Prediction of Recovery From Supplementary Motor Area Syndrome After Brain Tumor Surgery

Preoperative Diffusion Tensor Tractography Analysis and Postoperative Neurological Clinical Course

Kazunori Oda, MD; Fumio Yamaguchi, MD, PhD; Hiroyuki Enomoto, MD; Tadashi Higuchi, MD; Akio Morita, MD, PhD

Disclosures

Neurosurg Focus. 2018;44(6):e3 

In This Article

Abstract and Introduction

Abstract

Objective: Previous studies have suggested a correlation between interhemispheric sensorimotor networks and recovery from supplementary motor area (SMA) syndrome. In the present study, the authors examined the hypothesis that interhemispheric connectivity of the primary motor cortex in one hemisphere with the contralateral SMA may be important in the recovery from SMA syndrome. Further, they posited that motor cortical fiber connectivity with the SMA is related to the severity of SMA syndrome.

Methods: Patients referred to the authors' neurological surgery department were retrospectively analyzed for this study. All patients with tumors involving the unilateral SMA region, without involvement of the primary motor area, and diagnosed with SMA syndrome in the postoperative period were eligible for inclusion. Preoperative diffusion tensor imaging tractography (DTT) was used to examine the number of fiber tracts (NFidx) connecting the contralateral SMA to the ipsilateral primary motor area via the corpus callosum. Complete neurological examination had been performed in all patients in the pre- and postoperative periods. All patients were divided into two groups: those who recovered from SMA syndrome in ≤ 7 days (early recovery group) and those who recovered in ≥ 8 days (late recovery group). Differences between the two groups were assessed using the Student t-test and the chi-square test.

Results: Eleven patients (10 men, 1 woman) were included in the study. All patients showed transient postoperative motor deficits because of SMA syndrome. Tractography data revealed NFidx from the contralateral SMA to the ipsilateral primary motor area via the corpus callosum. The mean tumor volume (early 27.87 vs late 50.91 cm3, p = 0.028) and mean NFidx (early 8923.16 vs late 4726.4, p = 0.002) were significantly different between the two groups. Fisher exact test showed a significant difference in the days of recovery from SMA syndrome between patients with an NFidx > 8000 and those with an NFidx < 8000.

Conclusions: Diffusion tensor imaging tractography may be useful for predicting the speed of recovery from SMA syndrome. To the authors' knowledge, this is the first DTT study to identify interhemispheric connectivity of the SMA in patients with brain tumors.

Introduction

The supplementary motor area (SMA) is an eloquent area that plays an important role in the moving, planning, and learning of complicated actions, as well as the initiation of speech in the dominant hemisphere. The SMA is located in Brodmann area 6 and is defined by a single cortical field anterior to the leg representation of the primary motor cortex (PMC) along the medial aspect of the cerebral hemisphere down to the cingulate sulcus.[16,19] The SMA is composed of the SMA proper and the pre-SMA. The SMA proper is involved in planning, initiating, and coordinating complicated actions and in helping to maintain an erect posture, whereas the pre-SMA is involved in the cognitive aspects of complicated actions.[6,7]

The SMA has a high frequency of brain tumors, including up to 10% of de novo glioblastomas and 27% of low-grade gliomas.[4] Thus, the SMA is often a surgical target for tumor removal, and brain surgery in this area can lead to SMA syndrome. This syndrome was first reported to involve contralateral transient akinesia and mutism when the lesion was in the dominant hemisphere.[11,12] Resections of the SMA can cause immediate postoperative motor and speech deficits, which can resolve spontaneously and completely within days to months.[2,5] Thus, it is important for neurosurgeons to determine the anatomical and functional limits of an SMA resection and to identify SMA syndrome and monitor its course of recovery. However, the mechanism of recovery of SMA syndrome is poorly understood, although the contralateral SMA is thought to complement the function of the affected SMA.[1] Interestingly, Vassal et al. reported evidence of plasticity of the SMA, with large-scale modifications of the sensorimotor network, suggesting that interhemispheric connectivity may correlate with SMA syndrome recovery.[18]

In the present study, we hypothesized that interhemispheric connectivity of the PMC in one hemisphere with the contralateral SMA may play an important role in the recovery from SMA syndrome and that cortical fiber connections of the SMA may be associated with SMA syndrome recovery. To examine this hypothesis, we assessed preoperative diffusion tensor imaging (DTI) tractography (DTT) to determine the number of fibers extending from the contralateral SMA to the ipsilateral PMC, as well as the postoperative course of SMA syndrome, in patients with SMA syndrome following tumor removal.

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