Mini-strokes within Broca-caudate connections during left insular glioma awake surgery cause transient severe naming deficits

Objective

To provide an explanation for the intraoperative onset of severe naming deficits in the course of awake resection of left insular glioma.

Methods

We retrospectively reviewed a series of 14 patients operated on in awake conditions for a left insular IDH-mutated glioma. Preoperative MRI included high-resolution diffusion sequences, to which constrained spherical deconvolution pipeline was applied, to obtain a whole brain tractogram. Whole brain T1 parcellation was obtained by Freesurfer, allowing to dissect the tractogram and identify the connections between the caudate nucleus and Broca’s area. Postoperative MRI standard diffusion the day after surgery was performed, allowing to delineate and register to the preoperative MRI any area of hyperintense diffusion with low apparent diffusion coefficient. The pathway between pars triangularis (resp. opercularis) and Broca’s area were considered as damaged whenever more than 50% of streamlines were passing through the mini-strokes. Patients’ language abilities (including a picture naming task) were assessed and reported before, during and after surgery by certified speech therapists. Severe postoperative naming deficits were defined as a score lower than 40/80 items. Contingency tables were analyzed with Fisher exact test (statistical significance set at 0.05).

Results

Out the 14 patients, 8 patients had a mini-stroke on the immediate postoperative MRI. None of the 6 patients without any stroke had postoperative naming severe deficits. Five out the 8 patients with a mini-stroke had a severe postoperative naming deficit, characterized by strong verbal perseverations. This difference was statistically significant (exact Fisher test, p = 0.03). For the five patients with a deficit, the mini-stroke damaged either the pars triangularis – caudate pathway or the pars opercularis – caudate pathway, whenever the pars triangularis was resected after negative cortical mapping. For the three patients without severe postoperative naming deficit, the mini-stroke spared the Broca-caudate pathway. All patients recovered quasi-normal naming abilities at the 4-month postoperative evaluation.

Conclusions

The occurrence of mini-strokes within the connections between Broca’s area and the caudate nucleus explains the sudden naming deficits observed intraoperatively in some patients during awake resection of IDH-mutated insular glioma. Further studies are needed to better predict such event and to assess its impact on other cognitive functions.