Surgical outcome of motor deficits and neurological status in brainstem cavernous malformations based on preoperative diffusion tensor imaging: a prospective randomized clinical trial

Abstract

OBJECTIVE Surgical management of brainstem lesions is challenging due to the highly compact, eloquent anatomy of the brainstem. This study aimed to evaluate the safety and efficacy of preoperative diffusion tensor imaging (DTI) and diffusion tensor tractography (DTT) in brainstem cavernous malformations (CMs). METHODS A prospective randomized controlled clinical trial was performed by using stratified blocked randomization. The primary eligibility criterion of the study was being a surgical candidate for brainstem CMs (with informed consent). The study enrolled 23 patients who underwent preoperative DTI/DTT and 24 patients who did not (the control group). The pre- and postoperative muscle strength of both limbs and modified Rankin Scale (mRS) scores were evaluated. Muscle strength of any limb at 12 months after surgery at the clinic visit was the primary outcome; worsened muscle strength was considered to be a poor outcome. Outcome assessors were blinded to patient management. This study reports the preliminary results of the interim analysis. RESULTS The cohort included 47 patients (22 women) with a mean age of 35.7 years. The clinical baselines between these 2 groups were not significantly different. In the DTI/DTT group, the corticospinal tract was affected in 17 patients (73.9%): it was displaced, deformed/partially interrupted, or completely interrupted in 6, 7, and 4 patients, respectively. The surgical approach and brainstem entry point were adjusted in 3 patients (13.0%) based on DTI/DTT data. The surgical morbidity of the DTI/DTT group (7/23, 30.4%) was significantly lower than that of the control group (19/24, 79.2%, p = 0.001). At 12 months, the mean mRS score (1.1, p = 0.034) and percentage of patients with worsened motor deficits (4.3%, p = 0.006) were significantly lower in the DTI/DTT group than in the control group (1.7% and 37.5%). Multivariate logistic regression identified the absence of preoperative DTI/DTT (OR 0.06, 95% CI 0.01-0.73, p = 0.028) and use of the 2-point method (OR 4.15, 95% CI 1.38-12.49, p = 0.011) as independent adverse factors for a worsened motor deficit. The multivariate model found a significant correlation between poor mRS score and both an increased preoperative mRS score (t = 3.559, p = 0.001) and absence of preoperative DTI/DTT (t = -2.747, p = 0.009). CONCLUSIONS DTI/DTT noninvasively allowed for visualization of the anatomical relationship between vital tracts and pathologies as well as facilitated the brainstem surgical approach and entry-point decision making. The technique was valuable for complex neurosurgical planning to reduce morbidity. Nonetheless, DTI/DTT data should be interpreted cautiously. ■ CLASSIFICATION OF EVIDENCE Type of question: therapeutic; study design: randomized controlled trial; evidence: class I. Clinical trial registration no.: NCT01758211 (ClinicalTrials.gov).

Cerebral Cavernous Malformations, Developmental Venous Anomaly, and Its Coexistence: A Review

“…Magnetic Resonance Imaging MRI has been found to show a higher specificity to detect both symptomatic and asymptomatic lesions as well as cavernomas located in the posterior cranial fossa or the brainstem [27,28]. Based on the MRI images, cavernous angiomas can be classified into 4 types ( Table 2).…”

The role of diffusion tensor imaging and tractography in the surgical management of brainstem gliomas

“…Additionally, it may have promising value for the prediction of postoperative neurological function. 12,15,19 However, as brainstem gliomas behave differently from cavernous malformations and their ability to infiltrate the normal brain may vary depending on their genetic characteristics, the role of DTI/DTT in brainstem glioma surgery merits investigation. In our study, the number of changes in the CSTs in the deviation, deformation, and interruption groups were very similar.…”

“…In contrast, white matter tracts are more frequently deviated rather than destroyed by the lesions in brainstem cavernous malformations. 10,12 This discrepancy could be explained by the invasive nature of gliomas and indicate that these critical fibers are more vulnerable to surgical manipulation during an operation, thus meriting significant protective efforts. Understanding the anatomical relationship between the tumor and tracts is helpful to determine the approach, and many studies have shown that DTI/DTT is a highly valuable tool in preoperative surgical planning.…”

“…8 Additionally, DTI has been reported to be helpful in both the surgical planning and prediction of postoperative neurological function. [9][10][11][12][13] However, most of these applications are confined to supratentorial gliomas in eloquent areas and, most recently, brainstem cavernous malformations. The utility of DTI/DTT in brainstem glioma surgery has rarely been discussed.…”

Tractography in Neurosurgery: A Systematic Review of Current Applications

“…4,116 Some studies report tractography to be a valuable tool that has shaped the surgical strategy of intra-axial lesions profoundly. This includes approaches to the brainstem, 36,135,163,176,178,198,221,222,234 the insula, 58,179,182,291 the thalamus, 158,162,195,202 and the angular gyrus. 167…”