Skip to main content
Top
Published in: Basic Research in Cardiology 3/2011

01-05-2011 | Original Contribution

Effects of high thoracic epidural anesthesia on atrial electrophysiological characteristics and sympathetic nerve sprouting in a canine model of atrial fibrillation

Authors: Shu-sen Yang, Wei Han, Yong Cao, Guo Dong, Guo Zhou, Wei-min Li, Run-tao Gan, Hui-ying Chang, Zheng Wang

Published in: Basic Research in Cardiology | Issue 3/2011

Login to get access

Abstract

High thoracic epidural anesthesia (HTEA) blocks the afferent and efferent cardiac sympathetic nerve fibers and may affect atrial electrophysiological characteristics and nerve sprouting in patients with atrial fibrillation (AF). In this study, 18 dogs were randomly divided into a control group (n = 6), in which dogs were atrially paced at 400 beats/min for 6 weeks; an HTEA group (n = 6), in which dogs underwent atrial pacing and HTEA for 6 weeks; and a sham-operated group (n = 6), in which dogs underwent the operation but did not receive atrial pacing or HTEA. Electrophysiological examinations were performed in all groups. Cardiac nerves were immunocytochemically stained with anti-growth-associated protein 43 (GAP43) and anti-tyrosine hydroxylase (TH) antibodies. The protein expressions of nerve growth factor (NGF), GAP43 and TH in atrial myocardium were also studied by western blot. In addition, the plasma levels of C-reactive protein (CRP) and norepinephrine, as well as atrial production of superoxide anion (O 2 ·− ) and malondialdehyde, were measured. In the HTEA group, atrial effective refractory period increased (P < 0.05) and AF maintenance decreased (P < 0.01) significantly compared with the control group. The densities of GAP43-positive nerves and TH-positive nerves were significantly lower in the HTEA group compared with the control group. The protein levels of NGF, GAP43 and TH were also lower in the HTEA group compared with the control group. A significant positive correlation between the expressions of NGF and GAP43 (P < 0.01) was observed. A similar correlation was demonstrated for NGF and TH (P < 0.01) in our study. Furthermore, the plasma levels of CRP and norepinephrine, as well as the amount of O 2 ·− and malondialdehyde produced from myocardium, decreased in the HTEA group compared with the control group. In conclusion, HTEA inhibited electrical and nerve remodeling and reduced the maintenance of AF in a canine AF model, in which process HTEA exhibited anti-inflammatory and antioxidant effects, indicating that, in addition to the efferent cardiac sympathetic nerve, afferent fibers also play an important role in the initiation and/or maintenance of AF.
Literature
1.
go back to reference Ahlers O, Nachtigall I, Lenze J, Goldmann A, Schulte E, Höhne C, Fritz G, Keh D (2008) Intraoperative thoracic epidural anaesthesia attenuates stress-induced immunosuppression in patients undergoing major abdominal surgery. Br J Anaesth 101:781–787. doi:10.1093/bja/aen287 PubMedCrossRef Ahlers O, Nachtigall I, Lenze J, Goldmann A, Schulte E, Höhne C, Fritz G, Keh D (2008) Intraoperative thoracic epidural anaesthesia attenuates stress-induced immunosuppression in patients undergoing major abdominal surgery. Br J Anaesth 101:781–787. doi:10.​1093/​bja/​aen287 PubMedCrossRef
3.
go back to reference Ausma J, Wijffels M, Thoné F, Wouters L, Allessie M, Borgers M (1997) Structural changes of atrial myocardium due to sustained atrial fibrillation in the goat. Circulation 96:3157–3163 Ausma J, Wijffels M, Thoné F, Wouters L, Allessie M, Borgers M (1997) Structural changes of atrial myocardium due to sustained atrial fibrillation in the goat. Circulation 96:3157–3163
5.
go back to reference Bakhtiary F, Therapidis P, Dzemali O, Ak K, Ackermann H, Meininger D, Kessler P, Kleine P, Moritz A, Aybek T, Dogan S (2007) Impact of high thoracic epidural anesthesia on incidence of perioperative atrial fibrillation in off-pump coronary bypass grafting: a prospective randomized study. J Thorac Cardiovasc Surg 134:460–464. doi:10.1016/j.jtcvs.2007.03.043 PubMedCrossRef Bakhtiary F, Therapidis P, Dzemali O, Ak K, Ackermann H, Meininger D, Kessler P, Kleine P, Moritz A, Aybek T, Dogan S (2007) Impact of high thoracic epidural anesthesia on incidence of perioperative atrial fibrillation in off-pump coronary bypass grafting: a prospective randomized study. J Thorac Cardiovasc Surg 134:460–464. doi:10.​1016/​j.​jtcvs.​2007.​03.​043 PubMedCrossRef
6.
go back to reference Berendes E, Schmidt C, Van Aken H, Hartlage MG, Wirtz S, Reinecke H, Rothenburger M, Scheld HH, Schlüter B, Brodner G, Walter M (2003) Reversible cardiac sympathectomy by high thoracic epidural anesthesia improves regional left ventricular function in patients undergoing coronary artery bypass grafting: a randomized trial. Arch Surg 138:1283–1290. doi:10.1001/archsurg.138.12.1283 PubMedCrossRef Berendes E, Schmidt C, Van Aken H, Hartlage MG, Wirtz S, Reinecke H, Rothenburger M, Scheld HH, Schlüter B, Brodner G, Walter M (2003) Reversible cardiac sympathectomy by high thoracic epidural anesthesia improves regional left ventricular function in patients undergoing coronary artery bypass grafting: a randomized trial. Arch Surg 138:1283–1290. doi:10.​1001/​archsurg.​138.​12.​1283 PubMedCrossRef
7.
go back to reference Bruins P, te Velthuis H, Yazdanbakhsh AP, Jansen PG, van Hardevelt FW, de Beaumont EM, Wildevuur CR, Eijsman L, Trouwborst A, Hack CE (1997) Activation of the complement system during and after cardiopulmonary bypass surgery: postsurgery activation involves C-reactive protein and is associated with postoperative arrhythmia. Circulation 96:3542–3548 Bruins P, te Velthuis H, Yazdanbakhsh AP, Jansen PG, van Hardevelt FW, de Beaumont EM, Wildevuur CR, Eijsman L, Trouwborst A, Hack CE (1997) Activation of the complement system during and after cardiopulmonary bypass surgery: postsurgery activation involves C-reactive protein and is associated with postoperative arrhythmia. Circulation 96:3542–3548
8.
go back to reference Carnes CA, Chung MK, Nakayama T, Nakayama H, Baliga RS, Piao S, Kanderian A, Pavia S, Hamlin RL, McCarthy PM, Bauer JA, Van Wagoner DR (2001) Ascorbate attenuates atria pacing-induced peroxynitrite formation and electrical remodeling and decreases the incidence of postoperative atrial fibrillation. Circ Res 89:e32–e38. doi:10.1161/hh1801.097644 PubMedCrossRef Carnes CA, Chung MK, Nakayama T, Nakayama H, Baliga RS, Piao S, Kanderian A, Pavia S, Hamlin RL, McCarthy PM, Bauer JA, Van Wagoner DR (2001) Ascorbate attenuates atria pacing-induced peroxynitrite formation and electrical remodeling and decreases the incidence of postoperative atrial fibrillation. Circ Res 89:e32–e38. doi:10.​1161/​hh1801.​097644 PubMedCrossRef
10.
go back to reference Chang CM, Wu TJ, Zhou S, Doshi RN, Lee MH, Ohara T, Fishbein MC, Karagueuzian HS, Chen PS, Chen LS (2001) Nerve sprouting and sympathetic hyperinnervation in a canine model of atrial fibrillation produced by prolonged right atrial pacing. Circulation 103:22–25 Chang CM, Wu TJ, Zhou S, Doshi RN, Lee MH, Ohara T, Fishbein MC, Karagueuzian HS, Chen PS, Chen LS (2001) Nerve sprouting and sympathetic hyperinnervation in a canine model of atrial fibrillation produced by prolonged right atrial pacing. Circulation 103:22–25
11.
go back to reference Crystal E, Thorpe KE, Connolly SJ, Lamy A, Cybulsky I, Carroll S, Roberts R, Gent M (2004) Metoprolol prophylaxis against postoperative atrial fibrillation increases length of hospital stay in patients not on pre-operative beta blockers: the beta blocker length of stay (BLOS) trial. Heart 90:941–942. doi:10.1136/hrt.2003.016048 PubMedCrossRef Crystal E, Thorpe KE, Connolly SJ, Lamy A, Cybulsky I, Carroll S, Roberts R, Gent M (2004) Metoprolol prophylaxis against postoperative atrial fibrillation increases length of hospital stay in patients not on pre-operative beta blockers: the beta blocker length of stay (BLOS) trial. Heart 90:941–942. doi:10.​1136/​hrt.​2003.​016048 PubMedCrossRef
12.
go back to reference Dhingra RC, Deedwania PC, Cummings JM, Amat-Y-Leon F, Wu D, Denes P, Rosen KM (1978) Electrophysiologic effects of lidocaine on sinus node and atrium in patients with and without sinoatrial dysfunction. Circulation 57:448–454 Dhingra RC, Deedwania PC, Cummings JM, Amat-Y-Leon F, Wu D, Denes P, Rosen KM (1978) Electrophysiologic effects of lidocaine on sinus node and atrium in patients with and without sinoatrial dysfunction. Circulation 57:448–454
14.
go back to reference Elvan A, Pride HP, Eble JN, Zipes DP (1995) Radiofrequency catheter ablation of the atria reduces inducibility and duration of atrial fibrillation in dogs. Circulation 91:2235–2244 Elvan A, Pride HP, Eble JN, Zipes DP (1995) Radiofrequency catheter ablation of the atria reduces inducibility and duration of atrial fibrillation in dogs. Circulation 91:2235–2244
17.
18.
go back to reference Haghjoo M, Saravi M, Hashemi MJ, Hosseini S, Givtaj N, Ghafarinejad MH, Khamoushi AJ, Emkanjoo Z, Fazelifar AF, Alizadeh A, Sadr-Ameli MA (2007) Optimal beta-blocker for prevention of atrial fibrillation after on-pump coronary artery bypass graft surgery: carvedilol versus metoprolol. Heart Rhythm 4:1170–1174. doi:10.1016/j.hrthm.2007.04.022 PubMedCrossRef Haghjoo M, Saravi M, Hashemi MJ, Hosseini S, Givtaj N, Ghafarinejad MH, Khamoushi AJ, Emkanjoo Z, Fazelifar AF, Alizadeh A, Sadr-Ameli MA (2007) Optimal beta-blocker for prevention of atrial fibrillation after on-pump coronary artery bypass graft surgery: carvedilol versus metoprolol. Heart Rhythm 4:1170–1174. doi:10.​1016/​j.​hrthm.​2007.​04.​022 PubMedCrossRef
19.
go back to reference Hassankhani A, Steinhelper ME, Soonpaa MH, Katz EB, Taylor DA, Andrade-Rozental A, Factor SM, Steinberg JJ, Field LJ, Federoff HJ (1995) Overexpression of NGF within the heart of transgenic mice causes hyperinnervation, cardiac enlargement, and hyperplasia of ectopic cells. Dev Biol 169:309–321. doi:10.1006/dbio.1995.1146 PubMedCrossRef Hassankhani A, Steinhelper ME, Soonpaa MH, Katz EB, Taylor DA, Andrade-Rozental A, Factor SM, Steinberg JJ, Field LJ, Federoff HJ (1995) Overexpression of NGF within the heart of transgenic mice causes hyperinnervation, cardiac enlargement, and hyperplasia of ectopic cells. Dev Biol 169:309–321. doi:10.​1006/​dbio.​1995.​1146 PubMedCrossRef
20.
go back to reference Heusch G, Baumgart D, Camici P, Chilian W, Gregorini L, Hess O, Indolfi C, Rimoldi O (2000) α-Adrenergic coronary vasoconstriction and myocardial ischemia in humans. Circulation 101:689–694 Heusch G, Baumgart D, Camici P, Chilian W, Gregorini L, Hess O, Indolfi C, Rimoldi O (2000) α-Adrenergic coronary vasoconstriction and myocardial ischemia in humans. Circulation 101:689–694
21.
24.
go back to reference Jayachandran JV, Sih HJ, Winkle W, Zipes DP, Hutchins GD, Olgin JE (2000) Atrial fibrillation produced by prolonged rapid atrial pacing is associated with heterogeneous changes in atrial sympathetic innervation. Circulation 101:1185–1191 Jayachandran JV, Sih HJ, Winkle W, Zipes DP, Hutchins GD, Olgin JE (2000) Atrial fibrillation produced by prolonged rapid atrial pacing is associated with heterogeneous changes in atrial sympathetic innervation. Circulation 101:1185–1191
25.
go back to reference Kamibayashi T, Hayashi Y, Mammoto T, Yamatodani A, Taenaka N, Yoshiya I (1995) Thoracic epidural anesthesia attenuates halothane-induced myocardial sensitization to dysrhythmogenic effect of epinephrine in dogs. Anesthesiology 82:129–134. doi:10.1097/00000542-199501000-00017 PubMedCrossRef Kamibayashi T, Hayashi Y, Mammoto T, Yamatodani A, Taenaka N, Yoshiya I (1995) Thoracic epidural anesthesia attenuates halothane-induced myocardial sensitization to dysrhythmogenic effect of epinephrine in dogs. Anesthesiology 82:129–134. doi:10.​1097/​00000542-199501000-00017 PubMedCrossRef
27.
go back to reference Li Y, Li WM, Gong YT, Li BX, Liu W, Han W, Dong D, Sheng L, Xue JY, Zhang L, Chu S, Yang BF (2007) The effects of cilazapril and valsartan on the mRNA and protein expressions of atrial calpains and atrial structural remodeling in atrial fibrillation dogs. Basic Res Cardiol 102:245–256. doi:10.1007/s00395-007-0641-8 PubMedCrossRef Li Y, Li WM, Gong YT, Li BX, Liu W, Han W, Dong D, Sheng L, Xue JY, Zhang L, Chu S, Yang BF (2007) The effects of cilazapril and valsartan on the mRNA and protein expressions of atrial calpains and atrial structural remodeling in atrial fibrillation dogs. Basic Res Cardiol 102:245–256. doi:10.​1007/​s00395-007-0641-8 PubMedCrossRef
29.
go back to reference Mathew JP, Fontes ML, Tudor IC, Ramsay J, Duke P, Mazer CD, Barash PG, Hsu PH, Mangano DT, Investigators of the Ischemia Research and Education Foundation, Multicenter Study of Perioperative Ischemia Research Group (2004) A multicenter risk index for atrial fibrillation after cardiac surgery. JAMA 291:1720–1729. doi:10.1001/jama.291.14.1720 PubMedCrossRef Mathew JP, Fontes ML, Tudor IC, Ramsay J, Duke P, Mazer CD, Barash PG, Hsu PH, Mangano DT, Investigators of the Ischemia Research and Education Foundation, Multicenter Study of Perioperative Ischemia Research Group (2004) A multicenter risk index for atrial fibrillation after cardiac surgery. JAMA 291:1720–1729. doi:10.​1001/​jama.​291.​14.​1720 PubMedCrossRef
31.
go back to reference McMurray J, Køber L, Robertson M, Dargie H, Colucci W, Lopez-Sendon J, Remme W, Sharpe DN, Ford I (2005) Antiarrhythmic effect of carvedilol after acute myocardial infarction: results of the Carvedilol Post-Infarct Survival Control in Left Ventricular Dysfunction (CAPRICORN) trial. J Am Coll Cardiol 45:525–530. doi:10.1016/j.jacc.2004.09.076 PubMedCrossRef McMurray J, Køber L, Robertson M, Dargie H, Colucci W, Lopez-Sendon J, Remme W, Sharpe DN, Ford I (2005) Antiarrhythmic effect of carvedilol after acute myocardial infarction: results of the Carvedilol Post-Infarct Survival Control in Left Ventricular Dysfunction (CAPRICORN) trial. J Am Coll Cardiol 45:525–530. doi:10.​1016/​j.​jacc.​2004.​09.​076 PubMedCrossRef
32.
go back to reference Meissner A, Eckardt L, Kirchhof P, Weber T, Rolf N, Breithardt G, Van Aken H, Haverkamp W (2001) Effects of thoracic epidural anesthesia with and without autonomic nervous system blockade on cardiac monophasic action potentials and effective refractoriness in awake dogs. Anesthesiology 95:132–138. doi:10.1097/00000542-200107000-00023 PubMedCrossRef Meissner A, Eckardt L, Kirchhof P, Weber T, Rolf N, Breithardt G, Van Aken H, Haverkamp W (2001) Effects of thoracic epidural anesthesia with and without autonomic nervous system blockade on cardiac monophasic action potentials and effective refractoriness in awake dogs. Anesthesiology 95:132–138. doi:10.​1097/​00000542-200107000-00023 PubMedCrossRef
33.
go back to reference Mihm MJ, Yu F, Carnes CA, Reiser PJ, McCarthy PM, Van Wagoner DR, Bauer JA (2001) Impaired myofibrillar energetics and oxidative injury during human atrial fibrillation. Circulation 104:174–180 Mihm MJ, Yu F, Carnes CA, Reiser PJ, McCarthy PM, Van Wagoner DR, Bauer JA (2001) Impaired myofibrillar energetics and oxidative injury during human atrial fibrillation. Circulation 104:174–180
34.
go back to reference Moore CM, Cross MH, Desborough JP, Burrin JM, Macdonald IA, Hall GM (1995) Hormonal effects of thoracic extradural analgesia for cardiac surgery. Br J Anaesth 75:387–393 Moore CM, Cross MH, Desborough JP, Burrin JM, Macdonald IA, Hall GM (1995) Hormonal effects of thoracic extradural analgesia for cardiac surgery. Br J Anaesth 75:387–393
36.
go back to reference Olausson K, Magnusdottir H, Lurje L, Wennerblom B, Emanuelsson H, Ricksten SE (1997) Anti-ischemic and anti-anginal effects of thoracic epidural anesthesia versus those of conventional medical therapy in the treatment of severe refractory unstable angina pectoris. Circulation 96:2178–2182 Olausson K, Magnusdottir H, Lurje L, Wennerblom B, Emanuelsson H, Ricksten SE (1997) Anti-ischemic and anti-anginal effects of thoracic epidural anesthesia versus those of conventional medical therapy in the treatment of severe refractory unstable angina pectoris. Circulation 96:2178–2182
37.
go back to reference Palomero Rodríguez MA, Suarez Gonzalo L, Villar Alvarez F, Varela Crespo C, Moreno Gomez Limon I, Criado Jimenez A (2008) Thoracic epidural anesthesia decreases C-reactive protein levels in patients undergoing elective coronary artery bypass graft surgery with cardiopulmonary bypass. Minerva Anestesiol 74:619–626 Palomero Rodríguez MA, Suarez Gonzalo L, Villar Alvarez F, Varela Crespo C, Moreno Gomez Limon I, Criado Jimenez A (2008) Thoracic epidural anesthesia decreases C-reactive protein levels in patients undergoing elective coronary artery bypass graft surgery with cardiopulmonary bypass. Minerva Anestesiol 74:619–626
39.
40.
go back to reference Sato R, Koumi S (1995) Modulation of the inwardly rectifying K+ channel in isolated human atrial myocytes by alpha 1-adrenergic stimulation. J Membr Biol 148:185–191. doi:10.1007/BF00207274 PubMed Sato R, Koumi S (1995) Modulation of the inwardly rectifying K+ channel in isolated human atrial myocytes by alpha 1-adrenergic stimulation. J Membr Biol 148:185–191. doi:10.​1007/​BF00207274 PubMed
41.
go back to reference Scott NB, Turfrey DJ, Ray DA, Nzewi O, Sutcliffe NP, Lal AB, Norrie J, Nagels WJ, Ramayya GP (2001) A prospective randomized study of the potential benefits of thoracic epidural anesthesia and analgesia in patients undergoing coronary artery bypass grafting. Anesth Analg 93:528–535. doi:10.1097/00000539-200109000-00003 PubMedCrossRef Scott NB, Turfrey DJ, Ray DA, Nzewi O, Sutcliffe NP, Lal AB, Norrie J, Nagels WJ, Ramayya GP (2001) A prospective randomized study of the potential benefits of thoracic epidural anesthesia and analgesia in patients undergoing coronary artery bypass grafting. Anesth Analg 93:528–535. doi:10.​1097/​00000539-200109000-00003 PubMedCrossRef
42.
go back to reference Shakibi JG, Aryanpur I (1979) Electrophysiologic effects of lidocaine in children. Jpn Heart J 20: 271–276 Shakibi JG, Aryanpur I (1979) Electrophysiologic effects of lidocaine in children. Jpn Heart J 20: 271–276
44.
go back to reference van Veldhuisen DJ, Aass H, El Allaf D, Dunselman PH, Gullestad L, Halinen M, Kjekshus J, Ohlsson L, Wedel H, Wikstrand J, Study Group MERIT-HF (2006) Presence and development of atrial fibrillation in chronic heart failure. Experiences from the MERIT-HF Study. Eur J Heart Fail 8:539–546. doi:10.1016/j.ejheart.2006.01.015 PubMedCrossRef van Veldhuisen DJ, Aass H, El Allaf D, Dunselman PH, Gullestad L, Halinen M, Kjekshus J, Ohlsson L, Wedel H, Wikstrand J, Study Group MERIT-HF (2006) Presence and development of atrial fibrillation in chronic heart failure. Experiences from the MERIT-HF Study. Eur J Heart Fail 8:539–546. doi:10.​1016/​j.​ejheart.​2006.​01.​015 PubMedCrossRef
45.
49.
go back to reference Zhou S, Cao JM, Tebb ZD, Ohara T, Huang HL, Omichi C, Lee MH, KenKnight BH, Chen LS, Fishbein MC, Karagueuzian HS, Chen P-S (2001) Modulation of QT interval by cardiac sympathetic nerve sprouting and the mechanisms of ventricular arrhythmia in a canine model of sudden cardiac death. J Cardiovasc Electrophysiol 12:1068–1073. doi:10.1046/j.1540-8167.2001.01068.x PubMedCrossRef Zhou S, Cao JM, Tebb ZD, Ohara T, Huang HL, Omichi C, Lee MH, KenKnight BH, Chen LS, Fishbein MC, Karagueuzian HS, Chen P-S (2001) Modulation of QT interval by cardiac sympathetic nerve sprouting and the mechanisms of ventricular arrhythmia in a canine model of sudden cardiac death. J Cardiovasc Electrophysiol 12:1068–1073. doi:10.​1046/​j.​1540-8167.​2001.​01068.​x PubMedCrossRef
Metadata
Title
Effects of high thoracic epidural anesthesia on atrial electrophysiological characteristics and sympathetic nerve sprouting in a canine model of atrial fibrillation
Authors
Shu-sen Yang
Wei Han
Yong Cao
Guo Dong
Guo Zhou
Wei-min Li
Run-tao Gan
Hui-ying Chang
Zheng Wang
Publication date
01-05-2011
Publisher
Springer-Verlag
Published in
Basic Research in Cardiology / Issue 3/2011
Print ISSN: 0300-8428
Electronic ISSN: 1435-1803
DOI
https://doi.org/10.1007/s00395-011-0154-3

Other articles of this Issue 3/2011

Basic Research in Cardiology 3/2011 Go to the issue