AccScience Publishing / MI / Volume 1 / Issue 2 / DOI: 10.36922/mi.4389
Submit to MI
Cite this article
19
Download
426
Views
Journal Browser
Volume | Year
Issue
Search
Forthcoming Issue
Current Issue
View All
News and Announcements
View All
PERSPECTIVE ARTICLE

Is vagus nerve-mediated regulation of immunity an etiological target for therapeutic intervention in endometriosis?

Claire-Marie Rangon1,2†* ,  Shaoyuan Li3 ,  Peter S. Staats2,4† ,  Alba Boluda-Nicola5,6 ,  Jérôme Bouaziz5,6
Show Less
1 Department of Pediatrics, One Clinic, Paris, France
2 Vagus Nerve Society, Atlantic Beach, Florida, United States of America
3 Institute of Acupuncture and Moxibustion Academy of Chinese Medical Sciences, Beijing, China
4 National Spine and Pain Centers, Atlantic Beach, Florida, United States of America
5 Department of Gynecology and Obstetrics, One Clinic, Paris, France
6 Department of Research, One Clinic, Paris, France
MI 2024, 1(2), 46–56; https://doi.org/10.36922/mi.4389
Submitted: 31 July 2024 | Accepted: 19 September 2024 | Published: 15 October 2024
(This article belongs to the Special Issue Recent Advances in Immune Regulation by the Vagus Nerve)
© 2024 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Download PDF
Cite
XML
Abstract

Endometriosis is a complex chronic neuro-inflammatory disorder, affecting roughly 10% of reproductive-age women. It is characterized by the presence of endometrial-like tissue outside the uterus, which induces a chronic inflammatory reaction. This disease can present a wide range of symptoms, including chronic pain and infertility. Despite extensive research, the exact pathogenesis of endometriosis remains incompletely understood. New strategies and paradigms on pathogenesis and treatment are needed. Schematic factors contributing to the development of endometriosis lesions include genetic, hormonal, and immunological factors. Although genetics may contribute to the epidemiologically suggested heritability of endometriosis, epigenetics has gained an increasing consideration in research. Remarkably, microbiota dysbiosis, acting as a catalyst for the main acknowledged epigenetic etiologies (locally produced estradiol, pro-inflammatory cytokines, and hypoxic stress) demands further attention. Indeed, over the past 10 years, it has become clear that the vagus nerve, the fastest component of the microbiota-gut-brain axis, can efficiently control inflammation through the cholinergic anti-inflammatory pathway. Therefore, stimulation of the vagus nerve could be a good candidate for modulating the severity of endometriosis. The detrimental consequences of microbiome dysbiosis and the estrobolome activity on the initiation of the disease as well as counterpart dysfunctions in the central nervous system will be focused on, both supporting a key role of the vagus nerve since the early stage of endometriosis. Consequently, the rationale for using non-invasive vagus nerve stimulation will be discussed, introducing a fruitful shift of paradigm in this still enigmatic disease.

Keywords
Endometriosis
Pathophysiology
Epigenetics
Immunity
Microbiota-gut-brain axis
Non-invasive vagus nerve stimulation
Funding
None.
Conflict of interest
Claire-Marie Rangon and Peter S. Staats are the Guest Editors of this special issue but were not in any way involved in the editorial and peer-review process conducted for this paper, directly or indirectly. Peter S. Staats is the founder of the ElectroCore company which sells nVNS device called gammaCore. Separately, other authors declared that they have no known competing financial interests or personal relationships that could have influenced the work reported in this paper.
References
  1. Horne AW, Missmer SA. Pathophysiology, diagnosis, and management of endometriosis. BMJ. 2022;379:e070750. doi: 10.1136/bmj-2022-070750

 

  1. Dabi Y, Suisse S, Marie Y, et al. New class of RNA biomarker for endometriosis diagnosis: The potential of salivary piRNA expression. Eur J Obstet Gynecol Reprod Biol. 2023;291:88-95. doi: 10.1016/j.ejogrb.2023.10.015

 

  1. Bendifallah S, Suisse S, Puchar A, et al. Salivary MicroRNA signature for diagnosis of endometriosis. JCM. 2022;11(3):612. doi: 10.3390/jcm11030612

 

  1. Bendifallah S, Dabi Y, Suisse S, et al. Validation of a Salivary miRNA Signature of Endometriosis - Interim Data. NEJM Evid. 2023;2(7):EVIDoa2200282. doi: 10.1056/EVIDoa2200282

 

  1. Canis M, Abbott J, Abrao M, et al. A call for new theories on the pathogenesis and pathophysiology of endometriosis. J Minim Invasive Gynecol. 2024;31(5):371-377. doi: 10.1016/j.jmig.2024.02.004

 

  1. Bulun SE, Yilmaz BD, Sison C, et al. Endometriosis. Endocr Rev. 2019;40(4):1048-1079. doi: 10.1210/er.2018-00242

 

  1. Rahmioglu N, Mortlock S, Ghiasi M, et al. The genetic basis of endometriosis and comorbidity with other pain and inflammatory conditions. Nat Genet. 2023;55(3):423-436. doi: 10.1038/s41588-023-01323-z

 

  1. Xie ZW, He Y, Feng YX, Wang XH. Identification of programmed cell death-related genes and diagnostic biomarkers in endometriosis using a machine learning and Mendelian randomization approach. Front Endocrinol (Lausanne). 2024;15:1372221. doi: 10.3389/fendo.2024.1372221

 

  1. Marquardt RM, Tran DN, Lessey BA, Rahman MS, Jeong JW. Epigenetic dysregulation in endometriosis: Implications for pathophysiology and therapeutics. Endocr Rev. 2023;44(6):1074-1095. doi: 10.1210/endrev/bnad020

 

  1. Szukiewicz D, Stangret A, Ruiz-Ruiz C, et al. Estrogen- and Progesterone (P4)-Mediated Epigenetic Modifications of Endometrial Stromal Cells (EnSCs) and/or Mesenchymal Stem/Stromal Cells (MSCs) in the etiopathogenesis of endometriosis. Stem Cell Rev Rep. 2021;17(4):1174-1193. doi: 10.1007/s12015-020-10115-5

 

  1. Hsiao K, Wu M, Tsai S. Epigenetic regulation of the pathological process in endometriosis. Reprod Med Biol. 2017;16(4):314-319. doi: 10.1002/rmb2.12047

 

  1. McCallion A, Nasirzadeh Y, Lingegowda H, et al. Estrogen mediates inflammatory role of mast cells in endometriosis pathophysiology. Front Immunol. 2022;13:961599. doi: 10.3389/fimmu.2022.961599

 

  1. Jiang I, Yong PJ, Allaire C, Bedaiwy MA. Intricate connections between the microbiota and endometriosis. Int J Mol Sci. 2021;22(11):5644. doi: 10.3390/ijms22115644

 

  1. Hu S, Ding Q, Zhang W, Kang M, Ma J, Zhao L. Gut microbial beta-glucuronidase: A vital regulator in female estrogen metabolism. Gut Microbes. 2023;15(1):2236749. doi: 10.1080/19490976.2023.2236749

 

  1. Thaiss CA, Zmora N, Levy M, Elinav E. The microbiome and innate immunity. Nature. 2016;535(7610):65-74. doi: 10.1038/nature18847

 

  1. Olteanu G, Ciucă-Pană MA, Busnatu ȘS, et al. Unraveling the microbiome-human body axis: A comprehensive examination of therapeutic strategies, interactions and implications. Int J Mol Sci. 2024;25(10):5561. doi: 10.3390/ijms25105561

 

  1. Mujagic Z, Kasapi M, Jonkers DM, et al. Integrated fecal microbiome-metabolome signatures reflect stress and serotonin metabolism in irritable bowel syndrome. Gut Microbes. 2022;14(1):2063016. doi: 10.1080/19490976.2022.2063016

 

  1. Song Z, Ye W, Tao Y, et al. Transcriptome and 16S rRNA analyses reveal that hypoxic stress affects the antioxidant capacity of largemouth bass (Micropterus salmoides), resulting in intestinal tissue damage and structural changes in microflora. Antioxidants (Basel). 2022;12(1):1. doi: 10.3390/antiox12010001

 

  1. Zou N, Zhou Q, Zhang Y, et al. Transcutaneous auricular vagus nerve stimulation as a novel therapy connecting the central and peripheral systems: A review. Int J Surg. 2024;110:4993-5006. doi: 10.1097/JS9.0000000000001592

 

  1. Zizolfi B, Foreste V, Gallo A, Martone S, Giampaolino P, Di Spiezio Sardo A. Endometriosis and dysbiosis: State of art. Front Endocrinol (Lausanne). 2023;14:1140774. doi: 10.3389/fendo.2023.1140774

 

  1. Liang J, Li M, Zhang L, et al. Analysis of the microbiota composition in the genital tract of infertile patients with chronic endometritis or endometrial polyps. Front Cell Infect Microbiol. 2023;13:1125640. doi: 10.3389/fcimb.2023.1125640

 

  1. Ata B, Yildiz S, Turkgeldi E, et al. The endobiota study: Comparison of vaginal, cervical and gut microbiota between women with stage 3/4 endometriosis and healthy controls. Sci Rep. 2019;9(1):2204. doi: 10.1038/s41598-019-39700-6

 

  1. Yuan W, Wu Y, Chai X, Wu X. The colonized microbiota composition in the peritoneal fluid in women with endometriosis. Arch Gynecol Obstet. 2022;305(6):1573-1580. doi: 10.1007/s00404-021-06338-7

 

  1. Lee SR, Lee JC, Kim SH, et al. Altered composition of microbiota in women with ovarian endometrioma: Microbiome analyses of extracellular vesicles in the peritoneal fluid. Int J Mol Sci. 2021;22(9):4608. doi: 10.3390/ijms22094608

 

  1. Herup-Wheeler T, Shi M, Harvey ME, et al. High-fat diets promote peritoneal inflammation and augment endometriosis-associated abdominal hyperalgesia. Front Endocrinol (Lausanne). 2024;15:1336496. doi: 10.3389/fendo.2024.1336496

 

  1. Chadchan SB, Naik SK, Popli P, et al. Gut microbiota and microbiota-derived metabolites promotes endometriosis. Cell Death Discov. 2023;9(1):28. doi: 10.1038/s41420-023-01309-0

 

  1. Guo C, Zhang C. Role of the gut microbiota in the pathogenesis of endometriosis: A review. Front Microbiol. 2024;15:1363455. doi: 10.3389/fmicb.2024.1363455

 

  1. Wei Y, Tan H, Yang R, et al. Gut dysbiosis-derived β-glucuronidase promotes the development of endometriosis. Fertil Steril. 2023;120(3):682-694. doi: 10.1016/j.fertnstert.2023.03.032

 

  1. Tang F, Deng M, Xu C, et al. Unraveling the microbial puzzle: Exploring the intricate role of gut microbiota in endometriosis pathogenesis. Front Cell Infect Microbiol. 2024;14:1328419. doi: 10.3389/fcimb.2024.1328419

 

  1. Salmeri N, Sinagra E, Dolci C, et al. Microbiota in irritable bowel syndrome and endometriosis: Birds of a feather flock together-A review. Microorganisms. 2023;11(8):2089. doi: 10.3390/microorganisms11082089

 

  1. Chiaffarino F, Cipriani S, Ricci E, et al. Endometriosis and inflammatory bowel disease: A systematic review of the literature. Eur J Obstet Gynecol Reprod Biol. 2020;252:246-251. doi: 10.1016/j.ejogrb.2020.06.051

 

  1. Dang Y, Zhang S. Causal relationship between endometriosis and inflammatory bowel disease: A Mendelian randomization analyses. Clin Transl Med. 2024;14(1):e1496. doi: 10.1002/ctm2.1496

 

  1. Dang C, Chen Z, Chai Y, et al. Assessing the relationship between gut microbiota and endometriosis: A bidirectional two-sample Mendelian randomization analysis. BMC Womens Health. 2024;24(1):123. doi: 10.1186/s12905-024-02945-z

 

  1. Cao T, Wang Y, Huimin S. Causal effects between gut microbiota and endometriosis: A two-sample Mendelian randomisation study. J Obstet Gynaecol. 2024;44(1):2362415. doi: 10.1080/01443615.2024.2362415

 

  1. Haneishi Y, Furuya Y, Hasegawa M, Picarelli A, Rossi M, Miyamoto J. Inflammatory bowel diseases and gut microbiota. Int J Mol Sci. 2023;24(4):3817. doi: 10.3390/ijms24043817

 

  1. Willing BP, Dicksved J, Halfvarson J, et al. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology. 2010;139(6):1844-1854.e1. doi: 10.1053/j.gastro.2010.08.049

 

  1. Kim JS, Kirkland RA, Lee SH, et al. Gut microbiota composition modulates inflammation and structure of the vagal afferent pathway. Physiol Behav. 2020;225:113082. doi: 10.1016/j.physbeh.2020.113082

 

  1. Gonzales J, Gulbransen BD. The microbiota conducts the vasoactive intestinal polypeptide orchestra in the small intestine. Cell Mol Gastroenterol Hepatol. 2024;17(3):503-504. doi: 10.1016/j.jcmgh.2023.11.013

 

  1. Ericsson AC, Bains M, McAdams Z, et al. The G protein-coupled receptor, VPAC1, mediates vasoactive intestinal peptide-dependent functional homeostasis of the gut microbiota. Gastro Hep Adv. 2022;1(2):253-264. doi: 10.1016/j.gastha.2021.11.005

 

  1. Meroni M, Longo M, Dongiovanni P. Alcohol or gut microbiota: Who is the guilty? Int J Mol Sci. 2019;20(18):4568. doi: 10.3390/ijms20184568

 

  1. Harada T, Iwabe T, Terakawa N. Role of cytokines in endometriosis. Fertil Steril. 2001;76(1):1-10. doi: 10.1016/s0015-0282(01)01816-7

 

  1. Nothnick WB. Treating endometriosis as an autoimmune disease. Fertil Steril. 2001;76(2):223-231. doi: 10.1016/s0015-0282(01)01878-7

 

  1. Fahrenkrug J. Vasoactive intestinal polypeptide: Measurement, distribution and putative neurotransmitter function. Digestion. 1979;19(3):149-169. doi: 10.1159/000198339

 

  1. Martínez C, Juarranz Y, Gutiérrez-Cañas I, et al. A Clinical approach for the use of VIP axis in inflammatory and autoimmune diseases. Int J Mol Sci. 2019;21(1):65. doi: 10.3390/ijms21010065

 

  1. Ribatti D, Conconi MT, Nussdorfer GG. Nonclassic endogenous novel regulators of angiogenesis. Pharmacol Rev. 2007;59(2):185-205. doi: 10.1124/pr.59.2.3

 

  1. Pilzer I, Gozes I. VIP provides cellular protection through a specific splice variant of the PACAP receptor: A new neuroprotection target. Peptides. 2006;27(11):2867-2876. doi: 10.1016/j.peptides.2006.06.007

 

  1. Bourlev V, Moberg C, Ilyasova N, Davey E, Kunovac Kallak T, Olovsson M. Vasoactive intestinal peptide is upregulated in women with endometriosis and chronic pelvic pain. Am J Rep Immunol. 2018;80(3):e12857. doi: 10.1111/aji.12857

 

  1. Astruc A, Roux L, Robin F, et al. Advanced insights into human uterine innervation: Implications for endometriosis and pelvic pain. J Clin Med. 2024;13(5):1433. doi: 10.3390/jcm13051433

 

  1. Berard AR, Brubaker DK, Birse K, et al. Vaginal epithelial dysfunction is mediated by the microbiome, metabolome, and mTOR signaling. Cell Rep. 2023;42(5):112474. doi: 10.1016/j.celrep.2023.112474

 

  1. Seillet C, Luong K, Tellier J, et al. The neuropeptide VIP confers anticipatory mucosal immunity by regulating ILC3 activity. Nat Immunol. 2020;21(2):168-177. doi: 10.1038/s41590-019-0567-y

 

  1. Morampudi V, Conlin VS, Dalwadi U, et al. Vasoactive intestinal peptide prevents PKCε-induced intestinal epithelial barrier disruption during EPEC infection. Am J Physiol Gastrointest Liver Physiol. 2015;308(5):G389-G402. doi: 10.1152/ajpgi.00195.2014

 

  1. Yang J, Yang C, Yang Y, Jia N, Sun Q. Protection of vasoactive intestinal peptide on the blood-brain barrier dysfunction induced by focal cerebral ischemia in rats. J Stroke Cerebrovasc Dis. 2022;31(4):106160. doi: 10.1016/j.jstrokecerebrovasdis.2021.106160

 

  1. Da Silva MCM, de Souza Ferreira LP, Della Giustina A. It is time to change the definition: Endometriosis is no longer a pelvic disease. Clinics (Sao Paulo). 2024;79:100326. doi: 10.1016/j.clinsp.2024.100326

 

  1. Mokhtari T, Irandoost E, Sheikhbahaei F. Stress, pain, anxiety, and depression in endometriosis-Targeting glial activation and inflammation. Int Immunopharmacol. 2024;132:111942. doi: 10.1016/j.intimp.2024.111942

 

  1. Elefante C, Brancati GE, Oragvelidze E, Lattanzi L, Maremmani I, Perugi G. Psychiatric symptoms in patients with cerebral endometriosis: A case report and literature review. J Clin Med. 2022;11(23):7212. doi: 10.3390/jcm11237212

 

  1. Li T, Mamillapalli R, Ding S, et al. Endometriosis alters brain electrophysiology, gene expression and increases pain sensitization, anxiety, and depression in female mice. Biol Reprod. 2018;99(2):349-359. doi: 10.1093/biolre/ioy035

 

  1. Castro J, Maddern J, Erickson A, Harrington AM, Brierley SM. Peripheral and central neuroplasticity in a mouse model of endometriosis. J Neurochem. 2023;1-24. doi: 10.1111/jnc.15843

 

  1. Dodds KN, Beckett EAH, Evans SF, Hutchinson MR. Spinal glial adaptations occur in a minimally invasive mouse model of endometriosis: Potential implications for lesion etiology and persistent pelvic pain. Reprod Sci. 2019;26(3):357-369. doi: 10.1177/1933719118773405

 

  1. Bashir ST, Redden CR, Raj K, et al. Endometriosis leads to central nervous system-wide glial activation in a mouse model of endometriosis. J Neuroinflammation. 2023;20(1):59. doi: 10.1186/s12974-023-02713-0

 

  1. Samani EN, Mamillapalli R, Li F, et al. Micrometastasis of endometriosis to distant organs in a murine model. Oncotarget. 2019;10(23):2282-2291. doi: 10.18632/oncotarget.16889

 

  1. Ghosh D, Filaretova L, Bharti J, Roy KK, Sharma JB, Sengupta J. Pathophysiological basis of endometriosis-linked stress associated with pain and infertility: A conceptual review. Reprod Med. 2020;1(1):32-61. doi: 10.3390/reprodmed1010004

 

  1. Appleyard CB, Flores I, Torres-Reverón A. The link between stress and endometriosis: From animal models to the clinical scenario. Reprod Sci. 2020;27(9):1675-1686. doi: 10.1007/s43032-020-00205-7

 

  1. Marino JL, Holt VL, Chen C, Davis S. Shift Work, hCLOCK T3111C polymorphism, and endometriosis risk. Epidemiology. 2008;19(3):477-484. doi: 10.1097/EDE.0b013e31816b7378

 

  1. Siopi E, Galerne M, Rivagorda M, et al. Gut microbiota changes require vagus nerve integrity to promote depressive-like behaviors in mice. Mol Psychiatry. 2023;28(7):3002-3012. doi: 10.1038/s41380-023-02071-6

 

  1. Griffiths JA, Yoo BB, Thuy-Boun P, et al. Peripheral neuronal activation shapes the microbiome and alters gut physiology. Cell Rep. 2024;43(4):113953. doi: 10.1016/j.celrep.2024.113953

 

  1. Joo MK, Kim DH. Vagus nerve-dependent effects of fluoxetine on anxiety- and depression-like behaviors in mice. Eur J Pharmacol. 2023;953:175862. doi: 10.1016/j.ejphar.2023.175862

 

  1. Hao M, Liu X, Rong P, Li S, Guo SW. Reduced vagal tone in women with endometriosis and auricular vagus nerve stimulation as a potential therapeutic approach. Sci Rep. 2021;11(1):1345. doi: 10.1038/s41598-020-79750-9

 

  1. Sobstyl A, Chałupnik A, Mertowska P, Grywalska E. How do microorganisms influence the development of endometriosis? Participation of genital, intestinal and oral microbiota in metabolic regulation and immunopathogenesis of endometriosis. Int J Mol Sci. 2023;24(13):10920. doi: 10.3390/ijms241310920

 

  1. Zhang H, Zou H, Zhang C, Zhang S. Chronic endometritis and the endometrial microbiota: Implications for reproductive success in patients with recurrent implantation failure. Ann Clin Microbiol Antimicrob. 2024;23(1):49. doi: 10.1186/s12941-024-00710-6

 

  1. Plesniarski A, Siddik AB, Su RC. The microbiome as a key regulator of female genital tract barrier function. Front Cell Infect Microbiol. 2021;11:790627. doi: 10.3389/fcimb.2021.790627

 

  1. Castillo DF, Denson LA, Haslam DB, et al. The microbiome in adolescents with irritable bowel syndrome and changes with percutaneous electrical nerve field stimulation. Neurogastroenterol Motil. 2023;35(7):e14573. doi: 10.1111/nmo.14573

 

  1. Marasco G, Cremon C, Barbaro MR, Stanghellini V, Barbara G. Gut microbiota signatures and modulation in irritable bowel syndrome. Microbiome Res Rep. 2022;1:11. doi: 10.20517/mrr.2021.12

 

  1. Bonaz B. Unmet needs of drugs for irritable bowel syndrome and inflammatory bowel diseases: Interest of vagus nerve stimulation and hypnosis. Inflammopharmacology. 2024;32(2):1005-1015. doi: 10.1007/s10787-024-01446-7

 

  1. Bonaz B. Non-invasive vagus nerve stimulation: The future of inflammatory bowel disease treatment? Bioelectron Med. 2023;9(1):26. doi: 10.1186/s42234-023-00129-y

 

  1. D’Haens G, Eberhardson M, Cabrijan Z, et al. Neuroimmune modulation through vagus nerve stimulation reduces inflammatory activity in Crohn’s disease patients: A prospective open-label study. J Crohns Colitis. 2023;17(12):1897-1909. doi: 10.1093/ecco-jcc/jjad151

 

  1. Yan Q, Chen J, Ren X, et al. Vagus nerve stimulation relives irritable bowel syndrome and the associated depression via α7nAChR-mediated anti-inflammatory pathway. Neuroscience. 2023;530:26-37. doi: 10.1016/j.neuroscience.2023.08.026

 

  1. Keever KR, Yakubenko VP, Hoover DB. Neuroimmune nexus in the pathophysiology and therapy of inflammatory disorders: Role of α7 nicotinic acetylcholine receptors. Pharmacol Res. 2023;191:106758. doi: 10.1016/j.phrs.2023.106758

 

  1. Keever KR, Cui K, Casteel JL, et al. Cholinergic signaling via the α7 nicotinic acetylcholine receptor regulates the migration of monocyte-derived macrophages during acute inflammation. J Neuroinflammation. 2024;21(1):3. doi: 10.1186/s12974-023-03001-7

 

  1. Kavakbasi E, Van Assche E, Schwarte K, Hohoff C, Baune BT. Long-term immunomodulatory impact of VNS on Peripheral cytokine profiles and its relationship with clinical response in Difficult-to-Treat Depression (DTD). Int J Mol Sci. 2024;25(8):4196. doi: 10.3390/ijms25084196

 

  1. Fang YT, Lin YT, Tseng WL, et al. Neuroimmunomodulation of vagus nerve stimulation and the therapeutic implications. Front Aging Neurosci. 2023;15:1173987. doi: 10.3389/fnagi.2023.1173987

 

  1. Kelly MJ, Breathnach C, Tracey KJ, Donnelly SC. Manipulation of the inflammatory reflex as a therapeutic strategy. Cell Rep Med. 2022;3(7):100696. doi: 10.1016/j.xcrm.2022.100696

 

  1. Falvey A, Metz CN, Tracey KJ, Pavlov VA. Peripheral nerve stimulation and immunity: The expanding opportunities for providing mechanistic insight and therapeutic intervention. Int Immunol. 2022;34(2):107-118. doi: 10.1093/intimm/dxab068

 

  1. Bonaz B, Sinniger V, Pellissier S. Anti‐inflammatory properties of the vagus nerve: Potential therapeutic implications of vagus nerve stimulation. J Physiol. 2016;594(20):5781-5790. doi: 10.1113/JP271539

 

  1. Borovikova LV, Ivanova S, Zhang M, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 2000;405(6785):458-462. doi: 10.1038/35013070

 

  1. Hao M, Liu X, Guo SW. Activation of α7 nicotinic acetylcholine receptor retards the development of endometriosis. Reprod Biol Endocrinol. 2022;20(1):85. doi: 10.1186/s12958-022-00955-w

 

  1. Bonaz B. Anti‐inflammatory effects of vagal nerve stimulation with a special attention to intestinal barrier dysfunction. Neurogastroenterol Motil. 2022;34(10):e14456. doi: 10.1111/nmo.14456

 

  1. WangY, Tan Q, Pan M, et al. Minimally invasive vagus nerve stimulation modulates mast cell degranulation via the microbiota-gut-brain axis to ameliorate blood-brain barrier and intestinal barrier damage following ischemic stroke. Int Immunopharmacol. 2024;132:112030. doi: 10.1016/j.intimp.2024.112030

 

  1. Aizawa H, Inoue H, Shigyo M, et al. VIP antagonists enhance excitatory cholinergic neurotransmission in the human airway. Lung. 1994;172(3):159-167. doi: 10.1007/BF00175944

 

  1. Bremner JD, Gurel NZ, Wittbrodt MT, et al. Application of noninvasive vagal nerve stimulation to stress-related psychiatric disorders. J Pers Med. 2020;10(3):119. doi: 10.3390/jpm10030119

 

  1. Tan C, Qiao M, Ma Y, Luo Y, Fang J, Yang Y. The efficacy and safety of transcutaneous auricular vagus nerve stimulation in the treatment of depressive disorder: A systematic review and meta-analysis of randomized controlled trials. J Affect Disord. 2023;337:37-49. doi: 10.1016/j.jad.2023.05.048

 

  1. Sun L, Ma S, Yu Y, et al. Transcutaneous auricular vagus nerve stimulation ameliorates adolescent depressive‐ and anxiety‐like behaviors via hippocampus glycolysis and inflammation response. CNS Neurosci Ther. 2024;30(2):e14614. doi: 10.1111/cns.14614

 

  1. Okonogi T, Kuga N, Yamakawa M, Kayama T, Ikegaya Y, Sasaki T. Stress-induced vagal activity influences anxiety-relevant prefrontal and amygdala neuronal oscillations in male mice. Nat Commun. 2024;15(1):183. doi: 10.1038/s41467-023-44205-y

 

  1. Jiang Y, Li L, Tan X, Liu B, Zhang Y, Li C. miR‐210 mediates vagus nerve stimulation‐induced antioxidant stress and anti‐apoptosis reactions following cerebral ischemia/reperfusion injury in rats. J Neurochem. 2015;134(1):173-181. doi: 10.1111/jnc.13097

 

  1. Zhang Q, Zhang L, Lin G, Luo F. The protective role of vagus nerve stimulation in ischemia-reperfusion injury. Heliyon. 2024;10(10):e30952. doi: 10.1016/j.heliyon.2024.e30952

 

  1. Bie B, Wang Z, Chen Y, et al. Vagus nerve stimulation affects inflammatory response and anti-apoptosis reactions via regulating miR-210 in epilepsy rat model. Neuroreport. 2021;32(9):783-791. doi: 10.1097/WNR.0000000000001655

 

  1. Ouyang S, Chen W, Zeng G, et al. MicroRNA-183-3p up-regulated by vagus nerve stimulation mitigates chronic systolic heart failure via the reduction of BNIP3L-mediated autophagy. Gene. 2020;726:144136. doi: 10.1016/j.gene.2019.144136

 

  1. Kellett DO, Aziz Q, Humphries JD, et al. Transcriptional response of the heart to vagus nerve stimulation. Physiol Genomics. 2024;56(2):167-178. doi: 10.1152/physiolgenomics.00095.2023

 

  1. Sanders TH, Weiss J, Hogewood L, et al. Cognition-enhancing vagus nerve stimulation alters the epigenetic landscape. J Neurosci. 2019;39:3454-3469. doi: 10.1523/JNEUROSCI.2407-18.2019

 

  1. Zhang M, Xu T, Tong D, et al. Research advances in endometriosis-related signaling pathways: A review. Biomed Pharmacother. 2023;164:114909. doi: 10.1016/j.biopha.2023.114909

 

  1. Sun P, Zhou K, Wang S, et al. Involvement of MAPK/ NF-κB signaling in the activation of the cholinergic anti-inflammatory pathway in experimental colitis by chronic vagus nerve stimulation. PLoS One. 2013;8(8):e69424. doi: 10.1371/journal.pone.0069424

 

  1. Hervias T. An update on migraine: Current and new treatment options. JAAPA. 2024;37(5):1-7. doi: 10.1097/01.JAA.0000000000000014

 

  1. Mwamburi M, Tenaglia AT, Leibler EJ, Staats PS. Review of evidence on noninvasive vagus nerve stimulation for treatment of migraine: Efficacy, safety, and implications. Am J Manag Care. 2018;24(24 Suppl):S507-S516.

 

  1. Staats P, Giannakopoulos G, Blake J, Liebler E, Levy RM. The use of non-invasive vagus nerve stimulation to treat respiratory symptoms associated with COVID-19: A theoretical hypothesis and early clinical experience. Neuromodulation. 2020;23(6):784-788. doi: 10.1111/ner.13172

 

  1. Peterson D, Van Poppel M, Boling W, et al. Clinical safety and feasibility of a novel implantable neuroimmune modulation device for the treatment of rheumatoid arthritis: Initial results from the randomized, double-blind, sham-controlled RESET-RA study. Bioelectron Med. 2024;10(1):8. doi: 10.1186/s42234-023-00138-x

 

  1. Tornero C, Pastor E, Del Mar Garzando MD, et al. Non-invasive vagus nerve stimulation for COVID-19: Results from a randomized controlled trial (SAVIOR I). Front Neurol. 2022;13:820864. doi: 10.3389/fneur.2022.820864

 

  1. Chang YT, Lu TF, Sun L, et al. Case report: Malignant transformation of ovarian endometrioma during long term use of dienogest in a young lady. Front Oncol. 2024;14:1338472. doi: 10.3389/fonc.2024.1338472

 

  1. Ben-Menachem E, Revesz D, Simon BJ, Silberstein S. Surgically implanted and non-invasive vagus nerve stimulation: A review of efficacy, safety and tolerability. Eur J Neurol. 2015;22(9):1260-1268. doi: 10.1111/ene.12629

 

  1. Gidron Y, De Couck M, De Greve J. If you have an active vagus nerve, cancer stage may no longer be important. J Biol Regul Homeost Agents. 2014;28(2):195-201.

 

  1. De Couck M, Caers R, Spiegel D, Gidron Y. The role of the vagus nerve in cancer prognosis: A systematic and a comprehensive review. J Oncol. 2018;2018:1236787. doi: 10.1155/2018/1236787

 

  1. Guo SW. An overview of the current status of clinical trials on endometriosis: Issues and concerns. Fertil Steril. 2014;101(1):183-190.e4. doi: 10.1016/j.fertnstert.2013.08.050

 

  1. Xu Y, Deng Z, Fei F, Zhou S. An overview and comprehensive analysis of interdisciplinary clinical research in endometriosis based on trial registry. iScience. 2024;27(3):109298. doi: 10.1016/j.isci.2024.109298

 

  1. Guo SW, Groothuis PG. Is it time for a paradigm shift in drug research and development in endometriosis/adenomyosis? Hum Reprod Update. 2018;24(5):577-598. doi: 10.1093/humupd/dmy020

 

  1. Woodbury A, Staats P. Editorial: Non-invasive and minimally invasive vagus nerve stimulation for chronic pain. Front Pain Res (Lausanne). 2024;5:1402918. doi: 10.3389/fpain.2024.1402918

 

  1. Napadow V, Edwards RR, Cahalan CM, et al. Evoked pain analgesia in chronic pelvic pain patients using respiratory-gated auricular vagal afferent nerve stimulation. Pain Med. 2012;13(6):777-789. doi: 10.1111/j.1526-4637.2012.01385.x

 

  1. Dobson GP, Letson HL, Morris JL. Revolution in sepsis: A symptoms-based to a systems-based approach? J Biomed Sci. 2024;31(1):57. doi: 10.1186/s12929-024-01043-4

 

  1. Burla L, Kalaitzopoulos DR, Metzler JM, Scheiner D, Imesch P. Popularity of endocrine endometriosis drugs and limited alternatives in the present and foreseeable future: A survey among 1420 affected women. Eur J Obstet Gynecol Reprod Biol. 2021;262:232-238. doi: 10.1016/j.ejogrb.2021.05.040

 

  1. Saunders PTK, Horne AW. Endometriosis: Etiology, pathobiology, and therapeutic prospects. Cell. 2021; 184(11):2807-2824. doi: 10.1016/j.cell.2021.04.041

 

  1. Martinelli S, Nannini G, Cianchi F, Staderini F, Coratti F, Amedei A. Microbiota transplant and gynecological disorders: The bridge between present and future treatments. Microorganisms. 2023;11(10):2407. doi: 10.3390/microorganisms11102407

 

  1. Guidozzi F. Endometriosis-associated cancer. Climacteric. 2021;24(6):587-592. doi: 10.1080/13697137.2021.1948994

 

  1. Arab C, Vanderlei LCM, Da Silva Paiva L, et al. Cardiac autonomic modulation impairments in advanced breast cancer patients. Clin Res Cardiol. 2018;107(10):924-936. doi: 10.1007/s00392-018-1264-9

 

  1. Chen LH, Lo WC, Huang HY, Wu HM. A lifelong impact on endometriosis: Pathophysiology and pharmacological treatment. Int J Mol Sci. 2023;24(8):7503. doi: 10.3390/ijms24087503
Share
Back to top
Microbes & Immunity, Electronic ISSN: 3029-2883 Print ISSN: 3041-0886, Published by AccScience Publishing
We use cookies on our website to ensure you get the best experience.
Read more about our cookies here
Accept