164
Views
0
CrossRef citations to date
0
Altmetric
Review

The Role of Vagus Nerve Stimulation in Sepsis

ORCID Icon, , , , &
Pages 51-62 | Received 30 Jun 2020, Accepted 22 Sep 2020, Published online: 21 Oct 2020

References

  • Singer M , DeutschmanCS, SeymourCWet al. The third international consensus definitions for sepsis and septic shock (sepsis-3). JAMA315(8), 801–810 (2016).
  • Rittirsch D , FlierlMA, WardPA. Harmful molecular mechanisms in sepsis. Nat. Rev. Immunol.8(10), 776–787 (2008).
  • Nathan C . Points of control in inflammation. Nature420(6917), 846–852 (2002).
  • Freeman BD , NatansonC. Anti-inflammatory therapies in sepsis and septic shock. Expert Opin. Investig. Drugs9(7), 1651–1663 (2000).
  • Eichacker PQ , ParentC, KalilAet al. Risk and the efficacy of antiinflammatory agents. Am. J. Respir. Crit. Care Med.166(9), 1197–1205 (2002).
  • Fink MP . Animal models of sepsis. Virulence5(1), 143–153 (2014).
  • Lewis AJ , SeymourCW, RosengartMR. Current murine models of sepsis. Surg. Infect. (Larchmt).17(4), 385–393 (2016).
  • Ziegler EJ , FisherCJ, SprungCLet al. Treatment of gram-negative bacteremia and septic shock with HA-1A human monoclonal antibody against endotoxin. A randomized, double-blind, placebo-controlled trial. The HA-1A sepsis study group. N. Engl. J. Med.324(7), 429–436 (1991).
  • Tracey KJ , FongY, HesseDGet al. Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteraemia. Nature330(6149), 662–664 (1987).
  • Ali T , KaithaS, MahmoodS, FtesiA, StoneJ, BronzeMS. Clinical use of anti-TNF therapy and increased risk of infections. Drug Healthc. Patient Saf.5, 79–99 (2013).
  • Tracey KJ . The inflammatory reflex. Nature420(6917), 853–859 (2002).
  • Rosas-Ballina M , OlofssonPS, OchaniMet al. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science334(6052), 98–101 (2011).
  • Martelli D , McKinleyMJ, McAllenRM. The cholinergic anti-inflammatory pathway: a critical review. Auton. Neurosci.182, 65–69 (2014).
  • Huston JM , TraceyKJ. The pulse of inflammation: heart rate variability, the cholinergic anti-inflammatory pathway and implications for therapy. J. Intern. Med.269(1), 45–53 (2011).
  • Pavlov VA , TraceyKJ. Neural circuitry and immunity. Immunol. Res.63(1–3), 38–57 (2015).
  • Bratton BO , MartelliD, McKinleyMJ, TrevaksD, AndersonCR, McAllenRM. Neural regulation of inflammation: no neural connection from the vagus to splenic sympathetic neurons. Exp. Physiol.97(11), 1180–1185 (2012).
  • Pavlov VA , ChavanSS, TraceyKJ. Molecular and functional neuroscience in immunity. Annu. Rev. Immunol.36, 783–812 (2018).
  • Asad ZU , StavrakisS. Vagus nerve stimulation for the treatment of heart failure. Bioelectron. Med. (Lond.)2(1), 43–54 (2019).
  • Tran N , AsadZ, ElkholeyK, ScherlagBJ, PoSS, StavrakisS. Autonomic neuromodulation acutely ameliorates left ventricular strain in humans. J. Cardiovasc. Transl. Res.12(3), 221–230 (2019).
  • Stavrakis S , HumphreyMB, ScherlagBJet al. Low-level transcutaneous electrical vagus nerve stimulation suppresses atrial fibrillation. J. Am. Coll. Cardiol.65(9), 867–875 (2015).
  • Work group on major depressive disorder . Practice guideline for the treatment of patients with major depressive disorder. American Psychiatric Association (2010). https://psychiatryonline.org/pb/assets/raw/sitewide/practice_guidelines/guidelines/mdd.pdf
  • American Academy of Neurology. Update: vagus nerve stimulation for the treatment of epilepsy (2020). www.aan.com/Guidelines/home/GuidelineDetail/618
  • Funk DJ , ParrilloJE, KumarA. Sepsis and septic shock: a history. Crit. Care Clin.25(1), 83–101; viii (2009).
  • Angus DC , vander Poll T. Severe sepsis and septic shock. N. Engl. J. Med.369(9), 840–851 (2013).
  • Cerra FB . The systemic septic response: multiple systems organ failure. Crit. Care Clin.1(3), 591–607 (1985).
  • Cinel I , DellingerRP. Advances in pathogenesis and management of sepsis. Curr. Opin. Infect. Dis.20(4), 345–352 (2007).
  • Yang S , WangJ, BrandDD, ZhengSG. Role of TNF–TNF receptor 2 signal in regulatory T cells and its therapeutic implications. Front. Immunol.9 (2018).
  • Beutler B , KrochinN, MilsarkIW, LuedkeC, CeramiA. Control of cachectin (tumor necrosis factor) synthesis: mechanisms of endotoxin resistance. Science232(4753), 977–980 (1986).
  • Tracey KJ , BeutlerB, LowrySFet al. Shock and tissue injury induced by recombinant human cachectin. Science234(4775), 470–474 (1986).
  • Tracey KJ , FongY, HesseDGet al. Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteraemia. Nature330(6149), 662–664 (1987).
  • Knuefermann P , SakataY, BakerJSet al. Toll-like receptor 2 mediates Staphylococcus aureus-induced myocardial dysfunction and cytokine production in the heart. Circulation110(24), 3693–3698 (2004).
  • Suffredini AF , FrommRE, ParkerMMet al. The cardiovascular response of normal humans to the administration of endotoxin. N. Engl. J. Med.321(5), 280–287 (1989).
  • Pinsky MR , VincentJL, DeviereJ, AlegreM, KahnRJ, DupontE. Serum cytokine levels in human septic shock. Relation to multiple-system organ failure and mortality. Chest103(2), 565–575 (1993).
  • Sprung CL , AnnaneD, KehDet al. Hydrocortisone therapy for patients with septic shock. N. Engl. J. Med.358(2), 111–124 (2008).
  • Venkatesh B , FinferS, CohenJet al. Adjunctive glucocorticoid therapy in patients with septic shock. N. Engl. J. Med.378(9), 797–808 (2018).
  • Annane D , RenaultA, Brun-BuissonCet al. Hydrocortisone plus fludrocortisone for adults with septic shock. N. Engl. J. Med.378(9), 809–818 (2018).
  • Beutler B , MilsarkIW, CeramiAC. Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science229(4716), 869–871 (1985).
  • Reinhart K , KarzaiW. Anti-tumor necrosis factor therapy in sepsis: update on clinical trials and lessons learned. Crit. Care Med.29(Suppl. 7), S121–S125 (2001).
  • Opal SM , FisherCJ, DhainautJFet al. Confirmatory interleukin-1 receptor antagonist trial in severe sepsis: a Phase III, randomized, double-blind, placebo-controlled, multicenter trial. The interleukin-1 receptor antagonist sepsis investigator group. Crit. Care Med.25(7), 1115–1124 (1997).
  • Elenkov IJ , WilderRL, ChrousosGP, ViziES. The sympathetic nerve–an integrative interface between two supersystems: the brain and the immune system. Pharmacol. Rev.52(4), 595–638 (2000).
  • Nance DM , SandersVM. Autonomic innervation and regulation of the immune system (1987–2007). Brain Behav. Immun.21(6), 736–745 (2007).
  • Bellinger DL , MillarBA, PerezSet al. Sympathetic modulation of immunity: relevance to disease. Cell. Immunol.252(1–2), 27–56 (2008).
  • Steinman L . Elaborate interactions between the immune and nervous systems. Nat. Immunol.5(6), 575–581 (2004).
  • Swanson MA , LeeWT, SandersVM. IFN-gamma production by Th1 cells generated from naive CD4+ T cells exposed to norepinephrine. J. Immunol.166(1), 232–240 (2001).
  • Kohm AP , SandersVM. Norepinephrine and beta 2-adrenergic receptor stimulation regulate CD4+ T and B lymphocyte function in vitro and in vivo. Pharmacol. Rev.53(4), 487–525 (2001).
  • Harris TJ , WaltmanTJ, CarterSM, MaiselAS. Effect of prolonged catecholamine infusion on immunoregulatory function: implications in congestive heart failure. J. Am. Coll. Cardiol.26(1), 102–109 (1995).
  • Marvar PJ , ThabetSR, GuzikTJet al. Central and peripheral mechanisms of T-lymphocyte activation and vascular inflammation produced by angiotensin II-induced hypertension. Circ. Res.107(2), 263–270 (2010).
  • Wahle M , HanefeldG, BrunnSet al. Failure of catecholamines to shift T-cell cytokine responses toward a Th2 profile in patients with rheumatoid arthritis. Arthritis Res. Ther.8(5), R138 (2006).
  • Firestein GS . Evolving concepts of rheumatoid arthritis. Nature423(6937), 356–361 (2003).
  • Boldt J , MengesT, KuhnD, DiridisC, HempelmannG. Alterations in circulating vasoactive substances in the critically ill–a comparison between survivors and non-survivors. Intensive Care Med.21(3), 218–225 (1995).
  • Ostrowski SR , GaïniS, PedersenC, JohanssonPI. Sympathoadrenal activation and endothelial damage in patients with varying degrees of acute infectious disease: an observational study. J. Crit. Care30(1), 90–96 (2015).
  • Annane D , TraboldF, SharsharTet al. Inappropriate sympathetic activation at onset of septic shock: a spectral analysis approach. Am. J. Respir. Crit. Care Med.160(2), 458–465 (1999).
  • Czura CJ , TraceyKJ. Autonomic neural regulation of immunity. J. Intern. Med.257(2), 156–166 (2005).
  • Huston JM , OchaniM, Rosas-BallinaMet al. Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis. J. Exp. Med.203(7), 1623–1628 (2006).
  • Zhang S , PetroTM. The effect of nicotine on murine CD4 T cell responses. Int. J. Immunopharmacol.18(8–9), 467–478 (1996).
  • Ziemssen T , SiepmannT. The Investigation of the cardiovascular and sudomotor autonomic nervous system’a review. Front. Neurol.10 (2019).
  • Schmidt H , HoyerD, WilhelmJet al. The alteration of autonomic function in multiple organ dysfunction syndrome. Crit. Care Clin.24(1), 149–163 (2008).
  • Schmidt H , Müller-WerdanU, HoffmannTet al. Autonomic dysfunction predicts mortality in patients with multiple organ dysfunction syndrome of different age groups. Crit. Care Med.33(9), 1994–2002 (2005).
  • Bien M-Y , ShuiLin Y, ShihC-Het al. Comparisons of predictive performance of breathing pattern variability measured during T-piece, automatic tube compensation, and pressure support ventilation for weaning intensive care unit patients from mechanical ventilation. Crit. Care Med.39(10), 2253–2262 (2011).
  • Cutsforth-Gregory JK , BenarrochEE. Nucleus of the solitary tract, medullary reflexes, and clinical implications. Neurology88(12), 1187–1196 (2017).
  • Badke CM , MarsillioLE, Weese-MayerDE, Sanchez-PintoLN. Autonomic nervous system dysfunction in pediatric sepsis. Front. Pediatr.6 (2018).
  • Electrophysiology Task Force of the European Society of Cardiology the North American Society of Pacing . Heart rate variability. Circulation93(5), 1043–1065 (1996).
  • de Castilho FM , RibeiroALP, da SilvaJLP, NobreV, de SousaMR. Heart rate variability as predictor of mortality in sepsis: a prospective cohort study. PLoS ONE12(6), e0180060 (2017).
  • Tang CHH , ChanGSH, MiddletonPM, SavkinAV, LovellNH. Spectral analysis of heart period and pulse transit time derived from electrocardiogram and photoplethysmogram in sepsis patients. Annu. Int. Conf. IEEE Eng. Med. Biol. Soc.2009, 1781–1784 (2009).
  • Chen WL , ChenJH, HuangCC, KuoCD, HuangCI, LeeLS. Heart rate variability measures as predictors of in-hospital mortality in ED patients with sepsis. Am. J. Emerg. Med.26(4), 395–401 (2008).
  • Gomez Duque M , EncisoOlivera C, PeñaTorres E, SeguraDurán OD, NietoEstrada VH. [ECAIS study: inadvertent cardiovascular adverse events in sepsis]. Med. Intensiva36(5), 343–350 (2012).
  • Samsudin MI , LiuN, PrabhakarSMet al. A novel heart rate variability based risk prediction model for septic patients presenting to the emergency department. Medicine (Baltimore)97(23), e10866 (2018).
  • Brown SM , TateQ, JonesJPet al. Initial fractal exponent of heart rate variability is associated with success of early resuscitation in patients with severe sepsis or septic shock: a prospective cohort study. J. Crit. Care28(6), 959–963 (2013).
  • Tateishi Y , OdaS, NakamuraMet al. Depressed heart rate variability is associated with high IL-6 blood level and decline in the blood pressure in septic patients. Shock28(5), 549–553 (2007).
  • Pong JZ , Fook-ChongS, KohZXet al. Combining heart rate variability with disease severity score variables for mortality risk stratification in septic patients presenting at the emergency department. Int. J. Environ. Res. Public Health16(10), (2019).
  • Olshansky Brian , SabbahHani N, HauptmanPaul J, ColucciWilson S. Parasympathetic nervous system and heart failure. Circulation118(8), 863–871 (2008).
  • Bratton BO , MartelliD, McKinleyMJ, TrevaksD, AndersonCR, McAllenRM. Neural regulation of inflammation: no neural connection from the vagus to splenic sympathetic neurons. Exp. Physiol.97(11), 1180–1185 (2012).
  • Borovikova LV , IvanovaS, ZhangMet al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature405(6785), 458–462 (2000).
  • Rosas-Ballina M , OchaniM, ParrishWRet al. Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia. Proc. Natl Acad. Sci. USA105(31), 11008–11013 (2008).
  • Vida G , PeñaG, DeitchEA, UlloaL. α7-cholinergic receptor mediates vagal induction of splenic norepinephrine. J. Immunol.186(7), 4340–4346 (2011).
  • Bratton BO , MartelliD, McKinleyMJ, TrevaksD, AndersonCR, McAllenRM. Neural regulation of inflammation: no neural connection from the vagus to splenic sympathetic neurons. Exp. Physiol.97(11), 1180–1185 (2012).
  • Rosas-Ballina M , OchaniM, ParrishWRet al. Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia. Proc. Natl Acad. Sci. USA105(31), 11008–11013 (2008).
  • Wang H , YuM, OchaniMet al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature421(6921), 384–388 (2003).
  • Huston JM , OchaniM, Rosas-BallinaMet al. Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis. J. Exp. Med.203(7), 1623–1628 (2006).
  • Toyabe S , IiaiT, FukudaMet al. Identification of nicotinic acetylcholine receptors on lymphocytes in the periphery as well as thymus in mice. Immunology92(2), 201–205 (1997).
  • Bulloch K , DamavandyT, BadamchianM. Characterization of choline O-acetyltransferase (ChAT) in the BALB/C mouse spleen. Int. J. Neurosci.76(1–2), 141–149 (1994).
  • Kwan H , GarzoniL, LiuHLet al. Vagus nerve stimulation for treatment of inflammation: systematic review of animal models and clinical studies. Bioelectron. Med.3, 1–6 (2016).
  • Kessler W , DiedrichS, MengesPet al. The role of the vagus nerve: modulation of the inflammatory reaction in murine polymicrobial sepsis 2012. 467620 (2012).
  • Borovikova LV , IvanovaS, ZhangMet al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature405(6785), 458–462 (2000).
  • Huston JM , Gallowitsch-PuertaM, OchaniMet al. Transcutaneous vagus nerve stimulation reduces serum high mobility group box 1 levels and improves survival in murine sepsis. Crit. Care Med.35(12), 2762–2768 (2007).
  • Koopman FA , ChavanSS, MiljkoSet al. Vagus nerve stimulation inhibits cytokine production and attenuates disease severity in rheumatoid arthritis. Proc. Natl Acad. Sci. USA113(29), 8284–8289 (2016).
  • Kox M , van EijkLT, VerhaakTet al. Transvenous vagus nerve stimulation does not modulate the innate immune response during experimental human endotoxemia: a randomized controlled study. Arthritis Res. Ther.17, 150 (2015).
  • Stavrakis S , StonerJA, HumphreyMBet al. TREAT AF (transcutaneous electrical vagus nerve stimulation to suppress atrial fibrillation): a randomized clinical trial. JACC Clin. Electophysiol.6(3), 282–291 (2020).
  • Youness H Neuromodulation to regulate inflammation and autonomic imbalance in sepsis (NERINA-SEPSIS), (NCT03992378) (2020). https://clinicaltrials.gov/ct2/show/NCT03992378
  • Staats P , GiannakopoulosG, BlakeJ, LieblerE, LevyRM. The use of non-invasive vagus nerve stimulation to treat respiratory symptoms associated with COVID-19: a theoretical hypothesis and early clinical experience. Neuromodulation23(6), 784–788 (2020).
  • Tarn J , LeggS, MitchellS, SimonB, NgW-F. The Effects of noninvasive vagus nerve stimulation on fatigue and immune responses in patients with primary Sjögren's syndrome. Neuromodulation22(5), 580–585 (2019).
  • Cheema T . Study assessing vagus nerve stimulation in CoViD-19 respiratory symptoms (SAVIORII), (NCT04382391) (2020). https://clinicaltrials.gov/ct2/show/NCT04382391
  • Tornero C, Study assessing vagus nerve stimulation in CoViD-19 respiratory symptoms (SAVIOR), (NCT04368156) (2020). https://clinicaltrials.gov/ct2/show/NCT04368156
  • Nemecheck Technologies Vagus nerve stimulation ARDS prevention trial for COVID-19 hospitalized patients, (NCT04379037) (2020). https://clinicaltrials.gov/ct2/show/NCT04379037
  • Fondation Ophtalmologique Adolphe de Rothschild Impact of auricular vagus nerve neuromodulation on COVID-19 positive inpatients outcome (SOS-COVID19), (NCT04341415) (2020). https://clinicaltrials.gov/ct2/show/NCT04341415

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.