Anna V Dowling, Benjamin A Seitzman, Timothy J Mitchell, Michael Olufawo, Donna L Dierker, Hari Anandarajah, Ally Dworetsky, Alana McMichael, Catherine Jiang, Dennis L Barbour, Bradley L Schlaggar, David D Limbrick, Jennifer M Strahle, Joshua B Rubin, Joshua S Shimony, Stephanie M Perkins
{"title":"质子治疗儿童脑肿瘤患者的认知和脑系统分离。","authors":"Anna V Dowling, Benjamin A Seitzman, Timothy J Mitchell, Michael Olufawo, Donna L Dierker, Hari Anandarajah, Ally Dworetsky, Alana McMichael, Catherine Jiang, Dennis L Barbour, Bradley L Schlaggar, David D Limbrick, Jennifer M Strahle, Joshua B Rubin, Joshua S Shimony, Stephanie M Perkins","doi":"10.14338/IJPT-22-00039.1","DOIUrl":null,"url":null,"abstract":"<p><strong>Purpose: </strong>Pediatric brain tumor patients often experience significant cognitive sequelae. Resting-state functional MRI (rsfMRI) provides a measure of brain network organization, and we hypothesize that pediatric brain tumor patients treated with proton therapy will demonstrate abnormal brain network architecture related to cognitive outcome and radiation dosimetry.</p><p><strong>Participants and methods: </strong>Pediatric brain tumor patients treated with proton therapy were enrolled on a prospective study of cognitive assessment using the NIH Toolbox Cognitive Domain. rsfMRI was obtained in participants able to complete unsedated MRI. Brain system segregation (BSS), a measure of brain network architecture, was calculated for the whole brain, the high-level cognition association systems, and the sensory-motor systems.</p><p><strong>Results: </strong>Twenty-six participants were enrolled in the study for cognitive assessment, and 18 completed rsfMRI. There were baseline cognitive deficits in attention and inhibition and processing speed prior to radiation with worsening performance over time in multiple domains. Average BSS across the whole brain was significantly decreased in participants compared with healthy controls (1.089 and 1.101, respectively; <i>P</i> = 0.001). Average segregation of association systems was significantly lower in participants than in controls (<i>P</i> < 0.001) while there was no difference in the sensory motor networks (<i>P</i> = 0.70). Right hippocampus dose was associated with worse attention and inhibition (<i>P</i> < 0.05) and decreased segregation in the dorsal attention network (<i>P</i> < 0.05).</p><p><strong>Conclusion: </strong>Higher mean dose to the right hippocampus correlated with worse dorsal attention network segregation and worse attention and inhibition cognitive performance. Patients demonstrated alterations in brain network organization of association systems measured with rsfMRI; however, somatosensory system segregation was no different from healthy children. Further work with preradiation rsfMRI is needed to assess the effects of surgery and presence of a tumor on brain network architecture.</p>","PeriodicalId":36923,"journal":{"name":"International Journal of Particle Therapy","volume":null,"pages":null},"PeriodicalIF":2.1000,"publicationDate":"2023-07-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10563667/pdf/","citationCount":"0","resultStr":"{\"title\":\"Cognition and Brain System Segregation in Pediatric Brain Tumor Patients Treated with Proton Therapy.\",\"authors\":\"Anna V Dowling, Benjamin A Seitzman, Timothy J Mitchell, Michael Olufawo, Donna L Dierker, Hari Anandarajah, Ally Dworetsky, Alana McMichael, Catherine Jiang, Dennis L Barbour, Bradley L Schlaggar, David D Limbrick, Jennifer M Strahle, Joshua B Rubin, Joshua S Shimony, Stephanie M Perkins\",\"doi\":\"10.14338/IJPT-22-00039.1\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Purpose: </strong>Pediatric brain tumor patients often experience significant cognitive sequelae. Resting-state functional MRI (rsfMRI) provides a measure of brain network organization, and we hypothesize that pediatric brain tumor patients treated with proton therapy will demonstrate abnormal brain network architecture related to cognitive outcome and radiation dosimetry.</p><p><strong>Participants and methods: </strong>Pediatric brain tumor patients treated with proton therapy were enrolled on a prospective study of cognitive assessment using the NIH Toolbox Cognitive Domain. rsfMRI was obtained in participants able to complete unsedated MRI. Brain system segregation (BSS), a measure of brain network architecture, was calculated for the whole brain, the high-level cognition association systems, and the sensory-motor systems.</p><p><strong>Results: </strong>Twenty-six participants were enrolled in the study for cognitive assessment, and 18 completed rsfMRI. There were baseline cognitive deficits in attention and inhibition and processing speed prior to radiation with worsening performance over time in multiple domains. Average BSS across the whole brain was significantly decreased in participants compared with healthy controls (1.089 and 1.101, respectively; <i>P</i> = 0.001). Average segregation of association systems was significantly lower in participants than in controls (<i>P</i> < 0.001) while there was no difference in the sensory motor networks (<i>P</i> = 0.70). Right hippocampus dose was associated with worse attention and inhibition (<i>P</i> < 0.05) and decreased segregation in the dorsal attention network (<i>P</i> < 0.05).</p><p><strong>Conclusion: </strong>Higher mean dose to the right hippocampus correlated with worse dorsal attention network segregation and worse attention and inhibition cognitive performance. Patients demonstrated alterations in brain network organization of association systems measured with rsfMRI; however, somatosensory system segregation was no different from healthy children. Further work with preradiation rsfMRI is needed to assess the effects of surgery and presence of a tumor on brain network architecture.</p>\",\"PeriodicalId\":36923,\"journal\":{\"name\":\"International Journal of Particle Therapy\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":2.1000,\"publicationDate\":\"2023-07-24\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10563667/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"International Journal of Particle Therapy\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.14338/IJPT-22-00039.1\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2023/1/1 0:00:00\",\"PubModel\":\"eCollection\",\"JCR\":\"Q3\",\"JCRName\":\"ONCOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"International Journal of Particle Therapy","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.14338/IJPT-22-00039.1","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2023/1/1 0:00:00","PubModel":"eCollection","JCR":"Q3","JCRName":"ONCOLOGY","Score":null,"Total":0}
引用次数: 0
摘要
目的:儿童脑肿瘤患者经常会出现严重的认知后遗症。静息状态功能性MRI(rsfMRI)提供了一种脑网络组织的测量方法,我们假设接受质子治疗的儿童脑肿瘤患者将表现出与认知结果和辐射剂量测定相关的异常脑网络结构。参与者和方法:使用NIH Toolbox cognitive Domain对接受质子治疗的儿童脑肿瘤患者进行认知评估的前瞻性研究。rsfMRI是在能够完成未过时MRI的参与者中获得的。计算了整个大脑、高级认知联想系统和感觉运动系统的脑系统分离(BSS),这是一种衡量大脑网络结构的指标。结果:26名参与者被纳入该研究进行认知评估,18人完成了rsfMRI。辐射前,在注意力、抑制和处理速度方面存在基线认知缺陷,随着时间的推移,在多个领域的表现不断恶化。与健康对照组相比,参与者整个大脑的平均BSS显著降低(分别为1.089和1.101;P = 0.001)。参与者的平均关联系统分离显著低于对照组(P P = 0.70)。右侧海马剂量与更差的注意力和抑制有关(P P 结论:右海马平均剂量越高,背侧注意网络分离越差,注意和抑制认知表现越差。患者表现出用rsfMRI测量的关联系统的脑网络组织的改变;然而,体感系统分离与健康儿童没有什么不同。需要对预辐射rsfMRI进行进一步的研究,以评估手术和肿瘤对脑网络结构的影响。
Cognition and Brain System Segregation in Pediatric Brain Tumor Patients Treated with Proton Therapy.
Purpose: Pediatric brain tumor patients often experience significant cognitive sequelae. Resting-state functional MRI (rsfMRI) provides a measure of brain network organization, and we hypothesize that pediatric brain tumor patients treated with proton therapy will demonstrate abnormal brain network architecture related to cognitive outcome and radiation dosimetry.
Participants and methods: Pediatric brain tumor patients treated with proton therapy were enrolled on a prospective study of cognitive assessment using the NIH Toolbox Cognitive Domain. rsfMRI was obtained in participants able to complete unsedated MRI. Brain system segregation (BSS), a measure of brain network architecture, was calculated for the whole brain, the high-level cognition association systems, and the sensory-motor systems.
Results: Twenty-six participants were enrolled in the study for cognitive assessment, and 18 completed rsfMRI. There were baseline cognitive deficits in attention and inhibition and processing speed prior to radiation with worsening performance over time in multiple domains. Average BSS across the whole brain was significantly decreased in participants compared with healthy controls (1.089 and 1.101, respectively; P = 0.001). Average segregation of association systems was significantly lower in participants than in controls (P < 0.001) while there was no difference in the sensory motor networks (P = 0.70). Right hippocampus dose was associated with worse attention and inhibition (P < 0.05) and decreased segregation in the dorsal attention network (P < 0.05).
Conclusion: Higher mean dose to the right hippocampus correlated with worse dorsal attention network segregation and worse attention and inhibition cognitive performance. Patients demonstrated alterations in brain network organization of association systems measured with rsfMRI; however, somatosensory system segregation was no different from healthy children. Further work with preradiation rsfMRI is needed to assess the effects of surgery and presence of a tumor on brain network architecture.