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Cerebral cavernous malformations: natural history and prognosis after clinical deterioration with or without hemorrhage

Phillip J. Porter, Robert A. Willinsky, William Harper, and M. Christopher Wallace

✓ Despite recent studies of the natural history of cavernous malformations, there remains significant uncertainty concerning hemorrhage rates and the importance of lesion location. Controversy arises over varying definitions of “hemorrhage.” What is ultimately important to the patient is the occurrence of a neurological event, which may or may not be associated with radiologically documented hemorrhage, as well as the chance of recovery after such an event. The purpose of this study was to determine the rates of occurrence and sequelae of neurological events in 173 patients referred to our vascular malformation clinic with cavernous malformations.

All patient data were entered into a database. The mean age at presentation for the 173 patients was 37.5 years. The lesion location was deep (brainstem, cerebellar nuclei, thalamus, or basal ganglia) in 64 patients (37%) and superficial in 109 (63%). Thirty-one patients (18%) had multiple lesions. Disease presentation was due to seizures in 62 patients (36%), hemorrhage in 44 (25%), focal neurological deficit without documented hemorrhage in 35 (20%), headache alone in 11 (6%), and incidental findings in 21 patients (12%). The results obtained in the 110 patients eligible for follow-up review were used to derive information on the rates of hemorrhage and neurological events. An interval event (neurological deterioration) required both symptoms and signs. The total mean follow-up period was 46 months, the majority (65%) of which was prospective. There were 18 interval events in 427 patient-years of follow-up review, for an overall annual event rate of 4.2%. Location was the most important factor for predicting interval event occurrence, with significantly higher rates for deeply located (10.6%/year) compared with superficially located lesions (0%/year) (p = 0.0001). Of patients suffering a neurological event, only 37% had complete resolution of their deficits.

This largely prospective study indicates that deep cavernous malformations carry a worse prognosis than superficial lesions with respect to annual rates of neurological deterioration. The alarming rate of adverse clinical events occurring in patients with deep lesions is punctuated by the fact that less than one-half of them recover fully during long-term follow-up review.

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Pathological effects of angioplasty on vasospastic carotid arteries in a rabbit model

R. Loch Macdonald, M. Christopher Wallace, Walter J. Montanera, and Jennifer A. Glen

✓ To define the pathological effects of angioplasty on vasospastic arteries, 36 rabbits underwent angiography and induction of vasospasm by placement of blood-filled (vasospasm groups) or empty (control group) silastic sheaths around the cervical carotid arteries. Two (Day 2) or 7 days (Day 7) later, angiography was repeated and one carotid artery in each animal was dilated by balloon angioplasty. The rabbits were sacrificed 1 day, 7 days, or 3 to 4 weeks after angioplasty. Significant vasospasm developed after placement of silastic sheaths with blood (mean reductions in diameter 39% ± 6% at Day 2 and 48% ± 5% at Day 7). Arterial narrowing was less apparent in the control groups at Day 2 (24% ± 7%). Angioplasty performed on Day 2 significantly increased arterial diameters of vasospastic arteries (50% ± 7%; p < 0.05) but not those of control arteries (10% ± 6%, p > 0.05). Angioplasty performed on Day 7 increased the arterial diameters by a similar degree (47% ± 13%, not significant). Arteries remained dilated after angioplasty, although there was significant vasospasm 7 days after angioplasty when angioplasty was performed on Day 2. Blinded, semiquantitative histopathological study of the arteries showed that 3 to 4 weeks after angioplasty, there was significant endothelial proliferation and a trend for thinning of the tunica media. There were no significant changes in control arteries subjected to angioplasty. Angioplasty was not associated with significant arterial fibrosis as measured by hydroxyproline content (analysis of variance). The increase in endothelial proliferation and decrease in the thickness of the tunica media suggest that, in the rabbit model, angioplasty damages endothelial and smooth-muscle cells. This may be the basis for the observation that vasospastic arteries do not reconstrict after angioplasty.

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The effect of surgery on the severity of vasospasm

R. Loch Macdonald, M. Christopher Wallace, and Terry J. Coyne

✓ Intracranial aneurysm surgery performed between 4 and 12 days after subarachnoid hemorrhage (SAH) has been associated with an increased risk of delayed cerebral ischemia and poor outcome compared to surgery performed before or after this time. To investigate whether this increased risk is due to aggravation of vasospasm, the angiograms obtained before and after surgery in 56 patients operated on at various times after aneurysmal SAH were studied. Vasospasm was quantitated by measuring the diameters of intracranial arteries and expressed as the ratio of the diameters of the intracranial arteries to the diameter of the extracranial internal carotid artery. Aggressive surgical clot removal was not performed at surgery. To correct for differences in prognostic factors for vasospasm between patients operated on at different times after SAH, multiple regression analysis was performed using the arterial diameter ratio during vasospasm as the dependent variable and the prognostic factors for vasospasm, including the time of surgery, as independent variables. Equations predicting the severity of vasospasm could be generated using the clinical grade on admission, patient age, and preoperative arterial diameter ratio.

The time of surgery had no effect on vasospasm. Cerebral infarction due to vasospasm developed in five (15%) of 34 patients operated on within 3 days after SAH and in four (20%) of 20 operated on between 4 and 12 days after SAH (p = 0.66). A good outcome for these two groups was achieved in 88% and 85%, respectively (p = 1.00). These results suggest that the timing of surgery does not affect the development of vasospasm. Any increased risk of cerebral ischemia associated with surgery performed between 4 and 12 days after SAH is due to factors other than aggravation of vasospasm.

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Surgery for Occult Aneurysms

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Retroperitoneal lateral lumbar interbody fusion with titanium threaded fusion cages

Christopher E. Wolfla, Dennis J. Maiman, Frank J. Coufal, and James R. Wallace

Object. Intertransverse arthrodesis in which instrumentation is placed is associated with an excellent fusion rate; however, treatment of patients with symptomatic nonunion presents a number of difficulties. Revision posterior and traditional anterior procedures are associated with methodological problems. For example, in the latter, manipulation of the major vessels from L-2 to L-4 may be undesirable. The authors describe a method for performing retroperitoneal lumbar interbody fusion (LIF) in which a threaded cage is placed from L-2 through L-5 via a lateral trajectory, and they also detail a novel technique for implanting a cage from L-5 to S-1 via an oblique trajectory. Although they present data obtained over a 2-year period in the study of 15 patients, the focus of this report is primarily on describing the surgical procedure.

Methods. The lateral lumbar spine was exposed via a standard retroperitoneal approach. Using the anterior longitudinal ligament as a landmark, the L2–3 through L4–5 levels were fitted with instrumentation via a true lateral trajectory; the L5—S1 level was fitted with instrumentation via an oblique trajectory. A single cage was placed at each instrumented level.

Fifteen symptomatic patients in whom previous lumbar fusion had failed underwent retroperitoneal LIF. Thirty-eight levels were fitted with instrumentation. There have been no instrumentation-related failures, and fusion has occurred at 37 levels during the 2-year postoperative period.

Conclusions. The use of retroperitoneal LIF in which threaded fusion cages are used avoids the technical difficulties associated with repeated posterior procedures. In addition, it allows L2—S1 instrumentation to be placed anteriorly via a single surgical approach. This construct has been shown to be biomechanically sound in animal models, and it appears to be a useful alternative for the management of failed multilevel intertransverse arthrodesis.

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Intraoperative biplanar rotational angiography during neurovascular surgery

Technical note

Amir R. Dehdashti, Laurent Thines, Leodante B. Da Costa, Karel G. terBrugge, Robert A. Willinsky, M. Christopher Wallace, and Michael Tymianski


The purpose of this study was to evaluate the authors' initial experience with the integration of high-resolution rotational and biplanar angiography during neurovascular operative procedures.


Eight patients with intracerebral arteriovenous malformations (AVMs) and aneurysms underwent surgical treatment of their lesions in a combined endovascular surgical suite. After initial head positioning, preoperative biplane and rotational angiography was performed. Resection of the AVM or clipping of the aneurysm was then performed. Further biplane and rotational 3D angiograms were obtained intraoperatively to confirm satisfactory treatment.


One small residual AVM identified intraoperatively necessitated further resection. One aneurysm was clipped during endovascular inflation of an intracarotid balloon for temporary proximal control. The completeness of treatment was confirmed on intraoperative 3D rotational angiography in all cases, and there were no procedure-related complications.


Intraoperative rotational angiography performed in an integrated biplane angiography/surgery suite is a safe and useful adjunct to surgery and may enable combining endovascular and surgical procedures for the treatment of complex vascular lesions.

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Multidisciplinary care of occipital arteriovenous malformations: effect on nonhemorrhagic headache, vision, and outcome in a series of 135 patients

Clinical article

Amir R. Dehdashti, Laurent Thines, Robert A. Willinsky, Karel G. terBrugge, Michael L. Schwartz, Michael Tymianski, and M. Christopher Wallace


In this study, the authors evaluated how an appropriate allocation of patients with occipital arteriovenous malformations (AVMs) who were treated according to different strategies would affect nonhemorrhagic headache, visual function, and hemorrhage risk levels.


Of the 712 patients with brain AVMs in the Toronto Western Hospital prospective database, 135 had occipital AVMs. The treatment decision was based on patients' characteristics, presentation, and morphology of the AVM. The management modalities were correlated with their outcomes.


The mean follow-up period was 6.78 years. Nonhemorrhagic headache was the most frequent symptom (82 [61%] of 135 patients). Ninety-four patients underwent treatment with one or a combination of embolization, surgery, or radiosurgery, and 41 were simply observed. Of the 40 nontreated patients with nonhemorrhagic headache, only 12 (30%) showed improvement. In the observation group 2 patients (22%) had worsening of visual symptoms, and 2 experienced hemorrhage, for an annual hemorrhage rate of 0.7% per year; 1 patient died. In the treatment group, the improvement in nonhemorrhagic headache in 35 patients (83%) was significant (p < 0.0001). Visual deficit at presentation worsened in 2 (8%), and there were 8 new visual field deficits (9%). The visual worsening was not significantly different. There were 2 other neurological deficits (2%) and 2 deaths (2%) related to the AVM treatment. One AVM hemorrhaged. The annual hemorrhage rate was 0.1% per year. The hemorrhage risk in the observation and treatment groups was lower than the observed hemorrhage risk of all patients with AVMs (4.6%) at the authors' institution.


Appropriate selection of patients with occipital AVMs for one or a combination of treatment modalities yields a significant decrease in nonhemorrhagic headache without significant visual worsening. The multidisciplinary care of occipital AVMs can aim for an apparent decrease in hemorrhage risk.

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Overview of the current role of endovascular and surgical treatment in spinal dural arteriovenous fistulas

Amir R. Dehdashti, Leodante B. Da Costa, Karel G. terBrugge, Robert A. Willinsky, Michael Tymianski, and M. Christopher Wallace

Dural arteriovenous fistulas are the most common vascular malformations of the spinal cord. These benign vascular lesions are considered straightforward targets of surgical treatment and possibly endovascular embolization, but the outcome in these cases depends mainly on the extent of clinical dysfunction at the time of the diagnosis. A timely diagnosis is an equally important factor, with early treatment regardless of the type more likely to yield significant improvements in neurological functioning. The outcomes after surgical and endovascular treatment are similar if complete obliteration of the fistulous site is obtained. In the present study, the authors evaluated the current role of each modality in the management of these interesting lesions.

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Thrombophilic factors and the formation of dural arteriovenous fistulas

J. Marc C. Van Dijk, Karel G. Terbrugge, Felix J. Van Der Meer, M. Christopher Wallace, and Frits R. Rosendaal


Dural arteriovenous fistulas (DAVFs) are distinct neurovascular entities. Although their exact origins are unknown, venous thrombosis and venous hypertension are likely to be major inducing factors. To address the relationship between DAVFs and thrombophilic factors, the authors conducted a case-control study at a single institution and performed a metaanalysis of the literature.


Forty patients with DAVFs at Toronto Western Hospital were recruited to complete a questionnaire and to donate blood samples for factor V Leiden mutation and factor II G20210A mutation screening and assessment of coagulation factors. The questionnaire was designed to collect information on each participant's specific history of venous thrombosis, medications, and race. A control group of 33 healthy volunteers agreed to the same protocol. A MEDLINE search of the literature from 1966 to the present was conducted and three relevant series were found. The results of the present study were pooled with the data from the literature.


Combining institutional results with the results from the literature yielded a total of 121 patients and 178 control group members. Thrombophilic mutations were present in 16 patients and four healthy volunteers, with an odds ratio (OR) of 4.69 for factor V Leiden (95% confidence interval [CI] 1.24–17.69) and an OR of 10.87 for the prothrombin G20210A allele (95% CI 1.32–89.51). Levels of the basic coagulation profile, fibrinogen, and factor VIII were within normal limits.


Patients with the factor V Leiden and factor II G20210A mutations are at a higher risk for DAVFs. However, because these mutations are not implicated in the vast majority of DAVFs, routine screening is not recommended.

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Benign cranial dural arteriovenous fistulas: outcome of conservative management based on the natural history of the lesion

Junichiro Satomi, J. MARC C. van Dijk, Karel G. Terbrugge, Robert A. Willinsky, and M. Christopher Wallace

Object. Cranial dural arteriovenous fistulas (DAVFs) can be classified into benign or aggressive, based on their patterns of venous drainage. A benign condition requires the absence of cortical venous drainage (CVD). The clinical and angiographic features of a consecutive single-center group of 117 patients harboring benign cranial DAVFs were evaluated over time to validate the behavior and appropriate management of these lesions.

Methods. At the initial assessment four patients were asymptomatic. Two infants presented with congestive heart failure. All other patients presented with other benign symptoms: chronic headache, bruit, or orbital phenomena. Observational management was instituted in 73 patients (62%). Intolerable bruit or ophthalmological sequelae were deemed indications for palliative embolization in 43 patients and surgical treatment in one patient. A median follow-up period of 27.9 months (range 1 month—17.5 years) was available in 112 patients (95.7%), among whom repeated angiography was performed in 50. Overall, observational and palliative management resulted in a benign and tolerable level of disease in 110 (98.2%) of 112 cases. In two cases managed conservatively CVD developed. In both of these cases the conversion from benign to aggressive DAVF was associated with spontaneous progressive thrombosis of venous outlets.

Conclusions. The disease course of a cranial DAVF without CVD is indeed benign, obviating the need for a cure of these lesions. Symptoms are well tolerated with either observation or palliative treatment. After a long-term follow-up review of 68 patients, this conservative management resulted in a benign and tolerable level of disease in 98.5% of cases. It is noteworthy, however, that a benign DAVF carries a 2% risk of developing CVD, mandating close clinical follow-up review in such cases and renewed radiological evaluation in response to any deterioration in the patient's condition.