A Tractography-Based Grading Scale of Brain Arteriovenous Malformations Close to the Corticospinal Tract to Predict Motor Outcome After Surgery

Abstract

Background: Surgical decision-making for brain arteriovenous malformations (AVMs) close to the corticospinal tract (CST) is always challenging. The purpose of this study was to develop a tractography-based grading scale to improve preoperative risk prediction and patient selection. Methods: We analyzed a consecutive, surgically treated series of 90 patients with AVMs within a 10-mm range from the CST demonstrated by preoperative diffusion tensor tractography. Poor motor outcome was defined as persistent postoperative limb weakness. We examined the predictive ability of nidus-to-CST distance (NCD), the closest CST level (CCL), deep perforating artery supply, as well as variables of the supplemented Spetzler-Martin grading system. Three logistic models were derived from different multivariable logistic regression analyses, of which the most predictive model was selected to construct a prediction grading scale. Receiver operating characteristic analysis was conducted to test the predictive accuracy of the grading scale. Results: Twenty-one (23.3%) patients experienced persistent postoperative limb weakness after a mean 2.7-year follow-up. The most predictive logistic model showed NCD (P = 0.001), CCL (P = 0.017), patient age (P = 0.004), and AVM diffuseness (P = 0.021) were independent predictors for poor motor outcome. We constructed the CLAD grading scale incorporating these predictors. The predictive accuracy of the CLAD grade was better compared with the supplemented Spetzler-Martin grade (area under curve = 0.84 vs. 0.68, P = 0.023). Conclusions: Both NCD and CCL predict motor outcome after resection of AVMs close to the CST. We propose the CLAD grading scale as an effective risk-prediction tool in surgical decision-making. Clinical Trial Registration: www.ClinicalTrials.gov, identifier: NCT01758211 and NCT02868008.

Keywords: arteriovenous malformation; corticospinal tract; patient selection; surgery; tractography.

Figures

Figure 1

Graph showing receiver operating characteristic analysis for the three logistic models, the CLAD grading scale and the supp Spetzler-Martin grading system. The predictive accuracy of model B (area under purple curve = 0.88) was higher than that of model A (area under green curve = 0.76) and model C (area under orange curve = 0.78). The predictive accuracy of the CLAD grading scale (area under red curve = 0.84) was higher than that of the supp Spetzler-Martin grading system (area under blue curve = 0.68).

Figure 2

Preoperative magnetic resonance angiography (MRA) fused with the reconstructed corticospinal tract (CST) and digital subtraction angiography (DSA) of three individual AVM patients. (A–D) A 38-year-old woman who suffered twice intraventricular hemorrhage before treatment. (A,B) Axial MRA showing the deeply located periventricular AVM with the internal capsule involved. Fusion images demonstrated that the shortest nidus-to-CST distance (NCD) was 2.0 mm, and the closest CST level (CCL) was the posterior limb of the internal capsule (PLIC). (C,D) Angiograms (anteroposterior view of right ICA injection and lateral view of right VA injection) showing a diffuse nidus with deep venous drainage. Therefore, this patient had a supp Spetzler-Martin (supp S-M) grade of 7 (S2V1E1A2U0D1) and a CLAD grade of 5 (C2L1A1D1). After surgery, she experienced persistent left limb weakness (motor strength of 3-4 at the last follow-up). (E–H) A 21-year-old man who presented with remote temporal hemorrhage. (E,F) Axial MRA showing the AVM located in the deep sylvian fissure with involvement of the PLIC. The NCD of 0 mm and the CCL of PLIC was demonstrated by image fusion. (G,H) Angiograms (right ICA injection; anteroposterior view and lateral view) showing a compact nidus with superficial venous drainage. Therefore, he had a supp S-M grade of 5 (S2V0E1A2U0D0) and a CLAD grade of 5 (C3L1A1D0). He experienced persistent postoperative left upper limb weakness (motor strength of 4). The CLAD grade was more predictive for his motor outcome. (I–L) A 29-year-old man who presented with seizures. (I,J) Axial MRA showing the unruptured AVM abutting the precentral gyrus. Fusion images showed that the NCD was 7.9 mm, and the CCL was cortex or centrum semiovale. (K,L) Angiograms (right ICA injection; anteroposterior view and lateral view) demonstrating superficial venous drainage and a diffuse border (deeply). Therefore, the supp S-M grade was 7 (S2V0E1A2U1D1) and the CLAD grade was 3 (C1L0A1D1). This patient recovered fully postoperatively. The CLAD grade predicted better.