Data_Sheet_1_Altered Rich-Club Organization and Regional Topology Are Associated With Cognitive Decline in Patients With Frontal and Temporal Gliomas.PDF

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.

研究目的：目前普遍认为，胶质瘤与术前功能网络的拓扑结构改变密切相关；而肿瘤通常会引发多模态认知功能损害。脑结构是脑功能的基础，本研究旨在揭示额部与颞部胶质瘤患者中，与认知损害相关的白质（white matter, WM）结构网络的富俱乐部（rich-club）组织结构及其拓扑模式。
研究方法：本研究采用图论（graph theory）分析方法，对14名健康对照（controls, CN）、13例额部胶质瘤患者（frontal tumors, FTumor）及18例颞部胶质瘤患者（temporal tumors, TTumor）的白质结构网络的全局、局部拓扑组织模式及富俱乐部组织结构进行分析；并通过线性回归分析评估认知表现与拓扑参数改变之间的关联。
研究结果：与健康对照相比，额部胶质瘤患者与颞部胶质瘤患者的小世界属性（small-world properties）及全局网络效率均未出现明显改变，但局部网络效率存在异常。其次，两类患者均在左侧中央岛盖（rolandic operculum）的节点最短路径，以及右侧背外侧额上回、内侧额上回（superior frontal gyrus medial, SFGmed）的度中心性（degree centrality, DC）方面出现相似的损害。进一步对比发现，颞部胶质瘤患者的右侧背外侧额上回及内侧额上回的度中心性、右侧内侧额上回的介数中心性（betweenness），以及左侧额中回、右侧内侧额上回的节点效率（nodal efficiency）均显著高于额部胶质瘤患者。最后，两类患者的富俱乐部组织结构均遭到破坏：富俱乐部节点间的结构连接增强，而外周节点间的结构连接减弱。此外，颞部胶质瘤患者的局部效率改变与记忆功能相关，额部胶质瘤患者的局部效率改变则与信息处理速度相关。
研究结论：额部与颞部胶质瘤患者均保留了完整的全局拓扑结构，但其局部拓扑结构出现了与认知损害相关的改变，且二者在白质结构网络的区域拓扑组织上存在趋同与分化特征。这提示代偿机制在两类患者的全局拓扑结构维持中发挥关键作用；因此，构建脑肿瘤患者的结构连接组（structural connectome）将成为极具价值的医学资源，可帮助临床医师制定全面的术前规划方案。