Electroacupuncture treatment partly promotes the recovery time of postoperative ileus by activating the vagus nerve but not regulating local inflammation

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Fang, Jun Fan ^a   Fang, Jian Qiao ^a   Shao, Xiao Mei ^a   Du, Jun Ying ^a   Liang, Yi ^a   Wang, Wen ^a   Liu, Zhe ^a  

^a ZHEJIANG CHINESE MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ATROPINE; INTERLEUKIN 1BETA; PROTEIN C FOS; TUMOR NECROSIS FACTOR;

ABDOMEN; ANIMAL; CYTOLOGY; DRUG EFFECT; ELECTROACUPUNCTURE; ELECTRODE IMPLANT; GASTROINTESTINAL TRANSIT; GENETICS; ILEUS; IMMUNOLOGY; INFLAMMATION; LEUKOCYTE; METABOLISM; PATHOLOGY; PHYSIOLOGY; POSTOPERATIVE COMPLICATION; RAT; SMALL INTESTINE; SOLITARY TRACT NUCLEUS; STOMACH EMPTYING; SURGERY; VAGUS NERVE;

ABDOMEN; ANIMALS; ATROPINE; ELECTROACUPUNCTURE; ELECTRODES, IMPLANTED; GASTRIC EMPTYING; GASTROINTESTINAL TRANSIT; ILEUS; INFLAMMATION; INTERLEUKIN-1BETA; INTESTINE, SMALL; LEUKOCYTES; POSTOPERATIVE COMPLICATIONS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; SOLITARY NUCLEUS; TUMOR NECROSIS FACTOR-ALPHA; VAGUS NERVE;

EID: 85008319893     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep39801     Document Type: Article

References (58)

1. Boeckxstaens, G. E. & de Jonge, W. J. Neuroimmune mechanisms in postoperative ileus. Gut 58, 1300-1311, doi: 10.1136/gut.2008.169250 (2009).
2. Mattei, P. & Rombeau, J. L. Review of the pathophysiology and management of postoperative ileus. World J Surg 30, 1382-1391, doi: 10.1007/s00268-005-0613-9 (2006).
3. Kalff, J. C., Schraut, W. H., Simmons, R. L. & Bauer, A. J. Surgical manipulation of the gut elicits an intestinal muscularis inflammatory response resulting in postsurgical ileus. Ann Surg 228, 652-663 (1998).
4. Kalff, J. C., Schraut, W. H., Billiar, T. R., Simmons, R. L. & Bauer, A. J. Role of inducible nitric oxide synthase in postoperative intestinal smooth muscle dysfunction in rodents. Gastroenterology 118, 316-327 (2000).
5. de Jonge, W. J. et al. Postoperative ileus is maintained by intestinal immune infiltrates that activate inhibitory neural pathways in mice. Gastroenterology 125, 1137-1147 (2003).
6. Kreiss, C., Birder, L. A., Kiss, S., VanBibber, M. M. & Bauer, A. J. COX-2 dependent inflammation increases spinal Fos expression during rodent postoperative ileus. Gut 52, 527-534 (2003).
7. Chang, J. et al. Iatrogenic extracellular matrix disruption as a local trigger for postoperative ileus. J Surg Res 178, 632-639, doi: 10.1016/j.jss.2012.05.044 (2012).
8. Turler, A. et al. Leukocyte-derived inducible nitric oxide synthase mediates murine postoperative ileus. Ann Surg 244, 220-229, doi: 10.1097/01.sla.0000229963.37544.59 (2006).
9. Zittel, T. T., Reddy, S. N., Plourde, V. & Raybould, H. E. Role of spinal afferents and calcitonin gene-related peptide in the postoperative gastric ileus in anesthetized rats. Ann Surg 219, 79-87 (1994).
10. De Winter, B. Y. et al. Involvement of afferent neurons in the pathogenesis of endotoxin-induced ileus in mice: role of CGRP and TRPV1 receptors. Eur J Pharmacol 615, 177-184, doi: 10.1016/j.ejphar.2009.04.055 (2009).
11. Rychter, J. & Clave, P. Intestinal inflammation in postoperative ileus: pathogenesis and therapeutic targets. Gut 62, 1534-1535, doi: 10.1136/gutjnl-2012-304176 (2013).
12. Gao, Z. et al. Role of the vagus nerve on the development of postoperative ileus. Langenbecks Arch Surg 395, 407-411, doi: 10.1007/s00423-010-0594-5 (2010).
13. Lubbers, T., Buurman, W. & Luyer, M. Controlling postoperative ileus by vagal activation. World J Gastroenterol 16, 1683-1687 (2010).
14. Bonaz, B., Picq, C., Sinniger, V., Mayol, J. F. & Clarencon, D. Vagus nerve stimulation: from epilepsy to the cholinergic antiinflammatory pathway. Neurogastroenterol Motil 25, 208-221, doi: 10.1111/nmo.12076 (2013).
15. The, F. et al. Central activation of the cholinergic anti-inflammatory pathway reduces surgical inflammation in experimental postoperative ileus. Br J Pharmacol 163, 1007-1016, doi: 10.1111/j.1476-5381.2011.01296.x (2011).
16. Wang, K. et al. Ameliorating effect of transcutaneous electroacupuncture on impaired gastric accommodation induced by cold meal in healthy subjects. Evid Based Complement Alternat Med. 31, 561-566, doi: 10.1155/2016/345702510.1111/jgh.13168 (2016).
17. Pang, T. & Lu, C. Electroacupuncture at ST25 Inhibits Cisapride-Induced Gastric Motility in an Intensity-Dependent Manner. 2016, 3457025, doi: 10.1155/2016/3457025 (2016).
18. Zhang, C. X. & Guo, L. K. Dalitong granule combined with electroacupuncture in the treatment of functional dyspepsia: A randomized controlled trial. Chinese journal of integrative medicine 21, 743-750, doi: 10.1111/jgh.1316810.1007/s11655-015-2175- 5 (2015).
19. Jin, H., Liu, J., Foreman, R. D., Chen, J. D. & Yin, J. Electrical neuromodulation at acupoint ST36 normalizes impaired colonic motility induced by rectal distension in dogs. Am J Physiol Gastrointest Liver Physiol 309, G368-376, doi: 10.1152/ajpgi.00467.2014 (2015).
20. Ng, S. S. et al. Electroacupuncture reduces duration of postoperative ileus after laparoscopic surgery for colorectal cancer. Gastroenterology 144, 307-313 e301, doi: 10.1053/j.gastro.2012.10.050 (2013).
21. Li, Y. Q., Zhu, B., Rong, P. J., Ben, H. & Li, Y. H. Neural mechanism of acupuncture-modulated gastric motility. World J Gastroenterol 13, 709-716 (2007).
22. Luckey, A., Livingston, E. & Tache, Y. Mechanisms and treatment of postoperative ileus. Arch Surg 138, 206-214 (2003).
23. Iyer, S., Saunders, W. B. & Stemkowski, S. Economic burden of postoperative ileus associated with colectomy in the United States. Journal of managed care pharmacy: JMCP 15, 485-494 (2009).
24. Asgeirsson, T. et al. Postoperative ileus: it costs more than you expect. Journal of the American College of Surgeons 210, 228-231, doi: 10.1016/j.jamcollsurg.2009.09.028 (2010).
25. Wang, H., Shen, G. M., Liu, W. J., Huang, S. & Zhang, M. T. The Neural Mechanism by Which the Dorsal Vagal Complex Mediates the Regulation of the Gastric Motility by Weishu (RN12) and Zhongwan (BL21) Stimulation. Evid Based Complement Alternat Med 2013, 291764, doi: 10.1155/2013/291764 (2013).
26. Wehner, S., Vilz, T. O., Stoffels, B. & Kalff, J. C. Immune mediators of postoperative ileus. Langenbecks Arch Surg 397, 591-601, doi: 10.1007/s00423-012-0915-y (2012).
27. De Winter, B. Y. et al. Effect of adrenergic and nitrergic blockade on experimental ileus in rats. Br J Pharmacol 120, 464-468, doi: 10.1038/sj.bjp.0700913 (1997).
28. Kehlet, H. & Dahl, J. B. Anaesthesia, surgery, and challenges in postoperative recovery. Lancet (London, England) 362, 1921-1928, doi: 10.1016/s0140-6736(03)14966-5 (2003).
29. Taguchi, A. et al. Selective postoperative inhibition of gastrointestinal opioid receptors. The New England journal of medicine 345, 935-940, doi: 10.1056/NEJMoa010564 (2001).
30. Kehlet, H. Postoperative ileus-an update on preventive techniques. Nature clinical practice. Gastroenterology & hepatology 5, 552-558, doi: 10.1038/ncpgasthep1230 (2008).
31. van Bree, S. H. et al. Systemic inflammation with enhanced brain activation contributes to more severe delay in postoperative ileus. Neurogastroenterol Motil 25, e540-549, doi: 10.1111/nmo.12157 (2013).
32. Kalff, J. C. et al. Biphasic response to gut manipulation and temporal correlation of cellular infiltrates and muscle dysfunction in rat. Surgery 126, 498-509 (1999).
33. Kalff, J. C. et al. Surgically induced leukocytic infiltrates within the rat intestinal muscularis mediate postoperative ileus. Gastroenterology 117, 378-387 (1999).
34. Novitsky, Y. W., Litwin, D. E. & Callery, M. P. The net immunologic advantage of laparoscopic surgery. Surg Endosc 18, 1411-1419, doi: 10.1007/s00464-003-8275-x (2004).
35. The, F. O. et al. Intestinal handling-induced mast cell activation and inflammation in human postoperative ileus. Gut 57, 33-40, doi: 10.1136/gut.2007.120238 (2008).
36. de Jonge, W. J. et al. Mast cell degranulation during abdominal surgery initiates postoperative ileus in mice. Gastroenterology 127, 535-545 (2004).
37. Engel, D. R. et al. T helper type 1 memory cells disseminate postoperative ileus over the entire intestinal tract. Nat Med 16, 1407-1413, doi: 10.1038/nm.2255 (2010).
38. Schmidt, J. et al. Proinflammatory role of leukocyte-derived Egr-1 in the development of murine postoperative ileus. Gastroenterology 135, 926-936, 936 e921-922, doi: 10.1053/j.gastro.2008.05.079 (2008).
39. Boeckxstaens, G. E. et al. Activation of an adrenergic and vagally-mediated NANC pathway in surgery-induced fundic relaxation in the rat. Neurogastroenterol Motil 11, 467-474 (1999).
40. Schwarz, N. T. et al. Prostanoid production via COX-2 as a causative mechanism of rodent postoperative ileus. Gastroenterology 121, 1354-1371 (2001).
41. Pantelis, D. et al. Transient perioperative pharmacologic inhibition of muscularis macrophages as a target for prophylaxis of postoperative ileus does not affect anastomotic healing in mice. Surgery 148, 59-70, doi: 10.1016/j.surg.2009.12.010 (2010).
42. Borovikova, L. V. et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405, 458-462, doi: 10.1038/35013070 (2000).
43. Kox, M. & Pickkers, P. Modulation of the Innate Immune Response through the Vagus Nerve. Nephron 131, 79-84, doi: 10.1159/000435843 (2015).
44. Zabrodskii, P. F., Gromov, M. S. & Maslyakov, V. V. Effect of alpha7n-Acetylcholine Receptor Activation and Antibodies to TNFalpha on Mortality of Mice and Concentration of Proinflammatory Cytokines During Early Stage of Sepsis. Bull Exp Biol Med 159, 740-742, doi: 10.1007/s10517-015-3063-x (2015).
45. Wang, H. et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421, 384-388, doi: 10.1038/nature01339 (2003).
46. Amaral, F. A. et al. Endogenous acetylcholine controls the severity of polymicrobial sepsis-associated inflammatory response in mice. Current neurovascular research (2015).
47. Minutoli, L. et al. Melanocortin 4 receptor stimulation decreases pancreatitis severity in rats by activation of the cholinergic antiinflammatory pathway. Crit Care Med 39, 1089-1096, doi: 10.1097/CCM.0b013e318207ea80 (2011).
48. Munyaka, P. et al. Central muscarinic cholinergic activation alters interaction between splenic dendritic cell and CD4+ CD25- T cells in experimental colitis. PLoS One 9, e109272, doi: 10.1371/journal.pone.0109272 (2014).
49. Wu, Z., Boersema, G. S., Jeekel, J. & Lange, J. F. Nicotine gum chewing: a novel strategy to shorten duration of postoperative ileus via vagus nerve activation. Medical hypotheses 83, 352-354, doi: 10.1016/j.mehy.2014.06.011 (2014).
50. Matteoli, G. et al. A distinct vagal anti-inflammatory pathway modulates intestinal muscularis resident macrophages independent of the spleen. Gut 63, 938-948, doi: 10.1136/gutjnl-2013-304676 (2014).
51. Van Der Zanden, E. P., Boeckxstaens, G. E. & de Jonge, W. J. The vagus nerve as a modulator of intestinal inflammation. Neurogastroenterol Motil 21, 6-17, doi: 10.1111/j.1365-2982.2008.01252.x (2009).
52. Wang, H. et al. Electroacupuncture at Zusanli Prevents Severe Scalds-Induced Gut Ischemia and Paralysis by Activating the Cholinergic Pathway. Evid Based Complement Alternat Med 2015, 787393, doi: 10.1155/2015/787393 (2015).
53. Villegas-Bastida, A. et al. Electrical Stimulation at the ST36 Acupoint Protects against Sepsis Lethality and Reduces Serum TNF Levels through Vagus Nerve- and Catecholamine-Dependent Mechanisms. Evid Based Complement Alternat Med 2014, 451674, doi: 10.1155/2014/451674 (2014).
54. Ng, S. S. et al. Electroacupuncture reduces duration of postoperative ileus after laparoscopic surgery for colorectal cancer. Gastroenterology 144, 307-313.e301, doi: 10.1053/j.gastro.2012.10.050 (2013).
55. Tracey, K. J. The inflammatory reflex. Nature 420, 853-859, doi: 10.1038/nature01321 (2002).
56. de Jonge, W. J. et al. Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signaling pathway. Nat Immunol 6, 844-851, doi: 10.1038/ni1229 (2005).
57. Peters, J. H., McDougall, S. J., Mendelowitz, D., Koop, D. R. & Andresen, M. C. Isoflurane differentially modulates inhibitory and excitatory synaptic transmission to the solitary tract nucleus. Anesthesiology 108, 675-683, doi: 10.1097/ALN.0b013e318167af9a (2008).
58. van Bree, S. H. et al. New therapeutic strategies for postoperative ileus. Nat Rev Gastroenterol Hepatol 9, 675-683, doi: 10.1038/nrgastro.2012.134 (2012).