Anti-inflammatory effect of vagus nerve stimulation in a rat model of inflammatory bowel disease

Meregnani, Julien; Clarençon, Didier; Vivier, M.; Peinnequin, André; Mouret, Catherine; Sinniger, Valérie; Picq, C.; Job, Agnès; Canini, Frédéric; Jacquier-Sarlin, Muriel R.; Bonaz, Bruno

doi:10.1016/j.autneu.2010.10.007

Cited by 243 publications

(212 citation statements)

References 56 publications

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“…Colonic inflammation was evaluated by a global multivariate index of colitis taking into account i) body weight, temperature and locomotor activity, ii) areas of lesions and histological damage, iii) biological parameters such as myeloperoxidase activity, cytokine and cytokine-related mRNAs at the level of colonic damage and just above. VNS significantly improved the multivariate index of colitis (Meregnani et al, 2011). The inflammatory infiltrate just immediately above the major colonic lesion was significantly improved by VNS while a slight reduction was observed in the lesion thus arguing for a major efficacy of VNS on tissues that are less damaged (Meregnani et al, 2011).…”

Section: Experimental Rationalementioning

confidence: 85%

“…VNS significantly improved the multivariate index of colitis (Meregnani et al, 2011). The inflammatory infiltrate just immediately above the major colonic lesion was significantly improved by VNS while a slight reduction was observed in the lesion thus arguing for a major efficacy of VNS on tissues that are less damaged (Meregnani et al, 2011). Sun et al (Sun et al, 2013) performed chronic VNS (0.25 mA, 20 Hz, 500 ms) in a model of TNBS colitis in rats and recorded heart rate variability (HRV) as a marker of the sympatho-vagal balance.…”

Section: Experimental Rationalementioning

confidence: 99%

“…Physostigmine, which crosses the blood brain barrier, induced a greater improvement of colitis than neostigmine pretreatment thus suggesting than central cholinergic pathways have a greater protective effect than peripheral pathways (Miceli & Jacobson, 2003). Based on this study and the description of the CAP, our group has performed low frequency (5 Hz) VNS in chronically implanted freely moving rats with the other parameters classically used for epilepsy, supposed to activate vagal efferents, for 5 consecutive days in rats with trinitrobenzenesulfonic acid (TNBS) colitis, classically used as an experimental model of CD (Meregnani et al, 2011). Colonic inflammation was evaluated by a global multivariate index of colitis taking into account i) body weight, temperature and locomotor activity, ii) areas of lesions and histological damage, iii) biological parameters such as myeloperoxidase activity, cytokine and cytokine-related mRNAs at the level of colonic damage and just above.…”

Section: Experimental Rationalementioning

confidence: 99%

“…VN stimulation (VNS) is presently used in the treatment of drug resistant epilepsy and depression (Milby et al, 2008) based on the widespread central projections of the VN (Ruffoli et al, 2011). More recently, VNS has been shown to improve experimental models of septic shock and colitis (Borovikova et al, 2000;Meregnani et al, 2011). Translational pilot studies have been recently performed in chronic inflammatory disorders such as CD and rheumatoid arthritis (Bonaz et al, 2016;Koopman et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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Is-there a place for vagus nerve stimulation in inflammatory bowel diseases?

Bonaz

2018

Bioelectron Med

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The vagus nerve (VN), the longest nerve of the organism that innervates the gastrointestinal tract, is a mixed nerve composed of 80% of afferent and 20% of efferent fibers. The VN has anti-inflammatory properties, in particular an anti-TNFα effect through the cholinergic anti-inflammatory pathway. The VN is a key component of the autonomic nervous system, i.e. the parasympathetic nervous system. An imbalance of the autonomic nervous system, as represented by a low vagal tone, is described in many diseases and has a pro-inflammatory role. Inflammatory bowel diseases (IBD) are chronic disorders of the gastro-intestinal tract where TNFα is a key cytokine. VN stimulation (VNS), classically used for the treatment of drug resistant epilepsy and depression, would be of interest in the treatment of IBD. We have recently reported in a 6 month follow-up pilot study that VNS improves active Crohn's disease. Preliminary data of another pilot study confirm this interest. Similarly, VNS has recently been reported to improve rheumatoid arthritis, another TNFα mediated disease. Bioelectronic Medicine, as represented by VNS, opens new therapeutic avenues in the treatment of such chronic inflammatory disorders. In the present manuscript, we will focus on the interest of VNS in IBD.

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Section: Experimental Rationalementioning

confidence: 85%

Section: Experimental Rationalementioning

confidence: 99%

Section: Experimental Rationalementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Is-there a place for vagus nerve stimulation in inflammatory bowel diseases?

Bonaz

2018

Bioelectron Med

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“…The mechanisms of vagus nerve stimulation(VNS) for epilepsy have not been fully understood. However, anti-inflammatory properties of VNS have been reported in various experimental models of inflammation [160], even it is still unknown whether the anti-convulsive effect of VNS was mediated through this anti-inflammatory mechanism. Meanwhile, many recent studies have shown that ketogenic diet has anti-inflammatory effects and protects against excitotoxicity-mediated neuronal cell death [161, 162].…”

Section: Perspectivesmentioning

confidence: 99%

Modulation of Immunity and the Inflammatory Response: A New Target for Treating Drug-resistant Epilepsy

Líu²,

Qin³

2013

Current Neuropharmacology

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Until recently, epilepsy medical therapy is usually limited to anti-epileptic drugs (AEDs). However, approximately 1/3 of epilepsy patients, described as drug-resistant epilepsy (DRE) patients, still suffer from continuous frequent seizures despite receiving adequate AEDs treatment of sufficient duration. More recently, with the remarkable progress of immunology, immunity and inflammation are considered to be key elements of the pathobiology of epilepsy. Activation of inflammatory processes in brain tissue has been observed in both experimental seizure animal models and epilepsy patients. Anti-inflammatory and immunotherapies also showed significant anticonvulsant properties both in clinical and in experimental settings. The above emerging evidence indicates that modulation of immunity and inflammatory processes could serve as novel specific targets to achieve potential anticonvulsant effects for the patients with epilepsy, especially DRE. Herein we review the recent evidence supporting the role of inflammation in the development and perpetuation of seizures, and also discuss the recent achievements in modulation of inflammation and immunotherapy applied to the treatment of epilepsy. Apart from medical therapy, we also discuss the influences of surgery, ketogenic diet, and electroconvulsive therapy on immunity and inflammation in DRE patients. Taken together, a promising perspective is suggested for future immunomodulatory therapies in the treatment of patients with DRE.

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Neuronal and nonneuronal cholinergic structures in the mouse gastrointestinal tract and spleen

Gautron

Rutkowski

Burton

et al. 2013

J of Comparative Neurology

116

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Accumulating evidence demonstrates that acetylcholine can directly modulate immune function in peripheral tissues including the spleen and gastrointestinal tract. However, the anatomical relationships between the peripheral cholinergic system and immune cells located in these lymphoid tissues remain unclear due to inherent technical difficulties with currently available neuroanatomical methods. In this study, mice with specific expression of the tdTomato fluorescent protein in choline acetyltransferase (ChAT)-expressing cells were used to label preganglionic and postganglionic cholinergic neurons and their projections to lymphoid tissues. Notably, our anatomical observations revealed an abundant innervation in the intestinal lamina propria of the entire gastrointestinal tract principally originating from cholinergic enteric neurons. The aforementioned innervation frequently approached macrophages, plasma cells, and lymphocytes located in the lamina propria and, to a lesser extent, lymphocytes in the interfollicular areas of Peyer’s patches. In addition to the above innervation, we observed labeled epithelial cells in the gallbladder and lower intestines, as well as Microfold cells and T-cells within Peyer’s patches. In contrast, we found only a sparse innervation in the spleen consisting of neuronal fibers of spinal origin present around arterioles and in lymphocyte-containing areas of the white pulp. Lastly, a small population of ChAT-expressing lymphocytes was identified in the spleen including both T- and B-cells. In summary, this study describes the variety of cholinergic neuronal and nonneuronal cells in a position to modulate gastrointestinal and splenic immunity in the mouse.

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Anti-inflammatory effect of vagus nerve stimulation in a rat model of inflammatory bowel disease

Cited by 243 publications

References 56 publications

Is-there a place for vagus nerve stimulation in inflammatory bowel diseases?

Is-there a place for vagus nerve stimulation in inflammatory bowel diseases?

Modulation of Immunity and the Inflammatory Response: A New Target for Treating Drug-resistant Epilepsy

Neuronal and nonneuronal cholinergic structures in the mouse gastrointestinal tract and spleen

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