Anti-TNFα therapy in IBD alters brain activity reflecting visceral sensory function and cognitive-affective biases

Gray, Marcus A.; Chen, Chao; Staudacher, Heidi M; Kolosky, Natasha A.; Talley, Nicholas J.; Holtmann, Gerald

doi:10.1371/journal.pone.0193542

Cited by 47 publications

(36 citation statements)

References 60 publications

(57 reference statements)

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“…Second, small volume correction (SVC) was applied over the following cerebral regions: frontal gyrus, hippocampus, caudate nucleus, and cingulate cortex. In previous studies, these brain regions were aberrantly altered in patients with UC (Agostini et al, 2011; Gray et al, 2018). SVC was conducted by applying a familywise error (FWE) correction of p < 0.05 and a cluster size threshold of 20 contiguous voxels in the brain region (Vachon et al, 2013).…”

Section: Methodsmentioning

confidence: 78%

Aberrant Brain Function in Active-Stage Ulcerative Colitis Patients: A Resting-State Functional MRI Study

Fan

Zhang

et al. 2019

Front. Hum. Neurosci.

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Background : Patients with ulcerative colitis (UC) usually display cognitive impairments, such as memory loss, attention deficits, and declining executive functions, particularly during the active stage of the disease. However, the potential neurological mechanisms of these symptoms remain unclear. Method : Forty-one patients with mildly to moderately active UC, as well as 42 matched healthy controls, were recruited for an examination using psychological scales, cognitive function tests and resting-state functional magnetic resonance imaging (rs-fMRI). Seed points were identified via analysis of amplitude of low-frequency fluctuation (ALFF), and functional connectivity (FC) was calculated between these seed regions and other voxels in the whole brain. Correlation analyses were performed among clinical indexes, neuropsychological assessments and neuroimaging data. Result : Compared with the healthy controls, patients with UC exhibited lower ALFF values in the bilateral hippocampal/parahippocampal (HIPP/ParaHIPP) region and higher ALFF values in the left posterior cingulate cortex (PCC.L) and left middle frontal gyrus (MFG.L). With HIPP/ParaHIPP as the seed point, the strengths of the FC in the bilateral middle frontal gyri (MFG), anterior cingulate cortex (ACC), and left caudate nucleus (CAU.L) increased; using the PCC.L as the seed point, the strengths of the FC in the middle cingulate cortex (MCC) and the left angular gyrus (AUG.L) increased. These abnormal brain regions were mainly located in the limbic system. By analyzing the correlations between these brain regions and behavioral data, we observed a close correlation between decreased HIPP/ParaHIPP activity and memory loss; increased PCC activity and strength of FC with the AUG.L were related to dysfunction of executive function and attention network in patients with UC. Conclusion : Based on these results, the limbic lobe might be the core of the brain-gut axis (BGA) and play an important role in cognitive impairments, suggesting potential mechanisms for cognitive impairment in patients with UC in the active stage of the disease.

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Section: Methodsmentioning

confidence: 78%

Aberrant Brain Function in Active-Stage Ulcerative Colitis Patients: A Resting-State Functional MRI Study

Fan

Zhang

et al. 2019

Front. Hum. Neurosci.

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“…Patients with IBD display cognitive impairments and psychomotor performance, particularly during the active stage of the disease [35,36]. The treatment of patients with IBD by an anti-inflammatory drug alleviates the brain function involved in visceral sensitivity and cognitive-affective biases [37,38]. These findings suggest that the pathogenesis of psychiatric disorders is closely associated with the gut microbiota.…”

Section: Discussionmentioning

confidence: 98%

The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment

et al. 2020

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Background: In a pilot study, we found that feces transplantation from elderly individuals to mice significantly caused cognitive impairment. Paenalcaligenes hominis and Escherichia coli are increasingly detected in the feces of elderly adults and aged mice. Therefore, we isolated Paenalcaligenes hominis and Escherichia coli from the feces of elderly individuals and aged mice and examined their effects on the occurrence of age-related degenerative cognitive impairment and colonic inflammation in mice. Results: The transplantation of feces collected from elderly people and aged mice caused significantly more severe cognitive impairment in transplanted young mice than those from young adults and mice. Oral gavage of Paenalcaligenes hominis caused strong cognitive impairment and colitis in specific pathogen-free (SPF) and germfree mice. Escherichia coli also induced cognitive impairment and colitis in SPF mice. Oral gavage of Paenalcaligenes hominis, its extracellular vesicles (EVs), and/or lipopolysaccharide caused cognitive impairment and colitis in mice. However, celiac vagotomy significantly inhibited the occurrence of cognitive impairment, but not colitis, in mice exposed to Paenalcaligenes hominis or its EVs, whereas its lipopolysaccharide or Escherichia coli had no such effects. Vagotomy also inhibited the infiltration of EVs into the hippocampus. Conclusions: Paenalcaligenes hominis, particularly its EVs, can cause cognitive function-impaired disorders, such as Alzheimer's disease, and its EVs may penetrate the brain through the blood as well as the vagus nerve.

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“…It appears at least possible that these symptoms in a subgroup of patients are due to SIBO. It is also possible that SIBO‐related symptoms are more severe due to alterations of structural and/or sensory function in patients with IBD due to the effects of inflammatory mediators …”

Section: Discussionmentioning

confidence: 99%

Systematic review with meta‐analysis: the prevalence of small intestinal bacterial overgrowth in inflammatory bowel disease

Shah

Morrison

Burger

et al. 2019

Aliment Pharmacol Ther

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Background: Current data on small intestinal bacterial overgrowth (SIBO) in patients with inflammatory bowel diseases (IBD) are controversial.Aim: To conduct a systematic review and meta-analysis to determine the prevalence of SIBO in patients with ulcerative colitis (UC) and Crohn's disease (CD). Methods: Electronic databases were searched up to May 2018 for studies reporting prevalence of SIBO in IBD patients. The prevalence rate of SIBO among IBD patients and the odds ratio (OR) and 95% CI of SIBO in IBD patients compared with controls were calculated. Results: The final dataset included 11 studies (1175 adult patients with IBD and 407 controls), all utilising breath test for diagnosis of SIBO. The proportion of SIBO in IBD patients was 22.3% (95% CI 19.92-24.68). The OR for SIBO in IBD patients was 9.51 (95% CI 3.39-26.68) compared to non-IBD controls, and high in both CD (OR = 10.86; 95% CI 2.76-42.69) and UC (OR = 7.96; 95% CI 1.66-38.35). In patients with CD, subgroup analysis showed the presence of fibrostenosing disease (OR = 7.47; 95% CI 2.51-22.20) and prior bowel surgery (OR = 2.38; 95% CI 1.65-3.44), especially resection of the ileocecal valve, increased the odds of SIBO. Individual studies suggest that combined small and large bowel disease but not disease activity may be associated with SIBO. Conclusions: Overall, there is a substantial increase in the prevalence of SIBO in IBD patients compared to controls. Prior surgery and the presence of fibrostenosing disease are risk factors for SIBO in IBD. Additional supporting information will be found online in the Supporting Information section at the end of the article. How to cite this article: Shah A, Morrison M, Burger D, et al. Systematic review with meta-analysis: the prevalence of small intestinal bacterial overgrowth in inflammatory bowel disease.

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Anti-TNFα therapy in IBD alters brain activity reflecting visceral sensory function and cognitive-affective biases

Cited by 47 publications

References 60 publications

Aberrant Brain Function in Active-Stage Ulcerative Colitis Patients: A Resting-State Functional MRI Study

Aberrant Brain Function in Active-Stage Ulcerative Colitis Patients: A Resting-State Functional MRI Study

The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment

Systematic review with meta‐analysis: the prevalence of small intestinal bacterial overgrowth in inflammatory bowel disease

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