Vagal nerve stimulation started just prior to reperfusion limits infarct size and no-reflow

Basic Research in Cardiology

Volumn 110, Issue 5, 2015, Pages

  Uitterdijk, André ^a   Yetgin, Tuncay ^a   te Lintel Hekkert, Maaike ^a   Sneep, Stefan ^a   Krabbendam Peters, Ilona ^a   van Beusekom, Heleen M M ^a   Fischer, Trent M ^b   Cornelussen, Richard N ^c   Manintveld, Olivier C ^a   Merkus, Daphne ^a   Duncker, Dirk J ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b Medtronic Research and Technology ^*  (United States)

^c MEDTRONIC BAKKEN RESEARCH CENTER   (Netherlands)

Author keywords

Cardioprotection; Macrophages; Myocardial infarction; Neutrophils; Reperfusion injury; Swine

Indexed keywords

INTERLEUKIN 6; NITRIC OXIDE SYNTHASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRADYCARDIA; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY OCCLUSION; FEMALE; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE PRESSURE; HEART MUSCLE METABOLISM; HEART MUSCLE OXYGEN CONSUMPTION; HEART MUSCLE REPERFUSION; HEART PROTECTION; HEART RATE; INFLAMMATION; LANDRACE PIG; LEFT ANTERIOR DESCENDING CORONARY ARTERY; LEUKOCYTE MIGRATION; MACROPHAGE; MALE; NEUTROPHIL COUNT; NO REFLOW PHENOMENON; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; THERAPY EFFECT; VAGUS NERVE STIMULATION; YORKSHIRE PIG; ANIMAL; DISEASE MODEL; MYOCARDIAL REPERFUSION INJURY; PATHOPHYSIOLOGY; PIG; PROCEDURES;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; MALE; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; SUS SCROFA; VAGUS NERVE STIMULATION;

EID: 84940421915     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-015-0508-3     Document Type: Article

References (54)

1. Bonaz B, Picq C, Sinniger V, Mayol JF, Clarencon D (2013) Vagus nerve stimulation: from epilepsy to the cholinergic anti-inflammatory pathway. Neurogastroenterol Motil 25:208–221. doi:10.1111/Nmo.12076
2. Brutsaert DL (2003) Cardiac endothelial-myocardial signalling: its role in cardiac growth, contractile performance, and rhythmicity. Physiol Rev 83:59–115. doi:10.1152/physrev.00017.2002
3. Buchholz B, Donato M, Perez V, Deutsch AC, Hocht C, Del Mauro JS, Rodriguez M, Gelpi RJ (2014) Changes in the loading conditions induced by vagal stimulation modify the myocardial infarct size through sympathetic-parasympathetic interactions. Pflügers Arch 467:1509–1522. doi:10.1007/s00424-014-1591-2
4. Buchholz B, Donato M, Perez V, Ivalde FC, Hocht C, Buitrago E, Rodriguez M, Gelpi RJ (2012) Preischemic efferent vagal stimulation increases the size of myocardial infarction in rabbits. Role of the sympathetic nervous system. Int J Cardiol 155:490–491. doi:10.1016/j.ijcard.2011.12.082
5. Buckley NM, Gootman PM, Brazeau P, Matanic BP, Frasier ID, Gentles EL (1979) Cardiovascular function in anesthetized miniature swine. Lab Anim Sci 29:200–208
6. Burger DE, Lu X, Lei M, Xiang FL, Hammoud L, Jiang M, Wang H, Jones DL, Sims SM, Feng Q (2009) Neuronal nitric oxide synthase protects against myocardial infarction-induced ventricular arrhythmia and mortality in mice. Circulation 120:1345–1354. doi:10.1161/CIRCULATIONAHA.108.846402
7. Buschman HP, Storm CJ, Duncker DJ, Verdouw PD, van der Aa HE, van der Kemp P (2006) Heart rate control via vagus nerve stimulation. Neuromodulation 9:214–220. doi:10.1111/j.1525-1403.2006.00062.x
8. Calvillo L, Vanoli E, Andreoli E, Besana A, Omodeo E, Gnecchi M, Zerbi P, Vago G, Busca G, Schwartz PJ (2011) Vagal stimulation, through its nicotinic action, limits infarct size and the inflammatory response to myocardial ischemia and reperfusion. J Cardiovasc Pharmacol 58:500–507. doi:10.1097/Fjc.0b013e31822b7204
9. Davidson SM, Hausenloy D, Duchen MR, Yellon DM (2006) Signalling via the reperfusion injury signalling kinase (RISK) pathway links closure of the mitochondrial permeability transition pore to cardioprotection. Int J Biochem Cell Biol 38:414–419. doi:10.1016/j.biocel.2005.09.017
10. De Ferrari GM, Crijns HJ, Borggrefe M, Milasinovic G, Smid J, Zabel M, Gavazzi A, Sanzo A, Dennert R, Kuschyk J, Raspopovic S, Klein H, Swedberg K, Schwartz PJ (2011) Chronic vagus nerve stimulation: a new and promising therapeutic approach for chronic heart failure. Eur Heart J 32:847–855. doi:10.1093/eurheartj/ehq391
11. de Zeeuw S, Trines SA, Krams R, Verdouw PD, Duncker DJ (2000) Cardiovascular profile of the calcium sensitizer EMD 57033 in open-chest anaesthetized pigs with regionally stunned myocardium. Br J Pharmacol 129:1413–1422. doi:10.1038/sj.bjp.0703231
12. Dirksen MT, Laarman GJ, Simoons ML, Duncker DJGM (2007) Reperfusion injury in humans: a review of clinical trials on reperfusion injury inhibitory strategies. Cardiovasc Res 74:343–355. doi:10.1016/j.cardiores.2007.01.014
13. Duncker DJ, Klassen CL, Ishibashi Y, Herrlinger SH, Pavek TJ, Bache RJ (1996) Effect of temperature on myocardial infarction in swine. Am J Physiol 270:H1189–1199
14. Duncker DJ, Stubenitsky R, Tonino PA, Verdouw PD (2000) Nitric oxide contributes to the regulation of vasomotor tone but does not modulate O2-consumption in exercising swine. Cardiovasc Res 47:738–748. doi:10.1016/S0008-6363(00)00143-7
15. Galasso G, Schiekofer S, D’Anna C, Di Gioia G, Piccolo R, Niglio T, De Rosa R, Strisciuglio T, Cirillo P, Piscione F, Trimarco B (2014) No-reflow phenomenon: pathophysiology, diagnosis, prevention, and treatment. A review of the current literature and future perspectives. Angiology 65:180–189. doi:10.1177/0003319712474336
16. Hale SL, Dae MW, Kloner RA (2003) Hypothermia during reperfusion limits ‘no-reflow’ injury in a rabbit model of acute myocardial infarction. Cardiovasc Res 59:715–722. doi:10.1016/S0008-6363(03)00456-5
17. Hale SL, Herring MJ, Kloner RA (2013) Delayed treatment with hypothermia protects against the no-reflow phenomenon despite failure to reduce infarct size. J Am Heart Assoc 2:e004234. doi:10.1161/JAHA.112.004234
18. Heusch G, Kleinbongard P, Skyschally A (2013) Myocardial infarction and coronary microvascular obstruction: an intimate, but complicated relationship. Basic Res Cardiol 108:380. doi:10.1007/s00395-013-0380-y
19. Ibanez B, Heusch G, Ovize M, Van de Werf F (2015) Evolving therapies for myocardial ischemia/reperfusion injury. J Am Coll Cardiol 65:1455–1471. doi:10.1016/j.jacc.2015.02.032
20. Johnston GR, Webster NR (2009) Cytokines and the immunomodulatory function of the vagus nerve. Br J Anaesth 102:453–462. doi:10.1093/Bja/Aep037
21. Katare RG, Ando M, Kakinuma Y, Arikawa M, Handa T, Yamasaki F, Sato T (2009) Vagal nerve stimulation prevents reperfusion injury through inhibition of opening of mitochondrial permeability transition pore independent of the bradycardiac effect. J Thorac Cardiovasc Surg 137:223–231. doi:10.1016/j.jtcvs.2008.08.020
22. Katare RG, Ando M, Kakinuma Y, Arikawa M, Yamasaki F, Sato T (2010) Differential regulation of TNF receptors by vagal nerve stimulation protects heart against acute ischemic injury. J Mol Cell Cardiol 49:234–244. doi:10.1016/j.yjmcc.2010.03.007
23. Kawahara K, Takase M, Yamauchi Y (2003) Increased vulnerability to ischemia/reperfusion-induced ventricular tachyarrhythmias by pre-ischemic inhibition of nitric oxide synthase in isolated rat hearts. Cardiovasc Pathol 12:49–56. doi:10.1016/S1054-8807(02)00155-2
24. Kloner RA, Das S, Poole WK, Perrit R, Muller J, Cannon CP, Braunwald E (2001) Seasonal variation of myocardial infarct size. Am J Cardiol 88:1021–1024. doi:10.1016/S0002-9149(01)01981-6
25. Kong SS, Liu JJ, Hwang TC, Yu XJ, Zhao M, Zhao M, Yuan BX, Lu Y, Kang YM, Wang B, Zang WJ (2012) Optimizing the parameters of vagus nerve stimulation by uniform design in rats with acute myocardial infarction. Plos One 7:e42799. doi:10.1371/journal.pone.0042799
26. Koning MM, Gho BC, van Klaarwater E, Opstal RL, Duncker DJ, Verdouw PD (1996) Rapid ventricular pacing produces myocardial protection by nonischemic activation of K+ ATP channels. Circulation 93:178–186. doi:10.1161/01.CIR.93.1.178
27. Li XD, Yang YJ, Geng YJ, Jin C, Hu FH, Zhao JL, Zhang HT, Cheng YT, Qian HY, Wang LL, Zhang BJ, Wu YL (2010) Tongxinluo reduces myocardial no-reflow and ischemia-reperfusion injury by stimulating the phosphorylation of eNOS via the PKA pathway. Am J Physiol Heart Circ Physiol 299:H1255–1261. doi:10.1152/ajpheart.00459.2010
28. Manintveld OC, te Lintel Hekkert M, van der Ploeg NT, Verdouw PD, Duncker DJ (2009) Interaction between pre- and postconditioning in the in vivo rat heart. Exp Biol Med (Maywood) 234:1345–1354. doi:10.3181/0903-RM-121
29. Manintveld OC, Sluiter W, Dekkers DH, te Lintel Hekkert M, Lamers JM, Verdouw PD, Duncker DJ (2011) Involvement of reperfusion injury salvage kinases in preconditioning depends critically on the preconditioning stimulus. Exp Biol Med (Maywood) 236:874–882. doi:10.1258/ebm.2011.010260
30. Masci PG, Ganame J, Francone M, Desmet W, Lorenzoni V, Iacucci I, Barison A, Carbone I, Lombardi M, Agati L, Janssens S, Bogaert J (2011) Relationship between location and size of myocardial infarction and their reciprocal influences on post-infarction left ventricular remodelling. Eur Heart J 32:1640–1648. doi:10.1093/eurheartj/ehr064
31. Mewton N, Thibault H, Roubille F, Lairez O, Rioufol G, Sportouch C, Sanchez I, Bergerot C, Cung TT, Finet G, Angoulvant D, Revel D, Bonnefoy-Cudraz E, Elbaz M, Piot C, Sahraoui I, Croisille P, Ovize M (2013) Postconditioning attenuates no-reflow in STEMI patients. Basic Res Cardiol 108:383. doi:10.1007/s00395-013-0383-8
32. Musiolik J, van Caster P, Skyschally A, Boengler K, Gres P, Schulz R, Heusch G (2010) Reduction of infarct size by gentle reperfusion without activation of reperfusion injury salvage kinases in pigs. Cardiovasc Res 85:110–117. doi:10.1093/cvr/cvp271
33. Ndrepepa G, Tiroch K, Fusaro M, Keta D, Seyfarth M, Byrne RA, Pache J, Alger P, Mehilli J, Schomig A, Kastrati A (2010) 5-Year prognostic value of no-reflow phenomenon after percutaneous coronary intervention in patients with acute myocardial infarction. J Am Coll Cardiol 55:2383–2389. doi:10.1016/j.jacc.2009.12.054
34. Niccoli G, Burzotta F, Galiuto L, Crea F (2009) Myocardial no-reflow in humans. J Am Coll Cardiol 54:281–292. doi:10.1016/j.jacc.2009.03.054
35. Premchand RK, Sharma K, Mittal S, Monteiro R, Dixit S, Libbus I, DiCarlo LA, Ardell JL, Rector TS, Amurthur B, KenKnight BH, Anand IS (2014) Autonomic regulation therapy via left or right cervical vagus nerve stimulation in patients with chronic heart failure: results of the ANTHEM-HF trial. J Card Fail 20:808–816. doi:10.1016/j.cardfail.2014.08.009
36. Reffelmann T, Kloner RA (2002) Microvascular reperfusion injury: rapid expansion of anatomic no reflow during reperfusion in the rabbit. Am J Physiol Heart Circ Physiol 283:H1099–H1107. doi:10.1152/ajpheart.00270.2002
37. Rutecki P (1990) Anatomical, physiological, and theoretical basis for the antiepileptic effect of vagus nerve stimulation. Epilepsia 31(Suppl 2):S1–6. doi:10.1111/j.1528-1157.1990.tb05843.x
38. Schwartz BG, Kloner RA (2012) Coronary no reflow. J Mol Cell Cardiol 52:873–882. doi:10.1016/j.yjmcc.2011.06.009
39. Shinlapawittayatorn K, Chinda K, Palee S, Surinkaew S, Kumfu S, Kumphune S, Chattipakorn S, KenKnight BH, Chattipakorn N (2014) Vagus nerve stimulation initiated late during ischemia, but not reperfusion, exerts cardioprotection via amelioration of cardiac mitochondrial dysfunction. Heart Rhythm 11:2278–2288. doi:10.1016/j.hrthm.2014.08.001
40. Shinlapawittayatorn K, Chinda K, Palee S, Surinkaew S, Thunsiri K, Weerateerangkul P, Chattipakorn S, KenKnight BH, Chattipakorn N (2013) Low-amplitude, left vagus nerve stimulation significantly attenuates ventricular dysfunction and infarct size through prevention of mitochondrial dysfunction during acute ischemia-reperfusion injury. Heart Rhythm 10:1700–1707. doi:10.1016/j.hrthm.2013.08.009
41. Silber S, Albertsson P, Aviles FF, Camici PG, Colombo A, Hamm C, Jorgensen E, Marco J, Nordrehaug JE, Ruzyllo W, Urban P, Stone GW, Wijns W (2005) Guidelines for percutaneous coronary interventions—the task force for percutaneous coronary interventions of the European Society of Cardiology. Eur Heart J 26:804–847. doi:10.1093/eurheartj/ehi138
42. Skyschally A, van Caster P, Iliodromitis EK, Schulz R, Kremastinos DT, Heusch G (2009) Ischemic postconditioning: experimental models and protocol algorithms. Basic Res Cardiol 104:469–483. doi:10.1007/s00395-009-0040-4
43. Task Force on the management of ST-segment elevation acute myocardial infarction of the European Society of Cardiology (ESC), Steg PG, James SK, Atar D, Badano LP, Blomstrom-Lundqvist C, Borger MA, Di Mario C, Dickstein K, Ducrocq G, Fernandez-Aviles F, Gershlick AH, Giannuzzi P, Halvorsen S, Huber K, Juni P, Kastrati A, Knuuti J, Lenzen MJ, Mahaffey KW, Valgimigli M, van ‘t Hof A, Widimsky P, Zahger D (2012) ESC Guidelines for the management of acute myocardial infarction in patients presenting with ST-segment elevation. Eur Heart J 33:2569–2619. doi:10.1093/eurheartj/ehs215
44. Te Lintel Hekkert M, Dube GP, Regar E, de Boer M, Vranckx P, van der Giessen WJ, Serruys PW, Duncker DJ (2010) Preoxygenated hemoglobin-based oxygen carrier HBOC-201 annihilates myocardial ischemia during brief coronary artery occlusion in pigs. Am J Physiol Heart Circ Physiol 298:H1103–1113. doi:10.1152/ajpheart.00667.2009
45. Uitterdijk A, Sneep S, van Duin R, Krabbendam-Peters I, Gorsse-Bakker C, Duncker DJ, van der Giessen WJ, van Beusekom HM (2013) Serial measurement of hFABP and high sensitivity Troponin I post PCI in STEMI. How fast and accurate can myocardial infarct size and no-reflow be predicted? Am J Physiol Heart Circ Physiol 305:H1104–1110. doi:10.1152/ajpheart.00447.2013
46. Uthman BM, Wilder BJ, Penry JK, Dean C, Ramsay RE, Reid SA, Hammond EJ, Tarver WB, Wernicke JF (1993) Treatment of epilepsy by stimulation of the vagus nerve. Neurology 43:1338–1345. doi:10.1212/WNL.43.7.1338
47. Wagner D, Shelton R, Adams D, Garlie J, Rhee JK, Chen PS, Lin SF (2012) An interactive implantable vagal nerve stimulator for real-time modulation of cardiac autonomic control. Conf Proc IEEE Eng Med Biol Soc. doi:10.1109/EMBC.2012.6347300
48. Wang Q, Cheng Y, Xue FS, Yuan YJ, Xiong J, Li RP, Liao X, Liu JH (2012) Postconditioning with vagal stimulation attenuates local and systemic inflammatory responses to myocardial ischemia reperfusion injury in rats. Inflamm Res 61:1273–1282. doi:10.1007/s00011-012-0527-6
49. Wang Z, Yu L, Huang B, Wang S, Liao K, Saren G, Zhou X, Jiang H (2015) Low-level transcutaneous electrical stimulation of the auricular branch of vagus nerve ameliorates left ventricular remodeling and dysfunction by downregulation of matrix metalloproteinase 9 and transforming growth factor beta1. J Cardiovasc Pharmacol 65:342–348. doi:10.1097/FJC.0000000000000201
50. Wang Z, Yu L, Wang S, Huang B, Liao K, Saren G, Tan T, Jiang H (2014) Chronic intermittent low-level transcutaneous electrical stimulation of auricular branch of vagus nerve improves left ventricular remodeling in conscious dogs with healed myocardial infarction. Circ Heart Fail 7:1014–1021. doi:10.1161/CIRCHEARTFAILURE.114.001564
51. Wu E, Ortiz JT, Tejedor P, Lee DC, Bucciarelli-Ducci C, Kansal P, Carr JC, Holly TA, Lloyd-Jones D, Klocke FJ, Bonow RO (2008) Infarct size by contrast enhanced cardiac magnetic resonance is a stronger predictor of outcomes than left ventricular ejection fraction or end-systolic volume index: prospective cohort study. Heart 94:730–736. doi:10.1136/hrt.2007.122622
52. Yellon DM, Hausenloy DJ (2007) Myocardial reperfusion injury. N Engl J Med 357:1121–1135. doi:10.1056/NEJMra071667
53. Zannad F, De Ferrari GM, Tuinenburg AE, Wright D, Brugada J, Butter C, Klein H, Stolen C, Meyer S, Stein KM, Ramuzat A, Schubert B, Daum D, Neuzil P, Botman C, Castel MA, D’Onofrio A, Solomon SD, Wold N, Ruble SB (2015) Chronic vagal stimulation for the treatment of low ejection fraction heart failure: results of the NEural Cardiac TherApy foR Heart Failure (NECTAR-HF) randomized controlled trial. Eur Heart J 36:425–433. doi:10.1093/eurheartj/ehu345
54. Zhao M, He X, Bi XY, Yu XJ, Wier WG, Zang WJ (2013) Vagal stimulation triggers peripheral vascular protection through the cholinergic anti-inflammatory pathway in a rat model of myocardial ischemia/reperfusion. Basic Res Cardiol 108:345. doi:10.1007/S00395-013-0345-1