Long-term motor deficit in brain tumour surgery with preserved intra-operative motor-evoked potentials

Abstract

Muscle motor-evoked potentials are commonly monitored during brain tumour surgery in motor areas, as these are assumed to reflect the integrity of descending motor pathways, including the corticospinal tract. However, while the loss of muscle motor-evoked potentials at the end of surgery is associated with long-term motor deficits (muscle motor-evoked potential-related deficits), there is increasing evidence that motor deficit can occur despite no change in muscle motor-evoked potentials (muscle motor-evoked potential-unrelated deficits), particularly after surgery of non-primary regions involved in motor control. In this study, we aimed to investigate the incidence of muscle motor-evoked potential-unrelated deficits and to identify the associated brain regions. We retrospectively reviewed 125 consecutive patients who underwent surgery for peri-Rolandic lesions using intra-operative neurophysiological monitoring. Intraoperative changes in muscle motor-evoked potentials were correlated with motor outcome, assessed by the Medical Research Council scale. We performed voxel-lesion-symptom mapping to identify which resected regions were associated with short- and long-term muscle motor-evoked potential-associated motor deficits. Muscle motor-evoked potentials reductions significantly predicted long-term motor deficits. However, in more than half of the patients who experienced long-term deficits (12/22 patients), no muscle motor-evoked potential reduction was reported during surgery. Lesion analysis showed that muscle motor-evoked potential-related long-term motor deficits were associated with direct or ischaemic damage to the corticospinal tract, whereas muscle motor-evoked potential-unrelated deficits occurred when supplementary motor areas were resected in conjunction with dorsal premotor regions and the anterior cingulate. Our results indicate that long-term motor deficits unrelated to the corticospinal tract can occur more often than currently reported. As these deficits cannot be predicted by muscle motor-evoked potentials, a combination of awake and/or novel asleep techniques other than muscle motor-evoked potentials monitoring should be implemented.

Keywords: SMA-syndrome; brain mapping; intra-operative neurophysiological monitoring (IONM); motor-evoked potentials (MEPs); neuro-oncology.

Graphical Abstract

Figure 1

Motor outcome in relationship with MEP reduction for upper and lower limb. Upper limb: Motor deficits are shown in the left column and further sub-divided according to MEP variation into MEP-related (MEP drop >50% amplitude) and MEP-unrelated (motor deficit with no significant MEP-reduction). The bar charts show that MEP-unrelated deficits accounted for majority of deficits in the post-operative phase and half of the motor deficits at follow-up. MEP-unrelated motor deficits were fewer but more severe, normally long-lasting. Severity of motor deficits = Mild (MRC, ≤1), Moderate (MRC, >1 and ≤2) and Severe (MRC, >2).

Figure 2

VLSM analysis for MEP reduction and upper limb deficits. Short-term: (A) MEP-related short-term deficits occurred mainly for insular resections, whereas (B) MEP-unrelated short-term motor deficits were associated with damage of the pre-SMA and SMA. Long-term: (C) MEP-related long-term deficits in the upper limb occurred after lesioning of the white-matter deep within the hand knob as well as after insular resection, suggesting damage to the corticospinal tract. (D) On the other hand, MEP-unrelated deficits occurred when re-secting the pre-SMA and SMA combined with the dorsal pre-motor cortex and the anterior cingulate cortex. Long-term deficits for SMA resection: (E) re-section of the SMA caused both short-term and long-term MEP-unrelated deficits in our cohort of patients. When contrasting these two cohorts of patients, long-term MEP-unrelated deficits occurred when SMA and pre-SMA as well as the dorsal pre-motor to the anterior cingulate cortex were re-sected. In contrast, no other area was associated with short-term deficits (data not shown).