Effect of functional MRI-guided navigation on surgical outcomes: a prospective controlled trial in patients with arteriovenous malformations

J Neurosurg. 2017 Jun;126(6):1863-1872. doi: 10.3171/2016.4.JNS1616. Epub 2016 Jul 1.

Abstract

OBJECTIVE The impact of functional MRI (fMRI)-guided navigation on the surgical outcome of patients with arteriovenous malformations (AVMs) is undetermined. This large, randomized controlled trial (RCT) was designed to determine the safety and efficacy of fMRI-guided microsurgery of AVMs. This paper reports the preliminary results of the interim analysis. METHODS Between September 2012 and June 2015, eligible patients were randomized to the standard microsurgery group (control group) or the fMRI-guided surgery group (experimental group) in a 1:1 ratio. Patients in the control group underwent conventional digital subtraction angiography and MRI before surgery. The surgery was performed according to the standard procedure. However, patients in the experimental group underwent blood oxygen level-dependent (BOLD) fMRI and diffusion tensor imaging within 1 week before surgery. Moreover, preoperative eloquent brain tissue mapping and intraoperative fMRI navigation were performed in addition to the standard procedure. The preliminary end points were the total removal rate of AVMs and postoperative surgical complications. The primary end points were modified Rankin Scale (mRS) score (favorable: mRS Score 0-2; poor: mRS Score 3-6) and surgery-related permanent functional deficits (S-PFD) at the last clinic visit (≥ 6 months). Statistical analysis was performed using the statistical package from SPSS. RESULTS The interim analysis included 184 participants (93 in the experimental group and 91 in the control group). Patients were equally distributed between the 2 groups. Neither the preliminary nor the primary end points, including postoperative complications (p = 0.781), residual AVM (p = 1.000), last mRS score (p = 0.654), and S-PFD (p = 0.944) showed any significant difference between the control and experimental group. According to the results of the univariate analysis, eloquent adjacent brain tissue (OR 0.14; 95% CI 0.06-0.32; p < 0.001), large size of the nidus (OR 1.05; 95% CI 1.02-1.08; p = 0.002), or diffuse nidus (OR 3.05; 95% CI 1.42-6.58; p = 0.004) were all significantly associated with S-PFD. Additionally, a high Spetzler-Martin score (OR 3.54; 95% CI 2.08-6.02; p < 0.001), no previous hemorrhage (OR 2.35; 95% CI 1.00-5.54; p = 0.05), or a low preoperative mRS score (OR 0.42; 95% CI 0.17-1.00; p = 0.049) were also significantly associated with S-PFD. Multivariate analysis revealed that independent factors correlated with S-PFD were eloquent adjacent brain tissue (OR 0.17; 95% CI 0.04-0.70; p = 0.014) and low preoperative mRS score (OR 0.22; 95% CI 0.07-0.69; p = 0.009). CONCLUSIONS This preplanned interim analysis revealed no significant differences in the primary end points between the experimental and control group, prompting an early termination of this RCT. The preliminary data indicated that the additional intervention of fMRI navigation is not associated with a more favorable surgical outcome in patients with AVMs. The results indicated that eloquent adjacent brain tissue and a low preoperative mRS score are independent risk factors for S-PFD. Clinical trial registration no.: NCT01758211 ( clinicaltrials.gov ).

Keywords: AVM = arteriovenous malformation; BOLD = blood oxygen level dependent; DSA = digital subtraction angiography; DTI = diffusion tensor imaging; FOV = field of view; PRC = People's Republic of China; RCT = randomized controlled trial; ROIs = regions of interest; S-PFD = surgery-related permanent functional deficits; SM = Spetzler-Martin; TOF-MRA = time-of-flight MR angiography; cerebral arteriovenous malformations; diffusion tensor imaging; fMRI = functional MRI; functional magnetic resonance imaging; mRS = modified Rankin Scale; navigation; risk factor; surgery; vascular disorders.

Publication types

  • Randomized Controlled Trial

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Female
  • Humans
  • Intracranial Arteriovenous Malformations / diagnostic imaging*
  • Intracranial Arteriovenous Malformations / surgery*
  • Magnetic Resonance Imaging*
  • Male
  • Microsurgery*
  • Prospective Studies
  • Treatment Outcome
  • Young Adult

Associated data

  • ClinicalTrials.gov/NCT01758211