Bioelectronic medicine for restoring autonomic balance in autoimmune diseases
DOI:
https://doi.org/10.54844/gmiw.2022.0182Keywords:
vagus nerve stimulation, sacral nerve stimulation, sacral neuromodulation, autonomic functions, thyroiditis, psoriasis, inflammatory bowel disease, type 1 diabetesAbstract
The aim of this mini-review is to introduce most prevalent autoimmune diseases, emphasize the importance of sympathoparasympathetic imbalance in these autoimmune diseases, demonstrate how such imbalance can be effectively treated using the bioelectronic medicine, and describe potential mechanisms of bioelectronic medicine effects on the autoimmune
activity at the cellular and molecular levels.
References
Sisó-Almirall A, Kostov B, Martínez-Carbonell E, et al. The prevalence of 78 autoimmune diseases in Catalonia (MASCAT-PADRIS Big Data Project). Autoimmun Rev. 2020;19(2):102448. [PMID:31838161 DOI:10.1016/j.autrev.2019.102448]
Anaya JM, Herrán M, Beltrán S, Rojas M. Is post-COVID syndrome an autoimmune disease?. Expert Rev Clin Immunol. 2022;18(7):653-666. [PMID:35658801 DOI:10.1080/1744666X.2022.2085561]
Cooper GS, Stroehla BC. The epidemiology of autoimmune diseases. Autoimmun Rev. 2003;2(3):119-125. [PMID:12848952 DOI:10.1016/s1568-9972(03)00006-5]
Davis NF, Brady CM, Creagh T. Interstitial cystitis/painful bladder syndrome: epidemiology, pathophysiology and evidence-based treatment options. Eur J Obstet Gynecol Reprod Biol. 2014;175:30-37. [PMID:24480114 DOI:10.1016/j.ejogrb.2013.12.041]
Bellocchi C, Carandina A, Montinaro B, et al. The Interplay between Autonomic Nervous System and Inflammation across Systemic Autoimmune Diseases. Int J Mol Sci. 2022;23(5):2449. [PMID:35269591 DOI:10.3390/ijms23052449]
Valenza G, Citi L, Saul JP, Barbieri R. Measures of sympathetic and parasympathetic autonomic outflow from heartbeat dynamics. J Appl Physiol (1985). 2018;125(1):19-39. [PMID:29446712 DOI:10.1152/japplphysiol.00842.2017]
Adjei T, von Rosenberg W, Nakamura T, Chanwimalueang T, Mandic DP. The ClassA Framework: HRV Based Assessment of SNS and PNS Dynamics Without LF-HF Controversies. Front Physiol. 2019;10:505. [PMID:31133868 DOI:10.3389/fphys.2019.00505]
Ali MK, Chen JDZ. Roles of Heart Rate Variability in Assessing Autonomic Nervous System in Functional Gastrointestinal Disorders: A Systematic Review. Diagnostics (Basel). 2023;13(2):293. [PMID:36673103 DOI:10.3390/diagnostics13020293]
Ramanathan R, Jayabal M, Subramaniam M, Selvaraj V. Comparison of heart rate variability and classical autonomic function tests between type 2 diabetes mellitus and healthy volunteers. Indian J Clin Anat Physiol. 2020;7(1):27-31. [DOI:10.18231/j.ijcap.2020.007]
Videira G, Castro P, Vieira B, et al. Autonomic dysfunction in multiple sclerosis is better detected by heart rate variability and is not correlated with central autonomic network damage. J Neurol Sci. 2016;367:133-137. [DOI:10.1016/j.jns.2016.05.049]
Galetta F, Franzoni F, Fallahi P, et al. Changes in heart rate variability and QT dispersion in patients with overt hypothyroidism. Eur J Endocrinol. 2008;158(1):85-90. [PMID:18166821 DOI:10.1530/eje-07-0357]
Proietti I, Raimondi G, Skroza N, et al. Cardiovascular risk in psoriatic patients detected by heart rate variability (HRV) analysis. Drug Dev Res. 2014;75 Suppl 1:S81-S84. [PMID:25381987 DOI:10.1002/ddr.21204]
Hirten RP, Danieletto M, Scheel R, et al. Longitudinal Autonomic Nervous System Measures Correlate With Stress and Ulcerative Colitis Disease Activity and Predict Flare. Inflamm Bowel Dis. 2021;27(10):1576-1584. [PMID:33382065 DOI:10.1093/ibd/izaa323]
Gunterberg V, Simrén M, Öhman L, et al. Autonomic nervous system function predicts the inflammatory response over three years in newly diagnosed ulcerative colitis patients. Neurogastroenterol Motil. 2016;28(11):1655-1662. [PMID:27265090 DOI:10.1111/nmo.12865]
Sadowski A, Dunlap C, Lacombe A, Hanes D. Alterations in Heart Rate Variability Associated With Irritable Bowel Syndrome or Inflammatory Bowel Disease: A Systematic Review and Meta-Analysis. Clin Transl Gastroenterol. 2020;12(1):e00275. [PMID:33346998 DOI:10.14309/ctg.0000000000000275]
Kim KN, Yao Y, Ju SY. Heart rate variability and inflammatory bowel disease in humans: A systematic review and meta-analysis. Medicine (Baltimore). 2020;99(48):e23430. [PMID:33235125 DOI:10.1097/md.0000000000023430]
Jaiswal M, Urbina EM, Wadwa RP, et al. Reduced heart rate variability among youth with type 1 diabetes: the SEARCH CVD study. Diabetes Care. 2013;36(1):157-162. [PMID:22961570 DOI:10.2337/dc12-0463]
Guan L, Metzger DL, Lavoie PM, Collet JP. Glucose control and autonomic response during acute stress in youth with type 1 diabetes: A pilot study. Pediatr Diabetes. 2018;19(5):1020-1024. [PMID:29654713 DOI:10.1111/pedi.12680]
França da Silva AK, Destro Christofaro DG, Manata Vanzella L, Marques Vanderlei F, Lopez Laurino MJ, Marques Vanderlei LC. Relationship of the Aggregation of Cardiovascular Risk Factors in the Parasympathetic Modulation of Young People with Type 1 Diabetes. Medicina (Kaunas). 2019;55(9):534. [PMID:31454959 DOI:10.3390/medicina55090534]
Lazzerini PE, Acampa M, Capecchi PL, et al. Association between high sensitivity C-reactive protein, heart rate variability and corrected QT interval in patients with chronic inflammatory arthritis. Eur J Intern Med. 2013;24(4):368-374. [PMID:23517852 DOI:10.1016/j.ejim.2013.02.009]
Adlan AM, Veldhuijzen van Zanten JJCS, Lip GYH, Paton JFR, Kitas GD, Fisher JP. Cardiovascular autonomic regulation, inflammation and pain in rheumatoid arthritis. Auton Neurosci. 2017;208:137-145. [PMID:28927867 DOI:10.1016/j.autneu.2017.09.003]
Koopman FA, Tang MW, Vermeij J, et al. Autonomic Dysfunction Precedes Development of Rheumatoid Arthritis: A Prospective Cohort Study. EBioMedicine. 2016;6:231-237. [PMID:27211565 DOI:10.1016/j.ebiom.2016.02.029]
Stojanovich L, Milovanovich B, de Luka SR, et al. Cardiovascular autonomic dysfunction in systemic lupus, rheumatoid arthritis, primary Sjögren syndrome and other autoimmune diseases. Lupus. 2007;16(3):181-185. [PMID:17432103 DOI:10.1177/0961203306076223]
Birmingham K, Gradinaru V, Anikeeva P, et al. Bioelectronic medicines: a research roadmap. Nat Rev Drug Discov. 2014;13(6):399-400. [PMID:24875080 DOI:10.1038/nrd4351]
Thompson N, Mastitskaya S, Holder D. Avoiding off-target effects in electrical stimulation of the cervical vagus nerve: Neuroanatomical tracing techniques to study fascicular anatomy of the vagus nerve. J Neurosci Methods. 2019;325:108325. [PMID:31260728 DOI:10.1016/j.jneumeth.2019.108325]
Kucia K, Merk W, Zapalowicz K, Medrala T. Vagus Nerve Stimulation For Treatment Resistant Depression: Case Series Of Six Patients - Retrospective Efficacy And Safety Observation After One Year Follow Up. Neuropsychiatr Dis Treat. 2019;15:3247-3254. [PMID:31819452 DOI:10.2147/NDT.S217816]
Lee PC, Dixon J. Medical devices for the treatment of obesity. Nat Rev Gastroenterol Hepatol. 2017;14(9):553-564. [PMID:28698663 DOI:10.1038/nrgastro.2017.80]
US Food and Drug Administration. Premarket Approval P970003 for VNS Therapy System. FDA US Food and Drug Administration website. Accessed May 4, 2022. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpma/pma.cfm?id=P970003 [DOI:10.1037/e362142004-001]
US Food and Drug Administration. Premarket Approval P970003-S050 for VNS Therapy System. FDA website. Accessed May 4, 2022. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpma/pma.cfm?id=P970003S050 [DOI:10.1037/e362142004-001]
US Food and Drug Administration. Premarket Approval P2100007 for Vivistim System. FDA website. Accessed May 4, 2022. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpma/pma.cfm?id=P210007 [DOI:10.1037/e362142004-001]
ClinicalTrials.gov. Long Term Extension of Safety and Efficacy of Vagus Nerve Stimulator in Patients With Rheumatoid Arthritis (RA). ClinicalTrials.gov website. Published April 27, 2021. Updated April 27, 2021. Accessed March 14, 2023. https://clinicaltrials.gov/ct2/show/NCT04862117 [DOI:10.2169/naika.101.3002]
ClinicalTrials.gov. Vagus Nerve Stimulation for Moderate to Severe Rheumatoid Arthritis (RESET-RA). ClinicalTrials.gov website. Published September 07, 2020. Updated March 09, 2023. Accessed March 14, 2023. https://clinicaltrials.gov/ct2/show/NCT04539964 [DOI:10.1179/175709310x12845438122791]
ClinicalTrials.gov. ANTHEM-HFrEF Pivotal Study. ClinicalTrials.gov website. Published February 07, 2018. Updated June 02, 2022. Accessed March 14, 2023. https://clinicaltrials.gov/ct2/show/NCT03425422 [DOI:10.1179/175709310x12845438122791]
ClinicalTrials.gov. Neural Cardiac Therapy for Heart Failure Study (NECTAR-HF) (NECTAR-HF). ClinicalTrials.gov website. Published June 30, 2011. Updated March 03, 2023. Accessed March 14, 2023. https://clinicaltrials.gov/ct2/show/NCT01385176 [DOI:10.1179/175709310x12845438122791]
ClinicalTrials.gov. Relief of Acute Bronchoconstriction/Asthma Using the Non-Invasive AlphaCore Device. ClinicalTrials.gov website. Published February 15, 2012. Updated April 09, 2018. Accessed March 14, 2023. https://clinicaltrials.gov/ct2/show/NCT01532817 [DOI:10.1179/175709310x12845438122791]
Badran BW, Huffman SM, Dancy M, et al. A pilot randomized controlled trial of supervised, at-home, self-administered transcutaneous auricular vagus nerve stimulation (taVNS) to manage long COVID symptoms. Bioelectron Med. 2022;8(1):13. [PMID:36002874 DOI:10.1186/s42234-022-00094-y]
Merchant K, Zanos S, Datta-Chaudhuri T, Deutschman CS, Sethna CB. Transcutaneous auricular vagus nerve stimulation (taVNS) for the treatment of pediatric nephrotic syndrome: a pilot study. Bioelectron Med. 2022;8(1):1. [PMID:35078538 DOI:10.1186/s42234-021-00084-6]
ClinicalTrials.gov. Long Term Observational Study of a Vagal Nerve Stimulation Device in Crohn's Disease. ClinicalTrials.gov website. Published November 01, 2016. Updated August 03, 2017. Accessed March 14, 2023. https://clinicaltrials.gov/ct2/show/NCT02951650 [DOI:10.1179/175709310x12845438122791]
US Food and Drug Administration. Premarket Approval P130019 for Maestro Rechargeable System. FDA website. Accessed May 4, 2022. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpma/pma.cfm?id=P130019 [DOI:10.1037/e362142004-001]
Bray GA. Therapeutic Management of Obesity. In: Davidson MH, Toth PP, Maki KC, eds. Therapeutic Lipidology. Humana, Cham; 2021: 323-339. [DOI:10.1007/978-3-030-56514-5_17]
Tilborghs S, De Wachter S. Sacral neuromodulation for the treatment of overactive bladder: systematic review and future prospects. Expert Rev Med Devices. 2022;19(2):161-187. [PMID:35061951 DOI:10.1080/17434440.2022.2032655]
Weledji EP, Marti L. A historical perspective of sacral nerve stimulation (SNS) for bowel dysfunction. IJS: Short Reports. 2021;6(3):e25. [DOI:10.1097/sr9.0000000000000025]
Gurland B, Aytac E. Anatomy and physiology: Neurologic basis for the function of sacral nerve stimulation. Semin Colon Rectal Surg. 2017;28(4):156-159. [DOI:10.1053/j.scrs.2017.07.002]
US Food and Drug Administration. Premarket Approval P970004 for InterStim Therapy System. FDA website. Accessed March 15, 2023. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpma/pma.cfm?id=P970004 [DOI:10.1037/e413852005-001]
US Food and Drug Administration. Premarket Approval P080025 for InterStim Sacral Nerve Stimulation Therapy System. FDA website. Accessed March 15, 2023. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpma/pma.cfm?id=P080025 [DOI:10.1037/e413852005-001]
Noblett KL, Cadish LA. Sacral nerve stimulation for the treatment of refractory voiding and bowel dysfunction. Am J Obstet Gynecol. 2014;210(2):99-106. [PMID:23899452 DOI:10.1016/j.ajog.2013.07.025]
ClinicalTrials.gov. Sacral Nerve Stimulation for Mild-to-Moderate or Refractory Rheumatoid Arthritis. ClinicalTrials.gov website. Published March 29, 2021. Updated March 04, 2022. Accessed March 15, 2023. https://clinicaltrials.gov/ct2/show/NCT04821050 [DOI:10.1179/175709310x12845438122791]
ClinicalTrials.gov. Subsensory Sacral Nerve Stimulation for Irritable Bowel Syndrome. ClinicalTrials.gov website. Published September 24, 2013. Updated May 17, 2018. Accessed March 15, 2023. https://clinicaltrials.gov/ct2/show/NCT01948973 [DOI:10.1179/175709310x12845438122791]
Fassov J, Lundby L, Laurberg S, Buntzen S, Krogh K. Three-year follow-up of sacral nerve stimulation for patients with diarrhoea-predominant and mixed irritable bowel syndrome. Colorectal Dis. 2017;19(2):188-193. [PMID:27328645 DOI:10.1111/codi.13428]
ClinicalTrials.gov. Sacral Neuromodulation for Pelvic Pain Associated With Endometriosis. ClinicalTrials.gov website. Published May 04, 2017. Updated May 17, 2021. Accessed March 15, 2023. https://clinicaltrials.gov/ct2/show/NCT03139734 [DOI:10.1179/175709310x12845438122791]
Carnagarin R, Kiuchi MG, Goh G, et al. Role of the sympathetic nervous system in cardiometabolic control: implications for targeted multiorgan neuromodulation approaches. J Hypertens. 2021;39(8):1478-1489. [PMID:33657580 DOI:10.1097/hjh.0000000000002839]
Donegà M, Fjordbakk CT, Kirk J, et al. Human-relevant near-organ neuromodulation of the immune system via the splenic nerve. Proc Natl Acad Sci U S A. 2021;118(20):e2025428118. [PMID:33972441 DOI:10.1073/pnas.2025428118]
Sokal DM, McSloy A, Donegà M, et al. Splenic Nerve Neuromodulation Reduces Inflammation and Promotes Resolution in Chronically Implanted Pigs. Front Immunol. 2021;12:649786. [PMID:33859641 DOI:10.3389/fimmu.2021.649786]
Wilks SJ, Hara SA, Ross EK, et al. Non-clinical and Pre-clinical Testing to Demonstrate Safety of the Barostim Neo Electrode for Activation of Carotid Baroreceptors in Chronic Human Implants. Front Neurosci. 2017;11:438. [PMID:28824361 DOI:10.3389/fnins.2017.00438]
ClinicalTrials.gov. Splenic Stimulation for RA. ClinicalTrials.gov website. Published August 12, 2021. Updated October 26, 2021. Accessed March 15, 2023. https://clinicaltrials.gov/ct2/show/NCT05003310 [DOI:10.1179/175709310x12845438122791]
ClinicalTrials.gov. Safety of Splenic Stimulation for RA. ClinicalTrials.gov website. Published July 09, 2021. Updated October 26, 2021. Accessed March 15, 2023. https://clinicaltrials.gov/ct2/show/NCT04955899 [DOI:10.1179/175709310x12845438122791]
US Food and Drug Administration. Premarket Approval P180050 for Barostim Neo System. FDA website. Accessed March 15, 2023. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpma/pma.cfm?id=P180050 [DOI:10.1037/e413852005-001]
van Kleef MEAM, Bates MC, Spiering W. Endovascular Baroreflex Amplification for Resistant Hypertension. Curr Hypertens Rep. 2018;20(5):46. [PMID:29744599 DOI:10.1007/s11906-018-0840-8]
ClinicalTrials.gov. Controlling and Lowering Blood Pressure With the MobiusHD (CALM-DIEM). ClinicalTrials.gov website. Published July 11, 2016. Updated October 12, 2022. Accessed March 15, 2023. https://clinicaltrials.gov/ct2/show/NCT02827032 [DOI:10.1179/175709310x12845438122791]
ClinicalTrials.gov. CALM- 2 - Controlling and Lowering Blood Pressure With the MobiusHD (CALM-2). ClinicalTrials.gov website. Published June 07, 2017. Updated October 12, 2022. Accessed March 15, 2023. https://clinicaltrials.gov/ct2/show/NCT03179800 [DOI:10.1179/175709310x12845438122791]
Li YQ, Zhu B, Rong PJ, Ben H, Li YH. Neural mechanism of acupuncture-modulated gastric motility. World J Gastroenterol. 2007;13(5):709-716. [PMID:17278193 DOI:10.3748/wjg.v13.i5.709]
Ouyang H, Yin J, Wang Z, Pasricha PJ, Chen JD. Electroacupuncture accelerates gastric emptying in association with changes in vagal activity. Am J Physiol Gastrointest Liver Physiol. 2002;282(2):G390-G396. [PMID:11804862 DOI:10.1152/ajpgi.00272.2001]
Ouyang H, Xing J, Chen J. Electroacupuncture restores impaired gastric accommodation in vagotomized dogs. Dig Dis Sci. 2004;49(9):1418-1424. [PMID:15481313 DOI:10.1023/b:ddas.0000042240.05247.01]
Chen J, Song GQ, Yin J, Koothan T, Chen JD. Electroacupuncture improves impaired gastric motility and slow waves induced by rectal distension in dogs. Am J Physiol Gastrointest Liver Physiol. 2008;295(3):G614-G620. [PMID:18653722 DOI:10.1152/ajpgi.90322.2008]
Song J, Yin J, Chen J. Needleless transcutaneous electroacupuncture improves rectal distension-induced impairment in intestinal motility and slow waves via vagal mechanisms in dogs. Int J Clin Exp Med. 2015;8(3):4635-4646. [PMID:26064396 DOI:10.1016/s0016-5085(11)63357-x]
Fang JF, Fang JQ, Shao XM, et al. Electroacupuncture treatment partly promotes the recovery time of postoperative ileus by activating the vagus nerve but not regulating local inflammation. Sci Rep. 2017;7:39801. [PMID:28051128 DOI:10.1038/srep39801]
Pan WX, Fan AY, Chen S, Alemi SF. Acupuncture modulates immunity in sepsis: Toward a science-based protocol. Auton Neurosci. 2021;232:102793. [PMID:33684727 DOI:10.1016/j.autneu.2021.102793]
Takahashi T. Effect and mechanism of acupuncture on gastrointestinal diseases. Int Rev Neurobiol. 2013;111:273-294. [PMID:24215928 DOI:10.1016/B978-0-12-411545-3.00014-6]
Meng JB, Jiao YN, Xu XJ, et al. Electro-acupuncture attenuates inflammatory responses and intraabdominal pressure in septic patients: A randomized controlled trial. Medicine (Baltimore). 2018;97(17):e0555. [PMID:29703040 DOI:10.1097/md.0000000000010555]
Yang G, Zheng B, Yu Y, et al. Electroacupuncture at Zusanli (ST36), Guanyuan (CV4), and Qihai (CV6) Acupoints Regulates Immune Function in Patients with Sepsis via the PD-1 Pathway. Biomed Res Int. 2022;2022:7037497. [PMID:35860804 DOI:10.1155/2022/7037497]
Ge F, Ji Y, Ma XP. [Clinical effect observation of electroacupuncture combined with medicine in the treatment of ulcerative colitis]. China Modern Medicine. 2015;22(06):164-168. [DOI:10.47939/mh.v2i1.100]
Xie Yy, Li Ss, Ben Yh. Clinical observation on electroacupuncture plus long-snake moxibustion for rheumatoid arthritis due to kidney deficiency and cold coagulation. J Acupunct Tuina Sci. 2020;18(6):467-473. [DOI:10.1007/s11726-020-1216-6]
Tracey KJ. The inflammatory reflex. Nature. 2002;420(6917):853-859. [PMID:12490958 DOI:10.1038/nature01321]
Koopman FA, Chavan SS, Miljko S, et al. Vagus nerve stimulation inhibits cytokine production and attenuates disease severity in rheumatoid arthritis. Proc Natl Acad Sci U S A. 2016;113(29):8284-8289. [PMID:27382171 DOI:10.1073/pnas.1605635113]
Genovese MC, Gaylis NB, Sikes D, et al. Safety and efficacy of neurostimulation with a miniaturised vagus nerve stimulation device in patients with multidrug-refractory rheumatoid arthritis: a two-stage multicentre, randomised pilot study. The Lancet Rheumatology. 2020;2(9):e527-e538. [DOI:10.1016/s2665-9913(20)30172-7]
Aranow C, Atish-Fregoso Y, Lesser M, et al. Transcutaneous auricular vagus nerve stimulation reduces pain and fatigue in patients with systemic lupus erythematosus: a randomised, double-blind, sham-controlled pilot trial. Ann Rheum Dis. 2021;80(2):203-208. [PMID:33144299 DOI:10.1136/annrheumdis-2020-217872]
Bonaz B, Sinniger V, Hoffmann D, et al. Chronic vagus nerve stimulation in Crohn's disease: a 6-month follow-up pilot study. Neurogastroenterol Motil. 2016;28(6):948-953. [PMID:26920654 DOI:10.1111/nmo.12792]
D'Haens G, Cabrijan Z, Eberhardson M, et al. P574 The effects of vagus nerve stimulation in biologic-refractory Crohn’s disease: A prospective clinical trial. Journal of Crohn's and Colitis. 2018;12(supplement 1):S397-S398. [DOI:10.1093/ecco-jcc/jjx180.701]
Matteoli G, Gomez-Pinilla PJ, Nemethova A, et al. A distinct vagal anti-inflammatory pathway modulates intestinal muscularis resident macrophages independent of the spleen. Gut. 2014;63(6):938-948. [PMID:23929694 DOI:10.1136/gutjnl-2013-304676]
Costes LM, van der Vliet J, van Bree SH, Boeckxstaens GE, Cailotto C. Endogenous vagal activation dampens intestinal inflammation independently of splenic innervation in postoperative ileus. Auton Neurosci. 2014;185:76-82. [PMID:25103359 DOI:10.1016/j.autneu.2014.07.006]
Caravaca AS, Levine YA, Drake A, Eberhardson M, Olofsson PS. Vagus Nerve Stimulation Reduces Indomethacin-Induced Small Bowel Inflammation. Front Neurosci. 2022;15:730407. [PMID:35095387 DOI:10.3389/fnins.2021.730407]
Torres-Rosas R, Yehia G, Peña G, et al. Dopamine mediates vagal modulation of the immune system by electroacupuncture. Nat Med. 2014;20(3):291-295. [PMID:24562381 DOI:10.1038/nm.3479]
Ulloa L, Quiroz-Gonzalez S, Torres-Rosas R. Nerve Stimulation: Immunomodulation and Control of Inflammation. Trends Mol Med. 2017;23(12):1103-1120. [PMID:29162418 DOI:10.1016/j.molmed.2017.10.006]
Bratton BO, Martelli D, McKinley MJ, Trevaks D, Anderson CR, McAllen RM. Neural regulation of inflammation: no neural connection from the vagus to splenic sympathetic neurons. Exp Physiol. 2012;97(11):1180-1185. [PMID:22247284 DOI:10.1113/expphysiol.2011.061531]
Gonzalez-Gonzalez MA, Bendale GS, Wang K, Wallace GG, Romero-Ortega M. Platinized graphene fiber electrodes uncover direct spleen-vagus communication. Commun Biol. 2021;4(1):1097. [PMID:34535751 DOI:10.1038/s42003-021-02628-7]
Ulloa L. Bioelectronic neuro-immunology: Neuronal networks for sympathetic-splenic and vagal-adrenal control. Neuron. 2023;111(1):10-14. [PMID:36202096 DOI:10.1016/j.neuron.2022.09.015]
McKinley MJ, Martelli D, Trevizan-Baú P, McAllen RM. Divergent splanchnic sympathetic efferent nerve pathways regulate interleukin-10 and tumour necrosis factor-α responses to endotoxaemia. J Physiol. 2022;600(20):4521-4536. [PMID:36056471 DOI:10.1113/JP283217]
Yoshida K, Saku K, Kamada K, et al. Electrical Vagal Nerve Stimulation Ameliorates Pulmonary Vascular Remodeling and Improves Survival in Rats With Severe Pulmonary Arterial Hypertension. JACC Basic Transl Sci. 2018;3(5):657-671. [PMID: 30456337 DOI:10.1016/j.jacbts.2018.07.007]
Jo BG, Kim SH, Namgung U. Vagal afferent fibers contribute to the anti-inflammatory reactions by vagus nerve stimulation in concanavalin A model of hepatitis in rats. Mol Med. 2020;26(1):119. [PMID: 33272194 DOI:10.1186/s10020-020-00247-2]
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. [PMID: 33446725 DOI:10.1038/s41598-020-79750-9]
Fitchett A, Mastitskaya S, Aristovich K. Selective Neuromodulation of the Vagus Nerve. Front Neurosci. 2021;15:685872. [PMID:34108861 DOI:10.3389/fnins.2021.685872]
Noller CM, Levine YA, Urakov TM, Aronson JP, Nash MS. Vagus Nerve Stimulation in Rodent Models: An Overview of Technical Considerations. Front Neurosci. 2019;13:911. [PMID:31551679 DOI:10.3389/fnins.2019.00911]
Skandalakis LJ, Skandalakis JE. Colon and Anorectum. In: Skandalakis L, Skandalakis J, eds. Surgical Anatomy and Technique. Springer, New York, NY; 2014: 431-513. [DOI:10.1007/978-1-4614-8563-6_12]
Chen Z, Ni M, Li J, et al. Su1616–Anti-Inflammatory Effects and Mechanisms of Sacral Nerve Stimulation Performed Via Acupuncture Needles on Ulcerative Colitis. Gastroenterology. 2019;156(6):S-585. [DOI:10.1016/s0016-5085(19)38355-6]
Hernández-Hernández D, Padilla-Fernández B, Navarro-Galmés MÁ, Hess-Medler S, Castro-Romera MM, Castro-Díaz DM. Sacral Neuromodulation in the Management of Bladder Pain Syndrome/Interstitial Cystitis. Curr Bladder Dysfunct Rep. 2020;15(1):83-92. [DOI:10.1007/s11884-020-00579-z]
Tu L, Gharibani P, Zhang N, Yin J, Chen JD. Anti-inflammatory effects of sacral nerve stimulation: a novel spinal afferent and vagal efferent pathway. Am J Physiol Gastrointest Liver Physiol. 2020;318(4):G624-G634. [PMID:32068444 DOI:10.1152/ajpgi.00330.2019]
Ye F, Liu Y, Li S, Zhang S, Foreman RD, Chen JD. Sacral nerve stimulation increases gastric accommodation in rats: a spinal afferent and vagal efferent pathway. Am J Physiol Gastrointest Liver Physiol. 2020;318(3):G574-G581. [PMID:31984783 DOI:10.1152/ajpgi.00255.2019]
Martelli D, Yao ST, McKinley MJ, McAllen RM. Reflex control of inflammation by sympathetic nerves, not the vagus. The Journal of physiology. 2014;592(7):1677-1686. [PMID:24421357 DOI:10.1113/jphysiol.2013.268573]
Martelli D, Yao ST, McKinley MJ, McAllen RM. Reflex control of inflammation by sympathetic nerves, not the vagus. J Physiol. 2014;592(7):1677-1686. [PMID:24421357 DOI:10.1113/jphysiol.2013.268573]
Komegae EN, Farmer DGS, Brooks VL, McKinley MJ, McAllen RM, Martelli D. Vagal afferent activation suppresses systemic inflammation via the splanchnic anti-inflammatory pathway. Brain Behav Immun. 2018;73:441-449. [PMID:29883598 DOI:10.1016/j.bbi.2018.06.005]
Patel YA, Saxena T, Bellamkonda RV, Butera RJ. Kilohertz frequency nerve block enhances anti-inflammatory effects of vagus nerve stimulation. Sci Rep. 2017;7:39810. [PMID:28054557 DOI:10.1038/srep39810]
Bonaz B, Sinniger V, Pellissier S. Therapeutic Potential of Vagus Nerve Stimulation for Inflammatory Bowel Diseases. Front Neurosci. 2021;15:650971. [PMID:33828455 DOI:10.3389/fnins.2021.650971]
Tanaka S, Abe C, Abbott SBG, et al. Vagus nerve stimulation activates two distinct neuroimmune circuits converging in the spleen to protect mice from kidney injury. Proc Natl Acad Sci U S A. 2021;118(12):e2021758118. [PMID:33737395 DOI:10.1073/pnas.2021758118]
Liu S, Wang Z, Su Y, et al. A neuroanatomical basis for electroacupuncture to drive the vagal-adrenal axis. Nature. 2021;598(7882):641-645. [DOI:10.1038/s41586-021-04001-4]
Stakenborg N, Boeckxstaens GE. Bioelectronics in the brain-gut axis: focus on inflammatory bowel disease (IBD). Int Immunol. 2021;33(6):337-348. [PMID:33788920 DOI:10.1093/intimm/dxab014]
Serafini MA, Paz AH, Nunes NS. Cholinergic immunomodulation in inflammatory bowel diseases. Brain Behav Immun Health. 2021;19:100401. [PMID:34977822 DOI:10.1016/j.bbih.2021.100401]
Mikami Y, Tsunoda J, Kiyohara H, Taniki N, Teratani T, Kanai T. Vagus nerve-mediated intestinal immune regulation: therapeutic implications of inflammatory bowel diseases. Int Immunol. 2022;34(2):97-106. [PMID:34240133 DOI:10.1093/intimm/dxab039]
Rosas-Ballina M, Olofsson PS, Ochani M, et al. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science. 2011;334(6052):98-101. [PMID:21921156 DOI:10.1126/science.1209985]
Yang NN, Yang JW, Ye Y, et al. Electroacupuncture ameliorates intestinal inflammation by activating α7nAChR-mediated JAK2/STAT3 signaling pathway in postoperative ileus. Theranostics. 2021;11(9):4078-4089. [PMID:33754049 DOI:10.7150/thno.52574]
Tu L, Gharibani P, Yin J, Chen JDZ. Sacral nerve stimulation ameliorates colonic barrier functions in a rodent model of colitis. Neurogastroenterol Motil. 2020;32(10):e13916. [PMID:32537873 DOI:10.1111/nmo.13916]
Brégeon J, Coron E, Da Silva AC, et al. Sacral nerve stimulation enhances early intestinal mucosal repair following mucosal injury in a pig model. J Physiol. 2016;594(15):4309-4323. [PMID:26939757 DOI:10.1113/jp271783]
Meroni E, Stakenborg N, Gomez-Pinilla PJ, et al. Vagus Nerve Stimulation Promotes Epithelial Proliferation and Controls Colon Monocyte Infiltration During DSS-Induced Colitis. Front Med (Lausanne). 2021;8:694268. [PMID:34307422 DOI:10.3389/fmed.2021.694268]
Hu J, Hu W, Tang L, Wang Y. Fundamental Neurocircuit of Anti-inflammatory Effect by Electroacupuncture Stimulation Identified. Neurosci Bull. 2022;38(7):837-839. [PMID:35437620 DOI:10.1007/s12264-022-00849-2]
Liu S, Wang ZF, Su YS, et al. Somatotopic Organization and Intensity Dependence in Driving Distinct NPY-Expressing Sympathetic Pathways by Electroacupuncture. Neuron. 2020;108(3):436-450.e7. [PMID:32791039 DOI:10.1016/j.neuron.2020.07.015]
Published
How to Cite
Issue
Section
