243
Views
5
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Electroacupuncture at ST36 (Zusanli) Prevents T-Cell Lymphopenia and Improves Survival in Septic Mice

ORCID Icon, , , ORCID Icon, , ORCID Icon, ORCID Icon, & ORCID Icon show all
Pages 2819-2833 | Published online: 03 May 2022

References

  • Singer M, Deutschman CS, Seymour CW, et al. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA. 2016;315(8):801–810. doi:10.1001/jama.2016.0287
  • Marik PE. Early management of severe sepsis: concepts and controversies. Chest. 2014;145(6):1407–1418. doi:10.1378/chest.13-2104
  • Rudd KE, Johnson SC, Agesa KM, et al. Global, regional, and national sepsis incidence and mortality, 1990–2017: analysis for the Global Burden of Disease Study. Lancet. 2020;395(10219):200–211. doi:10.1016/S0140-6736(19)32989-7
  • Zhou F, Yu T, Du R, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020;395(10229):1054–1062. doi:10.1016/S0140-6736(20)30566-3
  • Fudim M, Qadri YJ, Ghadimi K, et al. Implications for neuromodulation therapy to control inflammation and related organ dysfunction in COVID-19. J Cardiovasc Transl Res. 2020;13(6):894–899. doi:10.1007/s12265-020-10031-6
  • Stevenson EK, Rubenstein AR, Radin GT, Wiener RS, Walkey AJ. Two decades of mortality trends among patients with severe sepsis: a comparative meta-analysis. Crit Care Med. 2014;42(3):625–631. doi:10.1097/CCM.0000000000000026
  • Kim JS, Kim SJ, Lee SM. Genipin attenuates sepsis-induced immunosuppression through inhibition of T lymphocyte apoptosis. Int Immunopharmacol. 2015;27(1):15–23. doi:10.1016/j.intimp.2015.04.034
  • Fathi N, Rezaei N. Lymphopenia in COVID-19: therapeutic opportunities. Cell Biol Int. 2020;44(9):1792–1797. doi:10.1002/cbin.11403
  • Tang Y, Liu J, Zhang D, Xu Z, Ji J, Wen C. Cytokine storm in COVID-19: the current evidence and treatment strategies. Front Immunol. 2020;11:1708. doi:10.3389/fimmu.2020.01708
  • Pena G, Cai B, Ramos L, Vida G, Deitch EA, Ulloa L. Cholinergic regulatory lymphocytes re-establish neuromodulation of innate immune responses in sepsis. J Immunol. 2011;187(2):718–725. doi:10.4049/jimmunol.1100013
  • Vida G, Pena G, Kanashiro A, et al. beta2-Adrenoreceptors of regulatory lymphocytes are essential for vagal neuromodulation of the innate immune system. FASEB J. 2011;25(12):4476–4485. doi:10.1096/fj.11-191007
  • Gyawali B, Ramakrishna K, Dhamoon AS. Sepsis: the evolution in definition, pathophysiology, and management. SAGE Open Med. 2019;7:2050312119835043. doi:10.1177/2050312119835043
  • Kashiouris MG, L’Heureux M, Cable CA, Fisher BJ, Leichtle SW, Fowler AA. The emerging role of vitamin C as a treatment for sepsis. Nutrients. 2020;12(2):292. doi:10.3390/nu12020292
  • Cohen J. The immunopathogenesis of sepsis. Nature. 2002;420(6917):885–891. doi:10.1038/nature01326
  • Ulloa L, Tracey KJ. The “cytokine profile”: a code for sepsis. Trends Mol Med. 2005;11(2):56–63. doi:10.1016/j.molmed.2004.12.007
  • Marshall JC. Why have clinical trials in sepsis failed? Trends Mol Med. 2014;20(4):195–203. doi:10.1016/j.molmed.2014.01.007
  • Hassan N, Slight R, Weiand D, et al. Preventing sepsis; how can artificial intelligence inform the clinical decision-making process? A systematic review. Int J Med Inform. 2021;150:104457. doi:10.1016/j.ijmedinf.2021.104457
  • Evans L, Rhodes A, Alhazzani W, et al. Surviving sepsis campaign: international guidelines for management of sepsis and septic shock 2021. Intensive Care Med. 2021;47(11):1181–1247. doi:10.1007/s00134-021-06506-y
  • Ma XY, Tian LX, Liang HP. Early prevention of trauma-related infection/sepsis. Mil Med Res. 2016;3:33. doi:10.1186/s40779-016-0104-3
  • Joseph B, Shimojo G, Li Z, et al. Glucose activates vagal control of hyperglycemia and inflammation in fasted mice. Sci Rep. 2019;9(1):1012. doi:10.1038/s41598-018-36298-z
  • Ulloa L. Electroacupuncture activates neurons to switch off inflammation. Nature. 2021;598(7882):573–574. doi:10.1038/d41586-021-02714-0
  • Matsumoto-Miyazaki J, Ushikoshi H, Miyata S, et al. Acupuncture and traditional herbal medicine therapy prevent delirium in patients with cardiovascular disease in intensive care units. Am J Chin Med. 2017;45(2):255–268. doi:10.1142/S0192415X17500161
  • Lv JQ, Li PC, Zhou L, Tang WF, Li N. Acupuncture at the P6 acupoint to prevent postoperative pain after craniotomy: a randomized, placebo-controlled study. Evid Based Complement Alternat Med. 2021;2021:6619855. doi:10.1155/2021/6619855
  • Zhu MF, Xing X, Lei S, et al. Electroacupuncture at bilateral zusanli points (ST36) protects intestinal mucosal immune barrier in sepsis. Evid Based Complement Alternat Med. 2015;2015:639412. doi:10.1155/2015/639412
  • Meng JB, Jiao YN, Zhang G, et al. Electroacupuncture improves intestinal dysfunction in septic patients: a randomised controlled trial. Biomed Res Int. 2018;2018:8293594. doi:10.1155/2018/8293594
  • 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
  • Torres-Rosas R, Yehia G, Pena G, et al. Dopamine mediates vagal modulation of the immune system by electroacupuncture. Nat Med. 2014;20(3):291–295. doi:10.1038/nm.3479
  • Dang CP, Leelahavanichkul A. Over-expression of miR-223 induces M2 macrophage through glycolysis alteration and attenuates LPS-induced sepsis mouse model, the cell-based therapy in sepsis. PLoS One. 2020;15(7):e0236038. doi:10.1371/journal.pone.0236038
  • Lai F, Ren Y, Lai C, et al. Acupuncture at Zusanli (ST36) for experimental sepsis: a systematic review. Evid Based Complement Alternat Med. 2020;2020:3620741. doi:10.1155/2020/3620741
  • Kadl A, Pontiller J, Exner M, Leitinger N. Single bolus injection of bilirubin improves the clinical outcome in a mouse model of endotoxemia. Shock. 2007;28(5):582–588. doi:10.1097/shk.0b013e31804d41dd
  • Su X, Wang L, Song Y, Bai C. Inhibition of inflammatory responses by ambroxol, a mucolytic agent, in a murine model of acute lung injury induced by lipopolysaccharide. Intensive Care Med. 2004;30(1):133–140. doi:10.1007/s00134-003-2001-y
  • Coimbra R, Porcides R, Loomis W, et al. HSPTX protects against hemorrhagic shock resuscitation-induced tissue injury: an attractive alternative to ringer’s lactate. J Trauma. 2006;60(1):41–51. doi:10.1097/01.ta.0000197417.03460.0a
  • Cai G, Sun K, Wang T, et al. Mechanism and effects of zearalenone on mouse T lymphocytes activation in vitro. Ecotoxicol Environ Saf. 2018;162:208–217. doi:10.1016/j.ecoenv.2018.06.055
  • Pan WX, Fan AY, Chen S, Alemi SF. Acupuncture modulates immunity in sepsis: toward a science-based protocol. Auton Neurosci. 2021;232:102793. doi:10.1016/j.autneu.2021.102793
  • Chavan SS, Tracey KJ. Regulating innate immunity with dopamine and electroacupuncture. Nat Med. 2014;20(3):239–241. doi:10.1038/nm.3501
  • Kushimoto S, Gando S, Ogura H, et al. Complementary role of hypothermia identification to the quick sequential organ failure assessment score in predicting patients with sepsis at high risk of mortality: a retrospective analysis from a multicenter, observational study. J Intensive Care Med. 2020;35(5):502–510. doi:10.1177/0885066618761637
  • Shimazui T, Nakada TA, Walley KR, et al. Significance of body temperature in elderly patients with sepsis. Crit Care. 2020;24(1):387. doi:10.1186/s13054-020-02976-6
  • Ramgopal S, Horvat CM, Adler MD. Association of triage hypothermia with in-hospital mortality among patients in the emergency department with suspected sepsis. J Crit Care. 2020;60:27–31. doi:10.1016/j.jcrc.2020.07.011
  • Kushimoto S, Gando S, Saitoh D, et al. The impact of body temperature abnormalities on the disease severity and outcome in patients with severe sepsis: an analysis from a multicenter, prospective survey of severe sepsis. Crit Care. 2013;17(6):R271. doi:10.1186/cc13106
  • Remick DG, Xioa H. Hypothermia and sepsis. Front Biosci. 2006;11:1006–1013. doi:10.2741/1858
  • Arons MM, Wheeler AP, Bernard GR, et al. Effects of ibuprofen on the physiology and survival of hypothermic sepsis. Ibuprofen in Sepsis Study Group. Crit Care Med. 1999;27(4):699–707. doi:10.1097/00003246-199904000-00020
  • Drewry AM, Fuller BM, Skrupky LP, Hotchkiss RS. The presence of hypothermia within 24 hours of sepsis diagnosis predicts persistent lymphopenia. Crit Care Med. 2015;43(6):1165–1169. doi:10.1097/CCM.0000000000000940
  • Huang CL, Tsai PS, Wang TY, Yan LP, Xu HZ, Huang CJ. Acupuncture stimulation of ST36 (Zusanli) attenuates acute renal but not hepatic injury in lipopolysaccharide-stimulated rats. Anesth Analg. 2007;104(3):646–654. doi:10.1213/01.ane.0000255288.68199.eb
  • Huang CL, Huang CJ, Tsai PS, Yan LP, Xu HZ. Acupuncture stimulation of ST-36 (Zusanli) significantly mitigates acute lung injury in lipopolysaccharide-stimulated rats. Acta Anaesthesiol Scand. 2006;50(6):722–730. doi:10.1111/j.1399-6576.2006.01029.x
  • Yu JB, Shi J, Gong LR, et al. Role of Nrf2/ARE pathway in protective effect of electroacupuncture against endotoxic shock-induced acute lung injury in rabbits. PLoS One. 2014;9(8):e104924. doi:10.1371/journal.pone.0104924
  • Zhang Z, Shi Y, Cai D, et al. Effect of electroacupuncture at ST36 on the intestinal mucosal mechanical barrier and expression of occludin in a rat model of sepsis. Acupunct Med. 2018;36(5):333–338. doi:10.1136/acupmed-2016-011187
  • MacFie J, O’Boyle C, Mitchell CJ, Buckley PM, Johnstone D, Sudworth P. Gut origin of sepsis: a prospective study investigating associations between bacterial translocation, gastric microflora, and septic morbidity. Gut. 1999;45(2):223–228. doi:10.1136/gut.45.2.223
  • Hu S, Du MH, Luo HM, et al. Electroacupuncture at Zusanli (ST36) prevents intestinal barrier and remote organ dysfunction following gut ischemia through activating the cholinergic anti-inflammatory-dependent mechanism. Evid Based Complement Alternat Med. 2013;2013:592127. doi:10.1155/2013/592127
  • Ulloa L. The vagus nerve and the nicotinic anti-inflammatory pathway. Nat Rev Drug Discov. 2005;4(8):673–684. doi:10.1038/nrd1797
  • Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506. doi:10.1016/S0140-6736(20)30183-5
  • Gholami M, Safari S, Ulloa L, Motaghinejad M. Neuropathies and neurological dysfunction induced by coronaviruses. J Neurovirol. 2021;27(3):380–396. doi:10.1007/s13365-021-00977-x
  • Guo XJ, Thomas PG. New fronts emerge in the influenza cytokine storm. Semin Immunopathol. 2017;39(5):541–550. doi:10.1007/s00281-017-0636-y
  • Georgescu AM, Banescu C, Azamfirei R, et al. Evaluation of TNF-alpha genetic polymorphisms as predictors for sepsis susceptibility and progression. BMC Infect Dis. 2020;20(1):221. doi:10.1186/s12879-020-4910-6
  • Parameswaran N, Patial S. Tumor necrosis factor-alpha signaling in macrophages. Crit Rev Eukaryot Gene Expr. 2010;20(2):87–103. doi:10.1615/CritRevEukarGeneExpr.v20.i2.10
  • Steeland S, Libert C, Vandenbroucke RE. A new venue of TNF targeting. Int J Mol Sci. 2018;19(5):1442. doi:10.3390/ijms19051442
  • Busch K, Kny M, Huang N, et al. Inhibition of the NLRP3/IL-1beta axis protects against sepsis-induced cardiomyopathy. J Cachexia Sarcopenia Muscle. 2021;12(6):1653–1668. doi:10.1002/jcsm.12763
  • Xiong S, Hong Z, Huang LS, et al. IL-1beta suppression of VE-cadherin transcription underlies sepsis-induced inflammatory lung injury. J Clin Invest. 2020;130(7):3684–3698. doi:10.1172/JCI136908
  • Huang L, Zhao X, Qi Y, et al. Sepsis-associated severe interleukin-6 storm in critical coronavirus disease 2019. Cell Mol Immunol. 2020;17(10):1092–1094. doi:10.1038/s41423-020-00522-6
  • Song J, Park DW, Moon S, et al. Diagnostic and prognostic value of interleukin-6, pentraxin 3, and procalcitonin levels among sepsis and septic shock patients: a prospective controlled study according to the Sepsis-3 definitions. BMC Infect Dis. 2019;19(1):968. doi:10.1186/s12879-019-4618-7
  • Chang X, Hu LF, Ma XJ, Yin J, Liu XY, Li JB. Influence of roflumilast on sepsis mice through the JAK/STAT signaling pathway. Eur Rev Med Pharmacol Sci. 2019;23(3):1335–1341. doi:10.26355/eurrev_201902_17028
  • Hojyo S, Uchida M, Tanaka K, et al. How COVID-19 induces cytokine storm with high mortality. Inflamm Regen. 2020;40:37. doi:10.1186/s41232-020-00146-3
  • Moore JB, June CH. Cytokine release syndrome in severe COVID-19. Science. 2020;368(6490):473–474. doi:10.1126/science.abb8925
  • Tanaka T, Narazaki M, Kishimoto T. Immunotherapeutic implications of IL-6 blockade for cytokine storm. Immunotherapy. 2016;8(8):959–970. doi:10.2217/imt-2016-0020
  • Guo HL, Shi FD, Zhou Q, et al. Interleukin-1beta protection against experimental sepsis in mice. Inflammation. 2021;44(1):358–370. doi:10.1007/s10753-020-01341-7
  • Pinheiro da silva F, Nizet V. Cell death during sepsis: integration of disintegration in the inflammatory response to overwhelming infection. Apoptosis. 2009;14(4):509–521. doi:10.1007/s10495-009-0320-3
  • Brady J, Horie S, Laffey JG. Role of the adaptive immune response in sepsis. Intensive Care Med Exp. 2020;8(Suppl 1):20. doi:10.1186/s40635-020-00309-z
  • Zou Q, Yang M, Yu M, Liu C. Influences of regulation of miR-126 on inflammation, Th17/Treg subpopulation differentiation, and lymphocyte apoptosis through caspase signaling pathway in sepsis. Inflammation. 2020;43(6):2287–2300. doi:10.1007/s10753-020-01298-7
  • Wang H, Liao H, Ochani M, et al. Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat Med. 2004;10(11):1216–1221. doi:10.1038/nm1124
  • Kanashiro A, Franchin M, Bassi GS, et al. Inhibition of spinal p38 MAPK prevents articular neutrophil infiltration in experimental arthritis via sympathetic activation. Fundam Clin Pharmacol. 2018;32(2):155–162. doi:10.1111/fcp.12338
  • Chu CM, Chiu LC, Yu CC, et al. Increased death of peripheral blood mononuclear cells after TLR4 inhibition in sepsis is not via TNF/TNF receptor-mediated apoptotic pathway. Mediators Inflamm. 2021;2021:2255017. doi:10.1155/2021/2255017
  • Kothari N, Bogra J, Abbas H, et al. Tumor necrosis factor gene polymorphism results in high TNF level in sepsis and septic shock. Cytokine. 2013;61(2):676–681. doi:10.1016/j.cyto.2012.11.016
  • Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol. 2009;7(2):99–109. doi:10.1038/nrmicro2070
  • Zheng X, Chen W, Gong F, Chen Y, Chen E. The role and mechanism of pyroptosis and potential therapeutic targets in sepsis: a review. Front Immunol. 2021;12:711939. doi:10.3389/fimmu.2021.711939
  • Zhuo L, Chen X, Sun Y, et al. Rapamycin inhibited pyroptosis and reduced the release of IL-1beta and IL-18 in the septic response. Biomed Res Int. 2020;2020:5960375. doi:10.1155/2020/5960375
  • Ulloa L, Quiroz-Gonzalez S, Torres-Rosas R. Nerve stimulation: immunomodulation and control of inflammation. Trends Mol Med. 2017;23(12):1103–1120. doi:10.1016/j.molmed.2017.10.006
  • Bassi GS, Kanashiro A, Coimbra NC, Terrando N, Maixner W, Ulloa L. Anatomical and clinical implications of vagal modulation of the spleen. Neurosci Biobehav Rev. 2020;112:363–373. doi:10.1016/j.neubiorev.2020.02.011