Department of Health, Medicine and Caring Sciences, Linköping University, Linköping, Sweden.
Department of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.
Brain Behav Immun. 2021 Feb;92:211-222. doi: 10.1016/j.bbi.2020.11.035. Epub 2020 Nov 26.
Irritable bowel syndrome (IBS) is a symptom-based disorder of gut-brain interactions generating abdominal pain. It is also associated with a vulnerability to develop extraintestinal symptoms, with fatigue often reported as one of the most disturbing. Fatigue is related to brain function and inflammation in several disorders, however, the mechanisms of such relations in IBS remain elusive. This study aimed to elucidate fatigue and its association with a resting state network of mesocorticolimbic regions of known importance in fatigue, and to explore the possible role of circulating TNF-α levels in IBS and healthy controls (HC). Resting state functional magnetic resonance imaging (fMRI) was conducted in 88 IBS patients and 47 HC of similar age and gender to investigate functional connectivity between mesocorticolimbic regions. Further, fatigue impact on daily life and plasma levels of the proinflammatory cytokine tumor necrosis factor-α (TNF-α), of known relevance to immune activation in IBS, were also measured. The selected mesocorticolimbic regions indeed formed a functionally connected network in all participants. The nucleus accumbens (NAc), in particular, exhibited functional connectivity to all other regions of interest. In IBS, fatigue impact on daily life was negatively correlated with the connectivity between NAc and dorsolateral prefrontal cortex bilaterally (left p = 0.019; right p = 0.038, corrected for multiple comparisons), while in HC, fatigue impact on daily life was positively correlated to the connectivity between the right NAc and anterior middle insula in both hemispheres (left p = 0.009; right p = 0.011). We found significantly higher levels of TNF-α in IBS patients compared to HC (p = 0.001) as well as a positive correlation between TNF-α and fatigue impact on daily life in IBS patients (rho = 0.25, p = 0.02) but not in HC (rho = -0.13, p = 0.37). There was no association between functional connectivity in the mesocorticolimbic network and plasma levels of TNF-α in either group In summary, this novel multimodal study provides the first evidence that the vulnerability to fatigue in IBS is associated with connectivity within a mesocorticolimbic network as well as immune activation. These findings warrant further investigation, both peripherally and potentially with measurements of central immune activation as well.
肠易激综合征(IBS)是一种基于症状的胃肠道-大脑相互作用紊乱,会产生腹痛。它还与发展为肠外症状的易感性有关,疲劳经常被报告为最令人困扰的症状之一。在几种疾病中,疲劳与大脑功能和炎症有关,然而,IBS 中这些关系的机制仍不清楚。本研究旨在阐明疲劳及其与已知对疲劳有重要作用的中脑边缘皮质网络的关联,并探讨循环 TNF-α 水平在 IBS 和健康对照组(HC)中的可能作用。对 88 名 IBS 患者和 47 名年龄和性别相似的 HC 进行静息状态功能磁共振成像(fMRI),以研究中脑边缘皮质网络中各区域之间的功能连接。此外,还测量了疲劳对日常生活的影响和促炎细胞因子肿瘤坏死因子-α(TNF-α)的血浆水平,TNF-α 已知与 IBS 中的免疫激活有关。所选的中脑边缘皮质网络实际上在所有参与者中形成了一个功能连接的网络。特别是,伏隔核(NAc)与所有其他感兴趣的区域均有功能连接。在 IBS 中,疲劳对日常生活的影响与双侧背外侧前额叶皮质(左侧 p = 0.019;右侧 p = 0.038,经多重比较校正)之间的 NAc 和背外侧前额叶皮质之间的连接呈负相关,而在 HC 中,疲劳对日常生活的影响与右侧 NAc 和两侧前岛叶之间的连接呈正相关(左侧 p = 0.009;右侧 p = 0.011)。与 HC 相比,IBS 患者的 TNF-α 水平显著升高(p = 0.001),并且 IBS 患者的 TNF-α 与疲劳对日常生活的影响之间存在正相关(rho = 0.25,p = 0.02),但在 HC 中则没有(rho = -0.13,p = 0.37)。两组患者的中脑边缘皮质网络的功能连接与 TNF-α 的血浆水平之间均无关联。总之,这项新的多模态研究首次提供了证据,表明 IBS 中对疲劳的易感性与中脑边缘皮质网络内的连接以及免疫激活有关。这些发现值得进一步研究,不仅要在外周进行研究,还可能需要进行中枢免疫激活的测量。