Increasing nodal vulnerability and nodal efficiency implied recovery time prolonging in patients with supplementary motor area syndrome

Shengyu Fang, Lianwang Li, Shimeng Weng, Zhong Zhang, Xing Fan, Tao Jiang, Yinyan Wang, Shengyu Fang, Lianwang Li, Shimeng Weng, Zhong Zhang, Xing Fan, Tao Jiang, Yinyan Wang

Abstract

Supplementary motor area (SMA) syndrome is a surgery-related complication that commonly occurs after removing SMA glioma, and needs weeks to recover. However, susceptible factors of patients suffering from SMA syndrome remain unknown. Graphic theory was applied to reveal topological properties of sensorimotor network (SMN) by processing resting-state functional magnetic resonance images in 66 patients with SMA gliomas. Patients were classified into SMA and non-SMA groups based on whether they suffered from SMA syndrome. We collected recovery time and used causal mediation analysis to find association between topological properties and recovery time. Compared with the non-SMA group, higher vulnerability (left: p = .0018; right: p = .0033) and lower fault tolerance (left: p = .0022; right: p = .0248) of the whole SMN were found in the SMA group. Moreover, higher nodal properties of lesional-hemispheric cingulate cortex (nodal efficiency: left, p = .0389; right, p = .0169; nodal vulnerability: left, p = .0185; right, p = .0085) and upper limb region of primary motor cortex (PMC; nodal efficiency: left, p = .0132; right, p = .0001; nodal vulnerability: left, p = .0091; right, p = .0209) were found in the SMA group. Nodal efficiency and nodal vulnerability of cingulate cortex and upper limb region of PMC were important predictors for SMA syndrome occurring and recovery time prolonging. Neurosurgeons should carefully deal with upper limb region of PMC and cingulate cortex, and protect them if these two region were unnecessary to damage during SMA glioma resection.

Keywords: awake craniotomy; causal mediation analysis; glioma; supplementary motor area syndrome; topological properties.

© 2022 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.

Figures

FIGURE 1
FIGURE 1
The locations of tumor, upper limb region of BA 4 (A4ul), and cingulate cortex. (a–d) Glioma did not involve in cingulate cortex or A4ul. (e–h) Glioma did not involve in A4ul but involve in cingulate cortex. (i–l) Glioma did not involve in cingulate cortex but involve in A4ul. (a, e, and i) Preoperative T1 and T2 images; (b, f, and j). Postoperative T1 and T2 images. (c, g, and k) Extent of tumor resection and location of cingulate cortex. The blue dotted line was cingulate sulcus. The red region was extent of tumor resection. (d, h, and l) Extent of tumor resection and location of the A4ul. The red region was extent of tumor resection, and the green region was the hand knob that represents the A4ul to region of tumor resection. If the d < 5 mm, the extent of tumor resection was defined as adjacent to/involving in the A4ul. Point C was the midpoint of Point A and Point B that two endpoints of hand knob. Point E was the point which was nearest to the Point C.
FIGURE 2
FIGURE 2
The information of patient recruitment
FIGURE 3
FIGURE 3
Differences of global properties between the SMA, non‐SMA, and healthy groups. (a) Comparison results when the glioma was in the left hemisphere. (b) Comparison results when the glioma was in the right hemisphere. BA, Brodmann area; SMA, supplementary motor area
FIGURE 4
FIGURE 4
Differences of nodal properties between the SMA, non‐SMA, and healthy groups when the glioma was in the left hemisphere. Node no. 2 (dark yellow) = medial BA 6; node no. 3 (pink) = ventrolateral BA 6; node no. 5 (green) = upper limb of BA 4; node no. 7 (green) = trunk region of BA 4; node no. 11 (light blue) = caudal ventrolateral BA 6; node no. 15 (light yellow) = left hemispheric upper limb and face of BA 1/2/3; node no. 16 (dark blue) = right hemispheric upper limb and face of BA 1/2/3; node 25 (black) = caudal area BA 23 (cingulate cortex). BA, Brodmann area; SMA, supplementary motor area
FIGURE 5
FIGURE 5
Differences of nodal properties between the SMA, non‐SMA, and healthy groups when the glioma was in the left hemisphere. Node no. 2 (dark yellow) = medial BA 6; node no. 4 (pink) = caudal dorsolateral BA 6; node no. 5 (dark green) = left hemispheric upper limb of BA 4; node no. 6 (light green) = right hemispheric upper limb of BA 4node; node no. 7 (orange) = trunk region of BA 4; node no. 8 (brown) = trunk region of BA 4; node no. 12 (light blue) = caudal ventrolateral BA 6; node no. 15 (light yellow) = left hemispheric upper limb and face of BA 1/2/3; node no. 16 (dark blue) = right hemispheric upper limb and face of BA 1/2/3; node 26 (black) = caudal area BA 23 (cingulate cortex). BA, Brodmann area; SMA, supplementary motor area
FIGURE 6
FIGURE 6
Causal mediation analysis of recovery time of SMA syndrome and nodal topological properties. The main factor to causing SMA syndrome and prolonged recovery time was that nodes (A4ul and A23c) were affected by surgical regions and postoperative edema, and increased nodal efficiency and nodal vulnerability before surgery of these two nodes mediated this phenomenon; SMA, supplementary motor area

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