Vagus nerve stimulation: a new promising therapeutic tool in inflammatory bowel disease
Open accessAbstract
Inflammatory bowel disease (IBD), that is Crohn's disease (CD) and ulcerative colitis, affects about 1.5 million persons in the USA and 2.2 million in Europe. The pathophysiology of IBD involves immunological, genetic and environmental factors. The treatment is medico‐surgical but suspensive. Anti‐TNFα agents have revolutionized the treatment of IBD but have side effects. In addition, a non‐negligible percentage of patients with IBD stop or take episodically their treatment. Consequently, a nondrug therapy targeting TNFα through a physiological pathway, devoid of major side effects and with a good cost‐effectiveness ratio, would be of interest. The vagus nerve has dual anti‐inflammatory properties through its afferent (i.e. hypothalamic–pituitary–adrenal axis) and efferent (i.e. the anti‐TNFα effect of the cholinergic anti‐inflammatory pathway) fibres. We have shown that there is an inverse relationship between vagal tone and plasma TNFα level in patients with CD, and have reported, for the first time, that chronic vagus nerve stimulation has anti‐inflammatory properties in a rat model of colitis and in a pilot study performed in seven patients with moderate CD. Two of these patients failed to improve after 3 months of vagus nerve stimulation but five were in deep remission (clinical, biological and endoscopic) at 6 months of follow‐up and vagal tone was restored. No major side effects were observed. Thus, vagus nerve stimulation provides a new therapeutic option in the treatment of CD.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The brain-gut axis is becoming increasingly important as a therapeutic target for gastrointestinal and psychiatric disorders, such as inflammatory bowel disease, depression, and posttraumatic stress disorder.
“The brain–gut axis is becoming increasingly important as a therapeutic target for gastrointestinal and psychiatric disorders, such as inflammatory bowel disease (IBD) (3), depression (4), and posttraumatic stress disorder (PTSD) (5).”
From Vagus Nerve as Modulator of the Brain–Gut Axis in Psychiatric and Inflammatory Disorders (2018) · cites this paper as [3]
In response to pathogens and other injurious stimuli, TNF-α is produced by activated macrophages, dendritic cells, and other cells in the mucosa.
“For example, in response to pathogens and other injurious stimuli, tumor-necrosis factor-alpha (TNF-α), a cytokine, is produced by activated macrophages, dendritic cells, and other cells in the mucosa (3, 65).”
From Vagus Nerve as Modulator of the Brain–Gut Axis in Psychiatric and Inflammatory Disorders (2018) · cites this paper as [3]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Heart Rate Variability: Standards of Measurement, Physiological Interpretation, and Clinical Use
Electrophysiology, T. F. O. T. E. S. O. C. T. N. A. (1996) · Circulation · doi:10.1161/01.cir.93.5.1043 · Cited by 17,159 · see citing works
Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin
Borovikova, L. V., Ivanova, S., Zhang, M., Yang, H., Botchkina, G. I., Watkins, L. R., Wang, H., Abumrad, N., Eaton, J. W., & Tracey, K. J. (2000) · Nature · doi:10.1038/35013070 · Cited by 4,211 · see citing works
Nicotinic acetylcholine receptor α7 subunit is an essential regulator of inflammation
Wang, H., Yu, M., Ochani, M., Amella, C. A., Tanovic, M., Susarla, S., Li, J. H., Wang, H., Yang, H., Ulloa, L., et al. (2003) · Nature · doi:10.1038/nature01339 · Cited by 3,228 · see citing works
Acetylcholine-Synthesizing T Cells Relay Neural Signals in a Vagus Nerve Circuit
Rosas-Ballina, M., Olofsson, P. S., Ochani, M., Valdés-Ferrer, S. I., Levine, Y. A., Reardon, C., Tusche, M. W., Pavlov, V. A., Andersson, U., Chavan, S., et al. (2011) · Science · doi:10.1126/science.1209985 · Cited by 1,551 · see citing works
Ricardo, J. A., & Koh, E. T. (1978) · Brain Research · doi:10.1016/0006-8993(78)91125-3 · Cited by 1,362 · see citing works
de Jonge, W. J., van der Zanden, E. P., The, F. O., Bijlsma, M. F., van Westerloo, D. J., Bennink, R. J., Berthoud, H.-R., Uematsu, S., Akira, S., van den Wijngaard, R. M., et al. (2005) · Nature Immunology · doi:10.1038/ni1229 · Cited by 1,074 · see citing works
Koopman, F. A., Chavan, S. S., Miljko, S., Grazio, S., Sokolovic, S., Schuurman, P. R., Mehta, A. D., Levine, Y. A., Faltys, M., Zitnik, R., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1605635113 · Cited by 1,024 · see citing works
The nerve supply of the human auricle
Peuker, E. T., & Filler, T. J. (2002) · Clinical Anatomy · doi:10.1002/ca.1089 · Cited by 782 · see citing works
The Brain Nucleus Locus Coeruleus: Restricted Afferent Control of a Broad Efferent Network
Aston‐Jones, G., Ennis, M. J., Pieribone, V. A., Nickell, W. T., & Shipley, M. T. (1986) · Science · doi:10.1126/science.3775363 · Cited by 778 · see citing works
The cholinergic anti-inflammatory pathway: a missing link in neuroimmunomodulation
Pavlov, V. A., Wang, H., Czura, C. J., Friedman, S. G., & Tracey, K. J. (2003) · Molecular Medicine · doi:10.1007/bf03402177 · Cited by 772 · see citing works
Frangos, E., Ellrich, J., & Komisaruk, B. R. (2014) · Brain stimulation · doi:10.1016/j.brs.2014.11.018 · Cited by 764 · see citing works
Taste pathways to hypothalamus and amygdala
Norgren, R. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901660103 · Cited by 761 · see citing works
Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia
Rosas‐Ballina, M., Ochani, M., Parrish, W. R., Ochani, K., Harris, Y., Huston, J. M., Chavan, S. S., & Tracey, K. J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803237105 · Cited by 757 · see citing works
Altschuler, S. M., Bao, X., Bieger, D., Hopkins, D. A., & Miselis, R. R. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902830207 · Cited by 754 · see citing works
Long-term treatment with vagus nerve stimulation in patients with refractory epilepsy
Morris, G. L., Mueller, W. M., & The Vagus Nerve Stimulation Study Group E–E (1999) · Neurology · doi:10.1212/wnl.53.8.1731 · Cited by 727 · see citing works
Groves, D. A., & Brown, V. J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.01.004 · Cited by 677 · see citing works
Brain–Gut Interactions in Inflammatory Bowel Disease
Bonaz, B. L., & Bernstein, C. N. (2013) · Gastroenterology · doi:10.1053/j.gastro.2012.10.003 · Cited by 667 · see citing works
Self-citationConrad, L. C. A., & Pfaff, D. W. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901690206 · Cited by 633 · see citing works
Strack, A. M., Sawyer, W. B., Hughes, J., Platt, K. B., & Loewy, A. D. (1989) · Brain Research · doi:10.1016/0006-8993(89)90098-x · Cited by 591 · see citing works
Bonaz, B., Sinniger, V., & Pellissier, S. (2016) · The Journal of Physiology · doi:10.1113/jp271539 · Cited by 561 · see citing works
Self-citationPharmacological stimulation of the cholinergic antiinflammatory pathway
Bernik, T. R., Friedman, S. G., Ochani, M., DiRaimo, R., Ulloa, L., Yang, H., Sudan, S., Czura, C. J., Ivanova, S. M., & Tracey, K. J. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20011714 · Cited by 529 · see citing works
Watkins, L. R., Goehler, L. E., Relton, J. K., Tartaglia, N., Silbert, L., Martin, D., & Maier, S. F. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(94)11105-r · Cited by 516 · see citing works
Chronic vagus nerve stimulation in Crohn's disease: a 6‐month follow‐up pilot study
Bonaz, B., Sinniger, V., Hoffmann, D., Clarençon, D., Mathieu, N., Dantzer, C., Vercueil, L., Picq, C., Trocmé, C., Faure, P., et al. (2016) · Neurogastroenterology & Motility · doi:10.1111/nmo.12792 · Cited by 492 · see citing works
Self-citationStrack, A. M., Sawyer, W. B., Platt, K. B., & Loewy, A. D. (1989) · Brain Research · doi:10.1016/0006-8993(89)90063-2 · Cited by 489 · see citing works
Penry, J. K., & Dean, J. C. (1990) · Epilepsia · doi:10.1111/j.1528-1157.1990.tb05848.x · Cited by 474 · see citing works
Wessler, I. K., Kirkpatrick, C. J., & Racké, K. (1998) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(97)00085-5 · Cited by 415 · see citing works
Matteoli, G., Gomez-Pinilla, P. J., Némethová, A., Giovangiulio, M. D., Cailotto, C., van Bree, S. V., Michel, K., Tracey, K., Schemann, M., Boesmans, W., et al. (2013) · Gut · doi:10.1136/gutjnl-2013-304676 · Cited by 412 · see citing works
Ghia, J., Blennerhassett, P. A., Kumar–Ondiveeran, H., Verdu, E. F., & Collins, S. M. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.08.016 · Cited by 404 · see citing works
Vagus nerve stimulation, side effects, and long-term safety
Ben-Menachem, E. (2001) · Journal of Clinical Neurophysiology · doi:10.1097/00004691-200109000-00005 · Cited by 400 · see citing works
Rush, A. J., Sackeïm, H. A., Marangell, L. B., George, M. S., Brannan, S. K., Thomas, S., Lavori, P., Howland, R. H., Kling, M. A., Rittberg, B. R., et al. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.05.024 · Cited by 399 · see citing works
Rethinking inflammation: neural circuits in the regulation of immunity
Olofsson, P. S., Rosas‐Ballina, M., Levine, Y. A., & Tracey, K. J. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01138.x · Cited by 393 · see citing works
The cholinergic anti-inflammatory pathway: A critical review
Martelli, D., McKinley, M. J., & McAllen, R. M. (2013) · Autonomic Neuroscience · doi:10.1016/j.autneu.2013.12.007 · Cited by 388 · see citing works
The Flinders sensitive line rats: a genetic animal model of depression
Overstreet, D. H. (1993) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80230-1 · Cited by 369 · see citing works
Topography of efferent vagal innervation of the rat gastrointestinal tract
Berthoud, H., Carlson, N. R., & Powley, T. L. (1991) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1991.260.1.r200 · Cited by 363 · see citing works
Bailey, P., & Bremer, F. (1938) · Journal of Neurophysiology · doi:10.1152/jn.1938.1.5.405 · Cited by 333 · see citing works
Goehler, L. E., Relton, J. K., Dripps, D. J., Kiechle, R., Tartaglia, N. R., Maier, S. F., & Watkins, L. R. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00020-8 · Cited by 326 · see citing works
Cygankiewicz, I., & Zaręba, W. (2013) · Handbook of clinical neurology · doi:10.1016/b978-0-444-53491-0.00031-6 · Cited by 323 · see citing works
Inoue, T., Abe, C., Sung, S. J., Moscalu, S., Jankowski, J., Huang, L., Ye, H., Rosin, D. L., Guyenet, P. G., & Okusa, M. D. (2016) · Journal of Clinical Investigation · doi:10.1172/jci83658 · Cited by 313 · see citing works
Anti-inflammatory effect of vagus nerve stimulation in a rat model of inflammatory bowel disease
Meregnani, J., Clarençon, D., Vivier, M., Peinnequin, A., Mouret, C., Sinniger, V., Picq, C., Job, A., Canini, F., Jacquier-Sarlin, M., et al. (2011) · Autonomic Neuroscience · doi:10.1016/j.autneu.2010.10.007 · Cited by 310 · see citing works
Self-citationEtiopathogenesis of inflammatory bowel diseases
Danese, S., & Fiocchi, C. (2006) · World Journal of Gastroenterology · doi:10.3748/wjg.v12.i30.4807 · Cited by 309 · see citing works
Nutritional stimulation of cholecystokinin receptors inhibits inflammation via the vagus nerve
Luyer, M. D., Greve, J. W. M., Hadfoune, M., Jacobs, J. A., Dejong, C. H., & Buurman, W. A. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20042397 · Cited by 295 · see citing works
Naritoku, D. K., Terry, W. J., & Helfert, R. H. (1995) · Epilepsy Research · doi:10.1016/0920-1211(95)00035-9 · Cited by 291 · see citing works
Stefan, H., Kreiselmeyer, G., Kerling, F., Kurzbuch, K., Rauch, C., Heers, M., Kasper, B. S., Hammen, T., Rzonsa, M., Pauli, E., et al. (2012) · Epilepsia · doi:10.1111/j.1528-1167.2012.03492.x · Cited by 270 · see citing works
Yoga and heart rate variability: a comprehensive review of the literature
Cohen, M., & Tyagi, A. (2016) · International Journal of Yoga · doi:10.4103/0973-6131.183712 · Cited by 269 · see citing works
Rinaman, L., Card, J. P., Schwaber, J. S., & Miselis, R. R. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-06-01985.1989 · Cited by 263 · see citing works
A review of functional neuroimaging studies of vagus nerve stimulation (VNS)
Chae, J.-H., Nahas, Z., Lomarev, M., Denslow, S., Lorberbaum, J. P., Bohning, D. E., & George, M. S. (2003) · Journal of Psychiatric Research · doi:10.1016/s0022-3956(03)00074-8 · Cited by 255 · see citing works
Sun, Y., Li, Q., Gui, H., Xu, D.-P., Yang, Y., Su, D., & Liu, X. (2013) · Cell Research · doi:10.1038/cr.2013.116 · Cited by 253 · see citing works
Cholinergic antiinflammatory pathway inhibition of tumor necrosis factor during ischemia reperfusion
Bernik, T. R., Friedman, S. G., Ochani, M., DiRaimo, R., Susarla, S., Czura, C. J., & Tracey, K. J. (2002) · Journal of Vascular Surgery · doi:10.1067/mva.2002.129643 · Cited by 228 · see citing works
Activation of the Cholinergic Anti-Inflammatory Pathway Ameliorates Postoperative Ileus in Mice
The, F. O., Boeckxstaens, G. E., Snoek, S. A., Cash, J. L., Bennink, R. J., LaRosa, G. J., van den Wijngaard, R. M., Greaves, D. R., & de Jonge, W. J. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.07.022 · Cited by 226 · see citing works
Krahl, S. E., Senanayake, S. S., & Handforth, A. (2001) · Epilepsia · doi:10.1046/j.1528-1157.2001.09700.x · Cited by 212 · see citing works
Pellissier, S., Dantzer, C., Mondillon, L., Trocme, C., Gauchez, A.-S., Ducros, V., Mathieu, N., Toussaint, B., Fournier, A., Canini, F., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0105328 · Cited by 212 · see citing works
Self-citationCentral connections of the sensory and motor nuclei of the vagus nerve
Sawchenko, P. E. (1983) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(83)90129-7 · Cited by 211 · see citing works
Sun, P., Zhou, K., Wang, S., Li, P., Chen, S., Lin, G., Zhao, Y., & Wang, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069424 · Cited by 208 · see citing works
Bratton, B. O., Martelli, D., McKinley, M. J., Trevaks, D., Anderson, C. R., & McAllen, R. M. (2012) · Experimental Physiology · doi:10.1113/expphysiol.2011.061531 · Cited by 206 · see citing works
Pellissier, S., Dantzer, C., Canini, F., Mathieu, N., & Bonaz, B. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.10.004 · Cited by 198 · see citing works
Self-citationCentral cholinergic activation of a vagus nerve - to spleen circuit alleviates experimental colitis
Ji, H., Rabbi, M. F., Labis, B., Pavlov, V. A., Tracey, K., & Ghia, J. (2013) · Mucosal Immunology · doi:10.1038/mi.2013.52 · Cited by 197 · see citing works
Vagus nerve stimulation for partial seizures
Panebianco, M., Rigby, A., Weston, J., & Marson, A. G. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd002896.pub2 · Cited by 192 · see citing works
The central organization of the vagus nerve innervating the colon of the rat
Altschuler, S. M., Escardo, J., Lynn, R. B., & Miselis, R. R. (1993) · Gastroenterology · doi:10.1016/0016-5085(93)90419-d · Cited by 183 · see citing works
Lomarev, M., Denslow, S., Nahas, Z., Chae, J.-H., George, M. S., & Bohning, D. E. (2002) · Journal of Psychiatric Research · doi:10.1016/s0022-3956(02)00013-4 · Cited by 175 · see citing works
Characterization of vagal innervation to the rat celiac, suprarenal and mesenteric ganglia
Berthoud, H., & Powley, T. L. (1993) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(93)90046-w · Cited by 173 · see citing works
Lerman, I. R., Hauger, R. L., Sorkin, L. S., Proudfoot, J. A., Davis, B. A., Huang, A., Lam, K. J. K., Simon, B. J., & Baker, D. G. (2016) · Neuromodulation Technology at the Neural Interface · doi:10.1111/ner.12398 · Cited by 168 · see citing works
Enteric neural crest-derived cells: Origin, identification, migration, and differentiation
Young, H. M., & Newgreen, D. F. (2001) · The Anatomical Record · doi:10.1002/1097-0185(20010101)262:1 · Cited by 163 · see citing works
Naritoku, D. K., Morales, A., Pencek, T. L., & WINKLER, D. (1992) · Pacing and Clinical Electrophysiology · doi:10.1111/j.1540-8159.1992.tb02935.x · Cited by 158 · see citing works
Costantini, T. W., Bansal, V., Krzyżaniak, M., Putnam, J. G., Peterson, C. Y., Loomis, W. H., Wolf, P. L., Baird, A., Eliceiri, B. P., & Coimbra, R. S. M. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00156.2010 · Cited by 153 · see citing works
J.L. Corning and vagal nerve stimulation for seizures in the 1880s
Lanska, D. J. (2002) · Neurology · doi:10.1212/wnl.58.3.452 · Cited by 152 · see citing works
Origin of noradrenergic innervation of the spleen in rats
Bellinger, D. L., Felten, S. Y., Lorton, D., & Felten, D. L. (1989) · Brain Behavior and Immunity · doi:10.1016/0889-1591(89)90029-9 · Cited by 146 · see citing works
Vagal tone: effects on sensitivity, motility, and inflammation
Bonaz, B. L., Sinniger, V., & Sonia Pellissier, A. (2016) · Neurogastroenterology & Motility · doi:10.1111/nmo.12817 · Cited by 146 · see citing works
Self-citationSurgical Technique for Implantation of the Neurocybernetic Prosthesis
Reid, S. A. (1990) · Epilepsia · doi:10.1111/j.1528-1157.1990.tb05847.x · Cited by 143 · see citing works
The Inflammatory Reflex and the Role of Complementary and Alternative Medical Therapies
Oke, S. L., & Tracey, K. J. (2009) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1393.013 · Cited by 137 · see citing works
Targeting TNF-α for the treatment of inflammatory bowel disease
Billiet, T., Rutgeerts, P. J., Ferrante, M., Assche, G. V., & Vermeire, S. (2013) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2014.858695 · Cited by 133 · see citing works
Gut-directed hypnotherapy significantly augments clinical remission in quiescent ulcerative colitis
Keefer, L., Taft, T. H., Kiebles, J. L., Martinovich, Z., Barrett, T. A., & Palsson, O. S. (2013) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.12449 · Cited by 132 · see citing works
Anti-Inflammatory Effects of Acupuncture Stimulation via the Vagus Nerve
Lim, H.-D., Kim, M., Lee, C. Y., & Namgung, U. (2016) · PLoS ONE · doi:10.1371/journal.pone.0151882 · Cited by 131 · see citing works
Disturbed Autonomic Nerve Function in Patients with Crohn's Disease
Lindgren, S. C., Lilja, B., Rosén, I., & Sundkvist, G. (1991) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365529108996495 · Cited by 129 · see citing works
Cailotto, C., Gomez‐Pinilla, P. J., Costes, L. M. M., van der Vliet, J., Giovangiulio, M. D., Némethova, A., Matteoli, G., & Boeckxstaens, G. E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087785 · Cited by 124 · see citing works
Neuronal and Nonneuronal Cholinergic Structures in the Mouse Gastrointestinal Tract and Spleen
Gautron, L., Rutkowski, J. M., Burton, M. D., Wei, W., Wan, Y., & Elmquist, J. (2013) · The Journal of comparative neurology · doi:10.1002/cne.23376 · Cited by 123 · see citing works
Zhao, Y. X., He, W., Jing, X. H., Liu, J. L., Rong, P. J., Ben, H., Liu, K., & Zhu, B. (2012) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2012/627023 · Cited by 122 · see citing works
Autonomic Dysfunction Precedes Development of Rheumatoid Arthritis: A Prospective Cohort Study
Koopman, F. A., Tang, M. W., Vermeij, J., de Hair, M. J. H., Choi, I. Y. K., Vervoordeldonk, M. J., Gerlag, D. M., Karemaker, J. M., & Tak, P. P. (2016) · EBioMedicine · doi:10.1016/j.ebiom.2016.02.029 · Cited by 117 · see citing works
Spleen Vagal Denervation Inhibits the Production of Antibodies to Circulating Antigens
Buijs, R. M., van der Vliet, J., Garidou, M.-L., Huitinga, I., & Escobar, C. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003152 · Cited by 113 · see citing works
Enteric Neuronal Density Contributes to the Severity of Intestinal Inflammation
Margolis, K. G., Stevanovic, K. D., Karamooz, N., Li, Z. S., Ahuja, A., D’Autréaux, F., Saurman, V. E., Chalazonitis, A., & Gershon, M. D. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.047 · Cited by 113 · see citing works
Does the vagus nerve mediate the sixth sense?
Zagon, A. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01929-9 · Cited by 110 · see citing works
Adverse events in IBD: to stop or continue immune suppressant and biologic treatment
McLean, L. P., & Cross, R. K. (2014) · Expert Review of Gastroenterology & Hepatology · doi:10.1586/17474124.2014.881715 · Cited by 110 · see citing works
Vagus nerve integrity and experimental colitis
Ghia, J., Blennerhassett, P. A., & Collins, S. M. (2007) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00098.2007 · Cited by 108 · see citing works
Loss of vagal anti-inflammatory effect: in vivo visualization and adoptive transfer
O’Mahony, C., van der Kleij, H. P. M., Bienenstock, J., Shanahan, F., & O’Mahony, L. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90904.2008 · Cited by 102 · see citing works
Vagus nerve stimulation: A new bioelectronics approach to treat rheumatoid arthritis?
Koopman, F. A., Schuurman, P. R., Vervoordeldonk, M. J., & Tak, P. P. (2014) · Best Practice & Research Clinical Rheumatology · doi:10.1016/j.berh.2014.10.015 · Cited by 99 · see citing works
Munyaka, P. M., Rabbi, M. F., Pavlov, V. A., Tracey, K. J., Khafipour, E., & Ghia, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109272 · Cited by 98 · see citing works
The splanchnic anti‐inflammatory pathway: could it be the efferent arm of the inflammatory reflex?
Martelli, D., Farmer, D., & Yao, S. T. (2016) · Experimental Physiology · doi:10.1113/ep085559 · Cited by 93 · see citing works
Macrophage‐like cells in the muscularis externa of mouse small intestine
Mikkelsen, H. B., Thuneberg, L., Rumessen, J. J., & Thorball, N. (1985) · The Anatomical Record · doi:10.1002/ar.1092130111 · Cited by 89 · see citing works
Effects of vagal stimulation on S-A and A-V nodes
Hamlin, R. L., & Cr, S. (1968) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1968.215.3.560 · Cited by 88 · see citing works
Central mechanisms of cranial nerve stimulation for epilepsy
Fanselow, E. E. (2012) · Surgical Neurology International · doi:10.4103/2152-7806.103014 · Cited by 80 · see citing works
Azam, M. A., Katz, J., Fashler, S. R., Changoor, T., Azargive, S., & Ritvo, P. (2015) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2015.06.005 · Cited by 78 · see citing works
Genetic and pharmacological models of cholinergic supersensitivity and affective disorders
Overstreet, D. H., Russell, R. W., Crocker, A. D., Gillin, J. C., & Janowsky, D. S. (1988) · Cellular and Molecular Life Sciences · doi:10.1007/bf01958920 · Cited by 78 · see citing works
Ruggiero, D. A., Underwood, M. D., Mann, J. J., Anwar, M., & Arango, V. (2000) · Journal of the Autonomic Nervous System · doi:10.1016/s0165-1838(99)00097-1 · Cited by 74 · see citing works
The Effect of the Cholinergic Anti‐Inflammatory Pathway on Experimental Colitis
Bai, A., Guo, Y., & Lü, N. (2007) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.2007.02011.x · Cited by 72 · see citing works
de Jonge, W. J., van der Zanden, E. P., The, F. O., Bijlsma, M. F., van Westerloo, D. J., Bennink, R. J., Berthoud, H., Uematsu, S., Akira, S., van den Wijngaard, R. M., et al. (2005) · Nature Immunology · doi:10.1038/ni0905-954b · Cited by 68 · see citing works
Das, U. N. (2010) · Journal of Inflammation Research · doi:10.2147/jir.s9425 · Cited by 63 · see citing works
Postshock Intervention With High-Lipid Enteral Nutrition Reduces Inflammation and Tissue Damage
de Haan, J.-J., Lubbers, T., Hadfoune, M., Luyer, M. D., Dejong, C. H., Buurman, W. A., & Greve, J.-W. M. (2008) · Annals of Surgery · doi:10.1097/sla.0b013e318188752c · Cited by 59 · see citing works
Cholinergic pathways modulate experimental dinitrobenzene sulfonic acid colitis in rats
Miceli, P. C., & Jacobson, K. (2003) · Autonomic Neuroscience · doi:10.1016/s1566-0702(03)00023-7 · Cited by 56 · see citing works
Klimaschewski, L. P., Kummer, W., & Heym, C. (1996) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19960901)35:1 · Cited by 55 · see citing works
Reyt, S., Picq, C. A., Sinniger, V., Clarençon, D., Bonaz, B. L., & Olivier David, A. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.05.021 · Cited by 55 · see citing works
Self-citationAnnoni, E. M., Xie, X., Lee, S. W., Libbus, I., KenKnight, B. H., Osborn, J. W., & Tolkacheva, E. G. (2015) · Physiological Reports · doi:10.14814/phy2.12476 · Cited by 55 · see citing works
Aubert, A. E., Verheyden, B., Beckers, F., Tack, J., & Vandenberghe, J. (2009) · Neuropsychobiology · doi:10.1159/000239686 · Cited by 53 · see citing works
Martelli, D., Yao, S. T., Mancera, J., McKinley, M. J., & McAllen, R. M. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00259.2014 · Cited by 53 · see citing works
THE HYPOTHALAMUS AND ENDOCRINE GLANDS
Harris, G. W. (1950) · British Medical Bulletin · doi:10.1093/oxfordjournals.bmb.a073628 · Cited by 51 · see citing works
Macneil, B. J., Jansen, A., Janz, L., Greenberg, A. H., & Nance, D. M. (1997) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1997.273.2.r609 · Cited by 49 · see citing works
Vagal Modulation of the Inflammatory Response in Sepsis
Wang, D.-W., Yin, Y.-M., & Yao, Y.-M. (2016) · International Reviews of Immunology · doi:10.3109/08830185.2015.1127369 · Cited by 48 · see citing works
Tyagi, A., Cohen, M. M., Reece, J., Telles, S., & Jones, L. (2016) · Applied Psychophysiology and Biofeedback · doi:10.1007/s10484-016-9340-2 · Cited by 48 · see citing works
de Haan, J. J., Hadfoune, M., Lubbers, T., Hodin, C. M. I. M., Lenaerts, K., Ito, A., Verbaeys, I., Skynner, M. J., Cailotto, C., van der Vliet, J., et al. (2013) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00333.2012 · Cited by 47 · see citing works
Clarençon, D., Sonia Pellissier, A., Sinniger, V., Kibleur, A., Hoffman, D., Vercueil, L., Olivier David, A., & Bonaz, B. L. (2014) · Brain stimulation · doi:10.1016/j.brs.2014.08.001 · Cited by 41 · see citing works
Self-citationMorishita, K., Coimbra, R. S. M., Langness, S. M., Eliceiri, B. P., & Costantini, T. W. (2015) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00097.2015 · Cited by 35 · see citing works
Downs, A. M., Bond, C. E., & Hoover, D. B. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.02.011 · Cited by 30 · see citing works
Impact of Anesthetics on Immune Functions in a Rat Model of Vagus Nerve Stimulation
Picq, C. A., Clarençon, D., Sinniger, V., Bonaz, B. L., & Mayol, J.-F. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067086 · Cited by 28 · see citing works
Self-citationANATOMIE MEDICO-CHIRURGICALE DU SYSTEME NERVEUX VEGETATIF. SYMPATHIQUE ET PARASYMPATHIQUE
Delmas, J.-C., & Laux, J. (1934) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-193402000-00090 · Cited by 28 · see citing works
Non-adherence to treatment in inflammatory bowel disease in Czech Republic
Červený, P., Bortlík, M., Vlček, J., Kuběna, A. A., & Lukáš, M. (2007) · Journal of Crohn s and Colitis · doi:10.1016/j.crohns.2007.08.002 · Cited by 19 · see citing works
The pig as preclinical model for laparoscopic vagus nerve stimulation
Wolthuis, A. M., Stakenborg, N., D’Hoore, A. J. L., & Boeckxstaens, G. E. (2015) · International Journal of Colorectal Disease · doi:10.1007/s00384-015-2435-z · Cited by 17 · see citing works
[Effect of afferent vagal stimulation on the electroencephalogram of the cat in cerebral isolation].
Zanchetti, A., Sc, W., & Moruzzi, G. (1952) · PubMed · Cited by 13 · see citing works
Rozman, J., Pečlin, P., Kneževič, I., Mirković, T., Geršak, B., & Podbregar, M. (2009) · Hypertension Research · doi:10.1038/hr.2009.140 · Cited by 8 · see citing works
The role of spleen in vagus nerve stimulation for treatment against septic shock in rats.
Xue, N., Liang, H. W., Yao, H., et al. (2011) · PubMed · Cited by 7 · see citing works
Defelipe (1999) · doi:10.1002/(sici)1096-9861(19990927)412:3
Flagged first, then by citations
Research works printed but not linked: 4
- Sharkey KA, Kroese AB. Consequences of intestinal inflam- mation on the enteric nervous system: neuronal activation induced by inflammatory mediators. Anat Rec 2001; 262: 79-90.
- Van Bockstaele E.J., Peoples J., Telegan P. Efferent projec- tions of the nucleus of the solitary tract to peri-locus coeruleus dendrites in rat brain: evidence for a monosynap- tic pathway. J Comp Neurol, 1999; 412: 410-28.
- Berthoud HR, Powley TL. Interaction between parasympa- thetic and sympathetic nerves in prevertebral ganglia: mor- phological evidence for vagal efferent innervation of ganglion cells in the rat. Microsc Res Tech 1996; 35: 80-6.
- Rush AJ, Marangell LB, Sackeim HA et al. Vagus nerve stimulation for treatment-resistant depression: a random- ized, controlled acute phase trial. Biol Psychiatry 2005; 58: 347-54.
Cited by
Sorted by citations
The vagus nerve at the interface of the microbiota-gut-brain axis
Bonaz, B., Bazin, T., & Pellissier, S. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00049 · Cited by 1,397 · see citing works
Self-citationVagus Nerve as Modulator of the Brain–Gut Axis in Psychiatric and Inflammatory Disorders
Breit, S., Kupferberg, A., Rogler, G., & Hasler, G. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00044 · Cited by 1,189 · see citing works
Bonaz, B., Sinniger, V., & Pellissier, S. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01452 · Cited by 405 · see citing works
Self-citationRapid gut dysbiosis induced by stroke exacerbates brain infarction in turn
Xu, K., Gao, X., Xia, G., Chen, M., Zeng, N., Wang, S., You, C., Tian, X., Di, H., Tang, W., et al. (2021) · Gut · doi:10.1136/gutjnl-2020-323263 · Cited by 308 · see citing works
Liu, C.-H., Yang, M.-H., Zhang, G.-Z., Wang, X.-X., Li, B., Li, M., Woelfer, M., Walter, M., & Wang, L. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01732-5 · Cited by 210 · see citing works
Labanski, A., Langhorst, J., Engler, H., & Elsenbruch, S. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.104501 · Cited by 200 · see citing works
Kolacz, J., Kovacic, K. K., & Porges, S. W. (2019) · Developmental Psychobiology · doi:10.1002/dev.21852 · Cited by 94 · see citing works
Role of the autonomic nervous system in osteoarthritis
Courties, A., Sellam, J., & Berenbaum, F. (2017) · Best Practice & Research Clinical Rheumatology · doi:10.1016/j.berh.2018.04.001 · Cited by 66 · see citing works
Palantzas, A., & Anagnostouli, M. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26178217 · Cited by 11 · see citing works
Prefrontal tDCS modulates autonomic responses in COVID-19 inpatients
Pinto, T. P., Inácio, J. C., de Aguiar, E., Ferreira, A. S., Sudo, F. K., Tovar-Moll, F., & Rodrigues, E. C. (2023) · Brain Stimulation · doi:10.1016/j.brs.2023.03.001 · Cited by 11 · see citing works
- Authors
- Bonaz, B., Sinniger, V., & Pellissier, S.
- Affiliations
- Inserm (FR)
- University Clinic of Hepato‐Gastroenterology University Hospital Grenoble France
- Corresponding author
- Bonaz, B.
- Venue
- Journal of Internal Medicine
- Publisher
- Wiley
- Published
- 2017-04-18
- Volume
- 282
- Issue
- 1
- Pages
- 46-63
- ISSN
- 0954-6820 (ISSN-L)
- 1365-2796
- OpenAlex
- W2607217038
- Cited by
- 213
- References
- 118
- Citations by year
- 2026: 28 · 2025: 36 · 2024: 19 · 2023: 23 · 2022: 16 · 2021: 17 · 2020: 25 · 2019: 18 · 2018: 22 · 2017: 9
- FWCI
- 1.94
- Type
- journal article
- Language
- en
- Open access
- green
- hal.science
- Locations
- Journal of Internal Medicine (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- vagus nerve stimulation, inflammatory bowel disease, Crohn's disease, ulcerative colitis, cholinergic anti-inflammatory pathway, vagal tone, TNF-α, hypothalamic-pituitary-adrenal axis, anti-TNF therapy, deep remission, rat colitis model
- MeSH terms
- Afferent Pathways, Complementary Therapies, Animals, Disease Models, Animal, Efferent Pathways, Humans, Splanchnic Nerves, Spleen, Vagus Nerve, Inflammatory Bowel Diseases, Vagus Nerve Stimulation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review