Abstract
ObjectivesGliomas are widely considered to be related to the altered topological organization of functional networks before operations. Tumors are usually thought to cause multimodal cognitive impairments. The structure is thought to form the basics of function, and the aim of this study was to reveal the rich-club organization and topological patterns of white matter (WM) structural networks associated with cognitive impairments in patients with frontal and temporal gliomas.MethodsGraph theory approaches were utilized to reveal the global and regional topological organization and rich-club organization of WM structural networks of 14 controls (CN), 13 frontal tumors (FTumor), and 18 temporal tumors (TTumor). Linear regression was used to assess the relationship between cognitive performances and altered topological parameters.ResultsWhen compared with CN, both FTumor and TTumor showed no alterations in small-world properties and global network efficiency, but instead showed altered local network efficiency. Second, FTumor and TTumor patients showed similar deficits in the nodal shortest path in the left rolandic operculum and degree centrality (DC) of the right dorsolateral and medial superior frontal gyrus (SFGmed). Third, compared to FTumor patients, TTumor patients showed a significantly higher DC in the right dorsolateral and SFGmed, a higher level of betweenness in the right SFGmed, and higher nodal efficiency in the left middle frontal gyrus and right SFGmed. Finally, rich-club organization was disrupted, with increased structural connectivity among rich-club nodes and reduced structural connectivity among peripheral nodes in FTumor and TTumor patients. Altered local efficiency in TTumor correlated with memory function, while altered local efficiency in FTumor correlated with the information processing speed.ConclusionBoth FTumor and TTumor presented an intact global topology and altered regional topology related to cognitive impairment and may also share the convergent and divergent regional topological organization of WM structural networks. This suggested that a compensatory mechanism plays a key role in global topology formation in both FTumor and TTumor patients, and as such, development of a structural connectome for patients with brain tumors would be an invaluable medical resource and allow clinicians to make comprehensive preoperative planning.
Highlights
Gliomas are the most frequently occurring type of primary brain tumors (Ostrom et al, 2014), and when the human brain is considered an exceedingly complex network, understanding its functional anatomy is essential for safe and effective neurosurgery
The key findings of this study are as follows: (i) compared to the CN group, FTumor and TTumor showed alterations in local efficiency; (ii) FTumor and TTumor patients showed similar deficits of the nodal shortest path in left rolandic operculum, and degree centrality in right dorsolateral superior frontal gyrus and SFGmed; and (iii) compared with FTumor patients, TTumor patients showed significantly higher DC in right dorsolateral and SFGmed, higher betweenness centrality (BC) in right SFGmed, and higher nodal efficiency (NE) in left middle frontal gyrus (MFG) and right SFGmed
It is reasonable that FTumor and TTumor may share convergent and divergent altered regional topological organization of WM structural networks, which is linked to specific cognitive impairment
Summary
Gliomas are the most frequently occurring type of primary brain tumors (Ostrom et al, 2014), and when the human brain is considered an exceedingly complex network, understanding its functional anatomy is essential for safe and effective neurosurgery. With many recent studies examining brain function, rather than limited to specific local functions, it shows that detecting abnormal patterns associated with cognitive impairment in the structural brain network in patients with gliomas is of increasing clinical importance in comprehensive preoperative planning. The development of complex network analysis using graph theory (i.e., connectome) in the brain offers the potential to identify the impacts of focal and diffuse pathologies in glioma patients (Fornito et al, 2013; Hart et al, 2016), such as rich-club organization (Yan et al, 2018; Wang et al, 2019), small-world characteristics (Iturria-Medina et al, 2011; Yan et al, 2018), betweenness (Iturria-Medina et al, 2011), and global and local network efficiency (Iturria-Medina et al, 2011; Shu et al, 2018). From the perspective of global impairment of neural networks, the graph theory can provide a novel pathway with which to further identify the structural and functional organization in glioma patients
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