk for grades .6 (39%-63%).

CONCLUSION: This study validates the predictive accuracy of the SM-Supp system in a multicenter cohort. An SM-Supp grade of 6 is a cutoff or boundary for AVM operability. Supplemented grading is currently the best method of estimating neurological outcomes after AVM surgery, and we recommend it as a starting point in the evaluation of AVM operability.

Management of perisylvian arteriovenous malformations

Management of perisylvian arteriovenous malformations

Neurosurg Focus 37 (3):E13, 2014

Sylvian arteriovenous malformations (sAVMs) are challenging lesions of the central nervous system. The natural history of these unique lesions as well as clinical outcomes following treatment of sAVMs has been limited to case series owing to the rarity of these lesions. The authors present their experience with sAVMs and review the literature.

Methods. In accordance with the Henry Ford Institutional Review Board, medical records of patients with sAVMs treated from 2000 to 2012 were reviewed. Clinical data were retrospectively collected to calculate pre- and posttreatment modified Rankin Scale scores for all patients.

Results. The authors identified 15 patients with sAVMs who received treatment. Of these, 12 were female and 3 were male, and the average age at presentation was 39.6 ± 12.94 years (± SD). Two patients (13.3%) had Spetzler- Martin Grade I lesions, 6 patients (40%) had Grade II lesions, 5 patients (33.3%) had Grade III lesions, and another 2 (13.3%) harbored Grade IV arteriovenous malformations (AVMs). According to the Sugita classification, 6 patients (40%) had medial lesions, 6 (40%) had lateral lesions, 2 (13.3%) had deep lesions, and 1 patient (6.67%) had a pure sAVM. Eight patients (53.3%) underwent stereotactic radiosurgery while 7 patients (46.7%) had microsurgical resection; 1 patient underwent surgical extirpation after incomplete response following radiosurgery. After treatment, 9 patients were unchanged from pretreatment (60%), 3 patients worsened, and 2 patients had improved functional outcome (20% and 13.3%, respectively). The authors’ literature search yielded 348 patients with sAVMs, most of them harboring Spetzler-Martin Grade II and III lesions. Approximately 98% of the patients underwent resection with excellent outcomes.

Conclusions. While the ideal choice of therapeutic modality for cerebral AVMs remains controversial in light of the recent publication of the ARUBA (A Randomized trial of Unruptured Brain AVMs) trial, a multidisciplinary treatment approach for the management of sAVMs can lead to acceptable neurological outcome.

Microsurgery for cerebral arteriovenous malformations: postoperative outcomes and predictors of complications in 264 cases


Neurosurg Focus 37 (3):E10, 2014

The authors conducted a study to assess the safety and efficacy of microsurgical resection of arteriovenous malformations (AVMs) and determine predictors of complications.

Methods. A total of 264 patients with cerebral AVMs were treated with microsurgical resection between 1994 and 2010 at the Jefferson Hospital for Neuroscience. A review of patient data was performed, including initial hemorrhage, clinical presentation, Spetzler-Martin (SM) grade, treatment modalities, clinical outcomes, and obliteration rates. Univariate and multivariate analyses were used to determine predictors of operative complications.

Results. Of the 264 patients treated with microsurgery, 120 (45%) patients initially presented with hemorrhage. There were 27 SM Grade I lesions (10.2%), 101 Grade II lesions (38.3%), 96 Grade III lesions (36.4%), 31 Grade IV lesions (11.7%), and 9 Grade V lesions (3.4%). Among these patients, 102 (38.6%) had undergone prior endovascular embolization. In all patients, resection resulted in complete obliteration of the AVM. Complications occurred in 19 (7.2%) patients and resulted in permanent neurological deficits in 5 (1.9%). In multivariate analysis, predictors of complications were increasing AVM size (OR 3.2, 95% CI 1.5–6.6; p = 0.001), increasing number of embolizations (OR 1.6, 95% CI 1.1–2.2; p = 0.01), and unruptured AVMs (OR 2.7, 95% CI 1–7.2; p = 0.05).

Conclusions. Microsurgical resection of AVMs is highly efficient and can be undertaken with low rates of morbidity at high-volume neurovascular centers. Unruptured and larger AVMs were associated with higher complication rates.

Neurosurgery Department. “La Fe” University Hospital. Valencia, Spain


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